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Controls Retinal Cell Division and Death through E2f1\nWork in the early 1990s showed that Rb loss triggers defects in neuronal cell cycle exit, survival, and differentiation [26–28]. Much of the death is an indirect consequence of probable hypoxia linked to placental defects [12–14]. However, targeted KO and chimeric studies reveal that Rb autonomously promotes cell cycle exit in newborn neurons, and is required for survival of a subset of neurons, particularly in the retina [2,3,13,14,56–59]. However, whether Rb also regulates differentiation is obscured by potentially indirect effects of ectopic division and death. Moreover, a mechanism though which Rb may regulate neuronal maturation has not been elucidated.\nHere, deleting E2f1 specifically rescued ectopic division and death in the Rb KO retina. Importantly, major Rb/E2f1 DKO neurons differentiated normally, and ERGs revealed the rescue of rod- and cone-mediated function, implicating a regular signal flow from photoreceptors to bipolar and amacrine cells. Division and death genes were induced in Rb KO cells, and deleting E2f1, but not E2f2 or E2f3, reversed these molecular events. E2f1 may also regulate differentiation targets, but whether this contributes to defects in retinal cell maturation is impossible to separate from potentially indirect consequences of deregulated division and death. In any case, it is clear that in most retinal cells, including photoreceptors [29], transcription factors that promote differentiation function independently of Rb.\nWe have also found that E2f1 deletion rescues cell-autonomous ectopic division, death, and differentiation defects in sporadic Rb KO clones generated using a Cre retrovirus vector (M. P. and R. B., unpublished data). These data are consistent with the observation that E2f1 overexpression in newborn photoreceptors drives ectopic division and apoptosis [60], and add to the growing evidence indicating that E2f1 is the major, and perhaps only, member of the three activating E2fs required to induce apoptosis in Rb KO cells [10,15]. Thus, deregulated E2f1 activity in the retina, whether resulting from the inactivation of Rb or from overexpression, promotes unscheduled cell division and triggers apoptosis in susceptible RTCs. E2f1, rather than other E2fs, may be a potential target for novel therapeutics to prevent retinoblastoma in RB1 +/− humans.\nOur ERG studies revealed rescue of the Rb KO rod–bipolar system, and almost complete restoration of the cone–bipolar system following E2f1 deletion. There was a slightly lower response in the Rb/E2f1 DKO retina relative to the E2f1 KO control retina. This difference might reflect a role for Rb in the development of cones, bipolar cells, or other cells that may contribute to the photopic ERG, including potentially SACs, which do have a serious defect in the Rb/E2f1 DKO retina.\n\nRb Controls SAC Differentiation through E2f3a\nComprehensive marker analysis revealed that, in striking contrast to other retinal neurons, E2f1 deletion did not suppress defects in Rb KO cholinergic SACs. Instead, we observed E2f1-independent defects in the synthesis and transport of a large cohort of SAC proteins. These data expand insight into the development of these important interneurons, but more critically, provide to our knowledge the first unambiguous evidence that Rb regulates neurogenesis beyond terminal mitosis. Rb binds more than 100 factors [43], and in several non-neuronal cells, such as skeletal muscle, adipocytes, and bone, it binds and potentiates tissue-specific transcription factors that promote differentiation [31–33]. The idea that Rb promotes muscle differentiation by potentiating Myod1 activity was contested [61], and other mechanisms proposed [62,63], but not involving E2f repression. Strikingly, however, we discovered that Rb promotes SAC differentiation through E2f3 (Figure 8).\nFigure 8 Rb Regulates Distinct Processes through E2f1 and E2f3a\nRed text and arrows indicate Rb-dependent events. Black text and arrows indicate events for which there is no direct evidence of Rb involvement. Rb does not appear to temper RPC expansion and is not required for differentiation of RPCs into RTCs, but is essential to couple RTC birth to terminal mitosis, thus locking them out of cycle. Rb performs this function by inhibiting E2f1. Rb is also required for SAC differentiation, and in this case, acts by inhibiting E2f3a. There is no direct evidence that Rb is required for terminal differentiation of other cell types. Colour codes and abbreviations as in Figure 1A. Rb regulation of SAC differentiation through E2f3 was independent of its role in controlling division or death: E2f3 deletion rescued Rb KO SAC defects but did not suppress aberrant proliferation or death, whereas E2f1 deletion reversed abnormal proliferation and death but did not rescue SAC differentiation. Double labelling confirmed that E2f1 but not E2f3 deletion reversed Rb KO SAC division. Moreover, deleting E2f1, but not E2f3, reversed deregulated expression of cell cycle and apoptotic genes in the Rb KO retina. E2f3 is expressed in a subset of CNS neurons (this work) and drives specific cell-cycle–independent defects in Rb KO forebrain neurons [53]. Thus, E2f3 inhibition is the first, and may be the only, mechanism by which Rb participates directly in neuronal differentiation.