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used gene targeting in ES cells to delete exon 3 in the Chaf1a gene, which encodes p150CAF-1 (Figure 1A). Chaf1a +/− mice were born at a Mendelian frequency, were of normal size and weight, displayed no obvious abnormalities, and were fertile. Crossing heterozygous mice failed to generate viable newborn Chaf1a −/− mice. Furthermore, no homozygous Chaf1a −/− embryos were detected at any of the post-implantation stages. However, we could detect Chaf1a −/− embryos at embryonic day 4 (E4) using a PCR strategy (Figure 1B). They represent only 10% of E4 embryos obtained from Chaf1a +/− mice intercrosses, suggesting that more than half of the homozygous mutant embryos had degenerated before this stage. Moreover, mutant embryos contained only eight to 16 cells at the E4 stage, instead of 32 cells observed for wild-type or heterozygous blastocysts (Figure 1C and 1D). Further analysis by light microscopy using immunofluorescence (IF) allowed us to compare wild-type and p150CAF-1-depleted embryos. A loss of p150CAF-1 staining could not be detected before the eight-cell stage (unpublished data) suggesting that maternally contributed protein is present in the embryo up to the four-cell stage. Thus, depletion of p150CAF-1 protein from this stage allows a maximum of two additional cell divisions before developmental arrest.\nFigure 1 Loss of p150CAF-1 Function Leads to Early Developmental Arrest and Alteration of Heterochromatin Organization\n(A) Generation of Chaf1a +/− mice by homologous recombination in ES cells. (Top) Scheme of the p150CAF1 protein indicating the interacting domains (ID) for HP1 and p60CAF-1, and the acidic domain (AD). (Middle) Structure of the murine Chaf1a gene. Blocks and lines represent exons and introns, respectively. A star indicates the translation initiation site. Below is shown the Chaf1a targeting vector, which includes genomic DNA homology regions (5 HR and 3 HR), the diphtheria toxin (DT), and neomycin selection genes. Recombined (Rec) ES cells and mice were identified by Southern blot using ScaI (S) and the indicated probe.\n(B) Breeding strategy used for the production of E4 Chaf1a −/− embryos. Genotyping was performed by PCR using the three oligonucleotide primers indicated in (A) (1, 2, and 3). An example of the result of a genotyping experiment is shown.\n(C) Immunodetection of p150CAF-1 (green) and HP1α (red) in E4 embryos derived from Chaf1a +/− intercrosses. Because Chaf1a +/+ and Chaf1a +/− embryos both stain positively for the presence of p150CAF-1, they are both designated as wild-type. p150CAF-1 expression, which indicates ongoing S phase, can be detected in most cells within the wild-type blastocyst (upper panel). The lower panel shows a 12-cell embryo labeling negatively for p150CAF-1. Only nonspecific background labeling can be observed. In each panel, the right-hand image shows the merge between the HP1α fluorescence and DAPI-stained DNA in blue. Pink color indicates the association of HP1 with DAPI-dense material. The bottom of each panel shows the magnification of a nucleus selected from the above embryo (white square). The arrowhead indicates the typical heterochromatin foci revealed by DAPI and HP1α staining in wild-type embryos. These foci are not visible in Chaf1a −/− embryos. DAPI and HP1α staining are diffuse within the nucleus of p150CAF-1-depleted embryos, with enrichment at the nuclear periphery, revealing abnormal heterochromatin organization. Scale bars represent 10 μm.\n(E) Wild-type embryos isolated at embryonic day 2 (E2, two cells), E2.5 (four cells), E3 (eight cells), E3.5 (16 cells), and E4 (32 cells) are shown. Heterochromatin was monitored by DAPI staining (upper panel) and HP1 immunolabeling (in red, lower panel).\n(F) Magnification of a nucleus (DAPI-stained) representative of each stage. The right-hand panel shows the nucleus of an ES cell. Scale bar represents 10 μm. Strikingly, we found that the nuclear organization of heterochromatin appeared abnormal in the nuclei of Chaf1a −/− embryos. Pericentric heterochromatin, the major component of constitutive heterochromatin, can easily be visualized in interphase nuclei by the fluorochrome DAPI and by immunostaining with HP1α [16,17–19]. In wild-type blastocysts and in mouse somatic cells, pericentric heterochromatin domains cluster together and form higher-order chromatin structures called chromocenters [20], which are visualized as DAPI-dense foci (Figure 1C). These structures were not detected in Chaf1a −/− embryos (Figure 1D). Since chromatin architecture and higher-order structures are important for genome function [21], we decided to characterize this phenotype in more detail. For this purpose, we examined the status of heterochromatin organization between the two-cell and blastocyst stages. In two-cell stage wild-type embryos, DAPI staining is diffuse and fibrillar, with regions of higher density around the nucleolar precursor bodies (Figure 1E). Heterochromatin domains are progressively assembled into DAPI-dense foci between the four-cell and 32-cell blastocyst stages (Figure 1F). Localization of HP1α confirmed that the structures visualized by DAPI staining correspond to constitutive heterochromatin (Figure 1E). Thus, the nuclear organization of heterochromatin is dramatically modified during pre-implantation development, between the two-cell and blastocyst stages. In Chaf1a −/− E4 embryos, which are arrested between the eight- and 16-cell stage, DAPI-dense foci were barely detectable (Figure 1D). Instead, DAPI staining was diffuse within the nucleus, with regions of higher density around the nucleoli and at the periphery of the nuclei (Figure 1D). Localization of HP1α showed a diffuse pattern similar to the DAPI, with some enrichment at the nuclear periphery, and around the nucleoli (Figure 1D). This abnormal organization of heterochromatin in Chaf1a −/− embryos is reminiscent of the heterochromatin organization found in two- to four-cell stage wild-type embryos (compare Figure 1D and 1F). These data evidence a key role for p150CAF-1 during pre-implantation development, and reveal that this protein is required for the proper 3-D organization of heterochromatin within embryonic cell nuclei.\nNext, we wondered whether a similar requirement for CAF-1 could also be observed in ES cells, which are derived from the blastocyst inner cell mass. Given the early developmental arrest observed in Chaf1a −/− embryos, such cells could not be derived directly from null embryos, and we thus used an RNAi strategy (Figure 2A). p150CAF-1 knockdown in ES cells was quantified by Western blot analysis and IF. (Figure S1). p150CAF-1 RNAi-depleted ES cells displayed a phenotype very similar to the cells of Chaf1a −/− E4 mice. DAPI-dense foci were lost, and we observed diffuse HP1α and DAPI staining around the nucleoli and at the periphery of the nucleus (Figure 2B). This result indicates that p150CAF-1 is essential for nuclear organization of heterochromatin in ES cells in a similar way to early pre-implantation embryos. Surprisingly, we did not observe this severe alteration in heterochromatin organization in primary mouse embryonic fibroblasts (MEFs) following p150CAF-1 depletion by RNAi. p150CAF-1 depletion in MEFs resulted in a strong inhibition of cell proliferation (unpublished data), but did not alter the clustering of heterochromatin domains (Figures 2C and S2). Similarly, p150CAF-1 depletion in 3T3 cells did not affect heterochromatin organization [16]. These observations reveal a specific function for CAF-1 in the early embryo and ES cells.\nFigure 2 Depletion of p150CAF-1 in ES Cells Results in a Severe Alteration of Heterochromatin Organization\n(A) Strategy used to deplete p150CAF-1 by RNAi in ES cells. The siRNA expression vector includes a puromycin selection cassette (Puro), the mouse H1 promoter, and the siRNA encoding sequence. ES cells were kept under puromycin selection during 48 h following transfection.\n(B) Abnormal heterochromatin organization in p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 (green) and HP1α (red) in ES cells transfected with control (cont) and p150CAF-1 siRNA. siRNA expression results in efficient p150CAF-1 depletion. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue. Scale bar = 10 μm.\n(C) Heterochromatin organization is not altered in p150CAF-1-depleted MEFs. Immunodetection of p150CAF-1 (green) and HP1α (red) in MEFs transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue.\n(D) PML bodies are not altered in p150CAF-1-depleted ES cells. Immunodetection of PML (red) in ES cells transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between PML fluorescence and DAPI-stained DNA in blue. We also wondered whether loss of p150CAF-1 in ES cells specifically affects the heterochromatin nuclear subcompartment, or whether it might result in a more global loss of nuclear organization and architecture. We used a specific antibody against the promyelocytic leukemia (PML) protein to study the fate of the PML nuclear bodies, which are well-characterized subnuclear structures [22]. We could not detect any significant difference in the distribution and aspect of PML nuclear bodies between control and p150CAF-1-depleted ES cells (Figure 2D). These data show that nuclear architecture is not globally altered following CAF-1 loss-of-function. In addition, Western blot analysis revealed that CAF-1 depletion did not result in altered levels of chromatin architectural proteins such as histone H3 and HP1α (Figure S1). Thus, CAF-1 is specifically required in early embryos and in ES cells for the proper organization of the heterochromatin subnuclear compartment.\nPrevious studies performed in mammalian cell lines showed that CAF-1 activity is required for S phase progression [16,23,24]. We show here that 3 d after transfection of the RNAi vector, p150CAF-1-depleted cells (identified by a complete absence of CAF-1 IF signal) appear still active for replication, as revealed by incorporation of the thymidine analog bromodeoxyuridine (BrdU) (Figure 3A), the PCNA (proliferating cell nuclear antigen) pattern (Figure 3B), and flow cytometry analysis (Figure 3C). Hence, in these cells, DNA replication persists despite the drastic changes in heterochromatin organization. However, 24 h later, ES cells cease to proliferate and die, revealing that p150CAF-1 is required for an essential cellular process, as in embryos. Altogether, our data demonstrate that loss of p150CAF-1 function in ES cells and early embryos alters first the organization of heterochromatin in the nucleus and, in a subsequent step, cell cycle and viability.