Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development
Mice out of step on X inactivation X-chromosome inactivation is an essential process in female mammals that compensates for the presence of two X-chromosomes by suppressing gene expression from one of them. A study of the early developmental time course of X-chromosome inactivation in mice, rabbits...
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| Veröffentlicht in: | Nature (London) 2011-04, Vol.472 (7343), p.370-374 |
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| creator | Okamoto, Ikuhiro Patrat, Catherine Thépot, Dominique Peynot, Nathalie Fauque, Patricia Daniel, Nathalie Diabangouaya, Patricia Wolf, Jean-Philippe Renard, Jean-Paul Duranthon, Véronique Heard, Edith |
| description | Mice out of step on X inactivation
X-chromosome inactivation is an essential process in female mammals that compensates for the presence of two X-chromosomes by suppressing gene expression from one of them. A study of the early developmental time course of X-chromosome inactivation in mice, rabbits and humans shows that the processes in mice, in which most of previous analyses have been done, differ significantly from those in other eutherian species. The study highlights a diversity in X-inactivation regulation that may reflect the changing nature of developmental processes during evolution.
X-chromosome inactivation (XCI) in female mammals allows dosage compensation for X-linked gene products between the sexes
1
. The developmental regulation of this process has been extensively investigated in mice, where the X chromosome of paternal origin (Xp) is silenced during early embryogenesis owing to imprinted expression of the regulatory RNA,
Xist
(X-inactive specific transcript). Paternal XCI is reversed in the inner cell mass of the blastocyst and random XCI subsequently occurs in epiblast cells. Here we show that other eutherian mammals have very different strategies for initiating XCI. In rabbits and humans, the
Xist
homologue is not subject to imprinting and XCI begins later than in mice. Furthermore,
Xist
is upregulated on both X chromosomes in a high proportion of rabbit and human embryo cells, even in the inner cell mass. In rabbits, this triggers XCI on both X chromosomes in some cells. In humans, chromosome-wide XCI has not initiated even by the blastocyst stage, despite the upregulation of
XIST
. The choice of which X chromosome will finally become inactive thus occurs downstream of
Xist
upregulation in both rabbits and humans, unlike in mice. Our study demonstrates the remarkable diversity in XCI regulation and highlights differences between mammals in their requirement for dosage compensation during early embryogenesis. |
| doi_str_mv | 10.1038/nature09872 |
| format | Article |
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X-chromosome inactivation is an essential process in female mammals that compensates for the presence of two X-chromosomes by suppressing gene expression from one of them. A study of the early developmental time course of X-chromosome inactivation in mice, rabbits and humans shows that the processes in mice, in which most of previous analyses have been done, differ significantly from those in other eutherian species. The study highlights a diversity in X-inactivation regulation that may reflect the changing nature of developmental processes during evolution.
X-chromosome inactivation (XCI) in female mammals allows dosage compensation for X-linked gene products between the sexes
1
. The developmental regulation of this process has been extensively investigated in mice, where the X chromosome of paternal origin (Xp) is silenced during early embryogenesis owing to imprinted expression of the regulatory RNA,
Xist
(X-inactive specific transcript). Paternal XCI is reversed in the inner cell mass of the blastocyst and random XCI subsequently occurs in epiblast cells. Here we show that other eutherian mammals have very different strategies for initiating XCI. In rabbits and humans, the
Xist
homologue is not subject to imprinting and XCI begins later than in mice. Furthermore,
Xist
is upregulated on both X chromosomes in a high proportion of rabbit and human embryo cells, even in the inner cell mass. In rabbits, this triggers XCI on both X chromosomes in some cells. In humans, chromosome-wide XCI has not initiated even by the blastocyst stage, despite the upregulation of
XIST
. The choice of which X chromosome will finally become inactive thus occurs downstream of
Xist
upregulation in both rabbits and humans, unlike in mice. Our study demonstrates the remarkable diversity in XCI regulation and highlights differences between mammals in their requirement for dosage compensation during early embryogenesis.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature09872</identifier><identifier>PMID: 21471966</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/136/2086 ; 631/208/182 ; 631/337/176/1433 ; Animal development ; Animals ; Biological and medical sciences ; Biological Evolution ; Blastocyst - metabolism ; Cell physiology ; Cell transformation and carcinogenesis. Action of oncogenes and antioncogenes ; Chromosomes ; Chromosomes, Mammalian - genetics ; Compensation ; Development Biology ; Dosage Compensation, Genetic - genetics ; Embryo, Mammalian - embryology ; Embryo, Mammalian - metabolism ; Embryonic growth stage ; Eutherians ; Female ; Females ; Fundamental and applied biological sciences. Psychology ; Gene Expression Regulation, Developmental - genetics ; Genes, X-Linked - genetics ; Genetic aspects ; Genetic engineering ; Genomic Imprinting - genetics ; Histones - metabolism ; Humanities and Social Sciences ; Humans ; Hypoxanthine Phosphoribosyltransferase - genetics ; Inactivation ; letter ; Life Sciences ; Male ; Males ; Mammals ; Mammals - embryology ; Mammals - genetics ; Mice ; Molecular and cellular biology ; multidisciplinary ; Observations ; Parthenogenesis ; Physiological aspects ; Rabbits ; Reproductive Biology ; RNA, Long Noncoding ; RNA, Untranslated - genetics ; Science ; Science (multidisciplinary) ; Species Specificity ; Up-Regulation - genetics ; X Chromosome - genetics ; X chromosome inactivation ; X Chromosome Inactivation - genetics</subject><ispartof>Nature (London), 2011-04, Vol.472 (7343), p.370-374</ispartof><rights>Springer Nature Limited 2011</rights><rights>2015 INIST-CNRS</rights><rights>COPYRIGHT 2011 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Apr 21, 2011</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c640t-3428efcc557bd3a75b40f169869c7842c28fc9bc9a105f7a717794ec6cd0fbeb3</citedby><cites>FETCH-LOGICAL-c640t-3428efcc557bd3a75b40f169869c7842c28fc9bc9a105f7a717794ec6cd0fbeb3</cites><orcidid>0000-0002-1126-4322 ; 0000-0001-8120-7481 ; 0000-0002-2251-1296</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature09872$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature09872$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24070021$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21471966$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01019321$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Okamoto, Ikuhiro</creatorcontrib><creatorcontrib>Patrat, Catherine</creatorcontrib><creatorcontrib>Thépot, Dominique</creatorcontrib><creatorcontrib>Peynot, Nathalie</creatorcontrib><creatorcontrib>Fauque, Patricia</creatorcontrib><creatorcontrib>Daniel, Nathalie</creatorcontrib><creatorcontrib>Diabangouaya, Patricia</creatorcontrib><creatorcontrib>Wolf, Jean-Philippe</creatorcontrib><creatorcontrib>Renard, Jean-Paul</creatorcontrib><creatorcontrib>Duranthon, Véronique</creatorcontrib><creatorcontrib>Heard, Edith</creatorcontrib><title>Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Mice out of step on X inactivation
X-chromosome inactivation is an essential process in female mammals that compensates for the presence of two X-chromosomes by suppressing gene expression from one of them. A study of the early developmental time course of X-chromosome inactivation in mice, rabbits and humans shows that the processes in mice, in which most of previous analyses have been done, differ significantly from those in other eutherian species. The study highlights a diversity in X-inactivation regulation that may reflect the changing nature of developmental processes during evolution.
X-chromosome inactivation (XCI) in female mammals allows dosage compensation for X-linked gene products between the sexes
1
. The developmental regulation of this process has been extensively investigated in mice, where the X chromosome of paternal origin (Xp) is silenced during early embryogenesis owing to imprinted expression of the regulatory RNA,
Xist
(X-inactive specific transcript). Paternal XCI is reversed in the inner cell mass of the blastocyst and random XCI subsequently occurs in epiblast cells. Here we show that other eutherian mammals have very different strategies for initiating XCI. In rabbits and humans, the
Xist
homologue is not subject to imprinting and XCI begins later than in mice. Furthermore,
Xist
is upregulated on both X chromosomes in a high proportion of rabbit and human embryo cells, even in the inner cell mass. In rabbits, this triggers XCI on both X chromosomes in some cells. In humans, chromosome-wide XCI has not initiated even by the blastocyst stage, despite the upregulation of
XIST
. The choice of which X chromosome will finally become inactive thus occurs downstream of
Xist
upregulation in both rabbits and humans, unlike in mice. Our study demonstrates the remarkable diversity in XCI regulation and highlights differences between mammals in their requirement for dosage compensation during early embryogenesis.</description><subject>631/136/2086</subject><subject>631/208/182</subject><subject>631/337/176/1433</subject><subject>Animal development</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Biological Evolution</subject><subject>Blastocyst - metabolism</subject><subject>Cell physiology</subject><subject>Cell transformation and carcinogenesis. Action of oncogenes and antioncogenes</subject><subject>Chromosomes</subject><subject>Chromosomes, Mammalian - genetics</subject><subject>Compensation</subject><subject>Development Biology</subject><subject>Dosage Compensation, Genetic - genetics</subject><subject>Embryo, Mammalian - embryology</subject><subject>Embryo, Mammalian - metabolism</subject><subject>Embryonic growth stage</subject><subject>Eutherians</subject><subject>Female</subject><subject>Females</subject><subject>Fundamental and applied biological sciences. 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genetics</topic><topic>X Chromosome - genetics</topic><topic>X chromosome inactivation</topic><topic>X Chromosome Inactivation - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Okamoto, Ikuhiro</creatorcontrib><creatorcontrib>Patrat, Catherine</creatorcontrib><creatorcontrib>Thépot, Dominique</creatorcontrib><creatorcontrib>Peynot, Nathalie</creatorcontrib><creatorcontrib>Fauque, Patricia</creatorcontrib><creatorcontrib>Daniel, Nathalie</creatorcontrib><creatorcontrib>Diabangouaya, Patricia</creatorcontrib><creatorcontrib>Wolf, Jean-Philippe</creatorcontrib><creatorcontrib>Renard, Jean-Paul</creatorcontrib><creatorcontrib>Duranthon, Véronique</creatorcontrib><creatorcontrib>Heard, Edith</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Okamoto, Ikuhiro</au><au>Patrat, Catherine</au><au>Thépot, Dominique</au><au>Peynot, Nathalie</au><au>Fauque, Patricia</au><au>Daniel, Nathalie</au><au>Diabangouaya, Patricia</au><au>Wolf, Jean-Philippe</au><au>Renard, Jean-Paul</au><au>Duranthon, Véronique</au><au>Heard, Edith</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2011-04-21</date><risdate>2011</risdate><volume>472</volume><issue>7343</issue><spage>370</spage><epage>374</epage><pages>370-374</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>Mice out of step on X inactivation
X-chromosome inactivation is an essential process in female mammals that compensates for the presence of two X-chromosomes by suppressing gene expression from one of them. A study of the early developmental time course of X-chromosome inactivation in mice, rabbits and humans shows that the processes in mice, in which most of previous analyses have been done, differ significantly from those in other eutherian species. The study highlights a diversity in X-inactivation regulation that may reflect the changing nature of developmental processes during evolution.