\nTo further dissect the mechanism of action of Rb in SACs we determined the E2f3 isoform it targets to promote differentiation. E2f3b was the primary candidate, since Rb and E2f3b collaborate to repress targets in quiescent cells in vitro [19]. However, in the first work to our knowledge to examine the function of any E2f protein isoform in vivo, we made the surprising observation that Rb regulates SAC differentiation through E2f3a (Figure 8). Formally, we cannot exclude the possibility that deleting E2f3b might also rescue SAC differentiation, but definitive proof will require analysis of E2f3b null mice. Nevertheless, our data prove that Rb definitely regulates SAC differentiation through the activating E2f3 isoform.\n\nDistinct E2f3a and E2f3b Localization\nThe subcellular location of E2f isoforms has not to our knowledge been addressed before. E2f3a and E2f3b share 110 C-terminal amino acids that encode the NLS, DNA-binding, marked box, transactivation, and Rb-binding domains [16], yet they exhibit different subcellular distribution in developing retinal cells. E2f3a is both nuclear and cytoplasmic, but E2f3b is always nuclear. The unique 121- and six-residue N-termini of E2f3a and E2f3b, respectively, likely mediate this difference. This region in E2f1, E2f2, and E2f3a binds Ccna2, establishing a negative regulatory loop that deactivates E2fs in mid-late S-phase [64,65]. However, even E2f3b, which lacks this domain, binds and is regulated by Ccna2 [18], so the domain difference may not explain the unique distributions we observed. Rb family and Tfdp proteins can also determine E2f localization [20–22], and we found that a portion of both Rb and Tfdp1 proteins are cytoplasmic in retinal cells. Indeed, immunostaining revealed that Rb and E2f3 colocalize to SAC processes.\nThe nuclear localization of E2f3b contrasts with that of other repressive E2fs in differentiating muscle, where E2f5 switches from the nucleus to cytoplasm, while E2f4 remains in both compartments [23]. The distinct compartmentalization of E2f3a and E2f3b in the retina suggests temporally and functionally distinct activities. Rb distribution matches that of E2f3a, consistent with its critical role in supporting SAC differentiation through E2f3a.\n\nEctopic Division and Differentiation\nRb is critical to ensure that many types of terminally differentiating cells leave the cell cycle (e.g., neurons, gut and skin epithelia, muscle, and lens fibres) (reviewed in [66]). Early overexpression studies in vitro suggested Rb might temper expansion of cycling cells, but KO studies in vivo indicate that its major role is to block division in terminally differentiating cells. In its absence, many (but clearly not all) aspects of differentiation go ahead relatively unperturbed. In the retina, differentiating transition cells are born in the absence of Rb, migrate to the correct layer, and express appropriate markers ([2] and this work). In brain, Rb KO neurons migrate away from the ventricular zone and switch on Tubb3 (βIII-tubulin), but continue to incorporate BrdU [13], and in gut epithelia, differentiated enterocytes migrate up the villi and activate expression of serotonin, yet continue to incorporate BrdU [67]. In the case of SACs, the differentiation defects we observed (e.g., loss of Slc18a3 and Chat) were not due to aberrant division, but it is possible there are other problems with these cells that are caused by ectopic division. Nevertheless, it is clear that many aspects of differentiation in multiple cell types are compatible with ectopic division. However, division of terminally differentiating cells is dangerous, since it may facilitate transformation, as is the case in retinoblastoma (reviewed in [66]).\n\nHow Does E2f3a Perturb SAC Differentiation?\nE2f3a could disrupt SAC differentiation through its well known role as a transcriptional activator, or, in view of the discovery that it is partially cytoplasmic, E2f3a may affect processes other than gene regulation. Both scenarios are feasible since E2fs regulate differentiation genes [44–48], and cell cycle regulators, such as Cdkn1b, have cytoplasmic activities that influence differentiation [68,69]. Many transcription factors shuttle between nucleus and cytoplasm during neurogenesis (e.g., [70] and references therein). It may be difficult to identify E2f3a-specific target genes or cytoplasmic proteins in SACs since these neurons are a small proportion (\u003c1%) of the total retina and only ~5.2% of amacrine neurons [38].\n\nDo E2fs Mediate All Rb Functions?\nOthers have suggested that Rb promotes differentiation in non-neuronal cells through E2f-independent means [31–33]. However, these studies did not assess whether these cell types differentiate normally if Rb is deleted along with one or more E2f family members. One study reported that Rb mutants that do not bind E2f still induce differentiation [30]. However, the binding assays were performed in solution, and we have found that several of these mutants do bind E2f, albeit weakly, on chromatin (T. Yu and R. B., unpublished data). It is possible that Rb-mediated potentiation of tissue-specific transcription factors may, at least in some cases, be a redundant activity, and that the only critical Rb function is to inhibit E2f. Our study is the first to our knowledge to assess comprehensively whether Rb KO cells can differentiate in the absence of different E2fs. In light of our findings, it will be important to reassess differentiation defects in other Rb KO tissues in the absence of individual and combined activating E2f family members."}

