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investigated the role of the Atrx protein in mouse development. By using a conditional knockout approach, we ablated the full-length Atrx protein first in ES cells and embryoid bodies, and then in developing mouse embryos.\n\nAtrx in ES Cells\nAtrxnull ES cells could not be recovered by direct targeting and were eventually generated by adopting a conditional targeting approach. This is consistent with our observation that Atrx is highly expressed in ES cells, and that the absence of full-length Atrx imparts a growth disadvantage relative to cells bearing a functional Atrx allele. At present, the cause of the proliferative delay in Atrxnull ES cells is not known. Interestingly, we demonstrated that apoptosis is not significantly up-regulated in ES cells lacking Atrx and is only mildly elevated in Atrxnull 7.5 dpc mouse embryos. In contrast, it was recently shown that the loss of Atrx markedly increased the apoptotic population in the differentiating cells of the embryonic cortex and postnatal hippocampus, when Atrx expression was ablated in the developing mouse forebrain using the Atrx flox allele described here [20]. The human ATRX protein has been shown to associate in a complex with Daxx [8], a protein that has been implicated in multiple pathways for the regulation of apoptosis [21]. It is possible that disruption of the mouse Atrx-Daxx complex (by ablation of the Atrx protein) could have triggered a universal proapoptotic response. However, our observations in ES cells demonstrate that the induction of apoptosis is not an automatic response triggered by the removal of Atrx in all cell types, and suggest that the inappropriate apoptosis observed in the Atrx-mutant forebrain may reflect a requirement for Atrx during terminal differentiation.\n\nAn Unexpected Role for Atrx in Development of the Mouse Trophoblast\nWe show that Atrxnull male mice are not viable and embryos die by around 9.5 dpc. Before death, Atrxnull embryos exhibit a markedly reduced mitotic index, suggesting a proliferative defect. Although the embryonic compartment of the conceptus appears initially normal, by 7.5 dpc Atrxnull embryos display abnormalities in development of the trophoblast, including a depletion in the population of TGCs surrounding the conceptus and a reduction in the size of the ectoplacental cone, which contains the diploid giant cell precursors [22]. TGCs are highly differentiated, postmitotic cells that ultimately form an epithelial layer at the periphery of the placenta, which interfaces with the maternal cells of the decidua [23]. These highly invasive cells are important for mediating initial invasion of the uterine tissue, but are also involved in remodelling the maternal decidua after implantation and in secreting hormones that regulate fetal and maternal growth [24]. Since Atrxnull embryos appear to implant normally, lethality is likely to arise due to a failure of TGC function later during development.\nEmbryonic lethality in mice in the absence of Atrx was a surprising finding, as there had been no suggestion of foetal loss in the human ATR-X syndrome. It is possible that the role of Atrx in the trophoblast is specific to mice and that ATRX has no role or is redundant in the human trophoblast. Indeed, the birth weight of babies with ATR-X syndrome is usually normal. An alternative explanation for the unexpectedly severe phenotype we observed in mice is that the Atrx Δ18Δneo deletion generated by Cre recombination completely ablates full-length Atrx protein (Figure 2E). In contrast, all disease-causing mutations characterised in human ATR-X pedigrees appear to give rise to hypomorphic alleles. Some full-length ATRX protein is detected in cases predicted to have truncating mutations (RJG, unpublished data), and residual ATPase activity in ATRX immunoprecipitates can be detected in Epstein-Barr virus-transformed lymphocytes of all human patients analysed to date (A. Argentaro and M. Mitson, unpublished data). The failure to observe a truly null ATRX allele among human patients strongly suggests that, as in the mouse, the complete absence of ATRX protein is incompatible with human fetal survival.\nWhile this study has revealed an unexpected role for Atrx in the murine trophectoderm, as a result of the early lethality observed in Atrxnull embryos it is not possible to rule out other roles for Atrx at later developmental stages in tissues of the embryo proper. Indeed, we show that Atrx is highly expressed throughout the entire developing embryo at 7.5 dpc (Figure 5B), and it is likely that Atrx function will turn out to be important for other differentiating tissues. Tetraploid aggregation experiments (in which mutant embryos are rescued with wild-type extraembryonic tissues) might shed more light on the role of Atrx during later mouse development, but these issues can be more subtly dissected by combining the conditional Atrx flox allele that we have generated with different tissue-specific Cre transgenes. As mentioned above, this approach has already revealed a critical role for Atrx during neuronal differentiation in adult mice [20]. Further evidence that Atrx is also required at later stages of mouse development is provided by the observed dramatic skewing against Atrx-negative cells in some somatic tissues of carrier female mice, whose tissues initially comprise a mosaic of Atrx-positive and Atrx-negative cells as a result of random X-inactivation (M. Muers, personal communication).\nAtrx joins an expanding list of mouse genes for which targeted disruption results in peri-implantation lethality as a result of trophoblast or placental abnormalities (reviewed in [25]). Comparison with other phenotypes might provide some insight into the role of Atrx in trophoblast development. Atrx-mutant embryos progress further than embryos nullizygous for factors involved in the initial specification of trophoblast stem cells (such as Cdx2) or in stem cell maintenance and proliferation (such as Eomes). Cdx2-mutant embryos fail to implant and die between 3.5 and 5.5 dpc [26], while Eomes-mutant blastocysts implant into the uterus, but arrest soon after implantation without forming organised embryonic or extraembryonic structures [27]. In contrast, Atrx-mutant embryos implant successfully and establish organised embryonic structures by 7.5 dpc. The Atrx-mutant phenotype closely resembles that observed in mice nullizygous for the basic helix-loop-helix transcription factor Hand1. Hand1-mutant conceptuses arrest at around 7.5 dpc and display a normal embryonic compartment, but, like Atrx-mutant embryos, ablation of Hand1 causes a reduction in the size of the ectoplacental cone and density of TGCs [28]. As with Atrx mutants, only arrested or resorbed Hand1-mutant conceptuses were recovered after 8.5 dpc. Also like Atrx, disruption of Hand1 specifically affects secondary giant cell formation, and primary trophoblast outgrowths from blastocysts appeared normal. Hand1 is required for terminal differentiation of secondary TGCs, and in its absence trophoblast cells arrest at a precursor stage in the ectoplacental cone [17,28]. Given the similarity of the Atrx- and Hand1-mutant phenotypes and the likelihood that Atrx acts as a transcriptional regulator by modifying chromatin structure, it will be of interest to determine whether Atrx is itself a regulator of Hand1 expression, or alternatively whether it acts as a co-regulator of one or more of the downstream transcriptional targets of Hand1. It is noteworthy that, in the brain-specific Atrx knockout mice, the defect was observed in terminally differentiating neurons [20]. The secondary TGCs affected in the universal Atrx knockout reported here represent one of the first terminally differentiated tissues in the developing mouse, and this may point to the requirement for Atrx in the high-level expression of some tissue-specific genes during the final stages of differentiation. Interestingly, the α-globin genes, the only confirmed transcriptional targets of regulation by human ATRX, are also highly expressed specifically during terminal differentiation within the erythroid lineage.