\nFigure 3 p150CAF-1 Depletion and Loss of Heterochromatin Organization Are Compatible with Active DNA Replication in ES Cells\n(A) ES cells were transfected with p150CAF-1 or control siRNA vectors. After 3 d under puromycin selection, cells were pulse-labeled for 10 min with BrdU and immediately analyzed by IF. No significant difference in BrdU incorporation could be detected between control and p150CAF-1-depleted cells. The right-hand image shows the merge between the p150CAF-1 and BrdU fluorescence. Scale bar = 10 μm.\n(B) Immunodetection of PCNA (red) revealed no significant difference in the formation of replication foci between control and p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 is shown in green and the merging of p150CAF-1 and PCNA appears in yellow.\n(C) Flow cytometry analysis showed a similar cell-cycle profile for control and p150CAF-1-depleted ES cells. Results are presented as the percentage of cells in each phase of the cell cycle (G1, S, G2/M), as defined by BrdU incorporation and DNA content. Data presented are the mean of three independent experiments; error bars indicate the standard deviation. All experiments were performed 3 d after transfection of the siRNA vectors. In order to better characterize the defects in heterochromatin organization, we performed two-color DNA fluorescence in situ hybridization (FISH) experiments to reveal the spatial distribution of pericentric and centric chromosomal regions, which in mouse are mainly composed of large blocks of major and minor satellite repeats, respectively [20]. Pericentric domains from different chromosomes form clusters, which are revealed by FISH as large spots that coincide with DAPI-dense foci in the interphase nucleus (Figure 4A). At the periphery of each pericentric domain, centric regions form individual entities (Figure 4A). In p150CAF-1 RNAi-depleted cells, we observed a disruption of pericentric heterochromatin clusters that coincides with the disappearance of DAPI-dense foci (Figure 4B). Individual pericentric domains from single chromosomes are now found either isolated or aggregated in a pattern less dense than the regular clusters observed in control cells (Figure 4B). Such aggregates, which are often found at the nuclear periphery, are also revealed by DAPI staining as a typical signature of p150CAF-1 loss-of-function. Quantification of fluorescence along a line randomly drawn across the nucleus revealed lower fluorescence intensity and a broader distribution of DAPI and major satellite hybridization signals in p150CAF-1-depleted cells (Figure 4C and 4D), indicating decondensation of pericentric heterochromatin domains. In contrast, centric domains showed an intensity and shape similar to control cells, suggesting that they remain unaffected by p150CAF-1 depletion (Figure 4C and 4D). In conclusion, these results show that p150CAF-1 is required for the proper condensation and clustering of pericentric heterochromatin domains.\nFigure 4 Depletion of p150CAF-1 Leads to Loss of Clustering, Altered Localization, and Decondensation of Pericentric Heterochromatin Domains\nDistribution of pericentric (red) and centric (green) domains was analyzed in the interphase nuclei of mouse ES cells by DNA FISH, using major satellite (pSAT) [47] and minor satellite (pMR150) [48] DNA probes, respectively. (A) In ES cells expressing control (cont) siRNA, pericentric regions from several chromosomes associate in clusters (red). These chromocenters form foci as revealed by DAPI staining (left-hand image), while centric regions (green) remain independent entities at the periphery of these domains. The right-hand image shows the merge between the pericentric and centric FISH signals.\n(B) The organization of pericentric domains was altered in cells expressing p150CAF-1 siRNA. Instead of forming well-defined chromocenters, pericentric domains were found either isolated or associated in heterogeneous aggregates of various sizes, often at the nuclear periphery. Scale bar = 10 μm.\n(C) Control ES cells. Fluorescence was quantified along a line randomly drawn across the nucleus in the merged image and data were plotted. One can distinguish clear peaks corresponding to chromocenters (red) and the condensed minor satellites (green).\n(D) ES cells expressing p150CAF-1 siRNA. p150CAF-1 depletion led to a lower fluorescence intensity and a broader distribution of signals corresponding to DAPI (blue) and major satellite hybridization (red, plot) while the organization of the minor satellites remained unaffected. Insets in the right-hand images show a typical chromocenter in control cells (C) and a disrupted chromocenter in p150CAF-1-depleted cells (D). Given the known role of CAF-1 in the deposition of histone H3.1 and H4 associated with DNA synthesis [11,12], we wondered whether this defect in higher-order chromatin organization could reflect an aberrant nucleosomal organization. Using DNase I and micrococcal nuclease (MNase) assays, we could not observe any significant difference between control and p150CAF-1-depleted ES cells at the level of bulk genome chromatin or at pericentric repeats (Figure 5). In a second series of experiments, we compared the association of histone H3 with chromatin in nuclei isolated from cells transfected with control and p150CAF-1 RNAi plasmid vectors. Nuclei were incubated in buffers with different salt concentrations ranging from 100 mM NaCl to 1 M NaCl. In all conditions, the amount of histone H3 remaining associated with chromatin was indistinguishable in control and p150CAF-1-depleted ES cells (unpublished data). Therefore, the loss of clustering and decondensation of pericentric heterochromatin are unlikely to be the consequence of severe defects in nucleosomal organization.\nFigure 5 Nucleosomal Organization Is Not Altered in p150CAF-1-Depleted ES Cells\nNuclei were prepared from ES cells transfected with control or p150CAF-1 siRNA vector. Nuclei were digested with increasing amounts of DNase I or MNase. (A) After digestion with the indicated nucleases, total DNA was prepared and run onto an agarose gel which was stained with ethidium bromide to reveal bulk genomic DNA.\n(B) The DNA was blotted onto a nylon membrane, which was then hybridized with the α-32P-labeled pSAT major satellite repeat probe [47]. Our findings showed that the nuclear localization of HP1α is severely altered in Chaf1a −/− embryos and p150CAF-1-depleted ES cells. We therefore examined the status of other epigenetic marks previously shown to characterize pericentric heterochromatin. We first tested DNA CpG methylation [25] at major satellite repeats and found no significant difference between control and p150CAF-1-depleted cells (Figure 6). As the LTM7 ES cell line that we used in our RNAi experiments is a female (XX) cell line, DNA methylation is globally reduced in these cells [26]. To rule out the possibility that hypomethylation of pericentric repeats might contribute to the destabilization of heterochromatin domains in p150CAF-1-depleted ES cells, we tested our RNAi plasmid vector in a XY ES cell line, and confirmed that loss of p150CAF-1 leads to disruption of heterochromatin organization independently of the degree of DNA methylation at pericentric repeats (unpublished data). We next analyzed specific histone modifications [27] in chromatin immunoprecipitation (ChIP) experiments using native chromatin [28]. We found that pericentric DNA was immunoprecipitated with a 2-fold lower efficiency with H4K20me3 [29,30] antibodies following p150CAF-1 depletion (Figure 7A and 7B). Immunoprecipitation of minor satellite repeats in the same experiment was less affected (Figure 7B), showing that loss of p150CAF-1 function mainly affects H4K20me3 at pericentric heterochromatin. Moreover, no significant difference in immunoprecipitation efficiency was detected at intracisternal A particle (IAP) elements (Figure 7B), which are noncentromeric repeated DNA elements also enriched in H4K20me3 [31]. This result shows that p150CAF-1 contributes to normal levels of H4K20me3 at pericentric heterochromatin, but not necessarily at other loci. The H3K9me3 mark [32] was also significantly reduced in p150CAF-1-depleted cells, though to a lesser extent than H4K20me3 (Figure 7A and 7B).\nFigure 6 DNA CpG Methylation at Pericentric Heterochromatin Is Not Altered in p150CAF-1-Depleted ES Cells\nTotal DNA was isolated from cells transfected with a control or the p150CAF-1 siRNA vector and digested with MaeII, whose recognition sequence is present in major satellite repeats. Digested DNA was run onto an agarose gel and analyzed by Southern blotting using the pSAT major satellite probe [47].\nFigure 7 Alteration of Epigenetic Marking at Pericentric Heterochromatin in p150CAF-1-Depleted Cells\n(A) p150CAF-1 depletion leads to reduced H4K20me3 and H3K9me3 at pericentric heterochromatin. Enrichment of histone marks at major satellite repeats was determined by ChIP from control (cont) and p150CAF-1 (p150) siRNA-expressing ES cells. DNA prepared from the input and the antibody-bound fraction were run onto an agarose gel and analyzed by Southern blot with the pSAT major satellite repeat probe [47].\n(B) Hybridization signals were quantified using an Instant Imager. After autoradiography, the membrane was stripped and rehybridized with a minor satellite probe [49]. After quantification, the membrane was stripped and rehybridized with an IAP LTR probe [50]. Results are presented as the amount of DNA immunoprecipitated from p150CAF-1-depleted ES cells divided by the DNA obtained from control cells. The figure shows the mean value and standard deviation of three independent ChIP experiments.\n(C and D) H3K9me3 and H4K20me3 fluorescence patterns are severely altered in p150CAF-1-depleted ES cells. Immunodetection of H3K9me3 (C, green), H4K20me3 (D, green), and HP1α (red) in control and p150CAF-1 siRNA-expressing ES cells. Merging of HP1α with H3K9me3 (C) and H4K20me3 (D) is shown in yellow. Scale bars represent 10 μm. In wild-type cells, most of H4K20me3 and H3K9me3 signals are present at the level of DAPI-dense domains when visualized by IF [29] (Figures 7C and 7D). H3K9me3 was severely perturbed in p150CAF-1-depleted cells, displaying a diffuse pattern similar to HP1α (Figure 7C). The H4K20me3 pattern was even more severely altered, showing both a loss of the typical dots revealed in control cells and a reduction in signal intensity (Figure 7D). Consistent with our ChIP experiments, residual H4K20me3 epitopes were detected at the level of relocated DAPI-dense material. Altogether, our results show that depletion of CAF-1 in ES cells leads to a simultaneous disruption of heterochromatin 3-D organization and an alteration in epigenetic marking."}