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Controls Retinal Cell Division and Death through E2f1\nWork in the early 1990s showed that Rb loss triggers defects in neuronal cell cycle exit, survival, and differentiation [26–28]. Much of the death is an indirect consequence of probable hypoxia linked to placental defects [12–14]. However, targeted KO and chimeric studies reveal that Rb autonomously promotes cell cycle exit in newborn neurons, and is required for survival of a subset of neurons, particularly in the retina [2,3,13,14,56–59]. However, whether Rb also regulates differentiation is obscured by potentially indirect effects of ectopic division and death. Moreover, a mechanism though which Rb may regulate neuronal maturation has not been elucidated.\nHere, deleting E2f1 specifically rescued ectopic division and death in the Rb KO retina. Importantly, major Rb/E2f1 DKO neurons differentiated normally, and ERGs revealed the rescue of rod- and cone-mediated function, implicating a regular signal flow from photoreceptors to bipolar and amacrine cells. Division and death genes were induced in Rb KO cells, and deleting E2f1, but not E2f2 or E2f3, reversed these molecular events. E2f1 may also regulate differentiation targets, but whether this contributes to defects in retinal cell maturation is impossible to separate from potentially indirect consequences of deregulated division and death. In any case, it is clear that in most retinal cells, including photoreceptors [29], transcription factors that promote differentiation function independently of Rb.\nWe have also found that E2f1 deletion rescues cell-autonomous ectopic division, death, and differentiation defects in sporadic Rb KO clones generated using a Cre retrovirus vector (M. P. and R. B., unpublished data). These data are consistent with the observation that E2f1 overexpression in newborn photoreceptors drives ectopic division and apoptosis [60], and add to the growing evidence indicating that E2f1 is the major, and perhaps only, member of the three activating E2fs required to induce apoptosis in Rb KO cells [10,15]. Thus, deregulated E2f1 activity in the retina, whether resulting from the inactivation of Rb or from overexpression, promotes unscheduled cell division and triggers apoptosis in susceptible RTCs. E2f1, rather than other E2fs, may be a potential target for novel therapeutics to prevent retinoblastoma in RB1 +/− humans.\nOur ERG studies revealed rescue of the Rb KO rod–bipolar system, and almost complete restoration of the cone–bipolar system following E2f1 deletion. There was a slightly lower response in the Rb/E2f1 DKO retina relative to the E2f1 KO control retina. This difference might reflect a role for Rb in the development of cones, bipolar cells, or other cells that may contribute to the photopic ERG, including potentially SACs, which do have a serious defect in the Rb/E2f1 DKO retina.\n\nRb Controls SAC Differentiation through E2f3a\nComprehensive marker analysis revealed that, in striking contrast to other retinal neurons, E2f1 deletion did not suppress defects in Rb KO cholinergic SACs. Instead, we observed E2f1-independent defects in the synthesis and transport of a large cohort of SAC proteins. These data expand insight into the development of these important interneurons, but more critically, provide to our knowledge the first unambiguous evidence that Rb regulates neurogenesis beyond terminal mitosis. Rb binds more than 100 factors [43], and in several non-neuronal cells, such as skeletal muscle, adipocytes, and bone, it binds and potentiates tissue-specific transcription factors that promote differentiation [31–33]. The idea that Rb promotes muscle differentiation by potentiating Myod1 activity was contested [61], and other mechanisms proposed [62,63], but not involving E2f repression. Strikingly, however, we discovered that Rb promotes SAC differentiation through E2f3 (Figure 8).\nFigure 8 Rb Regulates Distinct Processes through E2f1 and E2f3a\nRed text and arrows indicate Rb-dependent events. Black text and arrows indicate events for which there is no direct evidence of Rb involvement. Rb does not appear to temper RPC expansion and is not required for differentiation of RPCs into RTCs, but is essential to couple RTC birth to terminal mitosis, thus locking them out of cycle. Rb performs this function by inhibiting E2f1. Rb is also required for SAC differentiation, and in this case, acts by inhibiting E2f3a. There is no direct evidence that Rb is required for terminal differentiation of other cell types. Colour codes and abbreviations as in Figure 1A. Rb regulation of SAC differentiation through E2f3 was independent of its role in controlling division or death: E2f3 deletion rescued Rb KO SAC defects but did not suppress aberrant proliferation or death, whereas E2f1 deletion reversed abnormal proliferation and death but did not rescue SAC differentiation. Double labelling confirmed that E2f1 but not E2f3 deletion reversed Rb KO SAC division. Moreover, deleting E2f1, but not E2f3, reversed deregulated expression of cell cycle and apoptotic genes in the Rb KO retina. E2f3 is expressed in a subset of CNS neurons (this work) and drives specific cell-cycle–independent defects in Rb KO forebrain neurons [53]. Thus, E2f3 inhibition is the first, and may be the only, mechanism by which Rb participates directly in neuronal differentiation.