\n\nAtrx Escapes Imprinted X-Inactivation in Extraembryonic Tissues of Carrier Female Mice\nAnother surprising finding of this study is that, in carrier female embryos, a paternally inherited Atrx WT allele appears to escape the process of imprinted X-inactivation, which ordinarily silences the Xp chromosome in the extraembryonic compartment of female murine tissues [18]. Silencing of the Atrx WT allele on Xp should render these females null for Atrx in the extraembryonic tissues, since the normally active Xm chromosome carries the Atrx Δ18Δneo allele. Although not phenotypically normal, some Atrx carrier females developed to term and went on to reproduce. Thus, the failure to correctly silence the paternally derived Atrx WT allele in the extraembryonic tissues of carrier females is consistent with our observations that in Atrxnull males, the Atrx protein plays an essential role in the development of the trophoblast and is necessary for survival in utero in the mouse.\nThe survival of Atrx carrier females contrasts with the phenotypes seen in carriers of mutations of other murine X-linked genes known to be essential in the extraembryonic compartment. For example, targeted disruption of the dyskerin (Dkc1), glucose 6-phosphate dehydrogenase (G6PD), and choroideremia (Chm) genes cause embryonic lethality in null male embryos through defects of the extraembryonic-derived tissues [29–31]. Female mice carrying mutations of these genes on the maternally inherited X chromosome also die in utero, whereas females that inherit the mutation on the Xp chromosome survive. Thus, unlike Atrx, these genes and/or their effects on cell growth are unable to circumvent the processes that ultimately cause all cells in the extraembryonic tissues to express only the maternally derived X chromosome. How might expression of the paternal Atrx WT allele be maintained in the extraembryonic tissues of the Atrx carrier females?\nOne possibility is that, like some other X-linked genes, silencing of the Atrx gene on Xp is incomplete, such that there is always a low-level, leaky output of Atrx from a normally inactivated Xp chromosome in extraembryonic tissues. However, it was recently demonstrated that the paternal Atrx (called Xnp) allele is completely silenced in a normal mouse trophoblast stem cell line [32], suggesting that Atrx does not normally escape imprinted X-inactivation in the extraembryonic tissues of wild-type females. Thus, the expression of the Xp-linked Atrx WT allele that we observed is unique to female carriers of the Atrx null allele.\nPerhaps a more likely explanation for this phenomenon stems from experimental observations suggesting that imprinted X-inactivation is not imposed on all precursors of the mouse extraembryonic tissues: A subpopulation of cells may escape this process and make a random “choice” of which X chromosome will be inactivated. On average, 50% of the cells in this randomly inactivating subpopulation would be expected to maintain an active Xp chromosome. In support of this hypothesis, it has been demonstrated that expression of paternally transmitted X-linked lacZ [33,34] and GFP [35] transgenes failed to be silenced in a small subpopulation of extraembryonic cells. Further, it has been shown that in a subpopulation of extraembryonic cells, it is the Xm rather than the Xp that undergoes late replication, a molecular correlate of the inactive state [18,36]. Although initially small and quickly diluted in normal embryos, the cellular subpopulation that inactivates the Xm chromosome could rapidly expand to replace the normally imprinted cells in extraembryonic lineages if the normal silencing of Xp compromises cell growth or differentiation. Interestingly, it has been suggested that the size of the population that initially escapes imprinting may range widely (from 0% to 30%), even between genetically identical embryos [37], and this may account for the variable phenotype observed among females bearing Xm-linked mutant alleles of genes essential for normal extraembryonic development [38]. Put simply, carrier females bearing a small initial population of escaping cells would be more severely affected than those bearing a larger population. This could explain why we have observed significant phenotypic variation among Atrx carrier females, with some carriers dying in utero by 9.5 dpc (Table 1) and others developing to term.\nAnother possible mechanism is that inactivation of the paternal X proceeds normally in all cells, but subsequently the Atrx gene within individual cells is reactivated. Alternatively, in the absence of Atrx, the paternal allele may partially escape the normal process of silencing. In both of these cases, other genes on the paternal X chromosome must be inactivated and remain so, since blocking inactivation of the entire Xp chromosome causes embryonic lethality due to biallelic expression of X-linked genes in the trophoblast [39].\n\nSummary\nATR-X syndrome is the first human genetic disease known to be caused by mutations in a chromatin remodelling factor. At present we do not know how ATRX influences gene expression or what effect it has on cell behaviour. Nevertheless, we have previously noted that none of the natural mutations causing ATR-X syndrome are nulls, which suggests that it plays a critical role in normal development. Results of conditional inactivation of Atrx in the developing mouse forebrain, based on the Atrx flox allele described here, shows that Atrx exerts a major effect on terminally differentiating neurons. Conditional inactivation of Atrx in other tissues is underway. Here we have shown that animal-wide disruption of the Atrx gene causes a severe embryonic-lethal phenotype, revealing an essential role for Atrx in the formation of the murine trophoblast. In addition, Atrx appears to escape imprinted X-chromosome inactivation in the extraembryonic tissues of some carrier female mice."}