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used gene targeting in ES cells to delete exon 3 in the Chaf1a gene, which encodes p150CAF-1 (Figure 1A). Chaf1a +/− mice were born at a Mendelian frequency, were of normal size and weight, displayed no obvious abnormalities, and were fertile. Crossing heterozygous mice failed to generate viable newborn Chaf1a −/− mice. Furthermore, no homozygous Chaf1a −/− embryos were detected at any of the post-implantation stages. However, we could detect Chaf1a −/− embryos at embryonic day 4 (E4) using a PCR strategy (Figure 1B). They represent only 10% of E4 embryos obtained from Chaf1a +/− mice intercrosses, suggesting that more than half of the homozygous mutant embryos had degenerated before this stage. Moreover, mutant embryos contained only eight to 16 cells at the E4 stage, instead of 32 cells observed for wild-type or heterozygous blastocysts (Figure 1C and 1D). Further analysis by light microscopy using immunofluorescence (IF) allowed us to compare wild-type and p150CAF-1-depleted embryos. A loss of p150CAF-1 staining could not be detected before the eight-cell stage (unpublished data) suggesting that maternally contributed protein is present in the embryo up to the four-cell stage. Thus, depletion of p150CAF-1 protein from this stage allows a maximum of two additional cell divisions before developmental arrest.\nFigure 1 Loss of p150CAF-1 Function Leads to Early Developmental Arrest and Alteration of Heterochromatin Organization\n(A) Generation of Chaf1a +/− mice by homologous recombination in ES cells. (Top) Scheme of the p150CAF1 protein indicating the interacting domains (ID) for HP1 and p60CAF-1, and the acidic domain (AD). (Middle) Structure of the murine Chaf1a gene. Blocks and lines represent exons and introns, respectively. A star indicates the translation initiation site. Below is shown the Chaf1a targeting vector, which includes genomic DNA homology regions (5 HR and 3 HR), the diphtheria toxin (DT), and neomycin selection genes. Recombined (Rec) ES cells and mice were identified by Southern blot using ScaI (S) and the indicated probe.\n(B) Breeding strategy used for the production of E4 Chaf1a −/− embryos. Genotyping was performed by PCR using the three oligonucleotide primers indicated in (A) (1, 2, and 3). An example of the result of a genotyping experiment is shown.\n(C) Immunodetection of p150CAF-1 (green) and HP1α (red) in E4 embryos derived from Chaf1a +/− intercrosses. Because Chaf1a +/+ and Chaf1a +/− embryos both stain positively for the presence of p150CAF-1, they are both designated as wild-type. p150CAF-1 expression, which indicates ongoing S phase, can be detected in most cells within the wild-type blastocyst (upper panel). The lower panel shows a 12-cell embryo labeling negatively for p150CAF-1. Only nonspecific background labeling can be observed. In each panel, the right-hand image shows the merge between the HP1α fluorescence and DAPI-stained DNA in blue. Pink color indicates the association of HP1 with DAPI-dense material. The bottom of each panel shows the magnification of a nucleus selected from the above embryo (white square). The arrowhead indicates the typical heterochromatin foci revealed by DAPI and HP1α staining in wild-type embryos. These foci are not visible in Chaf1a −/− embryos. DAPI and HP1α staining are diffuse within the nucleus of p150CAF-1-depleted embryos, with enrichment at the nuclear periphery, revealing abnormal heterochromatin organization. Scale bars represent 10 μm.\n(E) Wild-type embryos isolated at embryonic day 2 (E2, two cells), E2.5 (four cells), E3 (eight cells), E3.5 (16 cells), and E4 (32 cells) are shown. Heterochromatin was monitored by DAPI staining (upper panel) and HP1 immunolabeling (in red, lower panel).\n(F) Magnification of a nucleus (DAPI-stained) representative of each stage. The right-hand panel shows the nucleus of an ES cell. Scale bar represents 10 μm. Strikingly, we found that the nuclear organization of heterochromatin appeared abnormal in the nuclei of Chaf1a −/− embryos. Pericentric heterochromatin, the major component of constitutive heterochromatin, can easily be visualized in interphase nuclei by the fluorochrome DAPI and by immunostaining with HP1α [16,17–19]. In wild-type blastocysts and in mouse somatic cells, pericentric heterochromatin domains cluster together and form higher-order chromatin structures called chromocenters [20], which are visualized as DAPI-dense foci (Figure 1C). These structures were not detected in Chaf1a −/− embryos (Figure 1D). Since chromatin architecture and higher-order structures are important for genome function [21], we decided to characterize this phenotype in more detail. For this purpose, we examined the status of heterochromatin organization between the two-cell and blastocyst stages. In two-cell stage wild-type embryos, DAPI staining is diffuse and fibrillar, with regions of higher density around the nucleolar precursor bodies (Figure 1E). Heterochromatin domains are progressively assembled into DAPI-dense foci between the four-cell and 32-cell blastocyst stages (Figure 1F). Localization of HP1α confirmed that the structures visualized by DAPI staining correspond to constitutive heterochromatin (Figure 1E). Thus, the nuclear organization of heterochromatin is dramatically modified during pre-implantation development, between the two-cell and blastocyst stages. In Chaf1a −/− E4 embryos, which are arrested between the eight- and 16-cell stage, DAPI-dense foci were barely detectable (Figure 1D). Instead, DAPI staining was diffuse within the nucleus, with regions of higher density around the nucleoli and at the periphery of the nuclei (Figure 1D). Localization of HP1α showed a diffuse pattern similar to the DAPI, with some enrichment at the nuclear periphery, and around the nucleoli (Figure 1D). This abnormal organization of heterochromatin in Chaf1a −/− embryos is reminiscent of the heterochromatin organization found in two- to four-cell stage wild-type embryos (compare Figure 1D and 1F). These data evidence a key role for p150CAF-1 during pre-implantation development, and reveal that this protein is required for the proper 3-D organization of heterochromatin within embryonic cell nuclei.\nNext, we wondered whether a similar requirement for CAF-1 could also be observed in ES cells, which are derived from the blastocyst inner cell mass. Given the early developmental arrest observed in Chaf1a −/− embryos, such cells could not be derived directly from null embryos, and we thus used an RNAi strategy (Figure 2A). p150CAF-1 knockdown in ES cells was quantified by Western blot analysis and IF. (Figure S1). p150CAF-1 RNAi-depleted ES cells displayed a phenotype very similar to the cells of Chaf1a −/− E4 mice. DAPI-dense foci were lost, and we observed diffuse HP1α and DAPI staining around the nucleoli and at the periphery of the nucleus (Figure 2B). This result indicates that p150CAF-1 is essential for nuclear organization of heterochromatin in ES cells in a similar way to early pre-implantation embryos. Surprisingly, we did not observe this severe alteration in heterochromatin organization in primary mouse embryonic fibroblasts (MEFs) following p150CAF-1 depletion by RNAi. p150CAF-1 depletion in MEFs resulted in a strong inhibition of cell proliferation (unpublished data), but did not alter the clustering of heterochromatin domains (Figures 2C and S2). Similarly, p150CAF-1 depletion in 3T3 cells did not affect heterochromatin organization [16]. These observations reveal a specific function for CAF-1 in the early embryo and ES cells.\nFigure 2 Depletion of p150CAF-1 in ES Cells Results in a Severe Alteration of Heterochromatin Organization\n(A) Strategy used to deplete p150CAF-1 by RNAi in ES cells. The siRNA expression vector includes a puromycin selection cassette (Puro), the mouse H1 promoter, and the siRNA encoding sequence. ES cells were kept under puromycin selection during 48 h following transfection.\n(B) Abnormal heterochromatin organization in p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 (green) and HP1α (red) in ES cells transfected with control (cont) and p150CAF-1 siRNA. siRNA expression results in efficient p150CAF-1 depletion. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue. Scale bar = 10 μm.\n(C) Heterochromatin organization is not altered in p150CAF-1-depleted MEFs. Immunodetection of p150CAF-1 (green) and HP1α (red) in MEFs transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue.\n(D) PML bodies are not altered in p150CAF-1-depleted ES cells. Immunodetection of PML (red) in ES cells transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between PML fluorescence and DAPI-stained DNA in blue. We also wondered whether loss of p150CAF-1 in ES cells specifically affects the heterochromatin nuclear subcompartment, or whether it might result in a more global loss of nuclear organization and architecture. We used a specific antibody against the promyelocytic leukemia (PML) protein to study the fate of the PML nuclear bodies, which are well-characterized subnuclear structures [22]. We could not detect any significant difference in the distribution and aspect of PML nuclear bodies between control and p150CAF-1-depleted ES cells (Figure 2D). These data show that nuclear architecture is not globally altered following CAF-1 loss-of-function. In addition, Western blot analysis revealed that CAF-1 depletion did not result in altered levels of chromatin architectural proteins such as histone H3 and HP1α (Figure S1). Thus, CAF-1 is specifically required in early embryos and in ES cells for the proper organization of the heterochromatin subnuclear compartment.\nPrevious studies performed in mammalian cell lines showed that CAF-1 activity is required for S phase progression [16,23,24]. We show here that 3 d after transfection of the RNAi vector, p150CAF-1-depleted cells (identified by a complete absence of CAF-1 IF signal) appear still active for replication, as revealed by incorporation of the thymidine analog bromodeoxyuridine (BrdU) (Figure 3A), the PCNA (proliferating cell nuclear antigen) pattern (Figure 3B), and flow cytometry analysis (Figure 3C). Hence, in these cells, DNA replication persists despite the drastic changes in heterochromatin organization. However, 24 h later, ES cells cease to proliferate and die, revealing that p150CAF-1 is required for an essential cellular process, as in embryos. Altogether, our data demonstrate that loss of p150CAF-1 function in ES cells and early embryos alters first the organization of heterochromatin in the nucleus and, in a subsequent step, cell cycle and viability.