\nTo further dissect the mechanism of action of Rb in SACs we determined the E2f3 isoform it targets to promote differentiation. E2f3b was the primary candidate, since Rb and E2f3b collaborate to repress targets in quiescent cells in vitro [19]. However, in the first work to our knowledge to examine the function of any E2f protein isoform in vivo, we made the surprising observation that Rb regulates SAC differentiation through E2f3a (Figure 8). Formally, we cannot exclude the possibility that deleting E2f3b might also rescue SAC differentiation, but definitive proof will require analysis of E2f3b null mice. Nevertheless, our data prove that Rb definitely regulates SAC differentiation through the activating E2f3 isoform.\n\nDistinct E2f3a and E2f3b Localization\nThe subcellular location of E2f isoforms has not to our knowledge been addressed before. E2f3a and E2f3b share 110 C-terminal amino acids that encode the NLS, DNA-binding, marked box, transactivation, and Rb-binding domains [16], yet they exhibit different subcellular distribution in developing retinal cells. E2f3a is both nuclear and cytoplasmic, but E2f3b is always nuclear. The unique 121- and six-residue N-termini of E2f3a and E2f3b, respectively, likely mediate this difference. This region in E2f1, E2f2, and E2f3a binds Ccna2, establishing a negative regulatory loop that deactivates E2fs in mid-late S-phase [64,65]. However, even E2f3b, which lacks this domain, binds and is regulated by Ccna2 [18], so the domain difference may not explain the unique distributions we observed. Rb family and Tfdp proteins can also determine E2f localization [20–22], and we found that a portion of both Rb and Tfdp1 proteins are cytoplasmic in retinal cells. Indeed, immunostaining revealed that Rb and E2f3 colocalize to SAC processes.\nThe nuclear localization of E2f3b contrasts with that of other repressive E2fs in differentiating muscle, where E2f5 switches from the nucleus to cytoplasm, while E2f4 remains in both compartments [23]. The distinct compartmentalization of E2f3a and E2f3b in the retina suggests temporally and functionally distinct activities. Rb distribution matches that of E2f3a, consistent with its critical role in supporting SAC differentiation through E2f3a.\n\nEctopic Division and Differentiation\nRb is critical to ensure that many types of terminally differentiating cells leave the cell cycle (e.g., neurons, gut and skin epithelia, muscle, and lens fibres) (reviewed in [66]). Early overexpression studies in vitro suggested Rb might temper expansion of cycling cells, but KO studies in vivo indicate that its major role is to block division in terminally differentiating cells. In its absence, many (but clearly not all) aspects of differentiation go ahead relatively unperturbed. In the retina, differentiating transition cells are born in the absence of Rb, migrate to the correct layer, and express appropriate markers ([2] and this work). In brain, Rb KO neurons migrate away from the ventricular zone and switch on Tubb3 (βIII-tubulin), but continue to incorporate BrdU [13], and in gut epithelia, differentiated enterocytes migrate up the villi and activate expression of serotonin, yet continue to incorporate BrdU [67]. In the case of SACs, the differentiation defects we observed (e.g., loss of Slc18a3 and Chat) were not due to aberrant division, but it is possible there are other problems with these cells that are caused by ectopic division. Nevertheless, it is clear that many aspects of differentiation in multiple cell types are compatible with ectopic division. However, division of terminally differentiating cells is dangerous, since it may facilitate transformation, as is the case in retinoblastoma (reviewed in [66]).\n\nHow Does E2f3a Perturb SAC Differentiation?\nE2f3a could disrupt SAC differentiation through its well known role as a transcriptional activator, or, in view of the discovery that it is partially cytoplasmic, E2f3a may affect processes other than gene regulation. Both scenarios are feasible since E2fs regulate differentiation genes [44–48], and cell cycle regulators, such as Cdkn1b, have cytoplasmic activities that influence differentiation [68,69]. Many transcription factors shuttle between nucleus and cytoplasm during neurogenesis (e.g., [70] and references therein). It may be difficult to identify E2f3a-specific target genes or cytoplasmic proteins in SACs since these neurons are a small proportion (\u003c1%) of the total retina and only ~5.2% of amacrine neurons [38].\n\nDo E2fs Mediate All Rb Functions?\nOthers have suggested that Rb promotes differentiation in non-neuronal cells through E2f-independent means [31–33]. However, these studies did not assess whether these cell types differentiate normally if Rb is deleted along with one or more E2f family members. One study reported that Rb mutants that do not bind E2f still induce differentiation [30]. However, the binding assays were performed in solution, and we have found that several of these mutants do bind E2f, albeit weakly, on chromatin (T. Yu and R. B., unpublished data). It is possible that Rb-mediated potentiation of tissue-specific transcription factors may, at least in some cases, be a redundant activity, and that the only critical Rb function is to inhibit E2f. Our study is the first to our knowledge to assess comprehensively whether Rb KO cells can differentiate in the absence of different E2fs. In light of our findings, it will be important to reassess differentiation defects in other Rb KO tissues in the absence of individual and combined activating E2f family members."}

