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Regulates Division and Death through E2f1\nWe used the α-Cre transgene to delete floxed Rb exon 19 at embryonic day (E) 10 in peripheral retina [2]. RbloxP/loxP;α-Cre mice were bred with strains lacking E2f1 or E2f2 in the germ line, or a strain carrying a floxed E2f3 allele [5]. RbloxP/loxP;E2f1+/− and RbloxP/loxP;E2f1+/−;α-Cre mice were bred to produce RbloxP/loxP;E2f1−/−;α-Cre mice at a frequency of 1/8 and littermate controls at the same or higher (1/4) frequency. For simplicity we will refer to the RbloxP/loxP;E2f1−/−;α-Cre peripheral retina as the Rb/E2f1 double knockout (DKO) retina. Similar strategies were employed in the case of E2f2 or E2f3. Cre-mediated excision of Rb and E2f3 alleles in the retina was confirmed by PCR as described previously [2,5].\nTo measure ectopic cell division, mice were pulse-labelled with bromodeoxyuridine (BrdU) 2 h before sacrifice and the peripheral retina analyzed for BrdU incorporation by immunofluorescence. As reported before [2,3], Rb KO retinas exhibited both spatial and temporal ectopic DNA synthesis (Figures 1C and S1A). This is easily detected at E14, E16, and postnatal day (P) 0 in the inner retina where abnormal BrdU+ ganglion and amacrine RTCs are located, or on the outermost region of the P0 retina, where BrdU+ photoreceptor RTCs reside (Figures S1A and S2, arrows) [2]. Ectopic RTC division in Rb KO retinas is even more obvious at P8 or P18, when division is completed in wild-type (WT) retina (Figures 1C and S1A). Strikingly, the ectopically positioned S-phase cells at E14, E16, and P0 and all the abnormal division at P8 and P18 were completely suppressed in the Rb/E2f1 DKO retina (Figures 1C, 1E, 1F, S1A, and S2). In contrast, deletion of E2f2 or E2f3 had no effect at any stage of development. Analysis of mitotic cells with anti–phosphohistone 3 (PH3)–specific antibodies confirmed that loss of E2f1, but not E2f2 or E2f3, suppressed ectopic division (Figure S3). Deleting one E2f1 allele partially suppressed ectopic S-phase and mitosis in Rb KO RTCs (Figures 1C, 1E, 1F, S1A, S2, and S3), suggesting that E2f1 drives ectopic division in Rb KO RTCs in a dose-dependent fashion. These data contrast with previous findings in the lens and CNS of Rb KO embryos, where deletion of any activating E2f suppresses ectopic division to some extent [6–9].\nLoss of Rb in the retina results in considerable RTC apoptosis, eliminating most bipolar and ganglion cells as well as many rods (Figure 2A–2D) [2,3]. The loss of Rb KO rods is evident from the thinner ONL, and the death of these cells as well as bipolar and ganglion neurons can be detected directly by double labelling for apoptotic and cell-type-specific markers [2] (M. P. and R. B., unpublished data). Loss of peripheral Rb KO ganglion cells is also evident from thinning of the optic nerve (D. C. and R. B., unpublished data). Deleting E2f1, but not E2f2 or E2f3, blocked this ectopic cell death in a dose-dependent fashion (Figures 1D, 1G, and S1B).\nFigure 2 E2f1 Deletion Rescues Ganglion, Rod, and Bipolar Cells in the Rb KO Retina\n(A) Horizontal retinal sections from mice of the indicated ages and genotypes were stained for nuclei (DAPI, blue) and markers that detect ganglion cells (Pou4f2, red), rods and cones (Sag [rod arrestin], green), and rod bipolar cells (Prkca, green, and Cabp5, red). Scale bars are 50 μm.\n(B) Quantification of Pou4f2+ ganglion cells.\n(C) Quantification of Prkca+ and Cabp5+ bipolar cells.\n(D) Thickness of the ONL, which represents the number of rods.\nError bars represent SD of measurements from three animals, and asterisks indicate a significant difference between retinas of WT and the indicated genotypes, unless indicated otherwise by connecting lines (*, p \u003c 0.05; **; p \u003c 0.01; ANOVA and Tukey HSD test).\n(E and F) ERGs were recorded from the indicated genotypes under dark-adapted (scotopic) conditions, and (E) intensity series and (F) b-wave amplitudes as a function of the logarithm of the flash intensity were determined. (F) Further illustrates that the relative influence of the mutations on the photoreceptors (indicated by the saturated a-wave amplitude, right graph) was not substantially different from their effect on the b-wave response (dominated by the bipolars, left graph) at the same intensity of 10 cd·s/m2. To investigate the molecular mechanism that underlies the unique role of E2f1, we assessed the expression of known E2f targets as well as other genes that regulate the cell cycle and apoptosis. Numerous positive and negative cell cycle and apoptotic regulators were up-regulated in the Rb KO retina (Figure 1H). Among the E2f family, E2f1, E2f2, E2f3a, and E2f7 were induced following Rb loss, but E2f3b, E2f4, and E2f5 were unaffected. Consistent with the BrdU and terminal dUTP nick-end labelling (TUNEL) analyses, E2f1 deletion specifically reversed all these molecular defects, but E2f3 deletion had no effect (Figure 1H).\n\nNormal Differentiation in the Rb/E2f1 DKO Retina\nBecause E2f1 deletion blocks abnormal division and death in the Rb KO retina, the Rb/E2f1 DKO retina provided a unique opportunity to evaluate whether Rb controls differentiation independent of cell cycle effects. The Rb/E2f1 DKO retina had many Sag+ (S-antigen/rod arrestin) photoreceptors, Pou4f2+ (Brn3b) ganglion cells, and numerous Prkca+/Cabp5+ bipolar neurons (Figure 2A–2D). In contrast, there was no such rescue of cell types in Rb/E2f2 or Rb/E2f3 DKO retinas (Figure S4). Analysis with general neuronal markers Mtap2 (MAP2) and Snap25, as well as other markers expressed in bipolar cells (Chx10, Rcvrn, Vsx1, Tacr3, and Atp2b1) and rod photoreceptors (Rho and Rcvrn) confirmed rescue of the Rb/E2f1 DKO retina (Table S1). Moreover, neurons exhibited the same complex morphology as in WT retina. Bipolar cell bodies were located in the INL and had ascending and descending processes ending in the OPL and IPL, respectively (Figure 2A). In addition, the Rb/E2f1 DKO retina had a healthy appearing ONL consisting of morphologically normal rods with descending processes ending in the OPL and ascending processes that terminated in inner and outer segments (Figure 2A). It was suggested that Rb might regulate photoreceptor differentiation, possibly through rod-specific transcription factors (Figure 1B) [29]. However, if Rb does regulate photoreceptor differentiation, it does so by inhibiting E2f1, not by potentiating rod differentiation factors, such as Otx2, Crx, or Nrl. It is impossible to tell whether E2f1 perturbs differentiation directly, by affecting the expression of genes that modulate maturation, and/or indirectly through its effects on proliferation and survival (Figure 1B).\nAs with ectopic division and apoptosis (Figure 1C and 1D), the rescue of Rb KO retinal bipolar, ganglion, and rod cells was dependent on E2f1 dose (Figure 2A–2D). Separate from its role in driving ectopic division of Rb KO RTCs, E2f1 also promotes normal RPC division since in its absence RPC proliferation drops ~2-fold (D. C. and R. B., unpublished data). This modest reduction of RPC numbers in the absence of E2f1 accounts for the slight reduction in the number of ganglion cells at P0, in the number of bipolar cells at P18 or P30, and in the thickness of the ONL at P18 or P30 in the E2f1 KO and Rb/E2f1 DKO retina (Figure 2B–2D). The morphology of E2f1 KO neurons was WT (Figure 2A). Despite a slight drop in absolute cell numbers, the proportion of Rb/E2f1 DKO and E2f1 KO bipolar cells was the same as WT (data not shown). Slightly reduced cell numbers were not due to residual RTC death since we have not observed ectopic apoptosis at any embryonic or postnatal stage in the developing Rb/E2f1 DKO retina (Figures 1D, 1G, and S2). Moreover, deleting Ccnd1, which acts upstream of Rb proteins, also reduces RPC number, but does not suppress any defect in the Rb KO retina (D. C. and R. B., unpublished data). Thus, slightly reduced RPC division and dramatic rescue of severe defects in Rb KO RTCs are distinct effects stemming from the deletion of E2f1.\n\nNormal Function of the Rb/E2f1 DKO Retina\nThe discovery that E2f1 loss rescues even the morphology of Rb KO neurons is surprising because Rb is thought to regulate differentiation primarily through E2f-independent pathways [30–33]. However, normal morphology may not equate to completely normal differentiation. Thus, we compared the electroretinograms (ERGs) of adult WT (α-Cre), E2f1−/−, α-Cre;RbloxP/loxP, and α-Cre;RbloxP/loxP;E2f1−/− mice. ERGs functionally assess visual signalling in the mammalian retina from photoreceptors to amacrine cells (but usually not gangion cells), and are dominated by rod and cone bipolar cells. Typically, an ERG signal begins with a negative deflection initiated by the photoreceptors (the a-wave), which is terminated by a large positive deflection due to the activation of ON bipolar cells (the b-wave).\nResponses to dim light in dark-adapted (scotopic) conditions specifically assess the rod system, and were defective in the Rb KO retina (Figure 2E). The substantial reduction of both a- and b-waves is consistent with rod and bipolar cell apoptosis [2]. The sensitivity of the residual response appeared unchanged, suggesting it arose from the Cre-negative portions of the retina. Responses were about the same in the WT and E2f1 KO retina, and, most importantly, also the Rb/E2f1 DKO response median lay at the lower end of the normal range for most intensities (Figure 2F). Thus, E2f1 deletion almost completely rescued the rod system in the Rb KO retina.\nLight-adapted (photopic) recordings to specifically assess the cone system yielded comparable results. Cones represent only 3% of photoreceptors and, unlike rods, develop without Rb, but they require rods for survival, and in the Rb KO retina, they have abnormal morphology and their synaptic targets, bipolar cells, are much depleted [2]. The photopic response, a product of cone and mainly bipolar activity, was much reduced by Rb loss, but was rescued considerably in the Rb/E2f1 DKO retina (Figure S5). Again, the median amplitude lay at the lower end of the E2f1 KO range. The photopic response in E2f1 KO mice was slightly reduced relative to WT (Figure S5B), possibly because E2f1 is required for maximal expansion of embryonic RPCs, and the E2f1 KO retina has, as noted earlier, slightly fewer cells than the WT retina, although cell type proportions are unaffected (D. C. and R. B., unpublished data). Thus, marginally subnormal photopic responses in the Rb/E2f1 DKO retina can be attributed to both a reduction of cone numbers in E2f1 KO mice alone, and a “genuine” slight reduction in cone function attributable to Rb loss relative to WT. This slight effect may relate to a true differentiation defect in a subset of amacrine cells discussed below. This discussion should not obscure the major outcome that E2f1 deletion recovers most of the ERG response. Thus, E2f1 deletion not only rescues morphology but also both rod and cone system function in the Rb KO retina.\n\nAbnormal SAC Differentiation Independent of Cell Cycle and Survival Defects\nERGs primarily assess photoreceptor and bipolar cell function, but may miss differentiation defects in other cells. To test for subtle differences we stained the Rb/E2f1 DKO retina with 43 markers (Table S1). Thirty-two proteins displayed identical patterns in WT, E2f1 KO, and Rb/E2f1 DKO retina (Table S1). The other 11 markers revealed a cell-cycle– and apoptosis-independent differentiation defect in SACs. We first studied Calb2 (calretinin), which marks a subset of amacrine and ganglion cell bodies as well as three tracks corresponding to their processes in the IPL (Figure 3A). Normal Calb2 staining was seen in the E2f1 KO IPL (data not shown). However, only one Calb2+ track was evident in the Rb KO IPL, and this defect was not rescued in the Rb/E2f1 DKO retina (Figure 3A). We quantified Calb2+ cell bodies in the Rb KO INL (corresponding to amacrine cell staining only) and observed a reduction from P8 onwards (Figures 3C and S6).\nFigure 3 Differentiation Defects in Rb KO SACs\n(A) P18 horizontal sections of WT, Rb KO, and Rb/E2f1 DKO retina were stained for nuclei (DAPI, blue), Calb2 (green), and Slc18a3 (red).\n(B) Confocal images of P30 horizontal sections of WT and Rb KO retina were stained for nuclei (DAPI, blue), Chat and Slc18a3 (both red), and Camk2a (green). In the Rb KO section, the red stain is Chat only, as Slc18a3 is missing (see [A]).\n(C) Quantification of dense Calb2+ cell bodies in the INL, total Slc18a3+ cell bodies, and Camk2a+ cell bodies in the INL. Error bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\nScale bars are 50 μm in (A) and 20 μm in (B). Of the three Calb2+ tracks in the IPL, the two outer tracks are from SACs, named after their extensive dendritic-tree-like morphology [37]. SACs are cholinergic, represent ~5.2% of amacrine neurons [38], and are critical for both direction selectivity [34,35] and spontaneous rhythmic activity that occurs during normal retinal development [36]. SACs in the INL synapse in the OFF layer of the IPL that responds to decreasing light, while displaced SACs in the GCL have processes that synapse in the nearby ON layer of the IPL that responds to increasing light (reviewed in [39]). Mature SAC processes stain specifically for Slc18a3 (vesicular acetyl choline transporter, VAChT) [37], and, significantly, this marker was absent in the peripheral Rb KO or Rb/E2f1 DKO P18 retina (Figures 3A and S7B). Chat, expressed from the same locus, is also SAC specific, but marks both cell bodies and processes of mature SACs [37]. Chat was seen in fewer cells in the mature Rb KO retina, and was present in the soma but absent from processes (Figure 3B). We obtained similar results for Sv2c, a synaptic vesicle protein found in SACs [40]; Kcnc1b and Kcnc2, potassium channels expressed on SAC soma and dendrites as well as a very small number of ganglion cells [41]; gamma-aminobutyric acid (GABA), an inhibitory neurotransmitter present in about half of amacrine cells including SACs, as well as horizontal and some bipolar neurons [37]; and Calb1 (calbindin), which is expressed in many amacrine cells and labels SAC process faintly (Figure S7A and S7B; Table S1; and data not shown). Finally, we also examined the effect of Rb deletion on SAC differentiation using a Chx10-Cre transgene that is expressed in a mosaic pattern across the retina, generating patches of Cre-expressing cells [42]. Consistent with the mosaic deletion pattern, we observed markedly reduced Chat/Slc18a3 staining in the IPL of Chx10-Cre;RbloxP/loxP retina compared to WT (Figure S7C). Together, these results suggest a role for Rb in SAC differentiation.\nThe above findings could indicate a defect in SAC specification, SAC survival, or the levels and/or transport of the markers described above. Camk2a marks both SACs and ganglion cells [37], but because ganglion cells are eliminated in the Rb KO retina, Camk2a is a specific SAC marker in this context. Importantly, Camk2a+ tracks and dendrites were present in both the WT and Rb KO retina (Figure 3B), and the number of Camk2a+ soma was similar in WT and Rb KO retina at P30 and beyond, although fewer cells stained in Rb KO retina at P18, suggesting a delay in its appearance (Figures 3C and S6B). Thus, Rb is not required for SAC survival or for process outgrowth, but rather it seems to regulate the expression and/or stability of Calb2, Calb1, Chat, Slc18a3, Sv2c, Kcnc1b, Kcnc2, and GABA in SACs, but leaves Camk2a expression virtually unaffected. The presence of Chat in some cell bodies but never in processes (Figure 3B) also suggests a transport defect. The developmental pattern of Slc18a3 expression also supported this notion. In mature WT SACs Slc18a3 is only in processes, but in early postnatal SACs, it is found in the cell body, and moves into emerging processes at approximately P4–P6. As noted above, Slc18a3 was absent at P18 in the Rb KO retina (Figure 3A); at P4 or P5 it was in cell bodies, yet was rarely present in Rb KO processes (Figures 4A and S6). Slc18a3 became virtually undetectable in Rb KO SACs by P8 (Figures 3C and S6C). These data suggest that Rb affects both the synthesis/stability and transport of SAC markers.