\nFigure 3 p150CAF-1 Depletion and Loss of Heterochromatin Organization Are Compatible with Active DNA Replication in ES Cells\n(A) ES cells were transfected with p150CAF-1 or control siRNA vectors. After 3 d under puromycin selection, cells were pulse-labeled for 10 min with BrdU and immediately analyzed by IF. No significant difference in BrdU incorporation could be detected between control and p150CAF-1-depleted cells. The right-hand image shows the merge between the p150CAF-1 and BrdU fluorescence. Scale bar = 10 μm.\n(B) Immunodetection of PCNA (red) revealed no significant difference in the formation of replication foci between control and p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 is shown in green and the merging of p150CAF-1 and PCNA appears in yellow.\n(C) Flow cytometry analysis showed a similar cell-cycle profile for control and p150CAF-1-depleted ES cells. Results are presented as the percentage of cells in each phase of the cell cycle (G1, S, G2/M), as defined by BrdU incorporation and DNA content. Data presented are the mean of three independent experiments; error bars indicate the standard deviation. All experiments were performed 3 d after transfection of the siRNA vectors. In order to better characterize the defects in heterochromatin organization, we performed two-color DNA fluorescence in situ hybridization (FISH) experiments to reveal the spatial distribution of pericentric and centric chromosomal regions, which in mouse are mainly composed of large blocks of major and minor satellite repeats, respectively [20]. Pericentric domains from different chromosomes form clusters, which are revealed by FISH as large spots that coincide with DAPI-dense foci in the interphase nucleus (Figure 4A). At the periphery of each pericentric domain, centric regions form individual entities (Figure 4A). In p150CAF-1 RNAi-depleted cells, we observed a disruption of pericentric heterochromatin clusters that coincides with the disappearance of DAPI-dense foci (Figure 4B). Individual pericentric domains from single chromosomes are now found either isolated or aggregated in a pattern less dense than the regular clusters observed in control cells (Figure 4B). Such aggregates, which are often found at the nuclear periphery, are also revealed by DAPI staining as a typical signature of p150CAF-1 loss-of-function. Quantification of fluorescence along a line randomly drawn across the nucleus revealed lower fluorescence intensity and a broader distribution of DAPI and major satellite hybridization signals in p150CAF-1-depleted cells (Figure 4C and 4D), indicating decondensation of pericentric heterochromatin domains. In contrast, centric domains showed an intensity and shape similar to control cells, suggesting that they remain unaffected by p150CAF-1 depletion (Figure 4C and 4D). In conclusion, these results show that p150CAF-1 is required for the proper condensation and clustering of pericentric heterochromatin domains.\nFigure 4 Depletion of p150CAF-1 Leads to Loss of Clustering, Altered Localization, and Decondensation of Pericentric Heterochromatin Domains\nDistribution of pericentric (red) and centric (green) domains was analyzed in the interphase nuclei of mouse ES cells by DNA FISH, using major satellite (pSAT) [47] and minor satellite (pMR150) [48] DNA probes, respectively. (A) In ES cells expressing control (cont) siRNA, pericentric regions from several chromosomes associate in clusters (red). These chromocenters form foci as revealed by DAPI staining (left-hand image), while centric regions (green) remain independent entities at the periphery of these domains. The right-hand image shows the merge between the pericentric and centric FISH signals.\n(B) The organization of pericentric domains was altered in cells expressing p150CAF-1 siRNA. Instead of forming well-defined chromocenters, pericentric domains were found either isolated or associated in heterogeneous aggregates of various sizes, often at the nuclear periphery. Scale bar = 10 μm.\n(C) Control ES cells. Fluorescence was quantified along a line randomly drawn across the nucleus in the merged image and data were plotted. One can distinguish clear peaks corresponding to chromocenters (red) and the condensed minor satellites (green).\n(D) ES cells expressing p150CAF-1 siRNA. p150CAF-1 depletion led to a lower fluorescence intensity and a broader distribution of signals corresponding to DAPI (blue) and major satellite hybridization (red, plot) while the organization of the minor satellites remained unaffected. Insets in the right-hand images show a typical chromocenter in control cells (C) and a disrupted chromocenter in p150CAF-1-depleted cells (D). Given the known role of CAF-1 in the deposition of histone H3.1 and H4 associated with DNA synthesis [11,12], we wondered whether this defect in higher-order chromatin organization could reflect an aberrant nucleosomal organization. Using DNase I and micrococcal nuclease (MNase) assays, we could not observe any significant difference between control and p150CAF-1-depleted ES cells at the level of bulk genome chromatin or at pericentric repeats (Figure 5). In a second series of experiments, we compared the association of histone H3 with chromatin in nuclei isolated from cells transfected with control and p150CAF-1 RNAi plasmid vectors. Nuclei were incubated in buffers with different salt concentrations ranging from 100 mM NaCl to 1 M NaCl. In all conditions, the amount of histone H3 remaining associated with chromatin was indistinguishable in control and p150CAF-1-depleted ES cells (unpublished data). Therefore, the loss of clustering and decondensation of pericentric heterochromatin are unlikely to be the consequence of severe defects in nucleosomal organization.\nFigure 5 Nucleosomal Organization Is Not Altered in p150CAF-1-Depleted ES Cells\nNuclei were prepared from ES cells transfected with control or p150CAF-1 siRNA vector. Nuclei were digested with increasing amounts of DNase I or MNase. (A) After digestion with the indicated nucleases, total DNA was prepared and run onto an agarose gel which was stained with ethidium bromide to reveal bulk genomic DNA.\n(B) The DNA was blotted onto a nylon membrane, which was then hybridized with the α-32P-labeled pSAT major satellite repeat probe [47]. Our findings showed that the nuclear localization of HP1α is severely altered in Chaf1a −/− embryos and p150CAF-1-depleted ES cells. We therefore examined the status of other epigenetic marks previously shown to characterize pericentric heterochromatin. We first tested DNA CpG methylation [25] at major satellite repeats and found no significant difference between control and p150CAF-1-depleted cells (Figure 6). As the LTM7 ES cell line that we used in our RNAi experiments is a female (XX) cell line, DNA methylation is globally reduced in these cells [26]. To rule out the possibility that hypomethylation of pericentric repeats might contribute to the destabilization of heterochromatin domains in p150CAF-1-depleted ES cells, we tested our RNAi plasmid vector in a XY ES cell line, and confirmed that loss of p150CAF-1 leads to disruption of heterochromatin organization independently of the degree of DNA methylation at pericentric repeats (unpublished data). We next analyzed specific histone modifications [27] in chromatin immunoprecipitation (ChIP) experiments using native chromatin [28]. We found that pericentric DNA was immunoprecipitated with a 2-fold lower efficiency with H4K20me3 [29,30] antibodies following p150CAF-1 depletion (Figure 7A and 7B). Immunoprecipitation of minor satellite repeats in the same experiment was less affected (Figure 7B), showing that loss of p150CAF-1 function mainly affects H4K20me3 at pericentric heterochromatin. Moreover, no significant difference in immunoprecipitation efficiency was detected at intracisternal A particle (IAP) elements (Figure 7B), which are noncentromeric repeated DNA elements also enriched in H4K20me3 [31]. This result shows that p150CAF-1 contributes to normal levels of H4K20me3 at pericentric heterochromatin, but not necessarily at other loci. The H3K9me3 mark [32] was also significantly reduced in p150CAF-1-depleted cells, though to a lesser extent than H4K20me3 (Figure 7A and 7B).\nFigure 6 DNA CpG Methylation at Pericentric Heterochromatin Is Not Altered in p150CAF-1-Depleted ES Cells\nTotal DNA was isolated from cells transfected with a control or the p150CAF-1 siRNA vector and digested with MaeII, whose recognition sequence is present in major satellite repeats. Digested DNA was run onto an agarose gel and analyzed by Southern blotting using the pSAT major satellite probe [47].\nFigure 7 Alteration of Epigenetic Marking at Pericentric Heterochromatin in p150CAF-1-Depleted Cells\n(A) p150CAF-1 depletion leads to reduced H4K20me3 and H3K9me3 at pericentric heterochromatin. Enrichment of histone marks at major satellite repeats was determined by ChIP from control (cont) and p150CAF-1 (p150) siRNA-expressing ES cells. DNA prepared from the input and the antibody-bound fraction were run onto an agarose gel and analyzed by Southern blot with the pSAT major satellite repeat probe [47].\n(B) Hybridization signals were quantified using an Instant Imager. After autoradiography, the membrane was stripped and rehybridized with a minor satellite probe [49]. After quantification, the membrane was stripped and rehybridized with an IAP LTR probe [50]. Results are presented as the amount of DNA immunoprecipitated from p150CAF-1-depleted ES cells divided by the DNA obtained from control cells. The figure shows the mean value and standard deviation of three independent ChIP experiments.\n(C and D) H3K9me3 and H4K20me3 fluorescence patterns are severely altered in p150CAF-1-depleted ES cells. Immunodetection of H3K9me3 (C, green), H4K20me3 (D, green), and HP1α (red) in control and p150CAF-1 siRNA-expressing ES cells. Merging of HP1α with H3K9me3 (C) and H4K20me3 (D) is shown in yellow. Scale bars represent 10 μm. In wild-type cells, most of H4K20me3 and H3K9me3 signals are present at the level of DAPI-dense domains when visualized by IF [29] (Figures 7C and 7D). H3K9me3 was severely perturbed in p150CAF-1-depleted cells, displaying a diffuse pattern similar to HP1α (Figure 7C). The H4K20me3 pattern was even more severely altered, showing both a loss of the typical dots revealed in control cells and a reduction in signal intensity (Figure 7D). Consistent with our ChIP experiments, residual H4K20me3 epitopes were detected at the level of relocated DAPI-dense material. Altogether, our results show that depletion of CAF-1 in ES cells leads to a simultaneous disruption of heterochromatin 3-D organization and an alteration in epigenetic marking."}

