Heterogeneity in Oct4 and Sox2 Targets Biases Cell Fate in 4-Cell Mouse Embryos
Identifieur interne : 000052 ( Main/Exploration ); précédent : 000051; suivant : 000053Heterogeneity in Oct4 and Sox2 Targets Biases Cell Fate in 4-Cell Mouse Embryos
Auteurs : Mubeen Goolam [Royaume-Uni] ; Antonio Scialdone [Royaume-Uni] ; Sarah J. L. Graham [Royaume-Uni] ; Iain C. Macaulay [Royaume-Uni] ; Agnieszka Jedrusik [Royaume-Uni] ; Anna Hupalowska [Royaume-Uni] ; Thierry Voet [Royaume-Uni, Belgique] ; John C. Marioni [Royaume-Uni] ; Magdalena Zernicka-Goetz [Royaume-Uni]Source :
- Cell [ 0092-8674 ] ; 2016.
Abstract
The major and essential objective of pre-implantation development is to establish embryonic and extra-embryonic cell fates. To address when and how this fundamental process is initiated in mammals, we characterize transcriptomes of all individual cells throughout mouse pre-implantation development. This identifies targets of master pluripotency regulators Oct4 and Sox2 as being highly heterogeneously expressed between blastomeres of the 4-cell embryo, with Sox21 showing one of the most heterogeneous expression profiles. Live-cell tracking demonstrates that cells with decreased Sox21 yield more extra-embryonic than pluripotent progeny. Consistently, decreasing Sox21 results in premature upregulation of the differentiation regulator Cdx2, suggesting that Sox21 helps safeguard pluripotency. Furthermore, Sox21 is elevated following increased expression of the histone H3R26-methylase CARM1 and is lowered following CARM1 inhibition, indicating the importance of epigenetic regulation. Therefore, our results indicate that heterogeneous gene expression, as early as the 4-cell stage, initiates cell-fate decisions by modulating the balance of pluripotency and differentiation.
Url:
DOI: 10.1016/j.cell.2016.01.047
PubMed: 27015307
PubMed Central: 4819611
Affiliations:
- Belgique, Royaume-Uni
- Angleterre, Angleterre de l'Est, Province du Brabant flamand
- Cambridge, Louvain
- Université de Cambridge
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type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Scialdone, Antonio" sort="Scialdone, Antonio" uniqKey="Scialdone A" first="Antonio" last="Scialdone">Antonio Scialdone</name><affiliation wicri:level="1"><nlm:aff id="aff2">European Bioinformatics Institute, European Molecular Biology Laboratory (EMBL-EBI), Wellcome Genome Campus, Cambridge CB10 1SD, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>European Bioinformatics Institute, European Molecular Biology Laboratory (EMBL-EBI), Wellcome Genome Campus, Cambridge CB10 1SD</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SD</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3">Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SA</wicri:noRegion></affiliation></author><author><name sortKey="Graham, Sarah J L" sort="Graham, Sarah J L" uniqKey="Graham S" first="Sarah J. L." last="Graham">Sarah J. L. Graham</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Macaulay, Iain C" sort="Macaulay, Iain C" uniqKey="Macaulay I" first="Iain C." last="Macaulay">Iain C. Macaulay</name><affiliation wicri:level="1"><nlm:aff id="aff3">Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SA</wicri:noRegion></affiliation></author><author><name sortKey="Jedrusik, Agnieszka" sort="Jedrusik, Agnieszka" uniqKey="Jedrusik A" first="Agnieszka" last="Jedrusik">Agnieszka Jedrusik</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Hupalowska, Anna" sort="Hupalowska, Anna" uniqKey="Hupalowska A" first="Anna" last="Hupalowska">Anna Hupalowska</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Voet, Thierry" sort="Voet, Thierry" uniqKey="Voet T" first="Thierry" last="Voet">Thierry Voet</name><affiliation wicri:level="1"><nlm:aff id="aff3">Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SA</wicri:noRegion></affiliation><affiliation wicri:level="3"><nlm:aff id="aff4">Laboratory of Reproductive Genomics, Department of Human Genetics, KU Leuven, Herestraat 49, 3000 Leuven, Belgium</nlm:aff><country xml:lang="fr">Belgique</country><wicri:regionArea>Laboratory of Reproductive Genomics, Department of Human Genetics, KU Leuven, Herestraat 49, 3000 Leuven</wicri:regionArea><placeName><region type="province" nuts="2">Province du Brabant flamand</region><settlement type="city">Louvain</settlement></placeName></affiliation></author><author><name sortKey="Marioni, John C" sort="Marioni, John C" uniqKey="Marioni J" first="John C." last="Marioni">John C. Marioni</name><affiliation wicri:level="1"><nlm:aff id="aff2">European Bioinformatics Institute, European Molecular Biology Laboratory (EMBL-EBI), Wellcome Genome Campus, Cambridge CB10 1SD, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>European Bioinformatics Institute, European Molecular Biology Laboratory (EMBL-EBI), Wellcome Genome Campus, Cambridge CB10 1SD</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SD</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3">Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Wellcome Trust Sanger Institute, Wellcome Genome Campus, Cambridge CB10 1SA</wicri:regionArea><wicri:noRegion>Cambridge CB10 1SA</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:aff id="aff5">Cancer Research UK-Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Cambridge CB2 