\nFigure 4 E2f3 Loss Rescues Differentiation of Rb KO SACs\n(A) Horizontal retinal sections of the indicated ages and genotypes were stained for nuclei (DAPI, blue), mitosis marker PH3 (green), and Slc18a3 (red), which marks SAC soma at early stages and processes from ~P5 onwards. Arrows show mitotic PH3+ nuclei in Rb KO, Rb/E2f2 DKO, and Rb/E2f3 DKO retinas. E2f1 loss rescues the ectopic mitosis and cell death defects, but not the SAC defect. E2f2 loss has no effect. E2f3 loss does not rescue the ectopic mitosis and cell loss defects, but rescues the SAC defect. Inactivating E2f1 and E2f3 together rescues the ectopic mitosis, cell death, and SAC defects.\n(B) The fraction of Camk2a+ cells that are Chat + and Slc18a3+ in the P30 retina.\n(C) Horizontal P5 retinal sections were stained for nuclei (DAPI, blue), Slc18a3 (green), and Isl1 (red). Arrows show double-labelled Isl1+/Slc18a3+ cells in the inner INL.\n(D) Horizontal P0 retinal sections of the indicated genotypes were stained for nuclei (DAPI, blue), cell division marker Mki67 (green), and Isl1 (red). Arrows show double-labelled dividing SACs.\n(E) The fraction of Isl1+ cells in the inner NBL (INBL) of P0 retinas that are dividing (Mki67+).\nError bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test). Scale bars in (A), (C), and (D) are 50 μm.\n\nRb Regulates SAC Differentiation through E2f3\nRb binds more than 100 proteins [43] and in some non-neuronal cells, such as skeletal muscle, adipocytes, and bone, Rb is thought to bind and potentiate tissue-specific transcription factors that promote differentiation [31–33]. Thus, we expected that Rb might interact with retina-specific factors to facilitate SAC differentiation. A direct role for E2f in mediating Rb-dependent differentiation defects (independent of cell cycle or death defects) has to our knowledge not been described, but because E2f can regulate some differentiation genes [44–48], we first tested whether E2f2 or E2f3 might perturb Rb KO SAC maturation. At multiple time points, E2f1 deletion suppressed ectopic mitosis (PH3+ cells), but did not reverse the SAC defect, and E2f2 deletion had no effect on either defect (Figure 4A). Remarkably, although E2f3 deletion did not reverse ectopic mitosis, it rescued Calb2, Slc18a3, Chat, GABA, Kcnc1b, Kcnc2, and Sv2c staining at multiple times (Figure 4A and data not shown). Rb/E2f3 DKO SAC tracks were slightly more disordered than in WT retina, most likely because of the absence of synaptic partner cells, which are killed by E2f1. Indeed, this minor defect was rescued in the Rb/E2f1/E2f3 triple knockout retina, where bipolar and ganglion cell death was rescued and SAC differentiation was restored (Figure 4A). E2f3 deletion alone did not affect SAC differentiation (Figure 4A); thus, it is unleashed E2f3 activity that is detrimental, and the critical role for Rb is to inhibit E2f3.\nWe quantified the fraction of Camk2a+ SACs in different genotypes and found that 60% of WT P30 Camk2a+ cells expressed Chat and Slc18a3, which dropped to only 5.6% in the Rb KO retina, and remained low at 3.7% in the Rb/E2f1 DKO retina, but rose to 91% in the Rb/E2f3 DKO retina (Figure 4B). The latter fraction is higher than WT because ganglion cells, which normally make up ~40% of Camk2a+ cells, are killed by apoptosis.\nTo quantify the effect of different E2fs on ectopic division specifically in SACs, we exploited Isl1 (Islet1). This marker is expressed in both SACs and ganglion cells, thus Isl1+ cells in the INL are exclusively SACs [49]. We found that 98.2% ± 1.8% of Isl1+ cells in the forming inner INL at P5 were also Slc18a3+, confirming that Isl1 is an excellent SAC marker (Figure 4C). Moreover, Isl1, unlike Slc18a3, is nuclear, which facilitates scoring of Isl1+/Mki67+ cells. It is also expressed earlier than Slc18a3, permitting analysis of SACs soon after their birth at ~E15; thus, we could study retina at P0, a time when ectopic division is high in the inner retina and prior to Rb-independent cell cycle exit associated with terminal differentiation [2]. At P0, no WT Isl1+ cells in the inner neuroblastic layer (NBL) (which is the future INL) were dividing, but 57 ± 14 Isl1+/Mki67+ cells were detected in the Rb KO inner NBL (Figure 4D). Indeed, about one-third of all Isl1+ cells in the entire inner NBL were dividing in the Rb KO retina, or ~50% in the periphery where Cre is expressed (Figure 4E and data not shown). This defect was suppressed in the Rb/E2f1 DKO retina, where we detected only 1 ± 1 dividing SAC, but not the Rb/E2f3 DKO retina, where there were 53 ± 8 dividing SACs (Figure 4D and 4E). We observed similar effects at P0 with Calb2, which marks newborn SACs and other amacrine cells (data not shown). Thus, in Rb KO SACs, E2f1 deletion suppresses ectopic division but not aberrant differentiation, whereas E2f3 deletion suppresses aberrant differentiation but not ectopic division.\n\nSpecific Expression of E2f3 in SACs and Other Subsets of CNS Neurons\nThe unique effect of E2f3 in disrupting the differentiation of SACs but not other retinal neurons might be due to cell-type-specific expression or cell-type-specific activity of E2f3. Determining between these two possibilities is not easy, as E2f immunostaining in mouse tissues is problematic. We did not solve this issue for E2f1 or E2f2, but used a modified protocol [50] to successfully track E2f3 expression (Figure 5). At P0, E2f3 was detected in RPCs, consistent with a putative role in normal proliferation (Figure 5A). The signal was specific as it was absent in the E2f3 KO peripheral retina (Figure 5A). As the retina differentiated and RPC division diminished, the number of E2f3+ cells also dropped, and by P8, when division is virtually over, only a subset of post-mitotic cells in the inner retina expressed E2f3 (Figure 5A). By P18, E2f3 was also detected in two tracks in the IPL (Figure 5A and 5B), reminiscent of SAC markers such as Chat and Slc18a3 (c.f. Figures 3 and 4). This cytoplasmic E2f3 staining was also specific, as it was absent in the E2f3 KO peripheral retina of α-Cre;E2f3loxP/loxP mice (Figure 5A). Indeed, double labelling with E2f3 (red) and Chat plus Slc18a3 (green) confirmed that E2f3 is present in both SAC soma and dendrites (Figure 5B). Rb protein was also detected in the inner retina (Figure 5A), and showed a similar distribution as E2f3 in SACs (Figure 5B), and was also present in mature ganglion cells and Müller cells as reported [51]. Rb staining in SAC processes was specific as it was absent in the peripheral retina of αCre;RbloxP/loxP mice (Figure 5A). These data suggest that Rb and E2f3 colocalize in SACs and that E2f3 triggers defects in SAC differentiation because it is specifically expressed in these retinal neurons.\nFigure 5 E2f3 and Rb Expression in SACs\n(A) Left panels: horizontal P0, P8, and P18 retinal sections of the indicated genotypes were stained for E2f3 (red) and DAPI (blue). The arrow indicates the junction between the E2f3 null peripheral and WT central P0 retina. Note the absence of E2f3 protein in the peripheral E2f3 KO RPCs at P0 and in peripheral inner retinal neurons at P18. Far right panel: P18 retinal sections of the indicated genotypes were stained for Rb (red) and DAPI (blue). Note the absence of Rb protein in the peripheral Rb KO inner retinal neurons.\n(B) WT P18 retinal sections were stained for nuclei (DAPI, blue), E2f3 (red) or Rb (red), and Chat plus Slc18a3 (green). Arrows indicate double-labelled soma. Note that the IPL processes are also double-labelled.\nScale bars are 50 μm. We also found that E2f3 is present in a specific subset of mature neurons in various brain regions (data not shown). For example, in the P20 amygdala, E2f3 colocalized with the general neuronal markers Mtap2 and Mecp2 [52], but not with Calb2, which marks a subset of neurons, or with the glial marker Gfap (data not shown). Unlike in retinal SACs, E2f3 was not coexpressed in Chat+ or Slc18a3+ cholinergic neurons located in various regions of the brain and spinal cord (data not shown). In agreement, we could not detect defects in cholinergic Rb KO neurons in the developing forebrain, but other Rb KO neurons in this region showed differentiation defects that were rescued by deleting E2f3 [53]. Together, these results suggest that the common mechanism by which Rb promotes neural differentiation is through E2f3 inhibition.\n\nDistinct Localization of E2f3 Isoforms\nAs noted above, E2f3 and Rb staining in SACs was both nuclear and cytoplasmic (Figure 5A and 5B). The antibody that worked in immunostaining recognizes a C-terminal region and thus, does not distinguish a/b isoforms. To our knowledge, the subcellular location of E2f3 isoforms has not been determined in any cell type. To verify the dual locations of E2f3 and to determine which isoforms were present in retina, we analyzed nuclear and cytoplasmic fractions by Western blot at different times during development. Analysis with the pan-E2f3 antibody (sc-878, Santa Cruz Biotechnology) detected a 55-kD E2f3a species and a 40-kD E2f3b polypeptide (Figure 6). To confirm that the upper species in our retinal lysates was E2f3a, we exploited novel mice that lack E2f3 exon 1a and thus express E2f3b exclusively (R. O. and G. L., unpublished data). The genotyping strategy is discussed in detail later and is outlined in Figure 7A. Western analysis confirmed that the upper band was absent in E2f3a−/− mice (Figures 6 and S8). Consistent with the drop in E2f3-expressing cells during WT retinal maturation (Figure 5A), the total amount of E2f3a was less at P18 compared to P0 (Figure 6). E2f3b was present in similar amounts at both time points. At P0 and P18, E2f3a was present in both nuclear and cytoplasmic fractions, but in marked contrast, E2f3b was exclusively nuclear at both times (Figure 6). Two closely migrating E2f3a bands were detected, more clearly evident at P18, of which the faster migrating species was dominant in nuclear and the slower species was dominant in cytoplasm (Figure 6). The identity of both as E2f3a species was confirmed by their absence in the P18 E2f3a KO retina (Figure S8). Analysis of Pou4f2, a nuclear transcription factor expressed in ganglion cells, showed that nuclear proteins had not contaminated the cytoplasmic fraction, and analysis of Slc18a3, a cytoplasmic SAC marker, confirmed that the reverse had also not occurred (Figure 6). These data show, to our knowledge for the first time, that E2f3a and E2f3b exhibit distinct patterns of subcellular distribution, and raise the possibility that E2f3a localization may be regulated by as yet unknown post-translational modifications.\nFigure 6 Subcellular Distribution of E2f3 Isoforms and Other Cell Cycle Proteins in the Developing Retina\nNuclear and cytoplasmic extracts from an equivalent number of retinal cells from mice of the indicated genotypes and ages were analyzed by Western blotting to detect the indicated proteins. Lysate from E2f3a−/− mice was used as a control to confirm the location of E2f3a protein. C, cytoplasmic extracts; N, nuclear extracts.\nFigure 7 The E2f3a Isoform Drives the Differentiation Defect in Rb KO SACs\n(A) Schematic diagrams of the mouse WT, E2f3a−/−, and the Cre-recombined floxed E2f3 loci (indicated here as E2f3−/− for simplicity). E2f3a−/− mice lack most of E2f3 exon 1a and part of intron 1a (red dotted box). Arrows indicate PCR primers. Genotyping of an E2f3a+/− mouse is shown on the right.\n(B) RT-PCR detection of E2f3a and E2f3b mRNA in the retina. The sequences of primers are 1aF (5′-GCCTCTACACCACGCCACAAG-3′), 1bF (5′-CGGAAATGCCCTTACAGC-3′), and 4R (5′-CTCAGTCACTTCTTTGGACAG-3′). WT retina expresses both E2f3a and E2f3b mRNA. As expected, E2f3a−/− retina lacks E2f3a mRNA and still expresses E2f3b mRNA. E2f3−/− retina lacks full-length E2f3a and E2f3b mRNAs, and instead expresses a truncated mRNA lacking exon 3.\n(C) Real-time RT-PCR analysis of E2f genes in P8 retinas of the indicated genotypes. Error bars represent SD of measurements from three animals, and asterisks indicate a significant difference between WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\n(D) Rescue of Rb KO SACs by E2f3a deletion. Horizontal retinal sections of the indicated genotypes and ages were stained for nuclei (DAPI, blue), M-phase (PH3, green), and the SAC marker Slc18a3 (red). E2f3a deletion does not suppress ectopic division, but rescues the SAC defect. Scale bars are 50 μm.\nM, molecular size marker. We also examined the distribution of other cell cycle regulators during retinal development. Like E2f3a, Rb was present in both the WT cytoplasm and nucleus at P0, but at P18, when the levels of Rb had increased, it was primarily nuclear (Figure 6). A very faint cytoplasmic Rb signal was evident at P18, which is consistent with Rb staining of SAC processes (Figure 5B), and with the very small proportion of SACs in the retina [38]. E2f1 was also detected in both nuclear and cytoplasmic fractions, although unlike E2f3a it was predominantly nuclear both at P0 and P18 (Figure 6). The E2f dimerization partner, Tfdp1, which lacks a nuclear localization signal [54], was primarily cytoplasmic at both P0 and P18, and the Cdk inhibitors Cdkn1a and Cdkn1b showed a similar pattern of distribution (Figure 6). Thus, among the cell cycle regulators we examined, most showed bivalent distribution, and E2f3b was unusual in its solely nuclear compartmentalization.\n\nRb Regulates SAC Differentiation through E2f3a\nTo test which E2f3 isoform is responsible for aberrant Rb KO SAC differentiation we exploited E2f3a−/− mice (Figure 7A). The genotyping strategy outlined in Figure 7A was used to distinguish the E2f3a, WT, and null alleles. Reverse transcriptase PCR (RT-PCR) confirmed the presence of both E2f3a and E2f3b RNA species in the developing WT retina, and the specific absence of E2f3a RNA in the E2f3a−/− retina (Figure 7B). E2f3a protein was absent in E2f3a−/− retinal lysate (Figures 6 and S8). Importantly, the levels of E2f3b message were similar in the Rb KO and Rb/E2f3a DKO retina, ruling out the possibility that any effects of E2f3a deletion we might observe were due to down-regulation of E2f3b (Figure 7C). Also, the levels of other E2fs were the same in the Rb KO, Rb/E2f3 DKO, and Rb/E2f3a DKO retina, ruling out any cross-regulatory effects (Figure 7C) [55]. E2f3a can trigger cell cycle induction, but because SAC defects are not linked to cell cycle perturbation (Figures 3A and 4), and in view of the predominant association between E2f3b and Rb in quiescent cells [16,19], we suspected that E2f3b may perturb differentiation in Rb KO SACs. Unexpectedly, however, E2f3a deletion suppressed the Rb KO SAC defect (Figure 7D). Thus, separate from its role in cell cycle control, Rb regulation of E2f3a is critical to ensure proper neuronal differentiation."}

