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The molecular logic of Nanog-induced self-renewal in mouse embryonic stem cells

Author

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  • Victor Heurtier

    (Institut Pasteur, CNRS UMR3738
    Sorbonne Université Collège Doctoral)

  • Nick Owens

    (Institut Pasteur, CNRS UMR3738)

  • Inma Gonzalez

    (Institut Pasteur, CNRS UMR3738)

  • Florian Mueller

    (Institut Pasteur, CNRS UMR 3691)

  • Caroline Proux

    (Institut Pasteur)

  • Damien Mornico

    (Institut Pasteur, CNRS USR 3756)

  • Philippe Clerc

    (Institut Pasteur, CNRS UMR3738)

  • Agnes Dubois

    (Institut Pasteur, CNRS UMR3738)

  • Pablo Navarro

    (Institut Pasteur, CNRS UMR3738)

Abstract

Transcription factor networks, together with histone modifications and signalling pathways, underlie the establishment and maintenance of gene regulatory architectures associated with the molecular identity of each cell type. However, how master transcription factors individually impact the epigenomic landscape and orchestrate the behaviour of regulatory networks under different environmental constraints is only partially understood. Here, we show that the transcription factor Nanog deploys multiple distinct mechanisms to enhance embryonic stem cell self-renewal. In the presence of LIF, which fosters self-renewal, Nanog rewires the pluripotency network by promoting chromatin accessibility and binding of other pluripotency factors to thousands of enhancers. In the absence of LIF, Nanog blocks differentiation by sustaining H3K27me3, a repressive histone mark, at developmental regulators. Among those, we show that the repression of Otx2 plays a preponderant role. Our results underscore the versatility of master transcription factors, such as Nanog, to globally influence gene regulation during developmental processes.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-09041-z
    DOI: 10.1038/s41467-019-09041-z
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    Cited by:

    1. Gemma Noviello & Rutger A. F. Gjaltema & Edda G. Schulz, 2023. "CasTuner is a degron and CRISPR/Cas-based toolkit for analog tuning of endogenous gene expression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Joyce J. Thompson & Daniel J. Lee & Apratim Mitra & Sarah Frail & Ryan K. Dale & Pedro P. Rocha, 2022. "Extensive co-binding and rapid redistribution of NANOG and GATA6 during emergence of divergent lineages," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. 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.
    4. Luca Pagliaroli & Patrizia Porazzi & Alyxandra T. Curtis & Chiara Scopa & Harald M. M. Mikkers & Christian Freund & Lucia Daxinger & Sandra Deliard & Sarah A. Welsh & Sarah Offley & Connor A. Ott & Br, 2021. "Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. Christian Much & Erika L. Lasda & Isabela T. Pereira & Tenaya K. Vallery & Daniel Ramirez & Jordan P. Lewandowski & Robin D. Dowell & Michael J. Smallegan & John L. Rinn, 2024. "The temporal dynamics of lncRNA Firre-mediated epigenetic and transcriptional regulation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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