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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]."}

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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]."}

{"project":"2_test","denotations":[{"id":"16628246-1152998-85799773","span":{"begin":365,"end":367},"obj":"1152998"},{"id":"16628246-12400016-85799774","span":{"begin":1394,"end":1396},"obj":"12400016"},{"id":"16628246-12169625-85799774","span":{"begin":1394,"end":1396},"obj":"12169625"},{"id":"16628246-15242790-85799774","span":{"begin":1394,"end":1396},"obj":"15242790"},{"id":"16628246-14661031-85799775","span":{"begin":2310,"end":2312},"obj":"14661031"},{"id":"16628246-7834909-85799776","span":{"begin":3124,"end":3126},"obj":"7834909"},{"id":"16628246-10794075-85799777","span":{"begin":3127,"end":3129},"obj":"10794075"},{"id":"16628246-11252054-85799778","span":{"begin":3140,"end":3142},"obj":"11252054"},{"id":"16628246-1152998-85799779","span":{"begin":3413,"end":3415},"obj":"1152998"},{"id":"16628246-958416-85799780","span":{"begin":3416,"end":3418},"obj":"958416"},{"id":"16628246-11698184-85799781","span":{"begin":3891,"end":3893},"obj":"11698184"},{"id":"16628246-11051544-85799782","span":{"begin":4058,"end":4060},"obj":"11051544"},{"id":"16628246-9009199-85799783","span":{"begin":4934,"end":4936},"obj":"9009199"},{"id":"T3361","span":{"begin":365,"end":367},"obj":"1152998"},{"id":"T78774","span":{"begin":1394,"end":1396},"obj":"12400016"},{"id":"T99673","span":{"begin":1394,"end":1396},"obj":"12169625"},{"id":"T50636","span":{"begin":1394,"end":1396},"obj":"15242790"},{"id":"T87099","span":{"begin":2310,"end":2312},"obj":"14661031"},{"id":"T81121","span":{"begin":3124,"end":3126},"obj":"7834909"},{"id":"T60587","span":{"begin":3127,"end":3129},"obj":"10794075"},{"id":"T75568","span":{"begin":3140,"end":3142},"obj":"11252054"},{"id":"T99758","span":{"begin":3413,"end":3415},"obj":"1152998"},{"id":"T9314","span":{"begin":3416,"end":3418},"obj":"958416"},{"id":"T45193","span":{"begin":3891,"end":3893},"obj":"11698184"},{"id":"T45487","span":{"begin":4058,"end":4060},"obj":"11051544"},{"id":"T9506","span":{"begin":4934,"end":4936},"obj":"9009199"}],"text":"Atrx 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]."}

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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]."}