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Regulates Division and Death through E2f1\nWe used the α-Cre transgene to delete floxed Rb exon 19 at embryonic day (E) 10 in peripheral retina [2]. RbloxP/loxP;α-Cre mice were bred with strains lacking E2f1 or E2f2 in the germ line, or a strain carrying a floxed E2f3 allele [5]. RbloxP/loxP;E2f1+/− and RbloxP/loxP;E2f1+/−;α-Cre mice were bred to produce RbloxP/loxP;E2f1−/−;α-Cre mice at a frequency of 1/8 and littermate controls at the same or higher (1/4) frequency. For simplicity we will refer to the RbloxP/loxP;E2f1−/−;α-Cre peripheral retina as the Rb/E2f1 double knockout (DKO) retina. Similar strategies were employed in the case of E2f2 or E2f3. Cre-mediated excision of Rb and E2f3 alleles in the retina was confirmed by PCR as described previously [2,5].\nTo measure ectopic cell division, mice were pulse-labelled with bromodeoxyuridine (BrdU) 2 h before sacrifice and the peripheral retina analyzed for BrdU incorporation by immunofluorescence. As reported before [2,3], Rb KO retinas exhibited both spatial and temporal ectopic DNA synthesis (Figures 1C and S1A). This is easily detected at E14, E16, and postnatal day (P) 0 in the inner retina where abnormal BrdU+ ganglion and amacrine RTCs are located, or on the outermost region of the P0 retina, where BrdU+ photoreceptor RTCs reside (Figures S1A and S2, arrows) [2]. Ectopic RTC division in Rb KO retinas is even more obvious at P8 or P18, when division is completed in wild-type (WT) retina (Figures 1C and S1A). Strikingly, the ectopically positioned S-phase cells at E14, E16, and P0 and all the abnormal division at P8 and P18 were completely suppressed in the Rb/E2f1 DKO retina (Figures 1C, 1E, 1F, S1A, and S2). In contrast, deletion of E2f2 or E2f3 had no effect at any stage of development. Analysis of mitotic cells with anti–phosphohistone 3 (PH3)–specific antibodies confirmed that loss of E2f1, but not E2f2 or E2f3, suppressed ectopic division (Figure S3). Deleting one E2f1 allele partially suppressed ectopic S-phase and mitosis in Rb KO RTCs (Figures 1C, 1E, 1F, S1A, S2, and S3), suggesting that E2f1 drives ectopic division in Rb KO RTCs in a dose-dependent fashion. These data contrast with previous findings in the lens and CNS of Rb KO embryos, where deletion of any activating E2f suppresses ectopic division to some extent [6–9].\nLoss of Rb in the retina results in considerable RTC apoptosis, eliminating most bipolar and ganglion cells as well as many rods (Figure 2A–2D) [2,3]. The loss of Rb KO rods is evident from the thinner ONL, and the death of these cells as well as bipolar and ganglion neurons can be detected directly by double labelling for apoptotic and cell-type-specific markers [2] (M. P. and R. B., unpublished data). Loss of peripheral Rb KO ganglion cells is also evident from thinning of the optic nerve (D. C. and R. B., unpublished data). Deleting E2f1, but not E2f2 or E2f3, blocked this ectopic cell death in a dose-dependent fashion (Figures 1D, 1G, and S1B).\nFigure 2 E2f1 Deletion Rescues Ganglion, Rod, and Bipolar Cells in the Rb KO Retina\n(A) Horizontal retinal sections from mice of the indicated ages and genotypes were stained for nuclei (DAPI, blue) and markers that detect ganglion cells (Pou4f2, red), rods and cones (Sag [rod arrestin], green), and rod bipolar cells (Prkca, green, and Cabp5, red). Scale bars are 50 μm.\n(B) Quantification of Pou4f2+ ganglion cells.\n(C) Quantification of Prkca+ and Cabp5+ bipolar cells.\n(D) Thickness of the ONL, which represents the number of rods.\nError bars represent SD of measurements from three animals, and asterisks indicate a significant difference between retinas of WT and the indicated genotypes, unless indicated otherwise by connecting lines (*, p \u003c 0.05; **; p \u003c 0.01; ANOVA and Tukey HSD test).\n(E and F) ERGs were recorded from the indicated genotypes under dark-adapted (scotopic) conditions, and (E) intensity series and (F) b-wave amplitudes as a function of the logarithm of the flash intensity were determined. (F) Further illustrates that the relative influence of the mutations on the photoreceptors (indicated by the saturated a-wave amplitude, right graph) was not substantially different from their effect on the b-wave response (dominated by the bipolars, left graph) at the same intensity of 10 cd·s/m2. To investigate the molecular mechanism that underlies the unique role of E2f1, we assessed the expression of known E2f targets as well as other genes that regulate the cell cycle and apoptosis. Numerous positive and negative cell cycle and apoptotic regulators were up-regulated in the Rb KO retina (Figure 1H). Among the E2f family, E2f1, E2f2, E2f3a, and E2f7 were induced following Rb loss, but E2f3b, E2f4, and E2f5 were unaffected. Consistent with the BrdU and terminal dUTP nick-end labelling (TUNEL) analyses, E2f1 deletion specifically reversed all these molecular defects, but E2f3 deletion had no effect (Figure 1H).\n\nNormal Differentiation in the Rb/E2f1 DKO Retina\nBecause E2f1 deletion blocks abnormal division and death in the Rb KO retina, the Rb/E2f1 DKO retina provided a unique opportunity to evaluate whether Rb controls differentiation independent of cell cycle effects. The Rb/E2f1 DKO retina had many Sag+ (S-antigen/rod arrestin) photoreceptors, Pou4f2+ (Brn3b) ganglion cells, and numerous Prkca+/Cabp5+ bipolar neurons (Figure 2A–2D). In contrast, there was no such rescue of cell types in Rb/E2f2 or Rb/E2f3 DKO retinas (Figure S4). Analysis with general neuronal markers Mtap2 (MAP2) and Snap25, as well as other markers expressed in bipolar cells (Chx10, Rcvrn, Vsx1, Tacr3, and Atp2b1) and rod photoreceptors (Rho and Rcvrn) confirmed rescue of the Rb/E2f1 DKO retina (Table S1). Moreover, neurons exhibited the same complex morphology as in WT retina. Bipolar cell bodies were located in the INL and had ascending and descending processes ending in the OPL and IPL, respectively (Figure 2A). In addition, the Rb/E2f1 DKO retina had a healthy appearing ONL consisting of morphologically normal rods with descending processes ending in the OPL and ascending processes that terminated in inner and outer segments (Figure 2A). It was suggested that Rb might regulate photoreceptor differentiation, possibly through rod-specific transcription factors (Figure 1B) [29]. However, if Rb does regulate photoreceptor differentiation, it does so by inhibiting E2f1, not by potentiating rod differentiation factors, such as Otx2, Crx, or Nrl. It is impossible to tell whether E2f1 perturbs differentiation directly, by affecting the expression of genes that modulate maturation, and/or indirectly through its effects on proliferation and survival (Figure 1B).\nAs with ectopic division and apoptosis (Figure 1C and 1D), the rescue of Rb KO retinal bipolar, ganglion, and rod cells was dependent on E2f1 dose (Figure 2A–2D). Separate from its role in driving ectopic division of Rb KO RTCs, E2f1 also promotes normal RPC division since in its absence RPC proliferation drops ~2-fold (D. C. and R. B., unpublished data). This modest reduction of RPC numbers in the absence of E2f1 accounts for the slight reduction in the number of ganglion cells at P0, in the number of bipolar cells at P18 or P30, and in the thickness of the ONL at P18 or P30 in the E2f1 KO and Rb/E2f1 DKO retina (Figure 2B–2D). The morphology of E2f1 KO neurons was WT (Figure 2A). Despite a slight drop in absolute cell numbers, the proportion of Rb/E2f1 DKO and E2f1 KO bipolar cells was the same as WT (data not shown). Slightly reduced cell numbers were not due to residual RTC death since we have not observed ectopic apoptosis at any embryonic or postnatal stage in the developing Rb/E2f1 DKO retina (Figures 1D, 1G, and S2). Moreover, deleting Ccnd1, which acts upstream of Rb proteins, also reduces RPC number, but does not suppress any defect in the Rb KO retina (D. C. and R. B., unpublished data). Thus, slightly reduced RPC division and dramatic rescue of severe defects in Rb KO RTCs are distinct effects stemming from the deletion of E2f1.\n\nNormal Function of the Rb/E2f1 DKO Retina\nThe discovery that E2f1 loss rescues even the morphology of Rb KO neurons is surprising because Rb is thought to regulate differentiation primarily through E2f-independent pathways [30–33]. However, normal morphology may not equate to completely normal differentiation. Thus, we compared the electroretinograms (ERGs) of adult WT (α-Cre), E2f1−/−, α-Cre;RbloxP/loxP, and α-Cre;RbloxP/loxP;E2f1−/− mice. ERGs functionally assess visual signalling in the mammalian retina from photoreceptors to amacrine cells (but usually not gangion cells), and are dominated by rod and cone bipolar cells. Typically, an ERG signal begins with a negative deflection initiated by the photoreceptors (the a-wave), which is terminated by a large positive deflection due to the activation of ON bipolar cells (the b-wave).\nResponses to dim light in dark-adapted (scotopic) conditions specifically assess the rod system, and were defective in the Rb KO retina (Figure 2E). The substantial reduction of both a- and b-waves is consistent with rod and bipolar cell apoptosis [2]. The sensitivity of the residual response appeared unchanged, suggesting it arose from the Cre-negative portions of the retina. Responses were about the same in the WT and E2f1 KO retina, and, most importantly, also the Rb/E2f1 DKO response median lay at the lower end of the normal range for most intensities (Figure 2F). Thus, E2f1 deletion almost completely rescued the rod system in the Rb KO retina.\nLight-adapted (photopic) recordings to specifically assess the cone system yielded comparable results. Cones represent only 3% of photoreceptors and, unlike rods, develop without Rb, but they require rods for survival, and in the Rb KO retina, they have abnormal morphology and their synaptic targets, bipolar cells, are much depleted [2]. The photopic response, a product of cone and mainly bipolar activity, was much reduced by Rb loss, but was rescued considerably in the Rb/E2f1 DKO retina (Figure S5). Again, the median amplitude lay at the lower end of the E2f1 KO range. The photopic response in E2f1 KO mice was slightly reduced relative to WT (Figure S5B), possibly because E2f1 is required for maximal expansion of embryonic RPCs, and the E2f1 KO retina has, as noted earlier, slightly fewer cells than the WT retina, although cell type proportions are unaffected (D. C. and R. B., unpublished data). Thus, marginally subnormal photopic responses in the Rb/E2f1 DKO retina can be attributed to both a reduction of cone numbers in E2f1 KO mice alone, and a “genuine” slight reduction in cone function attributable to Rb loss relative to WT. This slight effect may relate to a true differentiation defect in a subset of amacrine cells discussed below. This discussion should not obscure the major outcome that E2f1 deletion recovers most of the ERG response. Thus, E2f1 deletion not only rescues morphology but also both rod and cone system function in the Rb KO retina.\n\nAbnormal SAC Differentiation Independent of Cell Cycle and Survival Defects\nERGs primarily assess photoreceptor and bipolar cell function, but may miss differentiation defects in other cells. To test for subtle differences we stained the Rb/E2f1 DKO retina with 43 markers (Table S1). Thirty-two proteins displayed identical patterns in WT, E2f1 KO, and Rb/E2f1 DKO retina (Table S1). The other 11 markers revealed a cell-cycle– and apoptosis-independent differentiation defect in SACs. We first studied Calb2 (calretinin), which marks a subset of amacrine and ganglion cell bodies as well as three tracks corresponding to their processes in the IPL (Figure 3A). Normal Calb2 staining was seen in the E2f1 KO IPL (data not shown). However, only one Calb2+ track was evident in the Rb KO IPL, and this defect was not rescued in the Rb/E2f1 DKO retina (Figure 3A). We quantified Calb2+ cell bodies in the Rb KO INL (corresponding to amacrine cell staining only) and observed a reduction from P8 onwards (Figures 3C and S6).\nFigure 3 Differentiation Defects in Rb KO SACs\n(A) P18 horizontal sections of WT, Rb KO, and Rb/E2f1 DKO retina were stained for nuclei (DAPI, blue), Calb2 (green), and Slc18a3 (red).\n(B) Confocal images of P30 horizontal sections of WT and Rb KO retina were stained for nuclei (DAPI, blue), Chat and Slc18a3 (both red), and Camk2a (green). In the Rb KO section, the red stain is Chat only, as Slc18a3 is missing (see [A]).\n(C) Quantification of dense Calb2+ cell bodies in the INL, total Slc18a3+ cell bodies, and Camk2a+ cell bodies in the INL. Error bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\nScale bars are 50 μm in (A) and 20 μm in (B). Of the three Calb2+ tracks in the IPL, the two outer tracks are from SACs, named after their extensive dendritic-tree-like morphology [37]. SACs are cholinergic, represent ~5.2% of amacrine neurons [38], and are critical for both direction selectivity [34,35] and spontaneous rhythmic activity that occurs during normal retinal development [36]. SACs in the INL synapse in the OFF layer of the IPL that responds to decreasing light, while displaced SACs in the GCL have processes that synapse in the nearby ON layer of the IPL that responds to increasing light (reviewed in [39]). Mature SAC processes stain specifically for Slc18a3 (vesicular acetyl choline transporter, VAChT) [37], and, significantly, this marker was absent in the peripheral Rb KO or Rb/E2f1 DKO P18 retina (Figures 3A and S7B). Chat, expressed from the same locus, is also SAC specific, but marks both cell bodies and processes of mature SACs [37]. Chat was seen in fewer cells in the mature Rb KO retina, and was present in the soma but absent from processes (Figure 3B). We obtained similar results for Sv2c, a synaptic vesicle protein found in SACs [40]; Kcnc1b and Kcnc2, potassium channels expressed on SAC soma and dendrites as well as a very small number of ganglion cells [41]; gamma-aminobutyric acid (GABA), an inhibitory neurotransmitter present in about half of amacrine cells including SACs, as well as horizontal and some bipolar neurons [37]; and Calb1 (calbindin), which is expressed in many amacrine cells and labels SAC process faintly (Figure S7A and S7B; Table S1; and data not shown). Finally, we also examined the effect of Rb deletion on SAC differentiation using a Chx10-Cre transgene that is expressed in a mosaic pattern across the retina, generating patches of Cre-expressing cells [42]. Consistent with the mosaic deletion pattern, we observed markedly reduced Chat/Slc18a3 staining in the IPL of Chx10-Cre;RbloxP/loxP retina compared to WT (Figure S7C). Together, these results suggest a role for Rb in SAC differentiation.\nThe above findings could indicate a defect in SAC specification, SAC survival, or the levels and/or transport of the markers described above. Camk2a marks both SACs and ganglion cells [37], but because ganglion cells are eliminated in the Rb KO retina, Camk2a is a specific SAC marker in this context. Importantly, Camk2a+ tracks and dendrites were present in both the WT and Rb KO retina (Figure 3B), and the number of Camk2a+ soma was similar in WT and Rb KO retina at P30 and beyond, although fewer cells stained in Rb KO retina at P18, suggesting a delay in its appearance (Figures 3C and S6B). Thus, Rb is not required for SAC survival or for process outgrowth, but rather it seems to regulate the expression and/or stability of Calb2, Calb1, Chat, Slc18a3, Sv2c, Kcnc1b, Kcnc2, and GABA in SACs, but leaves Camk2a expression virtually unaffected. The presence of Chat in some cell bodies but never in processes (Figure 3B) also suggests a transport defect. The developmental pattern of Slc18a3 expression also supported this notion. In mature WT SACs Slc18a3 is only in processes, but in early postnatal SACs, it is found in the cell body, and moves into emerging processes at approximately P4–P6. As noted above, Slc18a3 was absent at P18 in the Rb KO retina (Figure 3A); at P4 or P5 it was in cell bodies, yet was rarely present in Rb KO processes (Figures 4A and S6). Slc18a3 became virtually undetectable in Rb KO SACs by P8 (Figures 3C and S6C). These data suggest that Rb affects both the synthesis/stability and transport of SAC markers.