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"subj":"T26556","obj":"T26555"},{"id":"R6608","pred":"_lexicallyChainedTo","subj":"T22775","obj":"T22774"},{"id":"R6609","pred":"_lexicallyChainedTo","subj":"T22805","obj":"T22804"},{"id":"R6610","pred":"_lexicallyChainedTo","subj":"T22860","obj":"T22859"}],"text":"Discussion\n\nRb Controls Retinal Cell Division and Death through E2f1\nWork in the early 1990s showed that Rb loss triggers defects in neuronal cell cycle exit, survival, and differentiation [26–28]. Much of the death is an indirect consequence of probable hypoxia linked to placental defects [12–14]. However, targeted KO and chimeric studies reveal that Rb autonomously promotes cell cycle exit in newborn neurons, and is required for survival of a subset of neurons, particularly in the retina [2,3,13,14,56–59]. However, whether Rb also regulates differentiation is obscured by potentially indirect effects of ectopic division and death. Moreover, a mechanism though which Rb may regulate neuronal maturation has not been elucidated.\nHere, deleting E2f1 specifically rescued ectopic division and death in the Rb KO retina. Importantly, major Rb/E2f1 DKO neurons differentiated normally, and ERGs revealed the rescue of rod- and cone-mediated function, implicating a regular signal flow from photoreceptors to bipolar and amacrine cells. Division and death genes were induced in Rb KO cells, and deleting E2f1, but not E2f2 or E2f3, reversed these molecular events. E2f1 may also regulate differentiation targets, but whether this contributes to defects in retinal cell maturation is impossible to separate from potentially indirect consequences of deregulated division and death. In any case, it is clear that in most retinal cells, including photoreceptors [29], transcription factors that promote differentiation function independently of Rb.\nWe have also found that E2f1 deletion rescues cell-autonomous ectopic division, death, and differentiation defects in sporadic Rb KO clones generated using a Cre retrovirus vector (M. P. and R. B., unpublished data). These data are consistent with the observation that E2f1 overexpression in newborn photoreceptors drives ectopic division and apoptosis [60], and add to the growing evidence indicating that E2f1 is the major, and perhaps only, member of the three activating E2fs required to induce apoptosis in Rb KO cells [10,15]. Thus, deregulated E2f1 activity in the retina, whether resulting from the inactivation of Rb or from overexpression, promotes unscheduled cell division and triggers apoptosis in susceptible RTCs. E2f1, rather than other E2fs, may be a potential target for novel therapeutics to prevent retinoblastoma in RB1 +/− humans.\nOur ERG studies revealed rescue of the Rb KO rod–bipolar system, and almost complete restoration of the cone–bipolar system following E2f1 deletion. There was a slightly lower response in the Rb/E2f1 DKO retina relative to the E2f1 KO control retina. This difference might reflect a role for Rb in the development of cones, bipolar cells, or other cells that may contribute to the photopic ERG, including potentially SACs, which do have a serious defect in the Rb/E2f1 DKO retina.\n\nRb Controls SAC Differentiation through E2f3a\nComprehensive marker analysis revealed that, in striking contrast to other retinal neurons, E2f1 deletion did not suppress defects in Rb KO cholinergic SACs. Instead, we observed E2f1-independent defects in the synthesis and transport of a large cohort of SAC proteins. These data expand insight into the development of these important interneurons, but more critically, provide to our knowledge the first unambiguous evidence that Rb regulates neurogenesis beyond terminal mitosis. Rb binds more than 100 factors [43], and in several non-neuronal cells, such as skeletal muscle, adipocytes, and bone, it binds and potentiates tissue-specific transcription factors that promote differentiation [31–33]. The idea that Rb promotes muscle differentiation by potentiating Myod1 activity was contested [61], and other mechanisms proposed [62,63], but not involving E2f repression. Strikingly, however, we discovered that Rb promotes SAC differentiation through E2f3 (Figure 8).\nFigure 8 Rb Regulates Distinct Processes through E2f1 and E2f3a\nRed text and arrows indicate Rb-dependent events. Black text and arrows indicate events for which there is no direct evidence of Rb involvement. Rb does not appear to temper RPC expansion and is not required for differentiation of RPCs into RTCs, but is essential to couple RTC birth to terminal mitosis, thus locking them out of cycle. Rb performs this function by inhibiting E2f1. Rb is also required for SAC differentiation, and in this case, acts by inhibiting E2f3a. There is no direct evidence that Rb is required for terminal differentiation of other cell types. Colour codes and abbreviations as in Figure 1A. Rb regulation of SAC differentiation through E2f3 was independent of its role in controlling division or death: E2f3 deletion rescued Rb KO SAC defects but did not suppress aberrant proliferation or death, whereas E2f1 deletion reversed abnormal proliferation and death but did not rescue SAC differentiation. Double labelling confirmed that E2f1 but not E2f3 deletion reversed Rb KO SAC division. Moreover, deleting E2f1, but not E2f3, reversed deregulated expression of cell cycle and apoptotic genes in the Rb KO retina. E2f3 is expressed in a subset of CNS neurons (this work) and drives specific cell-cycle–independent defects in Rb KO forebrain neurons [53]. Thus, E2f3 inhibition is the first, and may be the only, mechanism by which Rb participates directly in neuronal differentiation.