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investigated the role of the Atrx protein in mouse development. By using a conditional knockout approach, we ablated the full-length Atrx protein first in ES cells and embryoid bodies, and then in developing mouse embryos.\n\nAtrx in ES Cells\nAtrxnull ES cells could not be recovered by direct targeting and were eventually generated by adopting a conditional targeting approach. This is consistent with our observation that Atrx is highly expressed in ES cells, and that the absence of full-length Atrx imparts a growth disadvantage relative to cells bearing a functional Atrx allele. At present, the cause of the proliferative delay in Atrxnull ES cells is not known. Interestingly, we demonstrated that apoptosis is not significantly up-regulated in ES cells lacking Atrx and is only mildly elevated in Atrxnull 7.5 dpc mouse embryos. In contrast, it was recently shown that the loss of Atrx markedly increased the apoptotic population in the differentiating cells of the embryonic cortex and postnatal hippocampus, when Atrx expression was ablated in the developing mouse forebrain using the Atrx flox allele described here [20]. The human ATRX protein has been shown to associate in a complex with Daxx [8], a protein that has been implicated in multiple pathways for the regulation of apoptosis [21]. It is possible that disruption of the mouse Atrx-Daxx complex (by ablation of the Atrx protein) could have triggered a universal proapoptotic response. However, our observations in ES cells demonstrate that the induction of apoptosis is not an automatic response triggered by the removal of Atrx in all cell types, and suggest that the inappropriate apoptosis observed in the Atrx-mutant forebrain may reflect a requirement for Atrx during terminal differentiation.\n\nAn Unexpected Role for Atrx in Development of the Mouse Trophoblast\nWe show that Atrxnull male mice are not viable and embryos die by around 9.5 dpc. Before death, Atrxnull embryos exhibit a markedly reduced mitotic index, suggesting a proliferative defect. Although the embryonic compartment of the conceptus appears initially normal, by 7.5 dpc Atrxnull embryos display abnormalities in development of the trophoblast, including a depletion in the population of TGCs surrounding the conceptus and a reduction in the size of the ectoplacental cone, which contains the diploid giant cell precursors [22]. TGCs are highly differentiated, postmitotic cells that ultimately form an epithelial layer at the periphery of the placenta, which interfaces with the maternal cells of the decidua [23]. These highly invasive cells are important for mediating initial invasion of the uterine tissue, but are also involved in remodelling the maternal decidua after implantation and in secreting hormones that regulate fetal and maternal growth [24]. Since Atrxnull embryos appear to implant normally, lethality is likely to arise due to a failure of TGC function later during development.\nEmbryonic lethality in mice in the absence of Atrx was a surprising finding, as there had been no suggestion of foetal loss in the human ATR-X syndrome. It is possible that the role of Atrx in the trophoblast is specific to mice and that ATRX has no role or is redundant in the human trophoblast. Indeed, the birth weight of babies with ATR-X syndrome is usually normal. An alternative explanation for the unexpectedly severe phenotype we observed in mice is that the Atrx Δ18Δneo deletion generated by Cre recombination completely ablates full-length Atrx protein (Figure 2E). In contrast, all disease-causing mutations characterised in human ATR-X pedigrees appear to give rise to hypomorphic alleles. Some full-length ATRX protein is detected in cases predicted to have truncating mutations (RJG, unpublished data), and residual ATPase activity in ATRX immunoprecipitates can be detected in Epstein-Barr virus-transformed lymphocytes of all human patients analysed to date (A. Argentaro and M. Mitson, unpublished data). The failure to observe a truly null ATRX allele among human patients strongly suggests that, as in the mouse, the complete absence of ATRX protein is incompatible with human fetal survival.\nWhile this study has revealed an unexpected role for Atrx in the murine trophectoderm, as a result of the early lethality observed in Atrxnull embryos it is not possible to rule out other roles for Atrx at later developmental stages in tissues of the embryo proper. Indeed, we show that Atrx is highly expressed throughout the entire developing embryo at 7.5 dpc (Figure 5B), and it is likely that Atrx function will turn out to be important for other differentiating tissues. Tetraploid aggregation experiments (in which mutant embryos are rescued with wild-type extraembryonic tissues) might shed more light on the role of Atrx during later mouse development, but these issues can be more subtly dissected by combining the conditional Atrx flox allele that we have generated with different tissue-specific Cre transgenes. As mentioned above, this approach has already revealed a critical role for Atrx during neuronal differentiation in adult mice [20]. Further evidence that Atrx is also required at later stages of mouse development is provided by the observed dramatic skewing against Atrx-negative cells in some somatic tissues of carrier female mice, whose tissues initially comprise a mosaic of Atrx-positive and Atrx-negative cells as a result of random X-inactivation (M. Muers, personal communication).\nAtrx joins an expanding list of mouse genes for which targeted disruption results in peri-implantation lethality as a result of trophoblast or placental abnormalities (reviewed in [25]). Comparison with other phenotypes might provide some insight into the role of Atrx in trophoblast development. Atrx-mutant embryos progress further than embryos nullizygous for factors involved in the initial specification of trophoblast stem cells (such as Cdx2) or in stem cell maintenance and proliferation (such as Eomes). Cdx2-mutant embryos fail to implant and die between 3.5 and 5.5 dpc [26], while Eomes-mutant blastocysts implant into the uterus, but arrest soon after implantation without forming organised embryonic or extraembryonic structures [27]. In contrast, Atrx-mutant embryos implant successfully and establish organised embryonic structures by 7.5 dpc. The Atrx-mutant phenotype closely resembles that observed in mice nullizygous for the basic helix-loop-helix transcription factor Hand1. Hand1-mutant conceptuses arrest at around 7.5 dpc and display a normal embryonic compartment, but, like Atrx-mutant embryos, ablation of Hand1 causes a reduction in the size of the ectoplacental cone and density of TGCs [28]. As with Atrx mutants, only arrested or resorbed Hand1-mutant conceptuses were recovered after 8.5 dpc. Also like Atrx, disruption of Hand1 specifically affects secondary giant cell formation, and primary trophoblast outgrowths from blastocysts appeared normal. Hand1 is required for terminal differentiation of secondary TGCs, and in its absence trophoblast cells arrest at a precursor stage in the ectoplacental cone [17,28]. Given the similarity of the Atrx- and Hand1-mutant phenotypes and the likelihood that Atrx acts as a transcriptional regulator by modifying chromatin structure, it will be of interest to determine whether Atrx is itself a regulator of Hand1 expression, or alternatively whether it acts as a co-regulator of one or more of the downstream transcriptional targets of Hand1. It is noteworthy that, in the brain-specific Atrx knockout mice, the defect was observed in terminally differentiating neurons [20]. The secondary TGCs affected in the universal Atrx knockout reported here represent one of the first terminally differentiated tissues in the developing mouse, and this may point to the requirement for Atrx in the high-level expression of some tissue-specific genes during the final stages of differentiation. Interestingly, the α-globin genes, the only confirmed transcriptional targets of regulation by human ATRX, are also highly expressed specifically during terminal differentiation within the erythroid lineage.