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The Fgf/Erf/NCoR1/2 repressive axis controls trophoblast cell fate

Author

Listed:
  • Andreas Lackner

    (Medical University of Vienna)

  • Michael Müller

    (Medical University of Vienna)

  • Magdalena Gamperl

    (Medical University of Vienna)

  • Delyana Stoeva

    (Medical University of Vienna)

  • Olivia Langmann

    (Medical University of Vienna)

  • Henrieta Papuchova

    (Medical University of Vienna)

  • Elisabeth Roitinger

    (Institute of Molecular Pathology)

  • Gerhard Dürnberger

    (Institute of Molecular Pathology)

  • Richard Imre

    (Institute of Molecular Pathology)

  • Karl Mechtler

    (Institute of Molecular Pathology)

  • Paulina A. Latos

    (Medical University of Vienna)

Abstract

Placental development relies on coordinated cell fate decisions governed by signalling inputs. However, little is known about how signalling cues are transformed into repressive mechanisms triggering lineage-specific transcriptional signatures. Here, we demonstrate that upon inhibition of the Fgf/Erk pathway in mouse trophoblast stem cells (TSCs), the Ets2 repressor factor (Erf) interacts with the Nuclear Receptor Co-Repressor Complex 1 and 2 (NCoR1/2) and recruits it to key trophoblast genes. Genetic ablation of Erf or Tbl1x (a component of the NCoR1/2 complex) abrogates the Erf/NCoR1/2 interaction. This leads to mis-expression of Erf/NCoR1/2 target genes, resulting in a TSC differentiation defect. Mechanistically, Erf regulates expression of these genes by recruiting the NCoR1/2 complex and decommissioning their H3K27ac-dependent enhancers. Our findings uncover how the Fgf/Erf/NCoR1/2 repressive axis governs cell fate and placental development, providing a paradigm for Fgf-mediated transcriptional control.

Suggested Citation

  • Andreas Lackner & Michael Müller & Magdalena Gamperl & Delyana Stoeva & Olivia Langmann & Henrieta Papuchova & Elisabeth Roitinger & Gerhard Dürnberger & Richard Imre & Karl Mechtler & Paulina A. Lato, 2023. "The Fgf/Erf/NCoR1/2 repressive axis controls trophoblast cell fate," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38101-8
    DOI: 10.1038/s41467-023-38101-8
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    1. Ola Hermanson & Kristen Jepsen & Michael G. Rosenfeld, 2002. "N-CoR controls differentiation of neural stem cells into astrocytes," Nature, Nature, vol. 419(6910), pages 934-939, October.
    2. Yoshihiro Matsumura & Ryo Ito & Ayumu Yajima & Rei Yamaguchi & Toshiya Tanaka & Takeshi Kawamura & Kenta Magoori & Yohei Abe & Aoi Uchida & Takeshi Yoneshiro & Hiroyuki Hirakawa & Ji Zhang & Makoto Ar, 2021. "Spatiotemporal dynamics of SETD5-containing NCoR–HDAC3 complex determines enhancer activation for adipogenesis," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    3. Patrick Bryant & Gabriele Pozzati & Arne Elofsson, 2022. "Improved prediction of protein-protein interactions using AlphaFold2," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    4. Chen Chen & Wenjun Ouyang & Vadim Grigura & Qing Zhou & Kay Carnes & Hyunjung Lim & Guang-Quan Zhao & Silvia Arber & Natasza Kurpios & Theresa L. Murphy & Alec M. Cheng & John A. Hassell & Varadaraj C, 2005. "ERM is required for transcriptional control of the spermatogonial stem cell niche," Nature, Nature, vol. 436(7053), pages 1030-1034, August.
    5. Rene C. Adam & Hanseul Yang & Shira Rockowitz & Samantha B. Larsen & Maria Nikolova & Daniel S. Oristian & Lisa Polak & Meelis Kadaja & Amma Asare & Deyou Zheng & Elaine Fuchs, 2015. "Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice," Nature, Nature, vol. 521(7552), pages 366-370, May.
    6. Mu Gao & Davi Nakajima An & Jerry M. Parks & Jeffrey Skolnick, 2022. "AF2Complex predicts direct physical interactions in multimeric proteins with deep learning," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Kristen Jepsen & Derek Solum & Tianyuan Zhou & Robert J. McEvilly & Hyun-Jung Kim & Christopher K. Glass & Ola Hermanson & Michael G. Rosenfeld, 2007. "SMRT-mediated repression of an H3K27 demethylase in progression from neural stem cell to neuron," Nature, Nature, vol. 450(7168), pages 415-419, November.
    8. Caryn S. Ross-Innes & Rory Stark & Andrew E. Teschendorff & Kelly A. Holmes & H. Raza Ali & Mark J. Dunning & Gordon D. Brown & Ondrej Gojis & Ian O. Ellis & Andrew R. Green & Simak Ali & Suet-Feung C, 2012. "Differential oestrogen receptor binding is associated with clinical outcome in breast cancer," Nature, Nature, vol. 481(7381), pages 389-393, January.
    9. Patrick Bryant & Gabriele Pozzati & Arne Elofsson, 2022. "Author Correction: Improved prediction of protein-protein interactions using AlphaFold2," Nature Communications, Nature, vol. 13(1), pages 1-1, December.
    10. J. A. Hartigan & M. A. Wong, 1979. "A K‐Means Clustering Algorithm," Journal of the Royal Statistical Society Series C, Royal Statistical Society, vol. 28(1), pages 100-108, March.
    11. Paulina A. Latos & Angela Goncalves & David Oxley & Hisham Mohammed & Ernest Turro & Myriam Hemberger, 2015. "Fgf and Esrrb integrate epigenetic and transcriptional networks that regulate self-renewal of trophoblast stem cells," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
    12. Jiangming Luo & Robert Sladek & Jo-Ann Bader & Annie Matthyssen & Janet Rossant & Vincent Giguère, 1997. "Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-β," Nature, Nature, vol. 388(6644), pages 778-782, August.
    13. Bum-Kyu Lee & Yu jin Jang & Mijeong Kim & Lucy LeBlanc & Catherine Rhee & Jiwoon Lee & Samuel Beck & Wenwen Shen & Jonghwan Kim, 2019. "Super-enhancer-guided mapping of regulatory networks controlling mouse trophoblast stem cells," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
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