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Chaf1a +/− mice were born at a Mendelian frequency, were of normal size and weight, displayed no obvious abnormalities, and were fertile. Crossing heterozygous mice failed to generate viable newborn Chaf1a −/− mice. Furthermore, no homozygous Chaf1a −/− embryos were detected at any of the post-implantation stages. However, we could detect Chaf1a −/− embryos at embryonic day 4 (E4) using a PCR strategy (Figure 1B). They represent only 10% of E4 embryos obtained from Chaf1a +/− mice intercrosses, suggesting that more than half of the homozygous mutant embryos had degenerated before this stage. Moreover, mutant embryos contained only eight to 16 cells at the E4 stage, instead of 32 cells observed for wild-type or heterozygous blastocysts (Figure 1C and 1D). Further analysis by light microscopy using immunofluorescence (IF) allowed us to compare wild-type and p150CAF-1-depleted embryos. A loss of p150CAF-1 staining could not be detected before the eight-cell stage (unpublished data) suggesting that maternally contributed protein is present in the embryo up to the four-cell stage. Thus, depletion of p150CAF-1 protein from this stage allows a maximum of two additional cell divisions before developmental arrest.\nFigure 1 Loss of p150CAF-1 Function Leads to Early Developmental Arrest and Alteration of Heterochromatin Organization\n(A) Generation of Chaf1a +/− mice by homologous recombination in ES cells. (Top) Scheme of the p150CAF1 protein indicating the interacting domains (ID) for HP1 and p60CAF-1, and the acidic domain (AD). (Middle) Structure of the murine Chaf1a gene. Blocks and lines represent exons and introns, respectively. A star indicates the translation initiation site. Below is shown the Chaf1a targeting vector, which includes genomic DNA homology regions (5 HR and 3 HR), the diphtheria toxin (DT), and neomycin selection genes. Recombined (Rec) ES cells and mice were identified by Southern blot using ScaI (S) and the indicated probe.\n(B) Breeding strategy used for the production of E4 Chaf1a −/− embryos. Genotyping was performed by PCR using the three oligonucleotide primers indicated in (A) (1, 2, and 3). An example of the result of a genotyping experiment is shown.\n(C) Immunodetection of p150CAF-1 (green) and HP1α (red) in E4 embryos derived from Chaf1a +/− intercrosses. Because Chaf1a +/+ and Chaf1a +/− embryos both stain positively for the presence of p150CAF-1, they are both designated as wild-type. p150CAF-1 expression, which indicates ongoing S phase, can be detected in most cells within the wild-type blastocyst (upper panel). The lower panel shows a 12-cell embryo labeling negatively for p150CAF-1. Only nonspecific background labeling can be observed. In each panel, the right-hand image shows the merge between the HP1α fluorescence and DAPI-stained DNA in blue. Pink color indicates the association of HP1 with DAPI-dense material. The bottom of each panel shows the magnification of a nucleus selected from the above embryo (white square). The arrowhead indicates the typical heterochromatin foci revealed by DAPI and HP1α staining in wild-type embryos. These foci are not visible in Chaf1a −/− embryos. DAPI and HP1α staining are diffuse within the nucleus of p150CAF-1-depleted embryos, with enrichment at the nuclear periphery, revealing abnormal heterochromatin organization. Scale bars represent 10 μm.\n(E) Wild-type embryos isolated at embryonic day 2 (E2, two cells), E2.5 (four cells), E3 (eight cells), E3.5 (16 cells), and E4 (32 cells) are shown. Heterochromatin was monitored by DAPI staining (upper panel) and HP1 immunolabeling (in red, lower panel).\n(F) Magnification of a nucleus (DAPI-stained) representative of each stage. The right-hand panel shows the nucleus of an ES cell. Scale bar represents 10 μm. Strikingly, we found that the nuclear organization of heterochromatin appeared abnormal in the nuclei of Chaf1a −/− embryos. Pericentric heterochromatin, the major component of constitutive heterochromatin, can easily be visualized in interphase nuclei by the fluorochrome DAPI and by immunostaining with HP1α [16,17–19]. In wild-type blastocysts and in mouse somatic cells, pericentric heterochromatin domains cluster together and form higher-order chromatin structures called chromocenters [20], which are visualized as DAPI-dense foci (Figure 1C). These structures were not detected in Chaf1a −/− embryos (Figure 1D). Since chromatin architecture and higher-order structures are important for genome function [21], we decided to characterize this phenotype in more detail. For this purpose, we examined the status of heterochromatin organization between the two-cell and blastocyst stages. In two-cell stage wild-type embryos, DAPI staining is diffuse and fibrillar, with regions of higher density around the nucleolar precursor bodies (Figure 1E). Heterochromatin domains are progressively assembled into DAPI-dense foci between the four-cell and 32-cell blastocyst stages (Figure 1F). Localization of HP1α confirmed that the structures visualized by DAPI staining correspond to constitutive heterochromatin (Figure 1E). Thus, the nuclear organization of heterochromatin is dramatically modified during pre-implantation development, between the two-cell and blastocyst stages. In Chaf1a −/− E4 embryos, which are arrested between the eight- and 16-cell stage, DAPI-dense foci were barely detectable (Figure 1D). Instead, DAPI staining was diffuse within the nucleus, with regions of higher density around the nucleoli and at the periphery of the nuclei (Figure 1D). Localization of HP1α showed a diffuse pattern similar to the DAPI, with some enrichment at the nuclear periphery, and around the nucleoli (Figure 1D). This abnormal organization of heterochromatin in Chaf1a −/− embryos is reminiscent of the heterochromatin organization found in two- to four-cell stage wild-type embryos (compare Figure 1D and 1F). These data evidence a key role for p150CAF-1 during pre-implantation development, and reveal that this protein is required for the proper 3-D organization of heterochromatin within embryonic cell nuclei.\nNext, we wondered whether a similar requirement for CAF-1 could also be observed in ES cells, which are derived from the blastocyst inner cell mass. Given the early developmental arrest observed in Chaf1a −/− embryos, such cells could not be derived directly from null embryos, and we thus used an RNAi strategy (Figure 2A). p150CAF-1 knockdown in ES cells was quantified by Western blot analysis and IF. (Figure S1). p150CAF-1 RNAi-depleted ES cells displayed a phenotype very similar to the cells of Chaf1a −/− E4 mice. DAPI-dense foci were lost, and we observed diffuse HP1α and DAPI staining around the nucleoli and at the periphery of the nucleus (Figure 2B). This result indicates that p150CAF-1 is essential for nuclear organization of heterochromatin in ES cells in a similar way to early pre-implantation embryos. Surprisingly, we did not observe this severe alteration in heterochromatin organization in primary mouse embryonic fibroblasts (MEFs) following p150CAF-1 depletion by RNAi. p150CAF-1 depletion in MEFs resulted in a strong inhibition of cell proliferation (unpublished data), but did not alter the clustering of heterochromatin domains (Figures 2C and S2). Similarly, p150CAF-1 depletion in 3T3 cells did not affect heterochromatin organization [16]. These observations reveal a specific function for CAF-1 in the early embryo and ES cells.\nFigure 2 Depletion of p150CAF-1 in ES Cells Results in a Severe Alteration of Heterochromatin Organization\n(A) Strategy used to deplete p150CAF-1 by RNAi in ES cells. The siRNA expression vector includes a puromycin selection cassette (Puro), the mouse H1 promoter, and the siRNA encoding sequence. ES cells were kept under puromycin selection during 48 h following transfection.\n(B) Abnormal heterochromatin organization in p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 (green) and HP1α (red) in ES cells transfected with control (cont) and p150CAF-1 siRNA. siRNA expression results in efficient p150CAF-1 depletion. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue. Scale bar = 10 μm.\n(C) Heterochromatin organization is not altered in p150CAF-1-depleted MEFs. Immunodetection of p150CAF-1 (green) and HP1α (red) in MEFs transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue.\n(D) PML bodies are not altered in p150CAF-1-depleted ES cells. Immunodetection of PML (red) in ES cells transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between PML fluorescence and DAPI-stained DNA in blue. We also wondered whether loss of p150CAF-1 in ES cells specifically affects the heterochromatin nuclear subcompartment, or whether it might result in a more global loss of nuclear organization and architecture. We used a specific antibody against the promyelocytic leukemia (PML) protein to study the fate of the PML nuclear bodies, which are well-characterized subnuclear structures [22]. We could not detect any significant difference in the distribution and aspect of PML nuclear bodies between control and p150CAF-1-depleted ES cells (Figure 2D). These data show that nuclear architecture is not globally altered following CAF-1 loss-of-function. In addition, Western blot analysis revealed that CAF-1 depletion did not result in altered levels of chromatin architectural proteins such as histone H3 and HP1α (Figure S1). Thus, CAF-1 is specifically required in early embryos and in ES cells for the proper organization of the heterochromatin subnuclear compartment.\nPrevious studies performed in mammalian cell lines showed that CAF-1 activity is required for S phase progression [16,23,24]. We show here that 3 d after transfection of the RNAi vector, p150CAF-1-depleted cells (identified by a complete absence of CAF-1 IF signal) appear still active for replication, as revealed by incorporation of the thymidine analog bromodeoxyuridine (BrdU) (Figure 3A), the PCNA (proliferating cell nuclear antigen) pattern (Figure 3B), and flow cytometry analysis (Figure 3C). Hence, in these cells, DNA replication persists despite the drastic changes in heterochromatin organization. However, 24 h later, ES cells cease to proliferate and die, revealing that p150CAF-1 is required for an essential cellular process, as in embryos. Altogether, our data demonstrate that loss of p150CAF-1 function in ES cells and early embryos alters first the organization of heterochromatin in the nucleus and, in a subsequent step, cell cycle and viability.