\n\nAtrx Escapes Imprinted X-Inactivation in Extraembryonic Tissues of Carrier Female Mice\nAnother surprising finding of this study is that, in carrier female embryos, a paternally inherited Atrx WT allele appears to escape the process of imprinted X-inactivation, which ordinarily silences the Xp chromosome in the extraembryonic compartment of female murine tissues [18]. Silencing of the Atrx WT allele on Xp should render these females null for Atrx in the extraembryonic tissues, since the normally active Xm chromosome carries the Atrx Δ18Δneo allele. Although not phenotypically normal, some Atrx carrier females developed to term and went on to reproduce. Thus, the failure to correctly silence the paternally derived Atrx WT allele in the extraembryonic tissues of carrier females is consistent with our observations that in Atrxnull males, the Atrx protein plays an essential role in the development of the trophoblast and is necessary for survival in utero in the mouse.\nThe survival of Atrx carrier females contrasts with the phenotypes seen in carriers of mutations of other murine X-linked genes known to be essential in the extraembryonic compartment. For example, targeted disruption of the dyskerin (Dkc1), glucose 6-phosphate dehydrogenase (G6PD), and choroideremia (Chm) genes cause embryonic lethality in null male embryos through defects of the extraembryonic-derived tissues [29–31]. Female mice carrying mutations of these genes on the maternally inherited X chromosome also die in utero, whereas females that inherit the mutation on the Xp chromosome survive. Thus, unlike Atrx, these genes and/or their effects on cell growth are unable to circumvent the processes that ultimately cause all cells in the extraembryonic tissues to express only the maternally derived X chromosome. How might expression of the paternal Atrx WT allele be maintained in the extraembryonic tissues of the Atrx carrier females?\nOne possibility is that, like some other X-linked genes, silencing of the Atrx gene on Xp is incomplete, such that there is always a low-level, leaky output of Atrx from a normally inactivated Xp chromosome in extraembryonic tissues. However, it was recently demonstrated that the paternal Atrx (called Xnp) allele is completely silenced in a normal mouse trophoblast stem cell line [32], suggesting that Atrx does not normally escape imprinted X-inactivation in the extraembryonic tissues of wild-type females. Thus, the expression of the Xp-linked Atrx WT allele that we observed is unique to female carriers of the Atrx null allele.\nPerhaps a more likely explanation for this phenomenon stems from experimental observations suggesting that imprinted X-inactivation is not imposed on all precursors of the mouse extraembryonic tissues: A subpopulation of cells may escape this process and make a random “choice” of which X chromosome will be inactivated. On average, 50% of the cells in this randomly inactivating subpopulation would be expected to maintain an active Xp chromosome. In support of this hypothesis, it has been demonstrated that expression of paternally transmitted X-linked lacZ [33,34] and GFP [35] transgenes failed to be silenced in a small subpopulation of extraembryonic cells. Further, it has been shown that in a subpopulation of extraembryonic cells, it is the Xm rather than the Xp that undergoes late replication, a molecular correlate of the inactive state [18,36]. Although initially small and quickly diluted in normal embryos, the cellular subpopulation that inactivates the Xm chromosome could rapidly expand to replace the normally imprinted cells in extraembryonic lineages if the normal silencing of Xp compromises cell growth or differentiation. Interestingly, it has been suggested that the size of the population that initially escapes imprinting may range widely (from 0% to 30%), even between genetically identical embryos [37], and this may account for the variable phenotype observed among females bearing Xm-linked mutant alleles of genes essential for normal extraembryonic development [38]. Put simply, carrier females bearing a small initial population of escaping cells would be more severely affected than those bearing a larger population. This could explain why we have observed significant phenotypic variation among Atrx carrier females, with some carriers dying in utero by 9.5 dpc (Table 1) and others developing to term.\nAnother possible mechanism is that inactivation of the paternal X proceeds normally in all cells, but subsequently the Atrx gene within individual cells is reactivated. Alternatively, in the absence of Atrx, the paternal allele may partially escape the normal process of silencing. In both of these cases, other genes on the paternal X chromosome must be inactivated and remain so, since blocking inactivation of the entire Xp chromosome causes embryonic lethality due to biallelic expression of X-linked genes in the trophoblast [39].\n\nSummary\nATR-X syndrome is the first human genetic disease known to be caused by mutations in a chromatin remodelling factor. At present we do not know how ATRX influences gene expression or what effect it has on cell behaviour. Nevertheless, we have previously noted that none of the natural mutations causing ATR-X syndrome are nulls, which suggests that it plays a critical role in normal development. Results of conditional inactivation of Atrx in the developing mouse forebrain, based on the Atrx flox allele described here, shows that Atrx exerts a major effect on terminally differentiating neurons. Conditional inactivation of Atrx in other tissues is underway. Here we have shown that animal-wide disruption of the Atrx gene causes a severe embryonic-lethal phenotype, revealing an essential role for Atrx in the formation of the murine trophoblast. In addition, Atrx appears to escape imprinted X-chromosome inactivation in the extraembryonic tissues of some carrier female mice."}

{"project":"2_test","denotations":[{"id":"16628246-15668733-85799759","span":{"begin":1141,"end":1143},"obj":"15668733"},{"id":"16628246-12953102-85799760","span":{"begin":1221,"end":1222},"obj":"12953102"},{"id":"16628246-15077145-85799761","span":{"begin":1314,"end":1316},"obj":"15077145"},{"id":"16628246-6895086-85799762","span":{"begin":2386,"end":2388},"obj":"6895086"},{"id":"16628246-10873707-85799763","span":{"begin":2573,"end":2575},"obj":"10873707"},{"id":"16628246-7985020-85799764","span":{"begin":2818,"end":2820},"obj":"7985020"},{"id":"16628246-15668733-85799765","span":{"begin":5127,"end":5129},"obj":"15668733"},{"id":"16628246-11433360-85799766","span":{"begin":5671,"end":5673},"obj":"11433360"},{"id":"16628246-9052785-85799767","span":{"begin":6072,"end":6074},"obj":"9052785"},{"id":"16628246-10716450-85799768","span":{"begin":6234,"end":6236},"obj":"10716450"},{"id":"16628246-9500551-85799769","span":{"begin":6708,"end":6710},"obj":"9500551"},{"id":"16628246-10611232-85799770","span":{"begin":7132,"end":7134},"obj":"10611232"},{"id":"16628246-9500551-85799771","span":{"begin":7135,"end":7137},"obj":"9500551"},{"id":"16628246-15668733-85799772","span":{"begin":7639,"end":7641},"obj":"15668733"},{"id":"16628246-1152998-85799773","span":{"begin":8527,"end":8529},"obj":"1152998"},{"id":"16628246-12400016-85799774","span":{"begin":9556,"end":9558},"obj":"12400016"},{"id":"16628246-12169625-85799774","span":{"begin":9556,"end":9558},"obj":"12169625"},{"id":"16628246-15242790-85799774","span":{"begin":9556,"end":9558},"obj":"15242790"},{"id":"16628246-14661031-85799775","span":{"begin":10472,"end":10474},"obj":"14661031"},{"id":"16628246-7834909-85799776","span":{"begin":11286,"end":11288},"obj":"7834909"},{"id":"16628246-10794075-85799777","span":{"begin":11289,"end":11291},"obj":"10794075"},{"id":"16628246-11252054-85799778","span":{"begin":11302,"end":11304},"obj":"11252054"},{"id":"16628246-1152998-85799779","span":{"begin":11575,"end":11577},"obj":"1152998"},{"id":"16628246-958416-85799780","span":{"begin