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NANOG initiates epiblast fate through the coordination of pluripotency genes expression

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  • Nicolas Allègre

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

  • Sabine Chauveau

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

  • Cynthia Dennis

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

  • Yoan Renaud

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine
    Byonet)

  • Dimitri Meistermann

    (Université de Nantes, CHU Nantes, INSERM
    Université de Nantes, CNRS, LS2N)

  • Lorena Valverde Estrella

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

  • Pierre Pouchin

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

  • Michel Cohen-Tannoudji

    (Université Paris Cité, CNRS UMR3738, Epigenomics, Proliferation, and the Identity of Cells, Department of Developmental and Stem Cell Biology)

  • Laurent David

    (Université de Nantes, CHU Nantes, INSERM
    Université de Nantes, CHU Nantes, INSERM, CNRS, UMS Biocore)

  • Claire Chazaud

    (Université Clermont Auvergne, CNRS, INSERM, GReD Institute, Faculté de Médecine)

Abstract

The epiblast is the source of all mammalian embryonic tissues and of pluripotent embryonic stem cells. It differentiates alongside the primitive endoderm in a “salt and pepper” pattern from inner cell mass (ICM) progenitors during the preimplantation stages through the activity of NANOG, GATA6 and the FGF pathway. When and how epiblast lineage specification is initiated is still unclear. Here, we show that the coordinated expression of pluripotency markers defines epiblast identity. Conversely, ICM progenitor cells display random cell-to-cell variability in expression of various pluripotency markers, remarkably dissimilar from the epiblast signature and independently from NANOG, GATA6 and FGF activities. Coordination of pluripotency markers expression fails in Nanog and Gata6 double KO (DKO) embryos. Collectively, our data suggest that NANOG triggers epiblast specification by ensuring the coordinated expression of pluripotency markers in a subset of cells, implying a stochastic mechanism. These features are likely conserved, as suggested by analysis of human embryos.

Suggested Citation

  • Nicolas Allègre & Sabine Chauveau & Cynthia Dennis & Yoan Renaud & Dimitri Meistermann & Lorena Valverde Estrella & Pierre Pouchin & Michel Cohen-Tannoudji & Laurent David & Claire Chazaud, 2022. "NANOG initiates epiblast fate through the coordination of pluripotency genes expression," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30858-8
    DOI: 10.1038/s41467-022-30858-8
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    as
    1. Alessandro Fiorenzano & Emilia Pascale & Cristina D'Aniello & Dario Acampora & Cecilia Bassalert & Francesco Russo & Gennaro Andolfi & Mauro Biffoni & Federica Francescangeli & Ann Zeuner & Claudia An, 2016. "Cripto is essential to capture mouse epiblast stem cell and human embryonic stem cell pluripotency," Nature Communications, Nature, vol. 7(1), pages 1-16, November.
    2. Ian Chambers & Jose Silva & Douglas Colby & Jennifer Nichols & Bianca Nijmeijer & Morag Robertson & Jan Vrana & Ken Jones & Lars Grotewold & Austin Smith, 2007. "Nanog safeguards pluripotency and mediates germline development," Nature, Nature, vol. 450(7173), pages 1230-1234, December.
    3. Sonja Nowotschin & Manu Setty & Ying-Yi Kuo & Vincent Liu & Vidur Garg & Roshan Sharma & Claire S. Simon & Nestor Saiz & Rui Gardner & Stéphane C. Boutet & Deanna M. Church & Pamela A. Hoodless & Anna, 2019. "The emergent landscape of the mouse gut endoderm at single-cell resolution," Nature, Nature, vol. 569(7756), pages 361-367, May.
    4. Sabine C Fischer & Elena Corujo-Simon & Joaquin Lilao-Garzon & Ernst H K Stelzer & Silvia Muñoz-Descalzo, 2020. "The transition from local to global patterns governs the differentiation of mouse blastocysts," PLOS ONE, Public Library of Science, vol. 15(5), pages 1-29, May.
    5. Claudia Gerri & Afshan McCarthy & Gregorio Alanis-Lobato & Andrej Demtschenko & Alexandre Bruneau & Sophie Loubersac & Norah M. E. Fogarty & Daniel Hampshire & Kay Elder & Phil Snell & Leila Christie , 2020. "Initiation of a conserved trophectoderm program in human, cow and mouse embryos," Nature, Nature, vol. 587(7834), pages 443-447, November.
    6. Maria-Elena Torres-Padilla & David-Emlyn Parfitt & Tony Kouzarides & Magdalena Zernicka-Goetz, 2007. "Histone arginine methylation regulates pluripotency in the early mouse embryo," Nature, Nature, vol. 445(7124), pages 214-218, January.
    7. Néstor Saiz & Kiah M. Williams & Venkatraman E. Seshan & Anna-Katerina Hadjantonakis, 2016. "Asynchronous fate decisions by single cells collectively ensure consistent lineage composition in the mouse blastocyst," Nature Communications, Nature, vol. 7(1), pages 1-14, December.
    8. Victor Heurtier & Nick Owens & Inma Gonzalez & Florian Mueller & Caroline Proux & Damien Mornico & Philippe Clerc & Agnes Dubois & Pablo Navarro, 2019. "The molecular logic of Nanog-induced self-renewal in mouse embryonic stem cells," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    9. Angélique Richard & Loïs Boullu & Ulysse Herbach & Arnaud Bonnafoux & Valérie Morin & Elodie Vallin & Anissa Guillemin & Nan Papili Gao & Rudiyanto Gunawan & Jérémie Cosette & Ophélie Arnaud & Jean-Ja, 2016. "Single-Cell-Based Analysis Highlights a Surge in Cell-to-Cell Molecular Variability Preceding Irreversible Commitment in a Differentiation Process," PLOS Biology, Public Library of Science, vol. 14(12), pages 1-35, December.
    10. Yusuke Miyanari & Maria-Elena Torres-Padilla, 2012. "Control of ground-state pluripotency by allelic regulation of Nanog," Nature, Nature, vol. 483(7390), pages 470-473, March.
    11. Sissy E. Wamaitha & Katarzyna J. Grybel & Gregorio Alanis-Lobato & Claudia Gerri & Sugako Ogushi & Afshan McCarthy & Shantha K. Mahadevaiah & Lyn Healy & Rebecca A. Lea & Miriam Molina-Arcas & Liani G, 2020. "IGF1-mediated human embryonic stem cell self-renewal recapitulates the embryonic niche," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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