\nTo further dissect the mechanism of action of Rb in SACs we determined the E2f3 isoform it targets to promote differentiation. E2f3b was the primary candidate, since Rb and E2f3b collaborate to repress targets in quiescent cells in vitro [19]. However, in the first work to our knowledge to examine the function of any E2f protein isoform in vivo, we made the surprising observation that Rb regulates SAC differentiation through E2f3a (Figure 8). Formally, we cannot exclude the possibility that deleting E2f3b might also rescue SAC differentiation, but definitive proof will require analysis of E2f3b null mice. Nevertheless, our data prove that Rb definitely regulates SAC differentiation through the activating E2f3 isoform.\n\nDistinct E2f3a and E2f3b Localization\nThe subcellular location of E2f isoforms has not to our knowledge been addressed before. E2f3a and E2f3b share 110 C-terminal amino acids that encode the NLS, DNA-binding, marked box, transactivation, and Rb-binding domains [16], yet they exhibit different subcellular distribution in developing retinal cells. E2f3a is both nuclear and cytoplasmic, but E2f3b is always nuclear. The unique 121- and six-residue N-termini of E2f3a and E2f3b, respectively, likely mediate this difference. This region in E2f1, E2f2, and E2f3a binds Ccna2, establishing a negative regulatory loop that deactivates E2fs in mid-late S-phase [64,65]. However, even E2f3b, which lacks this domain, binds and is regulated by Ccna2 [18], so the domain difference may not explain the unique distributions we observed. Rb family and Tfdp proteins can also determine E2f localization [20–22], and we found that a portion of both Rb and Tfdp1 proteins are cytoplasmic in retinal cells. Indeed, immunostaining revealed that Rb and E2f3 colocalize to SAC processes.\nThe nuclear localization of E2f3b contrasts with that of other repressive E2fs in differentiating muscle, where E2f5 switches from the nucleus to cytoplasm, while E2f4 remains in both compartments [23]. The distinct compartmentalization of E2f3a and E2f3b in the retina suggests temporally and functionally distinct activities. Rb distribution matches that of E2f3a, consistent with its critical role in supporting SAC differentiation through E2f3a.\n\nEctopic Division and Differentiation\nRb is critical to ensure that many types of terminally differentiating cells leave the cell cycle (e.g., neurons, gut and skin epithelia, muscle, and lens fibres) (reviewed in [66]). Early overexpression studies in vitro suggested Rb might temper expansion of cycling cells, but KO studies in vivo indicate that its major role is to block division in terminally differentiating cells. In its absence, many (but clearly not all) aspects of differentiation go ahead relatively unperturbed. In the retina, differentiating transition cells are born in the absence of Rb, migrate to the correct layer, and express appropriate markers ([2] and this work). In brain, Rb KO neurons migrate away from the ventricular zone and switch on Tubb3 (βIII-tubulin), but continue to incorporate BrdU [13], and in gut epithelia, differentiated enterocytes migrate up the villi and activate expression of serotonin, yet continue to incorporate BrdU [67]. In the case of SACs, the differentiation defects we observed (e.g., loss of Slc18a3 and Chat) were not due to aberrant division, but it is possible there are other problems with these cells that are caused by ectopic division. Nevertheless, it is clear that many aspects of differentiation in multiple cell types are compatible with ectopic division. However, division of terminally differentiating cells is dangerous, since it may facilitate transformation, as is the case in retinoblastoma (reviewed in [66]).\n\nHow Does E2f3a Perturb SAC Differentiation?\nE2f3a could disrupt SAC differentiation through its well known role as a transcriptional activator, or, in view of the discovery that it is partially cytoplasmic, E2f3a may affect processes other than gene regulation. Both scenarios are feasible since E2fs regulate differentiation genes [44–48], and cell cycle regulators, such as Cdkn1b, have cytoplasmic activities that influence differentiation [68,69]. Many transcription factors shuttle between nucleus and cytoplasm during neurogenesis (e.g., [70] and references therein). It may be difficult to identify E2f3a-specific target genes or cytoplasmic proteins in SACs since these neurons are a small proportion (\u003c1%) of the total retina and only ~5.2% of amacrine neurons [38].\n\nDo E2fs Mediate All Rb Functions?\nOthers have suggested that Rb promotes differentiation in non-neuronal cells through E2f-independent means [31–33]. However, these studies did not assess whether these cell types differentiate normally if Rb is deleted along with one or more E2f family members. One study reported that Rb mutants that do not bind E2f still induce differentiation [30]. However, the binding assays were performed in solution, and we have found that several of these mutants do bind E2f, albeit weakly, on chromatin (T. Yu and R. B., unpublished data). It is possible that Rb-mediated potentiation of tissue-specific transcription factors may, at least in some cases, be a redundant activity, and that the only critical Rb function is to inhibit E2f. Our study is the first to our knowledge to assess comprehensively whether Rb KO cells can differentiate in the absence of different E2fs. In light of our findings, it will be important to reassess differentiation defects in other Rb KO tissues in the absence of individual and combined activating E2f family members."}