\nFigure 4 E2f3 Loss Rescues Differentiation of Rb KO SACs\n(A) Horizontal retinal sections of the indicated ages and genotypes were stained for nuclei (DAPI, blue), mitosis marker PH3 (green), and Slc18a3 (red), which marks SAC soma at early stages and processes from ~P5 onwards. Arrows show mitotic PH3+ nuclei in Rb KO, Rb/E2f2 DKO, and Rb/E2f3 DKO retinas. E2f1 loss rescues the ectopic mitosis and cell death defects, but not the SAC defect. E2f2 loss has no effect. E2f3 loss does not rescue the ectopic mitosis and cell loss defects, but rescues the SAC defect. Inactivating E2f1 and E2f3 together rescues the ectopic mitosis, cell death, and SAC defects.\n(B) The fraction of Camk2a+ cells that are Chat + and Slc18a3+ in the P30 retina.\n(C) Horizontal P5 retinal sections were stained for nuclei (DAPI, blue), Slc18a3 (green), and Isl1 (red). Arrows show double-labelled Isl1+/Slc18a3+ cells in the inner INL.\n(D) Horizontal P0 retinal sections of the indicated genotypes were stained for nuclei (DAPI, blue), cell division marker Mki67 (green), and Isl1 (red). Arrows show double-labelled dividing SACs.\n(E) The fraction of Isl1+ cells in the inner NBL (INBL) of P0 retinas that are dividing (Mki67+).\nError bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test). Scale bars in (A), (C), and (D) are 50 μm.\n\nRb Regulates SAC Differentiation through E2f3\nRb binds more than 100 proteins [43] and in some non-neuronal cells, such as skeletal muscle, adipocytes, and bone, Rb is thought to bind and potentiate tissue-specific transcription factors that promote differentiation [31–33]. Thus, we expected that Rb might interact with retina-specific factors to facilitate SAC differentiation. A direct role for E2f in mediating Rb-dependent differentiation defects (independent of cell cycle or death defects) has to our knowledge not been described, but because E2f can regulate some differentiation genes [44–48], we first tested whether E2f2 or E2f3 might perturb Rb KO SAC maturation. At multiple time points, E2f1 deletion suppressed ectopic mitosis (PH3+ cells), but did not reverse the SAC defect, and E2f2 deletion had no effect on either defect (Figure 4A). Remarkably, although E2f3 deletion did not reverse ectopic mitosis, it rescued Calb2, Slc18a3, Chat, GABA, Kcnc1b, Kcnc2, and Sv2c staining at multiple times (Figure 4A and data not shown). Rb/E2f3 DKO SAC tracks were slightly more disordered than in WT retina, most likely because of the absence of synaptic partner cells, which are killed by E2f1. Indeed, this minor defect was rescued in the Rb/E2f1/E2f3 triple knockout retina, where bipolar and ganglion cell death was rescued and SAC differentiation was restored (Figure 4A). E2f3 deletion alone did not affect SAC differentiation (Figure 4A); thus, it is unleashed E2f3 activity that is detrimental, and the critical role for Rb is to inhibit E2f3.\nWe quantified the fraction of Camk2a+ SACs in different genotypes and found that 60% of WT P30 Camk2a+ cells expressed Chat and Slc18a3, which dropped to only 5.6% in the Rb KO retina, and remained low at 3.7% in the Rb/E2f1 DKO retina, but rose to 91% in the Rb/E2f3 DKO retina (Figure 4B). The latter fraction is higher than WT because ganglion cells, which normally make up ~40% of Camk2a+ cells, are killed by apoptosis.\nTo quantify the effect of different E2fs on ectopic division specifically in SACs, we exploited Isl1 (Islet1). This marker is expressed in both SACs and ganglion cells, thus Isl1+ cells in the INL are exclusively SACs [49]. We found that 98.2% ± 1.8% of Isl1+ cells in the forming inner INL at P5 were also Slc18a3+, confirming that Isl1 is an excellent SAC marker (Figure 4C). Moreover, Isl1, unlike Slc18a3, is nuclear, which facilitates scoring of Isl1+/Mki67+ cells. It is also expressed earlier than Slc18a3, permitting analysis of SACs soon after their birth at ~E15; thus, we could study retina at P0, a time when ectopic division is high in the inner retina and prior to Rb-independent cell cycle exit associated with terminal differentiation [2]. At P0, no WT Isl1+ cells in the inner neuroblastic layer (NBL) (which is the future INL) were dividing, but 57 ± 14 Isl1+/Mki67+ cells were detected in the Rb KO inner NBL (Figure 4D). Indeed, about one-third of all Isl1+ cells in the entire inner NBL were dividing in the Rb KO retina, or ~50% in the periphery where Cre is expressed (Figure 4E and data not shown). This defect was suppressed in the Rb/E2f1 DKO retina, where we detected only 1 ± 1 dividing SAC, but not the Rb/E2f3 DKO retina, where there were 53 ± 8 dividing SACs (Figure 4D and 4E). We observed similar effects at P0 with Calb2, which marks newborn SACs and other amacrine cells (data not shown). Thus, in Rb KO SACs, E2f1 deletion suppresses ectopic division but not aberrant differentiation, whereas E2f3 deletion suppresses aberrant differentiation but not ectopic division.\n\nSpecific Expression of E2f3 in SACs and Other Subsets of CNS Neurons\nThe unique effect of E2f3 in disrupting the differentiation of SACs but not other retinal neurons might be due to cell-type-specific expression or cell-type-specific activity of E2f3. Determining between these two possibilities is not easy, as E2f immunostaining in mouse tissues is problematic. We did not solve this issue for E2f1 or E2f2, but used a modified protocol [50] to successfully track E2f3 expression (Figure 5). At P0, E2f3 was detected in RPCs, consistent with a putative role in normal proliferation (Figure 5A). The signal was specific as it was absent in the E2f3 KO peripheral retina (Figure 5A). As the retina differentiated and RPC division diminished, the number of E2f3+ cells also dropped, and by P8, when division is virtually over, only a subset of post-mitotic cells in the inner retina expressed E2f3 (Figure 5A). By P18, E2f3 was also detected in two tracks in the IPL (Figure 5A and 5B), reminiscent of SAC markers such as Chat and Slc18a3 (c.f. Figures 3 and 4). This cytoplasmic E2f3 staining was also specific, as it was absent in the E2f3 KO peripheral retina of α-Cre;E2f3loxP/loxP mice (Figure 5A). Indeed, double labelling with E2f3 (red) and Chat plus Slc18a3 (green) confirmed that E2f3 is present in both SAC soma and dendrites (Figure 5B). Rb protein was also detected in the inner retina (Figure 5A), and showed a similar distribution as E2f3 in SACs (Figure 5B), and was also present in mature ganglion cells and Müller cells as reported [51]. Rb staining in SAC processes was specific as it was absent in the peripheral retina of αCre;RbloxP/loxP mice (Figure 5A). These data suggest that Rb and E2f3 colocalize in SACs and that E2f3 triggers defects in SAC differentiation because it is specifically expressed in these retinal neurons.\nFigure 5 E2f3 and Rb Expression in SACs\n(A) Left panels: horizontal P0, P8, and P18 retinal sections of the indicated genotypes were stained for E2f3 (red) and DAPI (blue). The arrow indicates the junction between the E2f3 null peripheral and WT central P0 retina. Note the absence of E2f3 protein in the peripheral E2f3 KO RPCs at P0 and in peripheral inner retinal neurons at P18. Far right panel: P18 retinal sections of the indicated genotypes were stained for Rb (red) and DAPI (blue). Note the absence of Rb protein in the peripheral Rb KO inner retinal neurons.\n(B) WT P18 retinal sections were stained for nuclei (DAPI, blue), E2f3 (red) or Rb (red), and Chat plus Slc18a3 (green). Arrows indicate double-labelled soma. Note that the IPL processes are also double-labelled.\nScale bars are 50 μm. We also found that E2f3 is present in a specific subset of mature neurons in various brain regions (data not shown). For example, in the P20 amygdala, E2f3 colocalized with the general neuronal markers Mtap2 and Mecp2 [52], but not with Calb2, which marks a subset of neurons, or with the glial marker Gfap (data not shown). Unlike in retinal SACs, E2f3 was not coexpressed in Chat+ or Slc18a3+ cholinergic neurons located in various regions of the brain and spinal cord (data not shown). In agreement, we could not detect defects in cholinergic Rb KO neurons in the developing forebrain, but other Rb KO neurons in this region showed differentiation defects that were rescued by deleting E2f3 [53]. Together, these results suggest that the common mechanism by which Rb promotes neural differentiation is through E2f3 inhibition.\n\nDistinct Localization of E2f3 Isoforms\nAs noted above, E2f3 and Rb staining in SACs was both nuclear and cytoplasmic (Figure 5A and 5B). The antibody that worked in immunostaining recognizes a C-terminal region and thus, does not distinguish a/b isoforms. To our knowledge, the subcellular location of E2f3 isoforms has not been determined in any cell type. To verify the dual locations of E2f3 and to determine which isoforms were present in retina, we analyzed nuclear and cytoplasmic fractions by Western blot at different times during development. Analysis with the pan-E2f3 antibody (sc-878, Santa Cruz Biotechnology) detected a 55-kD E2f3a species and a 40-kD E2f3b polypeptide (Figure 6). To confirm that the upper species in our retinal lysates was E2f3a, we exploited novel mice that lack E2f3 exon 1a and thus express E2f3b exclusively (R. O. and G. L., unpublished data). The genotyping strategy is discussed in detail later and is outlined in Figure 7A. Western analysis confirmed that the upper band was absent in E2f3a−/− mice (Figures 6 and S8). Consistent with the drop in E2f3-expressing cells during WT retinal maturation (Figure 5A), the total amount of E2f3a was less at P18 compared to P0 (Figure 6). E2f3b was present in similar amounts at both time points. At P0 and P18, E2f3a was present in both nuclear and cytoplasmic fractions, but in marked contrast, E2f3b was exclusively nuclear at both times (Figure 6). Two closely migrating E2f3a bands were detected, more clearly evident at P18, of which the faster migrating species was dominant in nuclear and the slower species was dominant in cytoplasm (Figure 6). The identity of both as E2f3a species was confirmed by their absence in the P18 E2f3a KO retina (Figure S8). Analysis of Pou4f2, a nuclear transcription factor expressed in ganglion cells, showed that nuclear proteins had not contaminated the cytoplasmic fraction, and analysis of Slc18a3, a cytoplasmic SAC marker, confirmed that the reverse had also not occurred (Figure 6). These data show, to our knowledge for the first time, that E2f3a and E2f3b exhibit distinct patterns of subcellular distribution, and raise the possibility that E2f3a localization may be regulated by as yet unknown post-translational modifications.\nFigure 6 Subcellular Distribution of E2f3 Isoforms and Other Cell Cycle Proteins in the Developing Retina\nNuclear and cytoplasmic extracts from an equivalent number of retinal cells from mice of the indicated genotypes and ages were analyzed by Western blotting to detect the indicated proteins. Lysate from E2f3a−/− mice was used as a control to confirm the location of E2f3a protein. C, cytoplasmic extracts; N, nuclear extracts.\nFigure 7 The E2f3a Isoform Drives the Differentiation Defect in Rb KO SACs\n(A) Schematic diagrams of the mouse WT, E2f3a−/−, and the Cre-recombined floxed E2f3 loci (indicated here as E2f3−/− for simplicity). E2f3a−/− mice lack most of E2f3 exon 1a and part of intron 1a (red dotted box). Arrows indicate PCR primers. Genotyping of an E2f3a+/− mouse is shown on the right.\n(B) RT-PCR detection of E2f3a and E2f3b mRNA in the retina. The sequences of primers are 1aF (5′-GCCTCTACACCACGCCACAAG-3′), 1bF (5′-CGGAAATGCCCTTACAGC-3′), and 4R (5′-CTCAGTCACTTCTTTGGACAG-3′). WT retina expresses both E2f3a and E2f3b mRNA. As expected, E2f3a−/− retina lacks E2f3a mRNA and still expresses E2f3b mRNA. E2f3−/− retina lacks full-length E2f3a and E2f3b mRNAs, and instead expresses a truncated mRNA lacking exon 3.\n(C) Real-time RT-PCR analysis of E2f genes in P8 retinas of the indicated genotypes. Error bars represent SD of measurements from three animals, and asterisks indicate a significant difference between WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\n(D) Rescue of Rb KO SACs by E2f3a deletion. Horizontal retinal sections of the indicated genotypes and ages were stained for nuclei (DAPI, blue), M-phase (PH3, green), and the SAC marker Slc18a3 (red). E2f3a deletion does not suppress ectopic division, but rescues the SAC defect. Scale bars are 50 μm.\nM, molecular size marker. We also examined the distribution of other cell cycle regulators during retinal development. Like E2f3a, Rb was present in both the WT cytoplasm and nucleus at P0, but at P18, when the levels of Rb had increased, it was primarily nuclear (Figure 6). A very faint cytoplasmic Rb signal was evident at P18, which is consistent with Rb staining of SAC processes (Figure 5B), and with the very small proportion of SACs in the retina [38]. E2f1 was also detected in both nuclear and cytoplasmic fractions, although unlike E2f3a it was predominantly nuclear both at P0 and P18 (Figure 6). The E2f dimerization partner, Tfdp1, which lacks a nuclear localization signal [54], was primarily cytoplasmic at both P0 and P18, and the Cdk inhibitors Cdkn1a and Cdkn1b showed a similar pattern of distribution (Figure 6). Thus, among the cell cycle regulators we examined, most showed bivalent distribution, and E2f3b was unusual in its solely nuclear compartmentalization.\n\nRb Regulates SAC Differentiation through E2f3a\nTo test which E2f3 isoform is responsible for aberrant Rb KO SAC differentiation we exploited E2f3a−/− mice (Figure 7A). The genotyping strategy outlined in Figure 7A was used to distinguish the E2f3a, WT, and null alleles. Reverse transcriptase PCR (RT-PCR) confirmed the presence of both E2f3a and E2f3b RNA species in the developing WT retina, and the specific absence of E2f3a RNA in the E2f3a−/− retina (Figure 7B). E2f3a protein was absent in E2f3a−/− retinal lysate (Figures 6 and S8). Importantly, the levels of E2f3b message were similar in the Rb KO and Rb/E2f3a DKO retina, ruling out the possibility that any effects of E2f3a deletion we might observe were due to down-regulation of E2f3b (Figure 7C). Also, the levels of other E2fs were the same in the Rb KO, Rb/E2f3 DKO, and Rb/E2f3a DKO retina, ruling out any cross-regulatory effects (Figure 7C) [55]. E2f3a can trigger cell cycle induction, but because SAC defects are not linked to cell cycle perturbation (Figures 3A and 4), and in view of the predominant association between E2f3b and Rb in quiescent cells [16,19], we suspected that E2f3b may perturb differentiation in Rb KO SACs. Unexpectedly, however, E2f3a deletion suppressed the Rb KO SAC defect (Figure 7D). Thus, separate from its role in cell cycle control, Rb regulation of E2f3a is critical to ensure proper neuronal differentiation."}

