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Spatiotemporal dynamics of SETD5-containing NCoR–HDAC3 complex determines enhancer activation for adipogenesis

Author

Listed:
  • Yoshihiro Matsumura

    (The University of Tokyo)

  • Ryo Ito

    (Tohoku University Graduate School of Medicine)

  • Ayumu Yajima

    (The University of Tokyo
    Saga University)

  • Rei Yamaguchi

    (Tohoku University Graduate School of Medicine)

  • Toshiya Tanaka

    (The University of Tokyo)

  • Takeshi Kawamura

    (The University of Tokyo)

  • Kenta Magoori

    (The University of Tokyo)

  • Yohei Abe

    (The University of Tokyo)

  • Aoi Uchida

    (The University of Tokyo)

  • Takeshi Yoneshiro

    (The University of Tokyo)

  • Hiroyuki Hirakawa

    (The University of Tokyo
    Tokyo Medical and Dental University (TMDU), Graduate School)

  • Ji Zhang

    (The University of Tokyo
    Tohoku University Graduate School of Medicine)

  • Makoto Arai

    (The University of Tokyo
    Tohoku University Graduate School of Medicine)

  • Chaoran Yang

    (Tohoku University Graduate School of Medicine)

  • Ge Yang

    (Tohoku University Graduate School of Medicine)

  • Hiroki Takahashi

    (Tohoku University Graduate School of Medicine)

  • Hitomi Fujihashi

    (The University of Tokyo)

  • Ryo Nakaki

    (The University of Tokyo
    Rhelixa Inc)

  • Shogo Yamamoto

    (The University of Tokyo)

  • Satoshi Ota

    (The University of Tokyo)

  • Shuichi Tsutsumi

    (The University of Tokyo)

  • Shin-ichi Inoue

    (Tohoku University Graduate School of Medicine)

  • Hiroshi Kimura

    (Tokyo Institute of Technology)

  • Youichiro Wada

    (The University of Tokyo)

  • Tatsuhiko Kodama

    (The University of Tokyo)

  • Takeshi Inagaki

    (The University of Tokyo
    Gunma University)

  • Timothy F. Osborne

    (Diabetes and Metabolism of the Johns Hopkins University School of Medicine)

  • Hiroyuki Aburatani

    (The University of Tokyo)

  • Koichi Node

    (Saga University)

  • Juro Sakai

    (The University of Tokyo
    Tohoku University Graduate School of Medicine)

Abstract

Enhancer activation is essential for cell-type specific gene expression during cellular differentiation, however, how enhancers transition from a hypoacetylated “primed” state to a hyperacetylated-active state is incompletely understood. Here, we show SET domain-containing 5 (SETD5) forms a complex with NCoR-HDAC3 co-repressor that prevents histone acetylation of enhancers for two master adipogenic regulatory genes Cebpa and Pparg early during adipogenesis. The loss of SETD5 from the complex is followed by enhancer hyperacetylation. SETD5 protein levels were transiently increased and rapidly degraded prior to enhancer activation providing a mechanism for the loss of SETD5 during the transition. We show that induction of the CDC20 co-activator of the ubiquitin ligase leads to APC/C mediated degradation of SETD5 during the transition and this operates as a molecular switch that facilitates adipogenesis.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27321-5
    DOI: 10.1038/s41467-021-27321-5
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    References listed on IDEAS

    as
    1. Yohei Abe & Royhan Rozqie & Yoshihiro Matsumura & Takeshi Kawamura & Ryo Nakaki & Yuya Tsurutani & Kyoko Tanimura-Inagaki & Akira Shiono & Kenta Magoori & Kanako Nakamura & Shotaro Ogi & Shingo Kajimu, 2015. "JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
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    Cited by:

    1. Hiroki Takahashi & Ge Yang & Takeshi Yoneshiro & Yohei Abe & Ryo Ito & Chaoran Yang & Junna Nakazono & Mayumi Okamoto-Katsuyama & Aoi Uchida & Makoto Arai & Hitomi Jin & Hyunmi Choi & Myagmar Tumenjar, 2022. "MYPT1-PP1β phosphatase negatively regulates both chromatin landscape and co-activator recruitment for beige adipogenesis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. 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.
    3. Xiao Chen & Yinglu Li & Fang Zhu & Xinjing Xu & Brian Estrella & Manuel A. Pazos & John T. McGuire & Dimitris Karagiannis & Varun Sahu & Mustafo Mustafokulov & Claudio Scuoppo & Francisco J. Sánchez-R, 2023. "Context-defined cancer co-dependency mapping identifies a functional interplay between PRC2 and MLL-MEN1 complex in lymphoma," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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