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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 Some full-length ATRX protein is detected in cases predicted to have truncating mutations (RJG, unpublished data), and residual ATPase activity in ATRX immunoprecipitates can be detected in Epstein-Barr virus-transformed lymphocytes of all human patients analysed to date (A. Argentaro and M. Mitson, unpublished data).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."}
craft-ca-core-ex-dev
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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."}
2_test
{"project":"2_test","denotations":[{"id":"16628246-6895086-85799762","span":{"begin":600,"end":602},"obj":"6895086"},{"id":"16628246-10873707-85799763","span":{"begin":787,"end":789},"obj":"10873707"},{"id":"16628246-7985020-85799764","span":{"begin":1032,"end":1034},"obj":"7985020"},{"id":"16628246-15668733-85799765","span":{"begin":3341,"end":3343},"obj":"15668733"},{"id":"16628246-11433360-85799766","span":{"begin":3885,"end":3887},"obj":"11433360"},{"id":"16628246-9052785-85799767","span":{"begin":4286,"end":4288},"obj":"9052785"},{"id":"16628246-10716450-85799768","span":{"begin":4448,"end":4450},"obj":"10716450"},{"id":"16628246-9500551-85799769","span":{"begin":4922,"end":4924},"obj":"9500551"},{"id":"16628246-10611232-85799770","span":{"begin":5346,"end":5348},"obj":"10611232"},{"id":"16628246-9500551-85799771","span":{"begin":5349,"end":5351},"obj":"9500551"},{"id":"16628246-15668733-85799772","span":{"begin":5853,"end":5855},"obj":"15668733"},{"id":"T47412","span":{"begin":600,"end":602},"obj":"6895086"},{"id":"T89259","span":{"begin":787,"end":789},"obj":"10873707"},{"id":"T98024","span":{"begin":1032,"end":1034},"obj":"7985020"},{"id":"T95738","span":{"begin":3341,"end":3343},"obj":"15668733"},{"id":"T36669","span":{"begin":3885,"end":3887},"obj":"11433360"},{"id":"T78131","span":{"begin":4286,"end":4288},"obj":"9052785"},{"id":"T46656","span":{"begin":4448,"end":4450},"obj":"10716450"},{"id":"T27799","span":{"begin":4922,"end":4924},"obj":"9500551"},{"id":"T13124","span":{"begin":5346,"end":5348},"obj":"10611232"},{"id":"T42247","span":{"begin":5349,"end":5351},"obj":"9500551"},{"id":"T83367","span":{"begin":5853,"end":5855},"obj":"15668733"}],"text":"An 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."}
craft-ca-core-dev
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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."}