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Regulates Division and Death through E2f1\nWe used the α-Cre transgene to delete floxed Rb exon 19 at embryonic day (E) 10 in peripheral retina [2]. RbloxP/loxP;α-Cre mice were bred with strains lacking E2f1 or E2f2 in the germ line, or a strain carrying a floxed E2f3 allele [5]. RbloxP/loxP;E2f1+/− and RbloxP/loxP;E2f1+/−;α-Cre mice were bred to produce RbloxP/loxP;E2f1−/−;α-Cre mice at a frequency of 1/8 and littermate controls at the same or higher (1/4) frequency. For simplicity we will refer to the RbloxP/loxP;E2f1−/−;α-Cre peripheral retina as the Rb/E2f1 double knockout (DKO) retina. Similar strategies were employed in the case of E2f2 or E2f3. Cre-mediated excision of Rb and E2f3 alleles in the retina was confirmed by PCR as described previously [2,5].\nTo measure ectopic cell division, mice were pulse-labelled with bromodeoxyuridine (BrdU) 2 h before sacrifice and the peripheral retina analyzed for BrdU incorporation by immunofluorescence. As reported before [2,3], Rb KO retinas exhibited both spatial and temporal ectopic DNA synthesis (Figures 1C and S1A). This is easily detected at E14, E16, and postnatal day (P) 0 in the inner retina where abnormal BrdU+ ganglion and amacrine RTCs are located, or on the outermost region of the P0 retina, where BrdU+ photoreceptor RTCs reside (Figures S1A and S2, arrows) [2]. Ectopic RTC division in Rb KO retinas is even more obvious at P8 or P18, when division is completed in wild-type (WT) retina (Figures 1C and S1A). Strikingly, the ectopically positioned S-phase cells at E14, E16, and P0 and all the abnormal division at P8 and P18 were completely suppressed in the Rb/E2f1 DKO retina (Figures 1C, 1E, 1F, S1A, and S2). In contrast, deletion of E2f2 or E2f3 had no effect at any stage of development. Analysis of mitotic cells with anti–phosphohistone 3 (PH3)–specific antibodies confirmed that loss of E2f1, but not E2f2 or E2f3, suppressed ectopic division (Figure S3). Deleting one E2f1 allele partially suppressed ectopic S-phase and mitosis in Rb KO RTCs (Figures 1C, 1E, 1F, S1A, S2, and S3), suggesting that E2f1 drives ectopic division in Rb KO RTCs in a dose-dependent fashion. These data contrast with previous findings in the lens and CNS of Rb KO embryos, where deletion of any activating E2f suppresses ectopic division to some extent [6–9].\nLoss of Rb in the retina results in considerable RTC apoptosis, eliminating most bipolar and ganglion cells as well as many rods (Figure 2A–2D) [2,3]. The loss of Rb KO rods is evident from the thinner ONL, and the death of these cells as well as bipolar and ganglion neurons can be detected directly by double labelling for apoptotic and cell-type-specific markers [2] (M. P. and R. B., unpublished data). Loss of peripheral Rb KO ganglion cells is also evident from thinning of the optic nerve (D. C. and R. B., unpublished data). Deleting E2f1, but not E2f2 or E2f3, blocked this ectopic cell death in a dose-dependent fashion (Figures 1D, 1G, and S1B).\nFigure 2 E2f1 Deletion Rescues Ganglion, Rod, and Bipolar Cells in the Rb KO Retina\n(A) Horizontal retinal sections from mice of the indicated ages and genotypes were stained for nuclei (DAPI, blue) and markers that detect ganglion cells (Pou4f2, red), rods and cones (Sag [rod arrestin], green), and rod bipolar cells (Prkca, green, and Cabp5, red). Scale bars are 50 μm.\n(B) Quantification of Pou4f2+ ganglion cells.\n(C) Quantification of Prkca+ and Cabp5+ bipolar cells.\n(D) Thickness of the ONL, which represents the number of rods.\nError bars represent SD of measurements from three animals, and asterisks indicate a significant difference between retinas of WT and the indicated genotypes, unless indicated otherwise by connecting lines (*, p \u003c 0.05; **; p \u003c 0.01; ANOVA and Tukey HSD test).\n(E and F) ERGs were recorded from the indicated genotypes under dark-adapted (scotopic) conditions, and (E) intensity series and (F) b-wave amplitudes as a function of the logarithm of the flash intensity were determined. (F) Further illustrates that the relative influence of the mutations on the photoreceptors (indicated by the saturated a-wave amplitude, right graph) was not substantially different from their effect on the b-wave response (dominated by the bipolars, left graph) at the same intensity of 10 cd·s/m2. To investigate the molecular mechanism that underlies the unique role of E2f1, we assessed the expression of known E2f targets as well as other genes that regulate the cell cycle and apoptosis. Numerous positive and negative cell cycle and apoptotic regulators were up-regulated in the Rb KO retina (Figure 1H). Among the E2f family, E2f1, E2f2, E2f3a, and E2f7 were induced following Rb loss, but E2f3b, E2f4, and E2f5 were unaffected. Consistent with the BrdU and terminal dUTP nick-end labelling (TUNEL) analyses, E2f1 deletion specifically reversed all these molecular defects, but E2f3 deletion had no effect (Figure 1H).\n\nNormal Differentiation in the Rb/E2f1 DKO Retina\nBecause E2f1 deletion blocks abnormal division and death in the Rb KO retina, the Rb/E2f1 DKO retina provided a unique opportunity to evaluate whether Rb controls differentiation independent of cell cycle effects. The Rb/E2f1 DKO retina had many Sag+ (S-antigen/rod arrestin) photoreceptors, Pou4f2+ (Brn3b) ganglion cells, and numerous Prkca+/Cabp5+ bipolar neurons (Figure 2A–2D). In contrast, there was no such rescue of cell types in Rb/E2f2 or Rb/E2f3 DKO retinas (Figure S4). Analysis with general neuronal markers Mtap2 (MAP2) and Snap25, as well as other markers expressed in bipolar cells (Chx10, Rcvrn, Vsx1, Tacr3, and Atp2b1) and rod photoreceptors (Rho and Rcvrn) confirmed rescue of the Rb/E2f1 DKO retina (Table S1). Moreover, neurons exhibited the same complex morphology as in WT retina. Bipolar cell bodies were located in the INL and had ascending and descending processes ending in the OPL and IPL, respectively (Figure 2A). In addition, the Rb/E2f1 DKO retina had a healthy appearing ONL consisting of morphologically normal rods with descending processes ending in the OPL and ascending processes that terminated in inner and outer segments (Figure 2A). It was suggested that Rb might regulate photoreceptor differentiation, possibly through rod-specific transcription factors (Figure 1B) [29]. However, if Rb does regulate photoreceptor differentiation, it does so by inhibiting E2f1, not by potentiating rod differentiation factors, such as Otx2, Crx, or Nrl. It is impossible to tell whether E2f1 perturbs differentiation directly, by affecting the expression of genes that modulate maturation, and/or indirectly through its effects on proliferation and survival (Figure 1B).\nAs with ectopic division and apoptosis (Figure 1C and 1D), the rescue of Rb KO retinal bipolar, ganglion, and rod cells was dependent on E2f1 dose (Figure 2A–2D). Separate from its role in driving ectopic division of Rb KO RTCs, E2f1 also promotes normal RPC division since in its absence RPC proliferation drops ~2-fold (D. C. and R. B., unpublished data). This modest reduction of RPC numbers in the absence of E2f1 accounts for the slight reduction in the number of ganglion cells at P0, in the number of bipolar cells at P18 or P30, and in the thickness of the ONL at P18 or P30 in the E2f1 KO and Rb/E2f1 DKO retina (Figure 2B–2D). The morphology of E2f1 KO neurons was WT (Figure 2A). Despite a slight drop in absolute cell numbers, the proportion of Rb/E2f1 DKO and E2f1 KO bipolar cells was the same as WT (data not shown). Slightly reduced cell numbers were not due to residual RTC death since we have not observed ectopic apoptosis at any embryonic or postnatal stage in the developing Rb/E2f1 DKO retina (Figures 1D, 1G, and S2). Moreover, deleting Ccnd1, which acts upstream of Rb proteins, also reduces RPC number, but does not suppress any defect in the Rb KO retina (D. C. and R. B., unpublished data). Thus, slightly reduced RPC division and dramatic rescue of severe defects in Rb KO RTCs are distinct effects stemming from the deletion of E2f1.\n\nNormal Function of the Rb/E2f1 DKO Retina\nThe discovery that E2f1 loss rescues even the morphology of Rb KO neurons is surprising because Rb is thought to regulate differentiation primarily through E2f-independent pathways [30–33]. However, normal morphology may not equate to completely normal differentiation. Thus, we compared the electroretinograms (ERGs) of adult WT (α-Cre), E2f1−/−, α-Cre;RbloxP/loxP, and α-Cre;RbloxP/loxP;E2f1−/− mice. ERGs functionally assess visual signalling in the mammalian retina from photoreceptors to amacrine cells (but usually not gangion cells), and are dominated by rod and cone bipolar cells. Typically, an ERG signal begins with a negative deflection initiated by the photoreceptors (the a-wave), which is terminated by a large positive deflection due to the activation of ON bipolar cells (the b-wave).\nResponses to dim light in dark-adapted (scotopic) conditions specifically assess the rod system, and were defective in the Rb KO retina (Figure 2E). The substantial reduction of both a- and b-waves is consistent with rod and bipolar cell apoptosis [2]. The sensitivity of the residual response appeared unchanged, suggesting it arose from the Cre-negative portions of the retina. Responses were about the same in the WT and E2f1 KO retina, and, most importantly, also the Rb/E2f1 DKO response median lay at the lower end of the normal range for most intensities (Figure 2F). Thus, E2f1 deletion almost completely rescued the rod system in the Rb KO retina.\nLight-adapted (photopic) recordings to specifically assess the cone system yielded comparable results. Cones represent only 3% of photoreceptors and, unlike rods, develop without Rb, but they require rods for survival, and in the Rb KO retina, they have abnormal morphology and their synaptic targets, bipolar cells, are much depleted [2]. The photopic response, a product of cone and mainly bipolar activity, was much reduced by Rb loss, but was rescued considerably in the Rb/E2f1 DKO retina (Figure S5). Again, the median amplitude lay at the lower end of the E2f1 KO range. The photopic response in E2f1 KO mice was slightly reduced relative to WT (Figure S5B), possibly because E2f1 is required for maximal expansion of embryonic RPCs, and the E2f1 KO retina has, as noted earlier, slightly fewer cells than the WT retina, although cell type proportions are unaffected (D. C. and R. B., unpublished data). Thus, marginally subnormal photopic responses in the Rb/E2f1 DKO retina can be attributed to both a reduction of cone numbers in E2f1 KO mice alone, and a “genuine” slight reduction in cone function attributable to Rb loss relative to WT. This slight effect may relate to a true differentiation defect in a subset of amacrine cells discussed below. This discussion should not obscure the major outcome that E2f1 deletion recovers most of the ERG response. Thus, E2f1 deletion not only rescues morphology but also both rod and cone system function in the Rb KO retina.\n\nAbnormal SAC Differentiation Independent of Cell Cycle and Survival Defects\nERGs primarily assess photoreceptor and bipolar cell function, but may miss differentiation defects in other cells. To test for subtle differences we stained the Rb/E2f1 DKO retina with 43 markers (Table S1). Thirty-two proteins displayed identical patterns in WT, E2f1 KO, and Rb/E2f1 DKO retina (Table S1). The other 11 markers revealed a cell-cycle– and apoptosis-independent differentiation defect in SACs. We first studied Calb2 (calretinin), which marks a subset of amacrine and ganglion cell bodies as well as three tracks corresponding to their processes in the IPL (Figure 3A). Normal Calb2 staining was seen in the E2f1 KO IPL (data not shown). However, only one Calb2+ track was evident in the Rb KO IPL, and this defect was not rescued in the Rb/E2f1 DKO retina (Figure 3A). We quantified Calb2+ cell bodies in the Rb KO INL (corresponding to amacrine cell staining only) and observed a reduction from P8 onwards (Figures 3C and S6).\nFigure 3 Differentiation Defects in Rb KO SACs\n(A) P18 horizontal sections of WT, Rb KO, and Rb/E2f1 DKO retina were stained for nuclei (DAPI, blue), Calb2 (green), and Slc18a3 (red).\n(B) Confocal images of P30 horizontal sections of WT and Rb KO retina were stained for nuclei (DAPI, blue), Chat and Slc18a3 (both red), and Camk2a (green). In the Rb KO section, the red stain is Chat only, as Slc18a3 is missing (see [A]).\n(C) Quantification of dense Calb2+ cell bodies in the INL, total Slc18a3+ cell bodies, and Camk2a+ cell bodies in the INL. Error bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\nScale bars are 50 μm in (A) and 20 μm in (B). Of the three Calb2+ tracks in the IPL, the two outer tracks are from SACs, named after their extensive dendritic-tree-like morphology [37]. SACs are cholinergic, represent ~5.2% of amacrine neurons [38], and are critical for both direction selectivity [34,35] and spontaneous rhythmic activity that occurs during normal retinal development [36]. SACs in the INL synapse in the OFF layer of the IPL that responds to decreasing light, while displaced SACs in the GCL have processes that synapse in the nearby ON layer of the IPL that responds to increasing light (reviewed in [39]). Mature SAC processes stain specifically for Slc18a3 (vesicular acetyl choline transporter, VAChT) [37], and, significantly, this marker was absent in the peripheral Rb KO or Rb/E2f1 DKO P18 retina (Figures 3A and S7B). Chat, expressed from the same locus, is also SAC specific, but marks both cell bodies and processes of mature SACs [37]. Chat was seen in fewer cells in the mature Rb KO retina, and was present in the soma but absent from processes (Figure 3B). We obtained similar results for Sv2c, a synaptic vesicle protein found in SACs [40]; Kcnc1b and Kcnc2, potassium channels expressed on SAC soma and dendrites as well as a very small number of ganglion cells [41]; gamma-aminobutyric acid (GABA), an inhibitory neurotransmitter present in about half of amacrine cells including SACs, as well as horizontal and some bipolar neurons [37]; and Calb1 (calbindin), which is expressed in many amacrine cells and labels SAC process faintly (Figure S7A and S7B; Table S1; and data not shown). Finally, we also examined the effect of Rb deletion on SAC differentiation using a Chx10-Cre transgene that is expressed in a mosaic pattern across the retina, generating patches of Cre-expressing cells [42]. Consistent with the mosaic deletion pattern, we observed markedly reduced Chat/Slc18a3 staining in the IPL of Chx10-Cre;RbloxP/loxP retina compared to WT (Figure S7C). Together, these results suggest a role for Rb in SAC differentiation.\nThe above findings could indicate a defect in SAC specification, SAC survival, or the levels and/or transport of the markers described above. Camk2a marks both SACs and ganglion cells [37], but because ganglion cells are eliminated in the Rb KO retina, Camk2a is a specific SAC marker in this context. Importantly, Camk2a+ tracks and dendrites were present in both the WT and Rb KO retina (Figure 3B), and the number of Camk2a+ soma was similar in WT and Rb KO retina at P30 and beyond, although fewer cells stained in Rb KO retina at P18, suggesting a delay in its appearance (Figures 3C and S6B). Thus, Rb is not required for SAC survival or for process outgrowth, but rather it seems to regulate the expression and/or stability of Calb2, Calb1, Chat, Slc18a3, Sv2c, Kcnc1b, Kcnc2, and GABA in SACs, but leaves Camk2a expression virtually unaffected. The presence of Chat in some cell bodies but never in processes (Figure 3B) also suggests a transport defect. The developmental pattern of Slc18a3 expression also supported this notion. In mature WT SACs Slc18a3 is only in processes, but in early postnatal SACs, it is found in the cell body, and moves into emerging processes at approximately P4–P6. As noted above, Slc18a3 was absent at P18 in the Rb KO retina (Figure 3A); at P4 or P5 it was in cell bodies, yet was rarely present in Rb KO processes (Figures 4A and S6). Slc18a3 became virtually undetectable in Rb KO SACs by P8 (Figures 3C and S6C). These data suggest that Rb affects both the synthesis/stability and transport of SAC markers.