\nFigure 3 p150CAF-1 Depletion and Loss of Heterochromatin Organization Are Compatible with Active DNA Replication in ES Cells\n(A) ES cells were transfected with p150CAF-1 or control siRNA vectors. After 3 d under puromycin selection, cells were pulse-labeled for 10 min with BrdU and immediately analyzed by IF. No significant difference in BrdU incorporation could be detected between control and p150CAF-1-depleted cells. The right-hand image shows the merge between the p150CAF-1 and BrdU fluorescence. Scale bar = 10 μm.\n(B) Immunodetection of PCNA (red) revealed no significant difference in the formation of replication foci between control and p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 is shown in green and the merging of p150CAF-1 and PCNA appears in yellow.\n(C) Flow cytometry analysis showed a similar cell-cycle profile for control and p150CAF-1-depleted ES cells. Results are presented as the percentage of cells in each phase of the cell cycle (G1, S, G2/M), as defined by BrdU incorporation and DNA content. Data presented are the mean of three independent experiments; error bars indicate the standard deviation. All experiments were performed 3 d after transfection of the siRNA vectors. In order to better characterize the defects in heterochromatin organization, we performed two-color DNA fluorescence in situ hybridization (FISH) experiments to reveal the spatial distribution of pericentric and centric chromosomal regions, which in mouse are mainly composed of large blocks of major and minor satellite repeats, respectively [20]. Pericentric domains from different chromosomes form clusters, which are revealed by FISH as large spots that coincide with DAPI-dense foci in the interphase nucleus (Figure 4A). At the periphery of each pericentric domain, centric regions form individual entities (Figure 4A). In p150CAF-1 RNAi-depleted cells, we observed a disruption of pericentric heterochromatin clusters that coincides with the disappearance of DAPI-dense foci (Figure 4B). Individual pericentric domains from single chromosomes are now found either isolated or aggregated in a pattern less dense than the regular clusters observed in control cells (Figure 4B). Such aggregates, which are often found at the nuclear periphery, are also revealed by DAPI staining as a typical signature of p150CAF-1 loss-of-function. Quantification of fluorescence along a line randomly drawn across the nucleus revealed lower fluorescence intensity and a broader distribution of DAPI and major satellite hybridization signals in p150CAF-1-depleted cells (Figure 4C and 4D), indicating decondensation of pericentric heterochromatin domains. In contrast, centric domains showed an intensity and shape similar to control cells, suggesting that they remain unaffected by p150CAF-1 depletion (Figure 4C and 4D). In conclusion, these results show that p150CAF-1 is required for the proper condensation and clustering of pericentric heterochromatin domains.\nFigure 4 Depletion of p150CAF-1 Leads to Loss of Clustering, Altered Localization, and Decondensation of Pericentric Heterochromatin Domains\nDistribution of pericentric (red) and centric (green) domains was analyzed in the interphase nuclei of mouse ES cells by DNA FISH, using major satellite (pSAT) [47] and minor satellite (pMR150) [48] DNA probes, respectively. (A) In ES cells expressing control (cont) siRNA, pericentric regions from several chromosomes associate in clusters (red). These chromocenters form foci as revealed by DAPI staining (left-hand image), while centric regions (green) remain independent entities at the periphery of these domains. The right-hand image shows the merge between the pericentric and centric FISH signals.\n(B) The organization of pericentric domains was altered in cells expressing p150CAF-1 siRNA. Instead of forming well-defined chromocenters, pericentric domains were found either isolated or associated in heterogeneous aggregates of various sizes, often at the nuclear periphery. Scale bar = 10 μm.\n(C) Control ES cells. Fluorescence was quantified along a line randomly drawn across the nucleus in the merged image and data were plotted. One can distinguish clear peaks corresponding to chromocenters (red) and the condensed minor satellites (green).\n(D) ES cells expressing p150CAF-1 siRNA. p150CAF-1 depletion led to a lower fluorescence intensity and a broader distribution of signals corresponding to DAPI (blue) and major satellite hybridization (red, plot) while the organization of the minor satellites remained unaffected. Insets in the right-hand images show a typical chromocenter in control cells (C) and a disrupted chromocenter in p150CAF-1-depleted cells (D). Given the known role of CAF-1 in the deposition of histone H3.1 and H4 associated with DNA synthesis [11,12], we wondered whether this defect in higher-order chromatin organization could reflect an aberrant nucleosomal organization. Using DNase I and micrococcal nuclease (MNase) assays, we could not observe any significant difference between control and p150CAF-1-depleted ES cells at the level of bulk genome chromatin or at pericentric repeats (Figure 5). In a second series of experiments, we compared the association of histone H3 with chromatin in nuclei isolated from cells transfected with control and p150CAF-1 RNAi plasmid vectors. Nuclei were incubated in buffers with different salt concentrations ranging from 100 mM NaCl to 1 M NaCl. In all conditions, the amount of histone H3 remaining associated with chromatin was indistinguishable in control and p150CAF-1-depleted ES cells (unpublished data). Therefore, the loss of clustering and decondensation of pericentric heterochromatin are unlikely to be the consequence of severe defects in nucleosomal organization.\nFigure 5 Nucleosomal Organization Is Not Altered in p150CAF-1-Depleted ES Cells\nNuclei were prepared from ES cells transfected with control or p150CAF-1 siRNA vector. Nuclei were digested with increasing amounts of DNase I or MNase. (A) After digestion with the indicated nucleases, total DNA was prepared and run onto an agarose gel which was stained with ethidium bromide to reveal bulk genomic DNA.\n(B) The DNA was blotted onto a nylon membrane, which was then hybridized with the α-32P-labeled pSAT major satellite repeat probe [47]. Our findings showed that the nuclear localization of HP1α is severely altered in Chaf1a −/− embryos and p150CAF-1-depleted ES cells. We therefore examined the status of other epigenetic marks previously shown to characterize pericentric heterochromatin. We first tested DNA CpG methylation [25] at major satellite repeats and found no significant difference between control and p150CAF-1-depleted cells (Figure 6). As the LTM7 ES cell line that we used in our RNAi experiments is a female (XX) cell line, DNA methylation is globally reduced in these cells [26]. To rule out the possibility that hypomethylation of pericentric repeats might contribute to the destabilization of heterochromatin domains in p150CAF-1-depleted ES cells, we tested our RNAi plasmid vector in a XY ES cell line, and confirmed that loss of p150CAF-1 leads to disruption of heterochromatin organization independently of the degree of DNA methylation at pericentric repeats (unpublished data). We next analyzed specific histone modifications [27] in chromatin immunoprecipitation (ChIP) experiments using native chromatin [28]. We found that pericentric DNA was immunoprecipitated with a 2-fold lower efficiency with H4K20me3 [29,30] antibodies following p150CAF-1 depletion (Figure 7A and 7B). Immunoprecipitation of minor satellite repeats in the same experiment was less affected (Figure 7B), showing that loss of p150CAF-1 function mainly affects H4K20me3 at pericentric heterochromatin. Moreover, no significant difference in immunoprecipitation efficiency was detected at intracisternal A particle (IAP) elements (Figure 7B), which are noncentromeric repeated DNA elements also enriched in H4K20me3 [31]. This result shows that p150CAF-1 contributes to normal levels of H4K20me3 at pericentric heterochromatin, but not necessarily at other loci. The H3K9me3 mark [32] was also significantly reduced in p150CAF-1-depleted cells, though to a lesser extent than H4K20me3 (Figure 7A and 7B).\nFigure 6 DNA CpG Methylation at Pericentric Heterochromatin Is Not Altered in p150CAF-1-Depleted ES Cells\nTotal DNA was isolated from cells transfected with a control or the p150CAF-1 siRNA vector and digested with MaeII, whose recognition sequence is present in major satellite repeats. Digested DNA was run onto an agarose gel and analyzed by Southern blotting using the pSAT major satellite probe [47].\nFigure 7 Alteration of Epigenetic Marking at Pericentric Heterochromatin in p150CAF-1-Depleted Cells\n(A) p150CAF-1 depletion leads to reduced H4K20me3 and H3K9me3 at pericentric heterochromatin. Enrichment of histone marks at major satellite repeats was determined by ChIP from control (cont) and p150CAF-1 (p150) siRNA-expressing ES cells. DNA prepared from the input and the antibody-bound fraction were run onto an agarose gel and analyzed by Southern blot with the pSAT major satellite repeat probe [47].\n(B) Hybridization signals were quantified using an Instant Imager. After autoradiography, the membrane was stripped and rehybridized with a minor satellite probe [49]. After quantification, the membrane was stripped and rehybridized with an IAP LTR probe [50]. Results are presented as the amount of DNA immunoprecipitated from p150CAF-1-depleted ES cells divided by the DNA obtained from control cells. The figure shows the mean value and standard deviation of three independent ChIP experiments.\n(C and D) H3K9me3 and H4K20me3 fluorescence patterns are severely altered in p150CAF-1-depleted ES cells. Immunodetection of H3K9me3 (C, green), H4K20me3 (D, green), and HP1α (red) in control and p150CAF-1 siRNA-expressing ES cells. Merging of HP1α with H3K9me3 (C) and H4K20me3 (D) is shown in yellow. Scale bars represent 10 μm. In wild-type cells, most of H4K20me3 and H3K9me3 signals are present at the level of DAPI-dense domains when visualized by IF [29] (Figures 7C and 7D). H3K9me3 was severely perturbed in p150CAF-1-depleted cells, displaying a diffuse pattern similar to HP1α (Figure 7C). The H4K20me3 pattern was even more severely altered, showing both a loss of the typical dots revealed in control cells and a reduction in signal intensity (Figure 7D). Consistent with our ChIP experiments, residual H4K20me3 epitopes were detected at the level of relocated DAPI-dense material. Altogether, our results show that depletion of CAF-1 in ES cells leads to a simultaneous disruption of heterochromatin 3-D organization and an alteration in epigenetic marking."}