X-chromosome inactivation (XCI) in female mammals allows dosage compensation for X-linked gene products between the sexes
1
. The developmental regulation of this process has been extensively investigated in mice, where the X chromosome of paternal origin (Xp) is silenced during early embryogenesis owing to imprinted expression of the regulatory RNA,
Xist
(X-inactive specific transcript). Paternal XCI is reversed in the inner cell mass of the blastocyst and random XCI subsequently occurs in epiblast cells. Here we show that other eutherian mammals have very different strategies for initiating XCI. In rabbits and humans, the
Xist
homologue is not subject to imprinting and XCI begins later than in mice. Furthermore,
Xist
is upregulated on both X chromosomes in a high proportion of rabbit and human embryo cells, even in the inner cell mass. In rabbits, this triggers XCI on both X chromosomes in some cells. In humans, chromosome-wide XCI has not initiated even by the blastocyst stage, despite the upregulation of
XIST
. The choice of which X chromosome will finally become inactive thus occurs downstream of
Xist
upregulation in both rabbits and humans, unlike in mice. Our study demonstrates the remarkable diversity in XCI regulation and highlights differences between mammals in their requirement for dosage compensation during early embryogenesis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>21471966</pmid><doi>10.1038/nature09872</doi><tpages>5</tpages><orcidid>https://orcid.org/0000-0002-1126-4322</orcidid><orcidid>https://orcid.org/0000-0001-8120-7481</orcidid><orcidid>https://orcid.org/0000-0002-2251-1296</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0028-0836 |
| ispartof | Nature (London), 2011-04, Vol.472 (7343), p.370-374 |
| issn | 0028-0836 1476-4687 |
| language | eng |
| recordid | cdi_hal_primary_oai_HAL_hal_01019321v1 |
| source | MEDLINE; Nature Journals Online; SpringerLink Journals - AutoHoldings |
| subjects | 631/136/2086 631/208/182 631/337/176/1433 Animal development Animals Biological and medical sciences Biological Evolution Blastocyst - metabolism Cell physiology Cell transformation and carcinogenesis. Action of oncogenes and antioncogenes Chromosomes Chromosomes, Mammalian - genetics Compensation Development Biology Dosage Compensation, Genetic - genetics Embryo, Mammalian - embryology Embryo, Mammalian - metabolism Embryonic growth stage Eutherians Female Females Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Developmental - genetics Genes, X-Linked - genetics Genetic aspects Genetic engineering Genomic Imprinting - genetics Histones - metabolism Humanities and Social Sciences Humans Hypoxanthine Phosphoribosyltransferase - genetics Inactivation letter Life Sciences Male Males Mammals Mammals - embryology Mammals - genetics Mice Molecular and cellular biology multidisciplinary Observations Parthenogenesis Physiological aspects Rabbits Reproductive Biology RNA, Long Noncoding RNA, Untranslated - genetics Science Science (multidisciplinary) Species Specificity Up-Regulation - genetics X Chromosome - genetics X chromosome inactivation X Chromosome Inactivation - genetics |
| title | Eutherian mammals use diverse strategies to initiate X-chromosome inactivation during development |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T17%3A09%3A58IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Eutherian%20mammals%20use%20diverse%20strategies%20to%20initiate%20X-chromosome%20inactivation%20during%20development&rft.jtitle=Nature%20(London)&rft.au=Okamoto,%20Ikuhiro&rft.date=2011-04-21&rft.volume=472&rft.issue=7343&rft.spage=370&rft.epage=374&rft.pages=370-374&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature09872&rft_dat=%3Cgale_hal_p%3EA632494872%3C/gale_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=864819821&rft_id=info:pmid/21471966&rft_galeid=A632494872&rfr_iscdi=true |