":11578,"end":11580},"obj":"958416"},{"id":"16628246-11698184-85799781","span":{"begin":12053,"end":12055},"obj":"11698184"},{"id":"16628246-11051544-85799782","span":{"begin":12220,"end":12222},"obj":"11051544"},{"id":"16628246-9009199-85799783","span":{"begin":13096,"end":13098},"obj":"9009199"},{"id":"T69494","span":{"begin":1141,"end":1143},"obj":"15668733"},{"id":"T51832","span":{"begin":1221,"end":1222},"obj":"12953102"},{"id":"T83532","span":{"begin":1314,"end":1316},"obj":"15077145"},{"id":"T47412","span":{"begin":2386,"end":2388},"obj":"6895086"},{"id":"T89259","span":{"begin":2573,"end":2575},"obj":"10873707"},{"id":"T98024","span":{"begin":2818,"end":2820},"obj":"7985020"},{"id":"T95738","span":{"begin":5127,"end":5129},"obj":"15668733"},{"id":"T36669","span":{"begin":5671,"end":5673},"obj":"11433360"},{"id":"T78131","span":{"begin":6072,"end":6074},"obj":"9052785"},{"id":"T46656","span":{"begin":6234,"end":6236},"obj":"10716450"},{"id":"T27799","span":{"begin":6708,"end":6710},"obj":"9500551"},{"id":"T13124","span":{"begin":7132,"end":7134},"obj":"10611232"},{"id":"T42247","span":{"begin":7135,"end":7137},"obj":"9500551"},{"id":"T83367","span":{"begin":7639,"end":7641},"obj":"15668733"},{"id":"T3361","span":{"begin":8527,"end":8529},"obj":"1152998"},{"id":"T78774","span":{"begin":9556,"end":9558},"obj":"12400016"},{"id":"T99673","span":{"begin":9556,"end":9558},"obj":"12169625"},{"id":"T50636","span":{"begin":9556,"end":9558},"obj":"15242790"},{"id":"T87099","span":{"begin":10472,"end":10474},"obj":"14661031"},{"id":"T81121","span":{"begin":11286,"end":11288},"obj":"7834909"},{"id":"T60587","span":{"begin":11289,"end":11291},"obj":"10794075"},{"id":"T75568","span":{"begin":11302,"end":11304},"obj":"11252054"},{"id":"T99758","span":{"begin":11575,"end":11577},"obj":"1152998"},{"id":"T9314","span":{"begin":11578,"end":11580},"obj":"958416"},{"id":"T45193","span":{"begin":12053,"end":12055},"obj":"11698184"},{"id":"T45487","span":{"begin":12220,"end":12222},"obj":"11051544"},{"id":"T9506","span":{"begin":13096,"end":13098},"obj":"9009199"}],"text":"Discussion\nWe investigated the role of the Atrx protein in mouse development. By using a conditional knockout approach, we ablated the full-length Atrx protein first in ES cells and embryoid bodies, and then in developing mouse embryos.\n\nAtrx in ES Cells\nAtrxnull ES cells could not be recovered by direct targeting and were eventually generated by adopting a conditional targeting approach. This is consistent with our observation that Atrx is highly expressed in ES cells, and that the absence of full-length Atrx imparts a growth disadvantage relative to cells bearing a functional Atrx allele. At present, the cause of the proliferative delay in Atrxnull ES cells is not known. Interestingly, we demonstrated that apoptosis is not significantly up-regulated in ES cells lacking Atrx and is only mildly elevated in Atrxnull 7.5 dpc mouse embryos. In contrast, it was recently shown that the loss of Atrx markedly increased the apoptotic population in the differentiating cells of the embryonic cortex and postnatal hippocampus, when Atrx expression was ablated in the developing mouse forebrain using the Atrx flox allele described here [20]. The human ATRX protein has been shown to associate in a complex with Daxx [8], a protein that has been implicated in multiple pathways for the regulation of apoptosis [21]. It is possible that disruption of the mouse Atrx-Daxx complex (by ablation of the Atrx protein) could have triggered a universal proapoptotic response. However, our observations in ES cells demonstrate that the induction of apoptosis is not an automatic response triggered by the removal of Atrx in all cell types, and suggest that the inappropriate apoptosis observed in the Atrx-mutant forebrain may reflect a requirement for Atrx during terminal differentiation.\n\nAn Unexpected Role for Atrx in Development of the Mouse Trophoblast\nWe show that Atrxnull male mice are not viable and embryos die by around 9.5 dpc. Before death, Atrxnull embryos exhibit a markedly reduced mitotic index, suggesting a proliferative defect. Although the embryonic compartment of the conceptus appears initially normal, by 7.5 dpc Atrxnull embryos display abnormalities in development of the trophoblast, including a depletion in the population of TGCs surrounding the conceptus and a reduction in the size of the ectoplacental cone, which contains the diploid giant cell precursors [22]. TGCs are highly differentiated, postmitotic cells that ultimately form an epithelial layer at the periphery of the placenta, which interfaces with the maternal cells of the decidua [23]. These highly invasive cells are important for mediating initial invasion of the uterine tissue, but are also involved in remodelling the maternal decidua after implantation and in secreting hormones that regulate fetal and maternal growth [24]. Since Atrxnull embryos appear to implant normally, lethality is likely to arise due to a failure of TGC function later during development.\nEmbryonic lethality in mice in the absence of Atrx was a surprising finding, as there had been no suggestion of foetal loss in the human ATR-X syndrome. It is possible that the role of Atrx in the trophoblast is specific to mice and that ATRX has no role or is redundant in the human trophoblast. Indeed, the birth weight of babies with ATR-X syndrome is usually normal. An alternative explanation for the unexpectedly severe phenotype we observed in mice is that the Atrx Δ18Δneo deletion generated by Cre recombination completely ablates full-length Atrx protein (Figure 2E). In contrast, all disease-causing mutations characterised in human ATR-X pedigrees appear to give rise to hypomorphic alleles. Some full-length ATRX protein is detected in cases predicted to have truncating mutations (RJG, unpublished data), and residual ATPase activity in ATRX immunoprecipitates can be detected in Epstein-Barr virus-transformed lymphocytes of all human patients analysed to date (A. Argentaro and M. Mitson, unpublished data). The failure to observe a truly null ATRX allele among human patients strongly suggests that, as in the mouse, the complete absence of ATRX protein is incompatible with human fetal survival.\nWhile this study has revealed an unexpected role for Atrx in the murine trophectoderm, as a result of the early lethality observed in Atrxnull embryos it is not possible to rule out other roles for Atrx at later developmental stages in tissues of the embryo proper. Indeed, we show that Atrx is highly expressed throughout the entire developing embryo at 7.5 dpc (Figure 5B), and it is likely that Atrx function will turn out to be important for other differentiating tissues. Tetraploid aggregation experiments (in which mutant embryos are rescued with wild-type extraembryonic tissues) might shed more light on the role of Atrx during later mouse development, but these issues can be more subtly dissected by combining the conditional Atrx flox allele that we have generated with different tissue-specific Cre transgenes. As mentioned above, this approach has already revealed a critical role for Atrx during neuronal differentiation in adult mice [20]. Further evidence that Atrx is also required at later stages of mouse development is provided by the observed dramatic skewing against Atrx-negative cells in some somatic tissues of carrier female mice, whose tissues initially comprise a mosaic of Atrx-positive and Atrx-negative cells as a result of random X-inactivation (M. Muers, personal communication).