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used gene targeting in ES cells to delete exon 3 in the Chaf1a gene, which encodes p150CAF-1 (Figure 1A). Chaf1a +/− mice were born at a Mendelian frequency, were of normal size and weight, displayed no obvious abnormalities, and were fertile. Crossing heterozygous mice failed to generate viable newborn Chaf1a −/− mice. Furthermore, no homozygous Chaf1a −/− embryos were detected at any of the post-implantation stages. However, we could detect Chaf1a −/− embryos at embryonic day 4 (E4) using a PCR strategy (Figure 1B). They represent only 10% of E4 embryos obtained from Chaf1a +/− mice intercrosses, suggesting that more than half of the homozygous mutant embryos had degenerated before this stage. Moreover, mutant embryos contained only eight to 16 cells at the E4 stage, instead of 32 cells observed for wild-type or heterozygous blastocysts (Figure 1C and 1D). Further analysis by light microscopy using immunofluorescence (IF) allowed us to compare wild-type and p150CAF-1-depleted embryos. A loss of p150CAF-1 staining could not be detected before the eight-cell stage (unpublished data) suggesting that maternally contributed protein is present in the embryo up to the four-cell stage. Thus, depletion of p150CAF-1 protein from this stage allows a maximum of two additional cell divisions before developmental arrest.\nFigure 1 Loss of p150CAF-1 Function Leads to Early Developmental Arrest and Alteration of Heterochromatin Organization\n(A) Generation of Chaf1a +/− mice by homologous recombination in ES cells. (Top) Scheme of the p150CAF1 protein indicating the interacting domains (ID) for HP1 and p60CAF-1, and the acidic domain (AD). (Middle) Structure of the murine Chaf1a gene. Blocks and lines represent exons and introns, respectively. A star indicates the translation initiation site. Below is shown the Chaf1a targeting vector, which includes genomic DNA homology regions (5 HR and 3 HR), the diphtheria toxin (DT), and neomycin selection genes. Recombined (Rec) ES cells and mice were identified by Southern blot using ScaI (S) and the indicated probe.\n(B) Breeding strategy used for the production of E4 Chaf1a −/− embryos. Genotyping was performed by PCR using the three oligonucleotide primers indicated in (A) (1, 2, and 3). An example of the result of a genotyping experiment is shown.\n(C) Immunodetection of p150CAF-1 (green) and HP1α (red) in E4 embryos derived from Chaf1a +/− intercrosses. Because Chaf1a +/+ and Chaf1a +/− embryos both stain positively for the presence of p150CAF-1, they are both designated as wild-type. p150CAF-1 expression, which indicates ongoing S phase, can be detected in most cells within the wild-type blastocyst (upper panel). The lower panel shows a 12-cell embryo labeling negatively for p150CAF-1. Only nonspecific background labeling can be observed. In each panel, the right-hand image shows the merge between the HP1α fluorescence and DAPI-stained DNA in blue. Pink color indicates the association of HP1 with DAPI-dense material. The bottom of each panel shows the magnification of a nucleus selected from the above embryo (white square). The arrowhead indicates the typical heterochromatin foci revealed by DAPI and HP1α staining in wild-type embryos. These foci are not visible in Chaf1a −/− embryos. DAPI and HP1α staining are diffuse within the nucleus of p150CAF-1-depleted embryos, with enrichment at the nuclear periphery, revealing abnormal heterochromatin organization. Scale bars represent 10 μm.\n(E) Wild-type embryos isolated at embryonic day 2 (E2, two cells), E2.5 (four cells), E3 (eight cells), E3.5 (16 cells), and E4 (32 cells) are shown. Heterochromatin was monitored by DAPI staining (upper panel) and HP1 immunolabeling (in red, lower panel).\n(F) Magnification of a nucleus (DAPI-stained) representative of each stage. The right-hand panel shows the nucleus of an ES cell. Scale bar represents 10 μm. Strikingly, we found that the nuclear organization of heterochromatin appeared abnormal in the nuclei of Chaf1a −/− embryos. Pericentric heterochromatin, the major component of constitutive heterochromatin, can easily be visualized in interphase nuclei by the fluorochrome DAPI and by immunostaining with HP1α [16,17–19]. In wild-type blastocysts and in mouse somatic cells, pericentric heterochromatin domains cluster together and form higher-order chromatin structures called chromocenters [20], which are visualized as DAPI-dense foci (Figure 1C). These structures were not detected in Chaf1a −/− embryos (Figure 1D). Since chromatin architecture and higher-order structures are important for genome function [21], we decided to characterize this phenotype in more detail. For this purpose, we examined the status of heterochromatin organization between the two-cell and blastocyst stages. In two-cell stage wild-type embryos, DAPI staining is diffuse and fibrillar, with regions of higher density around the nucleolar precursor bodies (Figure 1E). Heterochromatin domains are progressively assembled into DAPI-dense foci between the four-cell and 32-cell blastocyst stages (Figure 1F). Localization of HP1α confirmed that the structures visualized by DAPI staining correspond to constitutive heterochromatin (Figure 1E). Thus, the nuclear organization of heterochromatin is dramatically modified during pre-implantation development, between the two-cell and blastocyst stages. In Chaf1a −/− E4 embryos, which are arrested between the eight- and 16-cell stage, DAPI-dense foci were barely detectable (Figure 1D). Instead, DAPI staining was diffuse within the nucleus, with regions of higher density around the nucleoli and at the periphery of the nuclei (Figure 1D). Localization of HP1α showed a diffuse pattern similar to the DAPI, with some enrichment at the nuclear periphery, and around the nucleoli (Figure 1D). This abnormal organization of heterochromatin in Chaf1a −/− embryos is reminiscent of the heterochromatin organization found in two- to four-cell stage wild-type embryos (compare Figure 1D and 1F). These data evidence a key role for p150CAF-1 during pre-implantation development, and reveal that this protein is required for the proper 3-D organization of heterochromatin within embryonic cell nuclei.\nNext, we wondered whether a similar requirement for CAF-1 could also be observed in ES cells, which are derived from the blastocyst inner cell mass. Given the early developmental arrest observed in Chaf1a −/− embryos, such cells could not be derived directly from null embryos, and we thus used an RNAi strategy (Figure 2A). p150CAF-1 knockdown in ES cells was quantified by Western blot analysis and IF. (Figure S1). p150CAF-1 RNAi-depleted ES cells displayed a phenotype very similar to the cells of Chaf1a −/− E4 mice. DAPI-dense foci were lost, and we observed diffuse HP1α and DAPI staining around the nucleoli and at the periphery of the nucleus (Figure 2B). This result indicates that p150CAF-1 is essential for nuclear organization of heterochromatin in ES cells in a similar way to early pre-implantation embryos. Surprisingly, we did not observe this severe alteration in heterochromatin organization in primary mouse embryonic fibroblasts (MEFs) following p150CAF-1 depletion by RNAi. p150CAF-1 depletion in MEFs resulted in a strong inhibition of cell proliferation (unpublished data), but did not alter the clustering of heterochromatin domains (Figures 2C and S2). Similarly, p150CAF-1 depletion in 3T3 cells did not affect heterochromatin organization [16]. These observations reveal a specific function for CAF-1 in the early embryo and ES cells.\nFigure 2 Depletion of p150CAF-1 in ES Cells Results in a Severe Alteration of Heterochromatin Organization\n(A) Strategy used to deplete p150CAF-1 by RNAi in ES cells. The siRNA expression vector includes a puromycin selection cassette (Puro), the mouse H1 promoter, and the siRNA encoding sequence. ES cells were kept under puromycin selection during 48 h following transfection.\n(B) Abnormal heterochromatin organization in p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 (green) and HP1α (red) in ES cells transfected with control (cont) and p150CAF-1 siRNA. siRNA expression results in efficient p150CAF-1 depletion. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue. Scale bar = 10 μm.\n(C) Heterochromatin organization is not altered in p150CAF-1-depleted MEFs. Immunodetection of p150CAF-1 (green) and HP1α (red) in MEFs transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between HP1α fluorescence and DAPI-stained DNA in blue.\n(D) PML bodies are not altered in p150CAF-1-depleted ES cells. Immunodetection of PML (red) in ES cells transfected with control (cont) or p150CAF-1 siRNA. The right-hand image shows the merge between PML fluorescence and DAPI-stained DNA in blue. We also wondered whether loss of p150CAF-1 in ES cells specifically affects the heterochromatin nuclear subcompartment, or whether it might result in a more global loss of nuclear organization and architecture. We used a specific antibody against the promyelocytic leukemia (PML) protein to study the fate of the PML nuclear bodies, which are well-characterized subnuclear structures [22]. We could not detect any significant difference in the distribution and aspect of PML nuclear bodies between control and p150CAF-1-depleted ES cells (Figure 2D). These data show that nuclear architecture is not globally altered following CAF-1 loss-of-function. In addition, Western blot analysis revealed that CAF-1 depletion did not result in altered levels of chromatin architectural proteins such as histone H3 and HP1α (Figure S1). Thus, CAF-1 is specifically required in early embryos and in ES cells for the proper organization of the heterochromatin subnuclear compartment.\nPrevious studies performed in mammalian cell lines showed that CAF-1 activity is required for S phase progression [16,23,24]. We show here that 3 d after transfection of the RNAi vector, p150CAF-1-depleted cells (identified by a complete absence of CAF-1 IF signal) appear still active for replication, as revealed by incorporation of the thymidine analog bromodeoxyuridine (BrdU) (Figure 3A), the PCNA (proliferating cell nuclear antigen) pattern (Figure 3B), and flow cytometry analysis (Figure 3C). Hence, in these cells, DNA replication persists despite the drastic changes in heterochromatin organization. However, 24 h later, ES cells cease to proliferate and die, revealing that p150CAF-1 is required for an essential cellular process, as in embryos. Altogether, our data demonstrate that loss of p150CAF-1 function in ES cells and early embryos alters first the organization of heterochromatin in the nucleus and, in a subsequent step, cell cycle and viability.