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Controls Retinal Cell Division and Death through E2f1\nWork in the early 1990s showed that Rb loss triggers defects in neuronal cell cycle exit, survival, and differentiation [26–28]. Much of the death is an indirect consequence of probable hypoxia linked to placental defects [12–14]. However, targeted KO and chimeric studies reveal that Rb autonomously promotes cell cycle exit in newborn neurons, and is required for survival of a subset of neurons, particularly in the retina [2,3,13,14,56–59]. However, whether Rb also regulates differentiation is obscured by potentially indirect effects of ectopic division and death. Moreover, a mechanism though which Rb may regulate neuronal maturation has not been elucidated.\nHere, deleting E2f1 specifically rescued ectopic division and death in the Rb KO retina. Importantly, major Rb/E2f1 DKO neurons differentiated normally, and ERGs revealed the rescue of rod- and cone-mediated function, implicating a regular signal flow from photoreceptors to bipolar and amacrine cells. Division and death genes were induced in Rb KO cells, and deleting E2f1, but not E2f2 or E2f3, reversed these molecular events. E2f1 may also regulate differentiation targets, but whether this contributes to defects in retinal cell maturation is impossible to separate from potentially indirect consequences of deregulated division and death. In any case, it is clear that in most retinal cells, including photoreceptors [29], transcription factors that promote differentiation function independently of Rb.\nWe have also found that E2f1 deletion rescues cell-autonomous ectopic division, death, and differentiation defects in sporadic Rb KO clones generated using a Cre retrovirus vector (M. P. and R. B., unpublished data). These data are consistent with the observation that E2f1 overexpression in newborn photoreceptors drives ectopic division and apoptosis [60], and add to the growing evidence indicating that E2f1 is the major, and perhaps only, member of the three activating E2fs required to induce apoptosis in Rb KO cells [10,15]. Thus, deregulated E2f1 activity in the retina, whether resulting from the inactivation of Rb or from overexpression, promotes unscheduled cell division and triggers apoptosis in susceptible RTCs. E2f1, rather than other E2fs, may be a potential target for novel therapeutics to prevent retinoblastoma in RB1 +/− humans.\nOur ERG studies revealed rescue of the Rb KO rod–bipolar system, and almost complete restoration of the cone–bipolar system following E2f1 deletion. There was a slightly lower response in the Rb/E2f1 DKO retina relative to the E2f1 KO control retina. This difference might reflect a role for Rb in the development of cones, bipolar cells, or other cells that may contribute to the photopic ERG, including potentially SACs, which do have a serious defect in the Rb/E2f1 DKO retina.\n\nRb Controls SAC Differentiation through E2f3a\nComprehensive marker analysis revealed that, in striking contrast to other retinal neurons, E2f1 deletion did not suppress defects in Rb KO cholinergic SACs. Instead, we observed E2f1-independent defects in the synthesis and transport of a large cohort of SAC proteins. These data expand insight into the development of these important interneurons, but more critically, provide to our knowledge the first unambiguous evidence that Rb regulates neurogenesis beyond terminal mitosis. Rb binds more than 100 factors [43], and in several non-neuronal cells, such as skeletal muscle, adipocytes, and bone, it binds and potentiates tissue-specific transcription factors that promote differentiation [31–33]. The idea that Rb promotes muscle differentiation by potentiating Myod1 activity was contested [61], and other mechanisms proposed [62,63], but not involving E2f repression. Strikingly, however, we discovered that Rb promotes SAC differentiation through E2f3 (Figure 8).\nFigure 8 Rb Regulates Distinct Processes through E2f1 and E2f3a\nRed text and arrows indicate Rb-dependent events. Black text and arrows indicate events for which there is no direct evidence of Rb involvement. Rb does not appear to temper RPC expansion and is not required for differentiation of RPCs into RTCs, but is essential to couple RTC birth to terminal mitosis, thus locking them out of cycle. Rb performs this function by inhibiting E2f1. Rb is also required for SAC differentiation, and in this case, acts by inhibiting E2f3a. There is no direct evidence that Rb is required for terminal differentiation of other cell types. Colour codes and abbreviations as in Figure 1A. Rb regulation of SAC differentiation through E2f3 was independent of its role in controlling division or death: E2f3 deletion rescued Rb KO SAC defects but did not suppress aberrant proliferation or death, whereas E2f1 deletion reversed abnormal proliferation and death but did not rescue SAC differentiation. Double labelling confirmed that E2f1 but not E2f3 deletion reversed Rb KO SAC division. Moreover, deleting E2f1, but not E2f3, reversed deregulated expression of cell cycle and apoptotic genes in the Rb KO retina. E2f3 is expressed in a subset of CNS neurons (this work) and drives specific cell-cycle–independent defects in Rb KO forebrain neurons [53]. Thus, E2f3 inhibition is the first, and may be the only, mechanism by which Rb participates directly in neuronal differentiation.