\nAtrx joins an expanding list of mouse genes for which targeted disruption results in peri-implantation lethality as a result of trophoblast or placental abnormalities (reviewed in [25]). Comparison with other phenotypes might provide some insight into the role of Atrx in trophoblast development. Atrx-mutant embryos progress further than embryos nullizygous for factors involved in the initial specification of trophoblast stem cells (such as Cdx2) or in stem cell maintenance and proliferation (such as Eomes). Cdx2-mutant embryos fail to implant and die between 3.5 and 5.5 dpc [26], while Eomes-mutant blastocysts implant into the uterus, but arrest soon after implantation without forming organised embryonic or extraembryonic structures [27]. In contrast, Atrx-mutant embryos implant successfully and establish organised embryonic structures by 7.5 dpc. The Atrx-mutant phenotype closely resembles that observed in mice nullizygous for the basic helix-loop-helix transcription factor Hand1. Hand1-mutant conceptuses arrest at around 7.5 dpc and display a normal embryonic compartment, but, like Atrx-mutant embryos, ablation of Hand1 causes a reduction in the size of the ectoplacental cone and density of TGCs [28]. As with Atrx mutants, only arrested or resorbed Hand1-mutant conceptuses were recovered after 8.5 dpc. Also like Atrx, disruption of Hand1 specifically affects secondary giant cell formation, and primary trophoblast outgrowths from blastocysts appeared normal. Hand1 is required for terminal differentiation of secondary TGCs, and in its absence trophoblast cells arrest at a precursor stage in the ectoplacental cone [17,28]. Given the similarity of the Atrx- and Hand1-mutant phenotypes and the likelihood that Atrx acts as a transcriptional regulator by modifying chromatin structure, it will be of interest to determine whether Atrx is itself a regulator of Hand1 expression, or alternatively whether it acts as a co-regulator of one or more of the downstream transcriptional targets of Hand1. It is noteworthy that, in the brain-specific Atrx knockout mice, the defect was observed in terminally differentiating neurons [20]. The secondary TGCs affected in the universal Atrx knockout reported here represent one of the first terminally differentiated tissues in the developing mouse, and this may point to the requirement for Atrx in the high-level expression of some tissue-specific genes during the final stages of differentiation. Interestingly, the α-globin genes, the only confirmed transcriptional targets of regulation by human ATRX, are also highly expressed specifically during terminal differentiation within the erythroid lineage.\n\nAtrx Escapes Imprinted X-Inactivation in Extraembryonic Tissues of Carrier Female Mice\nAnother surprising finding of this study is that, in carrier female embryos, a paternally inherited Atrx WT allele appears to escape the process of imprinted X-inactivation, which ordinarily silences the Xp chromosome in the extraembryonic compartment of female murine tissues [18]. Silencing of the Atrx WT allele on Xp should render these females null for Atrx in the extraembryonic tissues, since the normally active Xm chromosome carries the Atrx Δ18Δneo allele. Although not phenotypically normal, some Atrx carrier females developed to term and went on to reproduce. Thus, the failure to correctly silence the paternally derived Atrx WT allele in the extraembryonic tissues of carrier females is consistent with our observations that in Atrxnull males, the Atrx protein plays an essential role in the development of the trophoblast and is necessary for survival in utero in the mouse.\nThe survival of Atrx carrier females contrasts with the phenotypes seen in carriers of mutations of other murine X-linked genes known to be essential in the extraembryonic compartment. For example, targeted disruption of the dyskerin (Dkc1), glucose 6-phosphate dehydrogenase (G6PD), and choroideremia (Chm) genes cause embryonic lethality in null male embryos through defects of the extraembryonic-derived tissues [29–31]. Female mice carrying mutations of these genes on the maternally inherited X chromosome also die in utero, whereas females that inherit the mutation on the Xp chromosome survive. Thus, unlike Atrx, these genes and/or their effects on cell growth are unable to circumvent the processes that ultimately cause all cells in the extraembryonic tissues to express only the maternally derived X chromosome. How might expression of the paternal Atrx WT allele be maintained in the extraembryonic tissues of the Atrx carrier females?\nOne possibility is that, like some other X-linked genes, silencing of the Atrx gene on Xp is incomplete, such that there is always a low-level, leaky output of Atrx from a normally inactivated Xp chromosome in extraembryonic tissues. However, it was recently demonstrated that the paternal Atrx (called Xnp) allele is completely silenced in a normal mouse trophoblast stem cell line [32], suggesting that Atrx does not normally escape imprinted X-inactivation in the extraembryonic tissues of wild-type females. Thus, the expression of the Xp-linked Atrx WT allele that we observed is unique to female carriers of the Atrx null allele.\nPerhaps a more likely explanation for this phenomenon stems from experimental observations suggesting that imprinted X-inactivation is not imposed on all precursors of the mouse extraembryonic tissues: A subpopulation of cells may escape this process and make a random “choice” of which X chromosome will be inactivated. On average, 50% of the cells in this randomly inactivating subpopulation would be expected to maintain an active Xp chromosome. In support of this hypothesis, it has been demonstrated that expression of paternally transmitted X-linked lacZ [33,34] and GFP [35] transgenes failed to be silenced in a small subpopulation of extraembryonic cells. Further, it has been shown that in a subpopulation of extraembryonic cells, it is the Xm rather than the Xp that undergoes late replication, a molecular correlate of the inactive state [18,36]. Although initially small and quickly diluted in normal embryos, the cellular subpopulation that inactivates the Xm chromosome could rapidly expand to replace the normally imprinted cells in extraembryonic lineages if the normal silencing of Xp compromises cell growth or differentiation. Interestingly, it has been suggested that the size of the population that initially escapes imprinting may range widely (from 0% to 30%), even between genetically identical embryos [37], and this may account for the variable phenotype observed among females bearing Xm-linked mutant alleles of genes essential for normal extraembryonic development [38]. Put simply, carrier females bearing a small initial population of escaping cells would be more severely affected than those bearing a larger population. This could explain why we have observed significant phenotypic variation among Atrx carrier females, with some carriers dying in utero by 9.5 dpc (Table 1) and others developing to term.\nAnother possible mechanism is that inactivation of the paternal X proceeds normally in all cells, but subsequently the Atrx gene within individual cells is reactivated. Alternatively, in the absence of Atrx, the paternal allele may partially escape the normal process of silencing. In both of these cases, other genes on the paternal X chromosome must be inactivated and remain so, since blocking inactivation of the entire Xp chromosome causes embryonic lethality due to biallelic expression of X-linked genes in the trophoblast [39].\n\nSummary\nATR-X syndrome is the first human genetic disease known to be caused by mutations in a chromatin remodelling factor. At present we do not know how ATRX influences gene expression or what effect it has on cell behaviour. Nevertheless, we have previously noted that none of the natural mutations causing ATR-X syndrome are nulls, which suggests that it plays a critical role in normal development. Results of conditional inactivation of Atrx in the developing mouse forebrain, based on the Atrx flox allele described here, shows that Atrx exerts a major effect on terminally differentiating neurons. Conditional inactivation of Atrx in other tissues is underway. Here we have shown that animal-wide disruption of the Atrx gene causes a severe embryonic-lethal phenotype, revealing an essential role for Atrx in the formation of the murine trophoblast. In addition, Atrx appears to escape imprinted X-chromosome inactivation in the extraembryonic tissues of some carrier female mice."}