\nFigure 4 E2f3 Loss Rescues Differentiation of Rb KO SACs\n(A) Horizontal retinal sections of the indicated ages and genotypes were stained for nuclei (DAPI, blue), mitosis marker PH3 (green), and Slc18a3 (red), which marks SAC soma at early stages and processes from ~P5 onwards. Arrows show mitotic PH3+ nuclei in Rb KO, Rb/E2f2 DKO, and Rb/E2f3 DKO retinas. E2f1 loss rescues the ectopic mitosis and cell death defects, but not the SAC defect. E2f2 loss has no effect. E2f3 loss does not rescue the ectopic mitosis and cell loss defects, but rescues the SAC defect. Inactivating E2f1 and E2f3 together rescues the ectopic mitosis, cell death, and SAC defects.\n(B) The fraction of Camk2a+ cells that are Chat + and Slc18a3+ in the P30 retina.\n(C) Horizontal P5 retinal sections were stained for nuclei (DAPI, blue), Slc18a3 (green), and Isl1 (red). Arrows show double-labelled Isl1+/Slc18a3+ cells in the inner INL.\n(D) Horizontal P0 retinal sections of the indicated genotypes were stained for nuclei (DAPI, blue), cell division marker Mki67 (green), and Isl1 (red). Arrows show double-labelled dividing SACs.\n(E) The fraction of Isl1+ cells in the inner NBL (INBL) of P0 retinas that are dividing (Mki67+).\nError bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test). Scale bars in (A), (C), and (D) are 50 μm.\n\nRb Regulates SAC Differentiation through E2f3\nRb binds more than 100 proteins [43] and in some non-neuronal cells, such as skeletal muscle, adipocytes, and bone, Rb is thought to bind and potentiate tissue-specific transcription factors that promote differentiation [31–33]. Thus, we expected that Rb might interact with retina-specific factors to facilitate SAC differentiation. A direct role for E2f in mediating Rb-dependent differentiation defects (independent of cell cycle or death defects) has to our knowledge not been described, but because E2f can regulate some differentiation genes [44–48], we first tested whether E2f2 or E2f3 might perturb Rb KO SAC maturation. At multiple time points, E2f1 deletion suppressed ectopic mitosis (PH3+ cells), but did not reverse the SAC defect, and E2f2 deletion had no effect on either defect (Figure 4A). Remarkably, although E2f3 deletion did not reverse ectopic mitosis, it rescued Calb2, Slc18a3, Chat, GABA, Kcnc1b, Kcnc2, and Sv2c staining at multiple times (Figure 4A and data not shown). Rb/E2f3 DKO SAC tracks were slightly more disordered than in WT retina, most likely because of the absence of synaptic partner cells, which are killed by E2f1. Indeed, this minor defect was rescued in the Rb/E2f1/E2f3 triple knockout retina, where bipolar and ganglion cell death was rescued and SAC differentiation was restored (Figure 4A). E2f3 deletion alone did not affect SAC differentiation (Figure 4A); thus, it is unleashed E2f3 activity that is detrimental, and the critical role for Rb is to inhibit E2f3.\nWe quantified the fraction of Camk2a+ SACs in different genotypes and found that 60% of WT P30 Camk2a+ cells expressed Chat and Slc18a3, which dropped to only 5.6% in the Rb KO retina, and remained low at 3.7% in the Rb/E2f1 DKO retina, but rose to 91% in the Rb/E2f3 DKO retina (Figure 4B). The latter fraction is higher than WT because ganglion cells, which normally make up ~40% of Camk2a+ cells, are killed by apoptosis.\nTo quantify the effect of different E2fs on ectopic division specifically in SACs, we exploited Isl1 (Islet1). This marker is expressed in both SACs and ganglion cells, thus Isl1+ cells in the INL are exclusively SACs [49]. We found that 98.2% ± 1.8% of Isl1+ cells in the forming inner INL at P5 were also Slc18a3+, confirming that Isl1 is an excellent SAC marker (Figure 4C). Moreover, Isl1, unlike Slc18a3, is nuclear, which facilitates scoring of Isl1+/Mki67+ cells. It is also expressed earlier than Slc18a3, permitting analysis of SACs soon after their birth at ~E15; thus, we could study retina at P0, a time when ectopic division is high in the inner retina and prior to Rb-independent cell cycle exit associated with terminal differentiation [2]. At P0, no WT Isl1+ cells in the inner neuroblastic layer (NBL) (which is the future INL) were dividing, but 57 ± 14 Isl1+/Mki67+ cells were detected in the Rb KO inner NBL (Figure 4D). Indeed, about one-third of all Isl1+ cells in the entire inner NBL were dividing in the Rb KO retina, or ~50% in the periphery where Cre is expressed (Figure 4E and data not shown). This defect was suppressed in the Rb/E2f1 DKO retina, where we detected only 1 ± 1 dividing SAC, but not the Rb/E2f3 DKO retina, where there were 53 ± 8 dividing SACs (Figure 4D and 4E). We observed similar effects at P0 with Calb2, which marks newborn SACs and other amacrine cells (data not shown). Thus, in Rb KO SACs, E2f1 deletion suppresses ectopic division but not aberrant differentiation, whereas E2f3 deletion suppresses aberrant differentiation but not ectopic division.\n\nSpecific Expression of E2f3 in SACs and Other Subsets of CNS Neurons\nThe unique effect of E2f3 in disrupting the differentiation of SACs but not other retinal neurons might be due to cell-type-specific expression or cell-type-specific activity of E2f3. Determining between these two possibilities is not easy, as E2f immunostaining in mouse tissues is problematic. We did not solve this issue for E2f1 or E2f2, but used a modified protocol [50] to successfully track E2f3 expression (Figure 5). At P0, E2f3 was detected in RPCs, consistent with a putative role in normal proliferation (Figure 5A). The signal was specific as it was absent in the E2f3 KO peripheral retina (Figure 5A). As the retina differentiated and RPC division diminished, the number of E2f3+ cells also dropped, and by P8, when division is virtually over, only a subset of post-mitotic cells in the inner retina expressed E2f3 (Figure 5A). By P18, E2f3 was also detected in two tracks in the IPL (Figure 5A and 5B), reminiscent of SAC markers such as Chat and Slc18a3 (c.f. Figures 3 and 4). This cytoplasmic E2f3 staining was also specific, as it was absent in the E2f3 KO peripheral retina of α-Cre;E2f3loxP/loxP mice (Figure 5A). Indeed, double labelling with E2f3 (red) and Chat plus Slc18a3 (green) confirmed that E2f3 is present in both SAC soma and dendrites (Figure 5B). Rb protein was also detected in the inner retina (Figure 5A), and showed a similar distribution as E2f3 in SACs (Figure 5B), and was also present in mature ganglion cells and Müller cells as reported [51]. Rb staining in SAC processes was specific as it was absent in the peripheral retina of αCre;RbloxP/loxP mice (Figure 5A). These data suggest that Rb and E2f3 colocalize in SACs and that E2f3 triggers defects in SAC differentiation because it is specifically expressed in these retinal neurons.\nFigure 5 E2f3 and Rb Expression in SACs\n(A) Left panels: horizontal P0, P8, and P18 retinal sections of the indicated genotypes were stained for E2f3 (red) and DAPI (blue). The arrow indicates the junction between the E2f3 null peripheral and WT central P0 retina. Note the absence of E2f3 protein in the peripheral E2f3 KO RPCs at P0 and in peripheral inner retinal neurons at P18. Far right panel: P18 retinal sections of the indicated genotypes were stained for Rb (red) and DAPI (blue). Note the absence of Rb protein in the peripheral Rb KO inner retinal neurons.\n(B) WT P18 retinal sections were stained for nuclei (DAPI, blue), E2f3 (red) or Rb (red), and Chat plus Slc18a3 (green). Arrows indicate double-labelled soma. Note that the IPL processes are also double-labelled.\nScale bars are 50 μm. We also found that E2f3 is present in a specific subset of mature neurons in various brain regions (data not shown). For example, in the P20 amygdala, E2f3 colocalized with the general neuronal markers Mtap2 and Mecp2 [52], but not with Calb2, which marks a subset of neurons, or with the glial marker Gfap (data not shown). Unlike in retinal SACs, E2f3 was not coexpressed in Chat+ or Slc18a3+ cholinergic neurons located in various regions of the brain and spinal cord (data not shown). In agreement, we could not detect defects in cholinergic Rb KO neurons in the developing forebrain, but other Rb KO neurons in this region showed differentiation defects that were rescued by deleting E2f3 [53]. Together, these results suggest that the common mechanism by which Rb promotes neural differentiation is through E2f3 inhibition.\n\nDistinct Localization of E2f3 Isoforms\nAs noted above, E2f3 and Rb staining in SACs was both nuclear and cytoplasmic (Figure 5A and 5B). The antibody that worked in immunostaining recognizes a C-terminal region and thus, does not distinguish a/b isoforms. To our knowledge, the subcellular location of E2f3 isoforms has not been determined in any cell type. To verify the dual locations of E2f3 and to determine which isoforms were present in retina, we analyzed nuclear and cytoplasmic fractions by Western blot at different times during development. Analysis with the pan-E2f3 antibody (sc-878, Santa Cruz Biotechnology) detected a 55-kD E2f3a species and a 40-kD E2f3b polypeptide (Figure 6). To confirm that the upper species in our retinal lysates was E2f3a, we exploited novel mice that lack E2f3 exon 1a and thus express E2f3b exclusively (R. O. and G. L., unpublished data). The genotyping strategy is discussed in detail later and is outlined in Figure 7A. Western analysis confirmed that the upper band was absent in E2f3a−/− mice (Figures 6 and S8). Consistent with the drop in E2f3-expressing cells during WT retinal maturation (Figure 5A), the total amount of E2f3a was less at P18 compared to P0 (Figure 6). E2f3b was present in similar amounts at both time points. At P0 and P18, E2f3a was present in both nuclear and cytoplasmic fractions, but in marked contrast, E2f3b was exclusively nuclear at both times (Figure 6). Two closely migrating E2f3a bands were detected, more clearly evident at P18, of which the faster migrating species was dominant in nuclear and the slower species was dominant in cytoplasm (Figure 6). The identity of both as E2f3a species was confirmed by their absence in the P18 E2f3a KO retina (Figure S8). Analysis of Pou4f2, a nuclear transcription factor expressed in ganglion cells, showed that nuclear proteins had not contaminated the cytoplasmic fraction, and analysis of Slc18a3, a cytoplasmic SAC marker, confirmed that the reverse had also not occurred (Figure 6). These data show, to our knowledge for the first time, that E2f3a and E2f3b exhibit distinct patterns of subcellular distribution, and raise the possibility that E2f3a localization may be regulated by as yet unknown post-translational modifications.\nFigure 6 Subcellular Distribution of E2f3 Isoforms and Other Cell Cycle Proteins in the Developing Retina\nNuclear and cytoplasmic extracts from an equivalent number of retinal cells from mice of the indicated genotypes and ages were analyzed by Western blotting to detect the indicated proteins. Lysate from E2f3a−/− mice was used as a control to confirm the location of E2f3a protein. C, cytoplasmic extracts; N, nuclear extracts.\nFigure 7 The E2f3a Isoform Drives the Differentiation Defect in Rb KO SACs\n(A) Schematic diagrams of the mouse WT, E2f3a−/−, and the Cre-recombined floxed E2f3 loci (indicated here as E2f3−/− for simplicity). E2f3a−/− mice lack most of E2f3 exon 1a and part of intron 1a (red dotted box). Arrows indicate PCR primers. Genotyping of an E2f3a+/− mouse is shown on the right.\n(B) RT-PCR detection of E2f3a and E2f3b mRNA in the retina. The sequences of primers are 1aF (5′-GCCTCTACACCACGCCACAAG-3′), 1bF (5′-CGGAAATGCCCTTACAGC-3′), and 4R (5′-CTCAGTCACTTCTTTGGACAG-3′). WT retina expresses both E2f3a and E2f3b mRNA. As expected, E2f3a−/− retina lacks E2f3a mRNA and still expresses E2f3b mRNA. E2f3−/− retina lacks full-length E2f3a and E2f3b mRNAs, and instead expresses a truncated mRNA lacking exon 3.\n(C) Real-time RT-PCR analysis of E2f genes in P8 retinas of the indicated genotypes. Error bars represent SD of measurements from three animals, and asterisks indicate a significant difference between WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\n(D) Rescue of Rb KO SACs by E2f3a deletion. Horizontal retinal sections of the indicated genotypes and ages were stained for nuclei (DAPI, blue), M-phase (PH3, green), and the SAC marker Slc18a3 (red). E2f3a deletion does not suppress ectopic division, but rescues the SAC defect. Scale bars are 50 μm.\nM, molecular size marker. We also examined the distribution of other cell cycle regulators during retinal development. Like E2f3a, Rb was present in both the WT cytoplasm and nucleus at P0, but at P18, when the levels of Rb had increased, it was primarily nuclear (Figure 6). A very faint cytoplasmic Rb signal was evident at P18, which is consistent with Rb staining of SAC processes (Figure 5B), and with the very small proportion of SACs in the retina [38]. E2f1 was also detected in both nuclear and cytoplasmic fractions, although unlike E2f3a it was predominantly nuclear both at P0 and P18 (Figure 6). The E2f dimerization partner, Tfdp1, which lacks a nuclear localization signal [54], was primarily cytoplasmic at both P0 and P18, and the Cdk inhibitors Cdkn1a and Cdkn1b showed a similar pattern of distribution (Figure 6). Thus, among the cell cycle regulators we examined, most showed bivalent distribution, and E2f3b was unusual in its solely nuclear compartmentalization.\n\nRb Regulates SAC Differentiation through E2f3a\nTo test which E2f3 isoform is responsible for aberrant Rb KO SAC differentiation we exploited E2f3a−/− mice (Figure 7A). The genotyping strategy outlined in Figure 7A was used to distinguish the E2f3a, WT, and null alleles. Reverse transcriptase PCR (RT-PCR) confirmed the presence of both E2f3a and E2f3b RNA species in the developing WT retina, and the specific absence of E2f3a RNA in the E2f3a−/− retina (Figure 7B). E2f3a protein was absent in E2f3a−/− retinal lysate (Figures 6 and S8). Importantly, the levels of E2f3b message were similar in the Rb KO and Rb/E2f3a DKO retina, ruling out the possibility that any effects of E2f3a deletion we might observe were due to down-regulation of E2f3b (Figure 7C). Also, the levels of other E2fs were the same in the Rb KO, Rb/E2f3 DKO, and Rb/E2f3a DKO retina, ruling out any cross-regulatory effects (Figure 7C) [55]. E2f3a can trigger cell cycle induction, but because SAC defects are not linked to cell cycle perturbation (Figures 3A and 4), and in view of the predominant association between E2f3b and Rb in quiescent cells [16,19], we suspected that E2f3b may perturb differentiation in Rb KO SACs. Unexpectedly, however, E2f3a deletion suppressed the Rb KO SAC defect (Figure 7D). Thus, separate from its role in cell cycle control, Rb regulation of E2f3a is critical to ensure proper neuronal differentiation."}