\nTo further dissect the mechanism of action of Rb in SACs we determined the E2f3 isoform it targets to promote differentiation. E2f3b was the primary candidate, since Rb and E2f3b collaborate to repress targets in quiescent cells in vitro [19]. However, in the first work to our knowledge to examine the function of any E2f protein isoform in vivo, we made the surprising observation that Rb regulates SAC differentiation through E2f3a (Figure 8). Formally, we cannot exclude the possibility that deleting E2f3b might also rescue SAC differentiation, but definitive proof will require analysis of E2f3b null mice. Nevertheless, our data prove that Rb definitely regulates SAC differentiation through the activating E2f3 isoform.\n\nDistinct E2f3a and E2f3b Localization\nThe subcellular location of E2f isoforms has not to our knowledge been addressed before. E2f3a and E2f3b share 110 C-terminal amino acids that encode the NLS, DNA-binding, marked box, transactivation, and Rb-binding domains [16], yet they exhibit different subcellular distribution in developing retinal cells. E2f3a is both nuclear and cytoplasmic, but E2f3b is always nuclear. The unique 121- and six-residue N-termini of E2f3a and E2f3b, respectively, likely mediate this difference. This region in E2f1, E2f2, and E2f3a binds Ccna2, establishing a negative regulatory loop that deactivates E2fs in mid-late S-phase [64,65]. However, even E2f3b, which lacks this domain, binds and is regulated by Ccna2 [18], so the domain difference may not explain the unique distributions we observed. Rb family and Tfdp proteins can also determine E2f localization [20–22], and we found that a portion of both Rb and Tfdp1 proteins are cytoplasmic in retinal cells. Indeed, immunostaining revealed that Rb and E2f3 colocalize to SAC processes.\nThe nuclear localization of E2f3b contrasts with that of other repressive E2fs in differentiating muscle, where E2f5 switches from the nucleus to cytoplasm, while E2f4 remains in both compartments [23]. The distinct compartmentalization of E2f3a and E2f3b in the retina suggests temporally and functionally distinct activities. Rb distribution matches that of E2f3a, consistent with its critical role in supporting SAC differentiation through E2f3a.\n\nEctopic Division and Differentiation\nRb is critical to ensure that many types of terminally differentiating cells leave the cell cycle (e.g., neurons, gut and skin epithelia, muscle, and lens fibres) (reviewed in [66]). Early overexpression studies in vitro suggested Rb might temper expansion of cycling cells, but KO studies in vivo indicate that its major role is to block division in terminally differentiating cells. In its absence, many (but clearly not all) aspects of differentiation go ahead relatively unperturbed. In the retina, differentiating transition cells are born in the absence of Rb, migrate to the correct layer, and express appropriate markers ([2] and this work). In brain, Rb KO neurons migrate away from the ventricular zone and switch on Tubb3 (βIII-tubulin), but continue to incorporate BrdU [13], and in gut epithelia, differentiated enterocytes migrate up the villi and activate expression of serotonin, yet continue to incorporate BrdU [67]. In the case of SACs, the differentiation defects we observed (e.g., loss of Slc18a3 and Chat) were not due to aberrant division, but it is possible there are other problems with these cells that are caused by ectopic division. Nevertheless, it is clear that many aspects of differentiation in multiple cell types are compatible with ectopic division. However, division of terminally differentiating cells is dangerous, since it may facilitate transformation, as is the case in retinoblastoma (reviewed in [66]).\n\nHow Does E2f3a Perturb SAC Differentiation?\nE2f3a could disrupt SAC differentiation through its well known role as a transcriptional activator, or, in view of the discovery that it is partially cytoplasmic, E2f3a may affect processes other than gene regulation. Both scenarios are feasible since E2fs regulate differentiation genes [44–48], and cell cycle regulators, such as Cdkn1b, have cytoplasmic activities that influence differentiation [68,69]. Many transcription factors shuttle between nucleus and cytoplasm during neurogenesis (e.g., [70] and references therein). It may be difficult to identify E2f3a-specific target genes or cytoplasmic proteins in SACs since these neurons are a small proportion (\u003c1%) of the total retina and only ~5.2% of amacrine neurons [38].\n\nDo E2fs Mediate All Rb Functions?\nOthers have suggested that Rb promotes differentiation in non-neuronal cells through E2f-independent means [31–33]. However, these studies did not assess whether these cell types differentiate normally if Rb is deleted along with one or more E2f family members. One study reported that Rb mutants that do not bind E2f still induce differentiation [30]. However, the binding assays were performed in solution, and we have found that several of these mutants do bind E2f, albeit weakly, on chromatin (T. Yu and R. B., unpublished data). It is possible that Rb-mediated potentiation of tissue-specific transcription factors may, at least in some cases, be a redundant activity, and that the only critical Rb function is to inhibit E2f. Our study is the first to our knowledge to assess comprehensively whether Rb KO cells can differentiate in the absence of different E2fs. In light of our findings, it will be important to reassess differentiation defects in other Rb KO tissues in the absence of individual and combined activating E2f family members."}