\nFigure 3 p150CAF-1 Depletion and Loss of Heterochromatin Organization Are Compatible with Active DNA Replication in ES Cells\n(A) ES cells were transfected with p150CAF-1 or control siRNA vectors. After 3 d under puromycin selection, cells were pulse-labeled for 10 min with BrdU and immediately analyzed by IF. No significant difference in BrdU incorporation could be detected between control and p150CAF-1-depleted cells. The right-hand image shows the merge between the p150CAF-1 and BrdU fluorescence. Scale bar = 10 μm.\n(B) Immunodetection of PCNA (red) revealed no significant difference in the formation of replication foci between control and p150CAF-1-depleted ES cells. Immunodetection of p150CAF-1 is shown in green and the merging of p150CAF-1 and PCNA appears in yellow.\n(C) Flow cytometry analysis showed a similar cell-cycle profile for control and p150CAF-1-depleted ES cells. Results are presented as the percentage of cells in each phase of the cell cycle (G1, S, G2/M), as defined by BrdU incorporation and DNA content. Data presented are the mean of three independent experiments; error bars indicate the standard deviation. All experiments were performed 3 d after transfection of the siRNA vectors. In order to better characterize the defects in heterochromatin organization, we performed two-color DNA fluorescence in situ hybridization (FISH) experiments to reveal the spatial distribution of pericentric and centric chromosomal regions, which in mouse are mainly composed of large blocks of major and minor satellite repeats, respectively [20]. Pericentric domains from different chromosomes form clusters, which are revealed by FISH as large spots that coincide with DAPI-dense foci in the interphase nucleus (Figure 4A). At the periphery of each pericentric domain, centric regions form individual entities (Figure 4A). In p150CAF-1 RNAi-depleted cells, we observed a disruption of pericentric heterochromatin clusters that coincides with the disappearance of DAPI-dense foci (Figure 4B). Individual pericentric domains from single chromosomes are now found either isolated or aggregated in a pattern less dense than the regular clusters observed in control cells (Figure 4B). Such aggregates, which are often found at the nuclear periphery, are also revealed by DAPI staining as a typical signature of p150CAF-1 loss-of-function. Quantification of fluorescence along a line randomly drawn across the nucleus revealed lower fluorescence intensity and a broader distribution of DAPI and major satellite hybridization signals in p150CAF-1-depleted cells (Figure 4C and 4D), indicating decondensation of pericentric heterochromatin domains. In contrast, centric domains showed an intensity and shape similar to control cells, suggesting that they remain unaffected by p150CAF-1 depletion (Figure 4C and 4D). In conclusion, these results show that p150CAF-1 is required for the proper condensation and clustering of pericentric heterochromatin domains.\nFigure 4 Depletion of p150CAF-1 Leads to Loss of Clustering, Altered Localization, and Decondensation of Pericentric Heterochromatin Domains\nDistribution of pericentric (red) and centric (green) domains was analyzed in the interphase nuclei of mouse ES cells by DNA FISH, using major satellite (pSAT) [47] and minor satellite (pMR150) [48] DNA probes, respectively. (A) In ES cells expressing control (cont) siRNA, pericentric regions from several chromosomes associate in clusters (red). These chromocenters form foci as revealed by DAPI staining (left-hand image), while centric regions (green) remain independent entities at the periphery of these domains. The right-hand image shows the merge between the pericentric and centric FISH signals.\n(B) The organization of pericentric domains was altered in cells expressing p150CAF-1 siRNA. Instead of forming well-defined chromocenters, pericentric domains were found either isolated or associated in heterogeneous aggregates of various sizes, often at the nuclear periphery. Scale bar = 10 μm.\n(C) Control ES cells. Fluorescence was quantified along a line randomly drawn across the nucleus in the merged image and data were plotted. One can distinguish clear peaks corresponding to chromocenters (red) and the condensed minor satellites (green).\n(D) ES cells expressing p150CAF-1 siRNA. p150CAF-1 depletion led to a lower fluorescence intensity and a broader distribution of signals corresponding to DAPI (blue) and major satellite hybridization (red, plot) while the organization of the minor satellites remained unaffected. Insets in the right-hand images show a typical chromocenter in control cells (C) and a disrupted chromocenter in p150CAF-1-depleted cells (D). Given the known role of CAF-1 in the deposition of histone H3.1 and H4 associated with DNA synthesis [11,12], we wondered whether this defect in higher-order chromatin organization could reflect an aberrant nucleosomal organization. Using DNase I and micrococcal nuclease (MNase) assays, we could not observe any significant difference between control and p150CAF-1-depleted ES cells at the level of bulk genome chromatin or at pericentric repeats (Figure 5). In a second series of experiments, we compared the association of histone H3 with chromatin in nuclei isolated from cells transfected with control and p150CAF-1 RNAi plasmid vectors. Nuclei were incubated in buffers with different salt concentrations ranging from 100 mM NaCl to 1 M NaCl. In all conditions, the amount of histone H3 remaining associated with chromatin was indistinguishable in control and p150CAF-1-depleted ES cells (unpublished data). Therefore, the loss of clustering and decondensation of pericentric heterochromatin are unlikely to be the consequence of severe defects in nucleosomal organization.\nFigure 5 Nucleosomal Organization Is Not Altered in p150CAF-1-Depleted ES Cells\nNuclei were prepared from ES cells transfected with control or p150CAF-1 siRNA vector. Nuclei were digested with increasing amounts of DNase I or MNase. (A) After digestion with the indicated nucleases, total DNA was prepared and run onto an agarose gel which was stained with ethidium bromide to reveal bulk genomic DNA.\n(B) The DNA was blotted onto a nylon membrane, which was then hybridized with the α-32P-labeled pSAT major satellite repeat probe [47]. Our findings showed that the nuclear localization of HP1α is severely altered in Chaf1a −/− embryos and p150CAF-1-depleted ES cells. We therefore examined the status of other epigenetic marks previously shown to characterize pericentric heterochromatin. We first tested DNA CpG methylation [25] at major satellite repeats and found no significant difference between control and p150CAF-1-depleted cells (Figure 6). As the LTM7 ES cell line that we used in our RNAi experiments is a female (XX) cell line, DNA methylation is globally reduced in these cells [26]. To rule out the possibility that hypomethylation of pericentric repeats might contribute to the destabilization of heterochromatin domains in p150CAF-1-depleted ES cells, we tested our RNAi plasmid vector in a XY ES cell line, and confirmed that loss of p150CAF-1 leads to disruption of heterochromatin organization independently of the degree of DNA methylation at pericentric repeats (unpublished data). We next analyzed specific histone modifications [27] in chromatin immunoprecipitation (ChIP) experiments using native chromatin [28]. We found that pericentric DNA was immunoprecipitated with a 2-fold lower efficiency with H4K20me3 [29,30] antibodies following p150CAF-1 depletion (Figure 7A and 7B). Immunoprecipitation of minor satellite repeats in the same experiment was less affected (Figure 7B), showing that loss of p150CAF-1 function mainly affects H4K20me3 at pericentric heterochromatin. Moreover, no significant difference in immunoprecipitation efficiency was detected at intracisternal A particle (IAP) elements (Figure 7B), which are noncentromeric repeated DNA elements also enriched in H4K20me3 [31]. This result shows that p150CAF-1 contributes to normal levels of H4K20me3 at pericentric heterochromatin, but not necessarily at other loci. The H3K9me3 mark [32] was also significantly reduced in p150CAF-1-depleted cells, though to a lesser extent than H4K20me3 (Figure 7A and 7B).\nFigure 6 DNA CpG Methylation at Pericentric Heterochromatin Is Not Altered in p150CAF-1-Depleted ES Cells\nTotal DNA was isolated from cells transfected with a control or the p150CAF-1 siRNA vector and digested with MaeII, whose recognition sequence is present in major satellite repeats. Digested DNA was run onto an agarose gel and analyzed by Southern blotting using the pSAT major satellite probe [47].\nFigure 7 Alteration of Epigenetic Marking at Pericentric Heterochromatin in p150CAF-1-Depleted Cells\n(A) p150CAF-1 depletion leads to reduced H4K20me3 and H3K9me3 at pericentric heterochromatin. Enrichment of histone marks at major satellite repeats was determined by ChIP from control (cont) and p150CAF-1 (p150) siRNA-expressing ES cells. DNA prepared from the input and the antibody-bound fraction were run onto an agarose gel and analyzed by Southern blot with the pSAT major satellite repeat probe [47].\n(B) Hybridization signals were quantified using an Instant Imager. After autoradiography, the membrane was stripped and rehybridized with a minor satellite probe [49]. After quantification, the membrane was stripped and rehybridized with an IAP LTR probe [50]. Results are presented as the amount of DNA immunoprecipitated from p150CAF-1-depleted ES cells divided by the DNA obtained from control cells. The figure shows the mean value and standard deviation of three independent ChIP experiments.\n(C and D) H3K9me3 and H4K20me3 fluorescence patterns are severely altered in p150CAF-1-depleted ES cells. Immunodetection of H3K9me3 (C, green), H4K20me3 (D, green), and HP1α (red) in control and p150CAF-1 siRNA-expressing ES cells. Merging of HP1α with H3K9me3 (C) and H4K20me3 (D) is shown in yellow. Scale bars represent 10 μm. In wild-type cells, most of H4K20me3 and H3K9me3 signals are present at the level of DAPI-dense domains when visualized by IF [29] (Figures 7C and 7D). H3K9me3 was severely perturbed in p150CAF-1-depleted cells, displaying a diffuse pattern similar to HP1α (Figure 7C). The H4K20me3 pattern was even more severely altered, showing both a loss of the typical dots revealed in control cells and a reduction in signal intensity (Figure 7D). Consistent with our ChIP experiments, residual H4K20me3 epitopes were detected at the level of relocated DAPI-dense material. Altogether, our results show that depletion of CAF-1 in ES cells leads to a simultaneous disruption of heterochromatin 3-D organization and an alteration in epigenetic marking."}