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Regulates Division and Death through E2f1\nWe used the α-Cre transgene to delete floxed Rb exon 19 at embryonic day (E) 10 in peripheral retina [2]. RbloxP/loxP;α-Cre mice were bred with strains lacking E2f1 or E2f2 in the germ line, or a strain carrying a floxed E2f3 allele [5]. RbloxP/loxP;E2f1+/− and RbloxP/loxP;E2f1+/−;α-Cre mice were bred to produce RbloxP/loxP;E2f1−/−;α-Cre mice at a frequency of 1/8 and littermate controls at the same or higher (1/4) frequency. For simplicity we will refer to the RbloxP/loxP;E2f1−/−;α-Cre peripheral retina as the Rb/E2f1 double knockout (DKO) retina. Similar strategies were employed in the case of E2f2 or E2f3. Cre-mediated excision of Rb and E2f3 alleles in the retina was confirmed by PCR as described previously [2,5].\nTo measure ectopic cell division, mice were pulse-labelled with bromodeoxyuridine (BrdU) 2 h before sacrifice and the peripheral retina analyzed for BrdU incorporation by immunofluorescence. As reported before [2,3], Rb KO retinas exhibited both spatial and temporal ectopic DNA synthesis (Figures 1C and S1A). This is easily detected at E14, E16, and postnatal day (P) 0 in the inner retina where abnormal BrdU+ ganglion and amacrine RTCs are located, or on the outermost region of the P0 retina, where BrdU+ photoreceptor RTCs reside (Figures S1A and S2, arrows) [2]. Ectopic RTC division in Rb KO retinas is even more obvious at P8 or P18, when division is completed in wild-type (WT) retina (Figures 1C and S1A). Strikingly, the ectopically positioned S-phase cells at E14, E16, and P0 and all the abnormal division at P8 and P18 were completely suppressed in the Rb/E2f1 DKO retina (Figures 1C, 1E, 1F, S1A, and S2). In contrast, deletion of E2f2 or E2f3 had no effect at any stage of development. Analysis of mitotic cells with anti–phosphohistone 3 (PH3)–specific antibodies confirmed that loss of E2f1, but not E2f2 or E2f3, suppressed ectopic division (Figure S3). Deleting one E2f1 allele partially suppressed ectopic S-phase and mitosis in Rb KO RTCs (Figures 1C, 1E, 1F, S1A, S2, and S3), suggesting that E2f1 drives ectopic division in Rb KO RTCs in a dose-dependent fashion. These data contrast with previous findings in the lens and CNS of Rb KO embryos, where deletion of any activating E2f suppresses ectopic division to some extent [6–9].\nLoss of Rb in the retina results in considerable RTC apoptosis, eliminating most bipolar and ganglion cells as well as many rods (Figure 2A–2D) [2,3]. The loss of Rb KO rods is evident from the thinner ONL, and the death of these cells as well as bipolar and ganglion neurons can be detected directly by double labelling for apoptotic and cell-type-specific markers [2] (M. P. and R. B., unpublished data). Loss of peripheral Rb KO ganglion cells is also evident from thinning of the optic nerve (D. C. and R. B., unpublished data). Deleting E2f1, but not E2f2 or E2f3, blocked this ectopic cell death in a dose-dependent fashion (Figures 1D, 1G, and S1B).\nFigure 2 E2f1 Deletion Rescues Ganglion, Rod, and Bipolar Cells in the Rb KO Retina\n(A) Horizontal retinal sections from mice of the indicated ages and genotypes were stained for nuclei (DAPI, blue) and markers that detect ganglion cells (Pou4f2, red), rods and cones (Sag [rod arrestin], green), and rod bipolar cells (Prkca, green, and Cabp5, red). Scale bars are 50 μm.\n(B) Quantification of Pou4f2+ ganglion cells.\n(C) Quantification of Prkca+ and Cabp5+ bipolar cells.\n(D) Thickness of the ONL, which represents the number of rods.\nError bars represent SD of measurements from three animals, and asterisks indicate a significant difference between retinas of WT and the indicated genotypes, unless indicated otherwise by connecting lines (*, p \u003c 0.05; **; p \u003c 0.01; ANOVA and Tukey HSD test).\n(E and F) ERGs were recorded from the indicated genotypes under dark-adapted (scotopic) conditions, and (E) intensity series and (F) b-wave amplitudes as a function of the logarithm of the flash intensity were determined. (F) Further illustrates that the relative influence of the mutations on the photoreceptors (indicated by the saturated a-wave amplitude, right graph) was not substantially different from their effect on the b-wave response (dominated by the bipolars, left graph) at the same intensity of 10 cd·s/m2. To investigate the molecular mechanism that underlies the unique role of E2f1, we assessed the expression of known E2f targets as well as other genes that regulate the cell cycle and apoptosis. Numerous positive and negative cell cycle and apoptotic regulators were up-regulated in the Rb KO retina (Figure 1H). Among the E2f family, E2f1, E2f2, E2f3a, and E2f7 were induced following Rb loss, but E2f3b, E2f4, and E2f5 were unaffected. Consistent with the BrdU and terminal dUTP nick-end labelling (TUNEL) analyses, E2f1 deletion specifically reversed all these molecular defects, but E2f3 deletion had no effect (Figure 1H).\n\nNormal Differentiation in the Rb/E2f1 DKO Retina\nBecause E2f1 deletion blocks abnormal division and death in the Rb KO retina, the Rb/E2f1 DKO retina provided a unique opportunity to evaluate whether Rb controls differentiation independent of cell cycle effects. The Rb/E2f1 DKO retina had many Sag+ (S-antigen/rod arrestin) photoreceptors, Pou4f2+ (Brn3b) ganglion cells, and numerous Prkca+/Cabp5+ bipolar neurons (Figure 2A–2D). In contrast, there was no such rescue of cell types in Rb/E2f2 or Rb/E2f3 DKO retinas (Figure S4). Analysis with general neuronal markers Mtap2 (MAP2) and Snap25, as well as other markers expressed in bipolar cells (Chx10, Rcvrn, Vsx1, Tacr3, and Atp2b1) and rod photoreceptors (Rho and Rcvrn) confirmed rescue of the Rb/E2f1 DKO retina (Table S1). Moreover, neurons exhibited the same complex morphology as in WT retina. Bipolar cell bodies were located in the INL and had ascending and descending processes ending in the OPL and IPL, respectively (Figure 2A). In addition, the Rb/E2f1 DKO retina had a healthy appearing ONL consisting of morphologically normal rods with descending processes ending in the OPL and ascending processes that terminated in inner and outer segments (Figure 2A). It was suggested that Rb might regulate photoreceptor differentiation, possibly through rod-specific transcription factors (Figure 1B) [29]. However, if Rb does regulate photoreceptor differentiation, it does so by inhibiting E2f1, not by potentiating rod differentiation factors, such as Otx2, Crx, or Nrl. It is impossible to tell whether E2f1 perturbs differentiation directly, by affecting the expression of genes that modulate maturation, and/or indirectly through its effects on proliferation and survival (Figure 1B).\nAs with ectopic division and apoptosis (Figure 1C and 1D), the rescue of Rb KO retinal bipolar, ganglion, and rod cells was dependent on E2f1 dose (Figure 2A–2D). Separate from its role in driving ectopic division of Rb KO RTCs, E2f1 also promotes normal RPC division since in its absence RPC proliferation drops ~2-fold (D. C. and R. B., unpublished data). This modest reduction of RPC numbers in the absence of E2f1 accounts for the slight reduction in the number of ganglion cells at P0, in the number of bipolar cells at P18 or P30, and in the thickness of the ONL at P18 or P30 in the E2f1 KO and Rb/E2f1 DKO retina (Figure 2B–2D). The morphology of E2f1 KO neurons was WT (Figure 2A). Despite a slight drop in absolute cell numbers, the proportion of Rb/E2f1 DKO and E2f1 KO bipolar cells was the same as WT (data not shown). Slightly reduced cell numbers were not due to residual RTC death since we have not observed ectopic apoptosis at any embryonic or postnatal stage in the developing Rb/E2f1 DKO retina (Figures 1D, 1G, and S2). Moreover, deleting Ccnd1, which acts upstream of Rb proteins, also reduces RPC number, but does not suppress any defect in the Rb KO retina (D. C. and R. B., unpublished data). Thus, slightly reduced RPC division and dramatic rescue of severe defects in Rb KO RTCs are distinct effects stemming from the deletion of E2f1.\n\nNormal Function of the Rb/E2f1 DKO Retina\nThe discovery that E2f1 loss rescues even the morphology of Rb KO neurons is surprising because Rb is thought to regulate differentiation primarily through E2f-independent pathways [30–33]. However, normal morphology may not equate to completely normal differentiation. Thus, we compared the electroretinograms (ERGs) of adult WT (α-Cre), E2f1−/−, α-Cre;RbloxP/loxP, and α-Cre;RbloxP/loxP;E2f1−/− mice. ERGs functionally assess visual signalling in the mammalian retina from photoreceptors to amacrine cells (but usually not gangion cells), and are dominated by rod and cone bipolar cells. Typically, an ERG signal begins with a negative deflection initiated by the photoreceptors (the a-wave), which is terminated by a large positive deflection due to the activation of ON bipolar cells (the b-wave).\nResponses to dim light in dark-adapted (scotopic) conditions specifically assess the rod system, and were defective in the Rb KO retina (Figure 2E). The substantial reduction of both a- and b-waves is consistent with rod and bipolar cell apoptosis [2]. The sensitivity of the residual response appeared unchanged, suggesting it arose from the Cre-negative portions of the retina. Responses were about the same in the WT and E2f1 KO retina, and, most importantly, also the Rb/E2f1 DKO response median lay at the lower end of the normal range for most intensities (Figure 2F). Thus, E2f1 deletion almost completely rescued the rod system in the Rb KO retina.\nLight-adapted (photopic) recordings to specifically assess the cone system yielded comparable results. Cones represent only 3% of photoreceptors and, unlike rods, develop without Rb, but they require rods for survival, and in the Rb KO retina, they have abnormal morphology and their synaptic targets, bipolar cells, are much depleted [2]. The photopic response, a product of cone and mainly bipolar activity, was much reduced by Rb loss, but was rescued considerably in the Rb/E2f1 DKO retina (Figure S5). Again, the median amplitude lay at the lower end of the E2f1 KO range. The photopic response in E2f1 KO mice was slightly reduced relative to WT (Figure S5B), possibly because E2f1 is required for maximal expansion of embryonic RPCs, and the E2f1 KO retina has, as noted earlier, slightly fewer cells than the WT retina, although cell type proportions are unaffected (D. C. and R. B., unpublished data). Thus, marginally subnormal photopic responses in the Rb/E2f1 DKO retina can be attributed to both a reduction of cone numbers in E2f1 KO mice alone, and a “genuine” slight reduction in cone function attributable to Rb loss relative to WT. This slight effect may relate to a true differentiation defect in a subset of amacrine cells discussed below. This discussion should not obscure the major outcome that E2f1 deletion recovers most of the ERG response. Thus, E2f1 deletion not only rescues morphology but also both rod and cone system function in the Rb KO retina.\n\nAbnormal SAC Differentiation Independent of Cell Cycle and Survival Defects\nERGs primarily assess photoreceptor and bipolar cell function, but may miss differentiation defects in other cells. To test for subtle differences we stained the Rb/E2f1 DKO retina with 43 markers (Table S1). Thirty-two proteins displayed identical patterns in WT, E2f1 KO, and Rb/E2f1 DKO retina (Table S1). The other 11 markers revealed a cell-cycle– and apoptosis-independent differentiation defect in SACs. We first studied Calb2 (calretinin), which marks a subset of amacrine and ganglion cell bodies as well as three tracks corresponding to their processes in the IPL (Figure 3A). Normal Calb2 staining was seen in the E2f1 KO IPL (data not shown). However, only one Calb2+ track was evident in the Rb KO IPL, and this defect was not rescued in the Rb/E2f1 DKO retina (Figure 3A). We quantified Calb2+ cell bodies in the Rb KO INL (corresponding to amacrine cell staining only) and observed a reduction from P8 onwards (Figures 3C and S6).\nFigure 3 Differentiation Defects in Rb KO SACs\n(A) P18 horizontal sections of WT, Rb KO, and Rb/E2f1 DKO retina were stained for nuclei (DAPI, blue), Calb2 (green), and Slc18a3 (red).\n(B) Confocal images of P30 horizontal sections of WT and Rb KO retina were stained for nuclei (DAPI, blue), Chat and Slc18a3 (both red), and Camk2a (green). In the Rb KO section, the red stain is Chat only, as Slc18a3 is missing (see [A]).\n(C) Quantification of dense Calb2+ cell bodies in the INL, total Slc18a3+ cell bodies, and Camk2a+ cell bodies in the INL. Error bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\nScale bars are 50 μm in (A) and 20 μm in (B). Of the three Calb2+ tracks in the IPL, the two outer tracks are from SACs, named after their extensive dendritic-tree-like morphology [37]. SACs are cholinergic, represent ~5.2% of amacrine neurons [38], and are critical for both direction selectivity [34,35] and spontaneous rhythmic activity that occurs during normal retinal development [36]. SACs in the INL synapse in the OFF layer of the IPL that responds to decreasing light, while displaced SACs in the GCL have processes that synapse in the nearby ON layer of the IPL that responds to increasing light (reviewed in [39]). Mature SAC processes stain specifically for Slc18a3 (vesicular acetyl choline transporter, VAChT) [37], and, significantly, this marker was absent in the peripheral Rb KO or Rb/E2f1 DKO P18 retina (Figures 3A and S7B). Chat, expressed from the same locus, is also SAC specific, but marks both cell bodies and processes of mature SACs [37]. Chat was seen in fewer cells in the mature Rb KO retina, and was present in the soma but absent from processes (Figure 3B). We obtained similar results for Sv2c, a synaptic vesicle protein found in SACs [40]; Kcnc1b and Kcnc2, potassium channels expressed on SAC soma and dendrites as well as a very small number of ganglion cells [41]; gamma-aminobutyric acid (GABA), an inhibitory neurotransmitter present in about half of amacrine cells including SACs, as well as horizontal and some bipolar neurons [37]; and Calb1 (calbindin), which is expressed in many amacrine cells and labels SAC process faintly (Figure S7A and S7B; Table S1; and data not shown). Finally, we also examined the effect of Rb deletion on SAC differentiation using a Chx10-Cre transgene that is expressed in a mosaic pattern across the retina, generating patches of Cre-expressing cells [42]. Consistent with the mosaic deletion pattern, we observed markedly reduced Chat/Slc18a3 staining in the IPL of Chx10-Cre;RbloxP/loxP retina compared to WT (Figure S7C). Together, these results suggest a role for Rb in SAC differentiation.\nThe above findings could indicate a defect in SAC specification, SAC survival, or the levels and/or transport of the markers described above. Camk2a marks both SACs and ganglion cells [37], but because ganglion cells are eliminated in the Rb KO retina, Camk2a is a specific SAC marker in this context. Importantly, Camk2a+ tracks and dendrites were present in both the WT and Rb KO retina (Figure 3B), and the number of Camk2a+ soma was similar in WT and Rb KO retina at P30 and beyond, although fewer cells stained in Rb KO retina at P18, suggesting a delay in its appearance (Figures 3C and S6B). Thus, Rb is not required for SAC survival or for process outgrowth, but rather it seems to regulate the expression and/or stability of Calb2, Calb1, Chat, Slc18a3, Sv2c, Kcnc1b, Kcnc2, and GABA in SACs, but leaves Camk2a expression virtually unaffected. The presence of Chat in some cell bodies but never in processes (Figure 3B) also suggests a transport defect. The developmental pattern of Slc18a3 expression also supported this notion. In mature WT SACs Slc18a3 is only in processes, but in early postnatal SACs, it is found in the cell body, and moves into emerging processes at approximately P4–P6. As noted above, Slc18a3 was absent at P18 in the Rb KO retina (Figure 3A); at P4 or P5 it was in cell bodies, yet was rarely present in Rb KO processes (Figures 4A and S6). Slc18a3 became virtually undetectable in Rb KO SACs by P8 (Figures 3C and S6C). These data suggest that Rb affects both the synthesis/stability and transport of SAC markers.