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investigated the role of the Atrx protein in mouse development. By using a conditional knockout approach, we ablated the full-length Atrx protein first in ES cells and embryoid bodies, and then in developing mouse embryos.\n\nAtrx in ES Cells\nAtrxnull ES cells could not be recovered by direct targeting and were eventually generated by adopting a conditional targeting approach. This is consistent with our observation that Atrx is highly expressed in ES cells, and that the absence of full-length Atrx imparts a growth disadvantage relative to cells bearing a functional Atrx allele. At present, the cause of the proliferative delay in Atrxnull ES cells is not known. Interestingly, we demonstrated that apoptosis is not significantly up-regulated in ES cells lacking Atrx and is only mildly elevated in Atrxnull 7.5 dpc mouse embryos. In contrast, it was recently shown that the loss of Atrx markedly increased the apoptotic population in the differentiating cells of the embryonic cortex and postnatal hippocampus, when Atrx expression was ablated in the developing mouse forebrain using the Atrx flox allele described here [20]. The human ATRX protein has been shown to associate in a complex with Daxx [8], a protein that has been implicated in multiple pathways for the regulation of apoptosis [21]. It is possible that disruption of the mouse Atrx-Daxx complex (by ablation of the Atrx protein) could have triggered a universal proapoptotic response. However, our observations in ES cells demonstrate that the induction of apoptosis is not an automatic response triggered by the removal of Atrx in all cell types, and suggest that the inappropriate apoptosis observed in the Atrx-mutant forebrain may reflect a requirement for Atrx during terminal differentiation.\n\nAn Unexpected Role for Atrx in Development of the Mouse Trophoblast\nWe show that Atrxnull male mice are not viable and embryos die by around 9.5 dpc. Before death, Atrxnull embryos exhibit a markedly reduced mitotic index, suggesting a proliferative defect. Although the embryonic compartment of the conceptus appears initially normal, by 7.5 dpc Atrxnull embryos display abnormalities in development of the trophoblast, including a depletion in the population of TGCs surrounding the conceptus and a reduction in the size of the ectoplacental cone, which contains the diploid giant cell precursors [22]. TGCs are highly differentiated, postmitotic cells that ultimately form an epithelial layer at the periphery of the placenta, which interfaces with the maternal cells of the decidua [23]. These highly invasive cells are important for mediating initial invasion of the uterine tissue, but are also involved in remodelling the maternal decidua after implantation and in secreting hormones that regulate fetal and maternal growth [24]. Since Atrxnull embryos appear to implant normally, lethality is likely to arise due to a failure of TGC function later during development.\nEmbryonic lethality in mice in the absence of Atrx was a surprising finding, as there had been no suggestion of foetal loss in the human ATR-X syndrome. It is possible that the role of Atrx in the trophoblast is specific to mice and that ATRX has no role or is redundant in the human trophoblast. Indeed, the birth weight of babies with ATR-X syndrome is usually normal. An alternative explanation for the unexpectedly severe phenotype we observed in mice is that the Atrx Δ18Δneo deletion generated by Cre recombination completely ablates full-length Atrx protein (Figure 2E). In contrast, all disease-causing mutations characterised in human ATR-X pedigrees appear to give rise to hypomorphic alleles. Some full-length ATRX protein is detected in cases predicted to have truncating mutations (RJG, unpublished data), and residual ATPase activity in ATRX immunoprecipitates can be detected in Epstein-Barr virus-transformed lymphocytes of all human patients analysed to date (A. Argentaro and M. Mitson, unpublished data). The failure to observe a truly null ATRX allele among human patients strongly suggests that, as in the mouse, the complete absence of ATRX protein is incompatible with human fetal survival.\nWhile this study has revealed an unexpected role for Atrx in the murine trophectoderm, as a result of the early lethality observed in Atrxnull embryos it is not possible to rule out other roles for Atrx at later developmental stages in tissues of the embryo proper. Indeed, we show that Atrx is highly expressed throughout the entire developing embryo at 7.5 dpc (Figure 5B), and it is likely that Atrx function will turn out to be important for other differentiating tissues. Tetraploid aggregation experiments (in which mutant embryos are rescued with wild-type extraembryonic tissues) might shed more light on the role of Atrx during later mouse development, but these issues can be more subtly dissected by combining the conditional Atrx flox allele that we have generated with different tissue-specific Cre transgenes. As mentioned above, this approach has already revealed a critical role for Atrx during neuronal differentiation in adult mice [20]. Further evidence that Atrx is also required at later stages of mouse development is provided by the observed dramatic skewing against Atrx-negative cells in some somatic tissues of carrier female mice, whose tissues initially comprise a mosaic of Atrx-positive and Atrx-negative cells as a result of random X-inactivation (M. Muers, personal communication).