0RE, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cancer Research UK-Cambridge Institute, University of Cambridge, Li Ka Shing Centre, Cambridge CB2 0RE</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Zernicka Goetz, Magdalena" sort="Zernicka Goetz, Magdalena" uniqKey="Zernicka Goetz M" first="Magdalena" last="Zernicka-Goetz">Magdalena Zernicka-Goetz</name><affiliation wicri:level="4"><nlm:aff id="aff1">Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG, UK</nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Physiology, Development & Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3EG</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author></analytic><series><title level="j">Cell</title><idno type="ISSN">0092-8674</idno><idno type="eISSN">1097-4172</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Summary</title><p>The major and essential objective of pre-implantation development is to establish embryonic and extra-embryonic cell fates. To address when and how this fundamental process is initiated in mammals, we characterize transcriptomes of all individual cells throughout mouse pre-implantation development. This identifies targets of master pluripotency regulators Oct4 and Sox2 as being highly heterogeneously expressed between blastomeres of the 4-cell embryo, with Sox21 showing one of the most heterogeneous expression profiles. Live-cell tracking demonstrates that cells with decreased Sox21 yield more extra-embryonic than pluripotent progeny. Consistently, decreasing Sox21 results in premature upregulation of the differentiation regulator Cdx2, suggesting that Sox21 helps safeguard pluripotency. Furthermore, Sox21 is elevated following increased expression of the histone H3R26-methylase CARM1 and is lowered following CARM1 inhibition, indicating the importance of epigenetic regulation. Therefore, our results indicate that heterogeneous gene expression, as early as the 4-cell stage, initiates cell-fate decisions by modulating the balance of pluripotency and differentiation.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Anders, S" uniqKey="Anders S">S. Anders</name></author><author><name sortKey="Pyl, P T" uniqKey="Pyl P">P.T. Pyl</name></author><author><name sortKey="Huber, W" uniqKey="Huber W">W. Huber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Biase, F H" uniqKey="Biase F">F.H. Biase</name></author><author><name sortKey="Cao, X" uniqKey="Cao X">X. Cao</name></author><author><name sortKey="Zhong, S" uniqKey="Zhong S">S. Zhong</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bischoff, M" uniqKey="Bischoff M">M. Bischoff</name></author><author><name sortKey="Parfitt, D E" uniqKey="Parfitt D">D.E. 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Rossant</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Zernicka Goetz, M" uniqKey="Zernicka Goetz M">M. Zernicka-Goetz</name></author><author><name sortKey="Morris, S A" uniqKey="Morris S">S.A. Morris</name></author><author><name sortKey="Bruce, A W" uniqKey="Bruce A">A.W. Bruce</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Belgique</li><li>Royaume-Uni</li></country><region><li>Angleterre</li><li>Angleterre de l'Est</li><li>Province du Brabant flamand</li></region><settlement><li>Cambridge</li><li>Louvain</li></settlement><orgName><li>Université de Cambridge</li></orgName></list><tree><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Goolam, Mubeen" sort="Goolam, Mubeen" uniqKey="Goolam M" first="Mubeen" last="Goolam">Mubeen Goolam</name></region><name sortKey="Graham, Sarah J L" sort="Graham, Sarah J L" uniqKey="Graham S" first="Sarah J. L." last="Graham">Sarah J. L. Graham</name><name sortKey="Hupalowska, Anna" sort="Hupalowska, Anna" uniqKey="Hupalowska A" first="Anna" last="Hupalowska">Anna Hupalowska</name><name sortKey="Jedrusik, Agnieszka" sort="Jedrusik, Agnieszka" uniqKey="Jedrusik A" first="Agnieszka" last="Jedrusik">Agnieszka Jedrusik</name><name sortKey="Macaulay, Iain C" sort="Macaulay, Iain C" uniqKey="Macaulay I" first="Iain C." last="Macaulay">Iain C. Macaulay</name><name sortKey="Marioni, John C" sort="Marioni, John C" uniqKey="Marioni J" first="John C." last="Marioni">John C. Marioni</name><name sortKey="Marioni, John C" sort="Marioni, John C" uniqKey="Marioni J" first="John C." last="Marioni">John C. Marioni</name><name sortKey="Marioni, John C" sort="Marioni, John C" uniqKey="Marioni J" first="John C." last="Marioni">John C. Marioni</name><name sortKey="Scialdone, Antonio" sort="Scialdone, Antonio" uniqKey="Scialdone A" first="Antonio" last="Scialdone">Antonio Scialdone</name><name sortKey="Scialdone, Antonio" sort="Scialdone, Antonio" uniqKey="Scialdone A" first="Antonio" last="Scialdone">Antonio Scialdone</name><name sortKey="Voet, Thierry" sort="Voet, Thierry" uniqKey="Voet T" first="Thierry" last="Voet">Thierry Voet</name><name sortKey="Zernicka Goetz, Magdalena" sort="Zernicka Goetz, Magdalena" uniqKey="Zernicka Goetz M" first="Magdalena" last="Zernicka-Goetz">Magdalena Zernicka-Goetz</name></country><country name="Belgique"><region name="Province du Brabant flamand"><name sortKey="Voet, Thierry" sort="Voet, Thierry" uniqKey="Voet T" first="Thierry" last="Voet">Thierry Voet</name></region></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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