\nFigure 4 E2f3 Loss Rescues Differentiation of Rb KO SACs\n(A) Horizontal retinal sections of the indicated ages and genotypes were stained for nuclei (DAPI, blue), mitosis marker PH3 (green), and Slc18a3 (red), which marks SAC soma at early stages and processes from ~P5 onwards. Arrows show mitotic PH3+ nuclei in Rb KO, Rb/E2f2 DKO, and Rb/E2f3 DKO retinas. E2f1 loss rescues the ectopic mitosis and cell death defects, but not the SAC defect. E2f2 loss has no effect. E2f3 loss does not rescue the ectopic mitosis and cell loss defects, but rescues the SAC defect. Inactivating E2f1 and E2f3 together rescues the ectopic mitosis, cell death, and SAC defects.\n(B) The fraction of Camk2a+ cells that are Chat + and Slc18a3+ in the P30 retina.\n(C) Horizontal P5 retinal sections were stained for nuclei (DAPI, blue), Slc18a3 (green), and Isl1 (red). Arrows show double-labelled Isl1+/Slc18a3+ cells in the inner INL.\n(D) Horizontal P0 retinal sections of the indicated genotypes were stained for nuclei (DAPI, blue), cell division marker Mki67 (green), and Isl1 (red). Arrows show double-labelled dividing SACs.\n(E) The fraction of Isl1+ cells in the inner NBL (INBL) of P0 retinas that are dividing (Mki67+).\nError bars represent SD of measurements from three animals, and asterisks indicate significant differences between retinas of WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test). Scale bars in (A), (C), and (D) are 50 μm.\n\nRb Regulates SAC Differentiation through E2f3\nRb binds more than 100 proteins [43] and in some non-neuronal cells, such as skeletal muscle, adipocytes, and bone, Rb is thought to bind and potentiate tissue-specific transcription factors that promote differentiation [31–33]. Thus, we expected that Rb might interact with retina-specific factors to facilitate SAC differentiation. A direct role for E2f in mediating Rb-dependent differentiation defects (independent of cell cycle or death defects) has to our knowledge not been described, but because E2f can regulate some differentiation genes [44–48], we first tested whether E2f2 or E2f3 might perturb Rb KO SAC maturation. At multiple time points, E2f1 deletion suppressed ectopic mitosis (PH3+ cells), but did not reverse the SAC defect, and E2f2 deletion had no effect on either defect (Figure 4A). Remarkably, although E2f3 deletion did not reverse ectopic mitosis, it rescued Calb2, Slc18a3, Chat, GABA, Kcnc1b, Kcnc2, and Sv2c staining at multiple times (Figure 4A and data not shown). Rb/E2f3 DKO SAC tracks were slightly more disordered than in WT retina, most likely because of the absence of synaptic partner cells, which are killed by E2f1. Indeed, this minor defect was rescued in the Rb/E2f1/E2f3 triple knockout retina, where bipolar and ganglion cell death was rescued and SAC differentiation was restored (Figure 4A). E2f3 deletion alone did not affect SAC differentiation (Figure 4A); thus, it is unleashed E2f3 activity that is detrimental, and the critical role for Rb is to inhibit E2f3.\nWe quantified the fraction of Camk2a+ SACs in different genotypes and found that 60% of WT P30 Camk2a+ cells expressed Chat and Slc18a3, which dropped to only 5.6% in the Rb KO retina, and remained low at 3.7% in the Rb/E2f1 DKO retina, but rose to 91% in the Rb/E2f3 DKO retina (Figure 4B). The latter fraction is higher than WT because ganglion cells, which normally make up ~40% of Camk2a+ cells, are killed by apoptosis.\nTo quantify the effect of different E2fs on ectopic division specifically in SACs, we exploited Isl1 (Islet1). This marker is expressed in both SACs and ganglion cells, thus Isl1+ cells in the INL are exclusively SACs [49]. We found that 98.2% ± 1.8% of Isl1+ cells in the forming inner INL at P5 were also Slc18a3+, confirming that Isl1 is an excellent SAC marker (Figure 4C). Moreover, Isl1, unlike Slc18a3, is nuclear, which facilitates scoring of Isl1+/Mki67+ cells. It is also expressed earlier than Slc18a3, permitting analysis of SACs soon after their birth at ~E15; thus, we could study retina at P0, a time when ectopic division is high in the inner retina and prior to Rb-independent cell cycle exit associated with terminal differentiation [2]. At P0, no WT Isl1+ cells in the inner neuroblastic layer (NBL) (which is the future INL) were dividing, but 57 ± 14 Isl1+/Mki67+ cells were detected in the Rb KO inner NBL (Figure 4D). Indeed, about one-third of all Isl1+ cells in the entire inner NBL were dividing in the Rb KO retina, or ~50% in the periphery where Cre is expressed (Figure 4E and data not shown). This defect was suppressed in the Rb/E2f1 DKO retina, where we detected only 1 ± 1 dividing SAC, but not the Rb/E2f3 DKO retina, where there were 53 ± 8 dividing SACs (Figure 4D and 4E). We observed similar effects at P0 with Calb2, which marks newborn SACs and other amacrine cells (data not shown). Thus, in Rb KO SACs, E2f1 deletion suppresses ectopic division but not aberrant differentiation, whereas E2f3 deletion suppresses aberrant differentiation but not ectopic division.\n\nSpecific Expression of E2f3 in SACs and Other Subsets of CNS Neurons\nThe unique effect of E2f3 in disrupting the differentiation of SACs but not other retinal neurons might be due to cell-type-specific expression or cell-type-specific activity of E2f3. Determining between these two possibilities is not easy, as E2f immunostaining in mouse tissues is problematic. We did not solve this issue for E2f1 or E2f2, but used a modified protocol [50] to successfully track E2f3 expression (Figure 5). At P0, E2f3 was detected in RPCs, consistent with a putative role in normal proliferation (Figure 5A). The signal was specific as it was absent in the E2f3 KO peripheral retina (Figure 5A). As the retina differentiated and RPC division diminished, the number of E2f3+ cells also dropped, and by P8, when division is virtually over, only a subset of post-mitotic cells in the inner retina expressed E2f3 (Figure 5A). By P18, E2f3 was also detected in two tracks in the IPL (Figure 5A and 5B), reminiscent of SAC markers such as Chat and Slc18a3 (c.f. Figures 3 and 4). This cytoplasmic E2f3 staining was also specific, as it was absent in the E2f3 KO peripheral retina of α-Cre;E2f3loxP/loxP mice (Figure 5A). Indeed, double labelling with E2f3 (red) and Chat plus Slc18a3 (green) confirmed that E2f3 is present in both SAC soma and dendrites (Figure 5B). Rb protein was also detected in the inner retina (Figure 5A), and showed a similar distribution as E2f3 in SACs (Figure 5B), and was also present in mature ganglion cells and Müller cells as reported [51]. Rb staining in SAC processes was specific as it was absent in the peripheral retina of αCre;RbloxP/loxP mice (Figure 5A). These data suggest that Rb and E2f3 colocalize in SACs and that E2f3 triggers defects in SAC differentiation because it is specifically expressed in these retinal neurons.\nFigure 5 E2f3 and Rb Expression in SACs\n(A) Left panels: horizontal P0, P8, and P18 retinal sections of the indicated genotypes were stained for E2f3 (red) and DAPI (blue). The arrow indicates the junction between the E2f3 null peripheral and WT central P0 retina. Note the absence of E2f3 protein in the peripheral E2f3 KO RPCs at P0 and in peripheral inner retinal neurons at P18. Far right panel: P18 retinal sections of the indicated genotypes were stained for Rb (red) and DAPI (blue). Note the absence of Rb protein in the peripheral Rb KO inner retinal neurons.\n(B) WT P18 retinal sections were stained for nuclei (DAPI, blue), E2f3 (red) or Rb (red), and Chat plus Slc18a3 (green). Arrows indicate double-labelled soma. Note that the IPL processes are also double-labelled.\nScale bars are 50 μm. We also found that E2f3 is present in a specific subset of mature neurons in various brain regions (data not shown). For example, in the P20 amygdala, E2f3 colocalized with the general neuronal markers Mtap2 and Mecp2 [52], but not with Calb2, which marks a subset of neurons, or with the glial marker Gfap (data not shown). Unlike in retinal SACs, E2f3 was not coexpressed in Chat+ or Slc18a3+ cholinergic neurons located in various regions of the brain and spinal cord (data not shown). In agreement, we could not detect defects in cholinergic Rb KO neurons in the developing forebrain, but other Rb KO neurons in this region showed differentiation defects that were rescued by deleting E2f3 [53]. Together, these results suggest that the common mechanism by which Rb promotes neural differentiation is through E2f3 inhibition.\n\nDistinct Localization of E2f3 Isoforms\nAs noted above, E2f3 and Rb staining in SACs was both nuclear and cytoplasmic (Figure 5A and 5B). The antibody that worked in immunostaining recognizes a C-terminal region and thus, does not distinguish a/b isoforms. To our knowledge, the subcellular location of E2f3 isoforms has not been determined in any cell type. To verify the dual locations of E2f3 and to determine which isoforms were present in retina, we analyzed nuclear and cytoplasmic fractions by Western blot at different times during development. Analysis with the pan-E2f3 antibody (sc-878, Santa Cruz Biotechnology) detected a 55-kD E2f3a species and a 40-kD E2f3b polypeptide (Figure 6). To confirm that the upper species in our retinal lysates was E2f3a, we exploited novel mice that lack E2f3 exon 1a and thus express E2f3b exclusively (R. O. and G. L., unpublished data). The genotyping strategy is discussed in detail later and is outlined in Figure 7A. Western analysis confirmed that the upper band was absent in E2f3a−/− mice (Figures 6 and S8). Consistent with the drop in E2f3-expressing cells during WT retinal maturation (Figure 5A), the total amount of E2f3a was less at P18 compared to P0 (Figure 6). E2f3b was present in similar amounts at both time points. At P0 and P18, E2f3a was present in both nuclear and cytoplasmic fractions, but in marked contrast, E2f3b was exclusively nuclear at both times (Figure 6). Two closely migrating E2f3a bands were detected, more clearly evident at P18, of which the faster migrating species was dominant in nuclear and the slower species was dominant in cytoplasm (Figure 6). The identity of both as E2f3a species was confirmed by their absence in the P18 E2f3a KO retina (Figure S8). Analysis of Pou4f2, a nuclear transcription factor expressed in ganglion cells, showed that nuclear proteins had not contaminated the cytoplasmic fraction, and analysis of Slc18a3, a cytoplasmic SAC marker, confirmed that the reverse had also not occurred (Figure 6). These data show, to our knowledge for the first time, that E2f3a and E2f3b exhibit distinct patterns of subcellular distribution, and raise the possibility that E2f3a localization may be regulated by as yet unknown post-translational modifications.\nFigure 6 Subcellular Distribution of E2f3 Isoforms and Other Cell Cycle Proteins in the Developing Retina\nNuclear and cytoplasmic extracts from an equivalent number of retinal cells from mice of the indicated genotypes and ages were analyzed by Western blotting to detect the indicated proteins. Lysate from E2f3a−/− mice was used as a control to confirm the location of E2f3a protein. C, cytoplasmic extracts; N, nuclear extracts.\nFigure 7 The E2f3a Isoform Drives the Differentiation Defect in Rb KO SACs\n(A) Schematic diagrams of the mouse WT, E2f3a−/−, and the Cre-recombined floxed E2f3 loci (indicated here as E2f3−/− for simplicity). E2f3a−/− mice lack most of E2f3 exon 1a and part of intron 1a (red dotted box). Arrows indicate PCR primers. Genotyping of an E2f3a+/− mouse is shown on the right.\n(B) RT-PCR detection of E2f3a and E2f3b mRNA in the retina. The sequences of primers are 1aF (5′-GCCTCTACACCACGCCACAAG-3′), 1bF (5′-CGGAAATGCCCTTACAGC-3′), and 4R (5′-CTCAGTCACTTCTTTGGACAG-3′). WT retina expresses both E2f3a and E2f3b mRNA. As expected, E2f3a−/− retina lacks E2f3a mRNA and still expresses E2f3b mRNA. E2f3−/− retina lacks full-length E2f3a and E2f3b mRNAs, and instead expresses a truncated mRNA lacking exon 3.\n(C) Real-time RT-PCR analysis of E2f genes in P8 retinas of the indicated genotypes. Error bars represent SD of measurements from three animals, and asterisks indicate a significant difference between WT and the indicated genotypes (*, p \u003c0.05; **; p \u003c0.01; ANOVA and Tukey HSD test).\n(D) Rescue of Rb KO SACs by E2f3a deletion. Horizontal retinal sections of the indicated genotypes and ages were stained for nuclei (DAPI, blue), M-phase (PH3, green), and the SAC marker Slc18a3 (red). E2f3a deletion does not suppress ectopic division, but rescues the SAC defect. Scale bars are 50 μm.\nM, molecular size marker. We also examined the distribution of other cell cycle regulators during retinal development. Like E2f3a, Rb was present in both the WT cytoplasm and nucleus at P0, but at P18, when the levels of Rb had increased, it was primarily nuclear (Figure 6). A very faint cytoplasmic Rb signal was evident at P18, which is consistent with Rb staining of SAC processes (Figure 5B), and with the very small proportion of SACs in the retina [38]. E2f1 was also detected in both nuclear and cytoplasmic fractions, although unlike E2f3a it was predominantly nuclear both at P0 and P18 (Figure 6). The E2f dimerization partner, Tfdp1, which lacks a nuclear localization signal [54], was primarily cytoplasmic at both P0 and P18, and the Cdk inhibitors Cdkn1a and Cdkn1b showed a similar pattern of distribution (Figure 6). Thus, among the cell cycle regulators we examined, most showed bivalent distribution, and E2f3b was unusual in its solely nuclear compartmentalization.\n\nRb Regulates SAC Differentiation through E2f3a\nTo test which E2f3 isoform is responsible for aberrant Rb KO SAC differentiation we exploited E2f3a−/− mice (Figure 7A). The genotyping strategy outlined in Figure 7A was used to distinguish the E2f3a, WT, and null alleles. Reverse transcriptase PCR (RT-PCR) confirmed the presence of both E2f3a and E2f3b RNA species in the developing WT retina, and the specific absence of E2f3a RNA in the E2f3a−/− retina (Figure 7B). E2f3a protein was absent in E2f3a−/− retinal lysate (Figures 6 and S8). Importantly, the levels of E2f3b message were similar in the Rb KO and Rb/E2f3a DKO retina, ruling out the possibility that any effects of E2f3a deletion we might observe were due to down-regulation of E2f3b (Figure 7C). Also, the levels of other E2fs were the same in the Rb KO, Rb/E2f3 DKO, and Rb/E2f3a DKO retina, ruling out any cross-regulatory effects (Figure 7C) [55]. E2f3a can trigger cell cycle induction, but because SAC defects are not linked to cell cycle perturbation (Figures 3A and 4), and in view of the predominant association between E2f3b and Rb in quiescent cells [16,19], we suspected that E2f3b may perturb differentiation in Rb KO SACs. Unexpectedly, however, E2f3a deletion suppressed the Rb KO SAC defect (Figure 7D). Thus, separate from its role in cell cycle control, Rb regulation of E2f3a is critical to ensure proper neuronal differentiation."}