\nAtrx joins an expanding list of mouse genes for which targeted disruption results in peri-implantation lethality as a result of trophoblast or placental abnormalities (reviewed in [25]). Comparison with other phenotypes might provide some insight into the role of Atrx in trophoblast development. Atrx-mutant embryos progress further than embryos nullizygous for factors involved in the initial specification of trophoblast stem cells (such as Cdx2) or in stem cell maintenance and proliferation (such as Eomes). Cdx2-mutant embryos fail to implant and die between 3.5 and 5.5 dpc [26], while Eomes-mutant blastocysts implant into the uterus, but arrest soon after implantation without forming organised embryonic or extraembryonic structures [27]. In contrast, Atrx-mutant embryos implant successfully and establish organised embryonic structures by 7.5 dpc. The Atrx-mutant phenotype closely resembles that observed in mice nullizygous for the basic helix-loop-helix transcription factor Hand1. Hand1-mutant conceptuses arrest at around 7.5 dpc and display a normal embryonic compartment, but, like Atrx-mutant embryos, ablation of Hand1 causes a reduction in the size of the ectoplacental cone and density of TGCs [28]. As with Atrx mutants, only arrested or resorbed Hand1-mutant conceptuses were recovered after 8.5 dpc. Also like Atrx, disruption of Hand1 specifically affects secondary giant cell formation, and primary trophoblast outgrowths from blastocysts appeared normal. Hand1 is required for terminal differentiation of secondary TGCs, and in its absence trophoblast cells arrest at a precursor stage in the ectoplacental cone [17,28]. Given the similarity of the Atrx- and Hand1-mutant phenotypes and the likelihood that Atrx acts as a transcriptional regulator by modifying chromatin structure, it will be of interest to determine whether Atrx is itself a regulator of Hand1 expression, or alternatively whether it acts as a co-regulator of one or more of the downstream transcriptional targets of Hand1. It is noteworthy that, in the brain-specific Atrx knockout mice, the defect was observed in terminally differentiating neurons [20]. The secondary TGCs affected in the universal Atrx knockout reported here represent one of the first terminally differentiated tissues in the developing mouse, and this may point to the requirement for Atrx in the high-level expression of some tissue-specific genes during the final stages of differentiation. Interestingly, the α-globin genes, the only confirmed transcriptional targets of regulation by human ATRX, are also highly expressed specifically during terminal differentiation within the erythroid lineage.\n\nAtrx Escapes Imprinted X-Inactivation in Extraembryonic Tissues of Carrier Female Mice\nAnother surprising finding of this study is that, in carrier female embryos, a paternally inherited Atrx WT allele appears to escape the process of imprinted X-inactivation, which ordinarily silences the Xp chromosome in the extraembryonic compartment of female murine tissues [18]. Silencing of the Atrx WT allele on Xp should render these females null for Atrx in the extraembryonic tissues, since the normally active Xm chromosome carries the Atrx Δ18Δneo allele. Although not phenotypically normal, some Atrx carrier females developed to term and went on to reproduce. Thus, the failure to correctly silence the paternally derived Atrx WT allele in the extraembryonic tissues of carrier females is consistent with our observations that in Atrxnull males, the Atrx protein plays an essential role in the development of the trophoblast and is necessary for survival in utero in the mouse.\nThe survival of Atrx carrier females contrasts with the phenotypes seen in carriers of mutations of other murine X-linked genes known to be essential in the extraembryonic compartment. For example, targeted disruption of the dyskerin (Dkc1), glucose 6-phosphate dehydrogenase (G6PD), and choroideremia (Chm) genes cause embryonic lethality in null male embryos through defects of the extraembryonic-derived tissues [29–31]. Female mice carrying mutations of these genes on the maternally inherited X chromosome also die in utero, whereas females that inherit the mutation on the Xp chromosome survive. Thus, unlike Atrx, these genes and/or their effects on cell growth are unable to circumvent the processes that ultimately cause all cells in the extraembryonic tissues to express only the maternally derived X chromosome. How might expression of the paternal Atrx WT allele be maintained in the extraembryonic tissues of the Atrx carrier females?\nOne possibility is that, like some other X-linked genes, silencing of the Atrx gene on Xp is incomplete, such that there is always a low-level, leaky output of Atrx from a normally inactivated Xp chromosome in extraembryonic tissues. However, it was recently demonstrated that the paternal Atrx (called Xnp) allele is completely silenced in a normal mouse trophoblast stem cell line [32], suggesting that Atrx does not normally escape imprinted X-inactivation in the extraembryonic tissues of wild-type females. Thus, the expression of the Xp-linked Atrx WT allele that we observed is unique to female carriers of the Atrx null allele.\nPerhaps a more likely explanation for this phenomenon stems from experimental observations suggesting that imprinted X-inactivation is not imposed on all precursors of the mouse extraembryonic tissues: A subpopulation of cells may escape this process and make a random “choice” of which X chromosome will be inactivated. On average, 50% of the cells in this randomly inactivating subpopulation would be expected to maintain an active Xp chromosome. In support of this hypothesis, it has been demonstrated that expression of paternally transmitted X-linked lacZ [33,34] and GFP [35] transgenes failed to be silenced in a small subpopulation of extraembryonic cells. Further, it has been shown that in a subpopulation of extraembryonic cells, it is the Xm rather than the Xp that undergoes late replication, a molecular correlate of the inactive state [18,36]. Although initially small and quickly diluted in normal embryos, the cellular subpopulation that inactivates the Xm chromosome could rapidly expand to replace the normally imprinted cells in extraembryonic lineages if the normal silencing of Xp compromises cell growth or differentiation. Interestingly, it has been suggested that the size of the population that initially escapes imprinting may range widely (from 0% to 30%), even between genetically identical embryos [37], and this may account for the variable phenotype observed among females bearing Xm-linked mutant alleles of genes essential for normal extraembryonic development [38]. Put simply, carrier females bearing a small initial population of escaping cells would be more severely affected than those bearing a larger population. This could explain why we have observed significant phenotypic variation among Atrx carrier females, with some carriers dying in utero by 9.5 dpc (Table 1) and others developing to term.\nAnother possible mechanism is that inactivation of the paternal X proceeds normally in all cells, but subsequently the Atrx gene within individual cells is reactivated. Alternatively, in the absence of Atrx, the paternal allele may partially escape the normal process of silencing. In both of these cases, other genes on the paternal X chromosome must be inactivated and remain so, since blocking inactivation of the entire Xp chromosome causes embryonic lethality due to biallelic expression of X-linked genes in the trophoblast [39].\n\nSummary\nATR-X syndrome is the first human genetic disease known to be caused by mutations in a chromatin remodelling factor. At present we do not know how ATRX influences gene expression or what effect it has on cell behaviour. Nevertheless, we have previously noted that none of the natural mutations causing ATR-X syndrome are nulls, which suggests that it plays a critical role in normal development. Results of conditional inactivation of Atrx in the developing mouse forebrain, based on the Atrx flox allele described here, shows that Atrx exerts a major effect on terminally differentiating neurons. Conditional inactivation of Atrx in other tissues is underway. Here we have shown that animal-wide disruption of the Atrx gene causes a severe embryonic-lethal phenotype, revealing an essential role for Atrx in the formation of the murine trophoblast. In addition, Atrx appears to escape imprinted X-chromosome inactivation in the extraembryonic tissues of some carrier female mice."}