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HSF1 phosphorylation establishes an active chromatin state via the TRRAP–TIP60 complex and promotes tumorigenesis

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  • Mitsuaki Fujimoto

    (Yamaguchi University School of Medicine)

  • Ryosuke Takii

    (Yamaguchi University School of Medicine)

  • Masaki Matsumoto

    (Niigata University)

  • Mariko Okada

    (Yamaguchi University School of Medicine)

  • Keiich I. Nakayama

    (Kyushu University)

  • Ryuichiro Nakato

    (University of Tokyo)

  • Katsunori Fujiki

    (University of Tokyo)

  • Katsuhiko Shirahige

    (University of Tokyo)

  • Akira Nakai

    (Yamaguchi University School of Medicine)

Abstract

Transcriptional regulation by RNA polymerase II is associated with changes in chromatin structure. Activated and promoter-bound heat shock transcription factor 1 (HSF1) recruits transcriptional co-activators, including histone-modifying enzymes; however, the mechanisms underlying chromatin opening remain unclear. Here, we demonstrate that HSF1 recruits the TRRAP-TIP60 acetyltransferase complex in HSP72 promoter during heat shock in a manner dependent on phosphorylation of HSF1-S419. TRIM33, a bromodomain-containing ubiquitin ligase, is then recruited to the promoter by interactions with HSF1 and a TIP60-mediated acetylation mark, and cooperates with the related factor TRIM24 for mono-ubiquitination of histone H2B on K120. These changes in histone modifications are triggered by phosphorylation of HSF1-S419 via PLK1, and stabilize the HSF1-transcription complex in HSP72 promoter. Furthermore, HSF1-S419 phosphorylation is constitutively enhanced in and promotes proliferation of melanoma cells. Our results provide mechanisms for HSF1 phosphorylation-dependent establishment of an active chromatin status, which is important for tumorigenesis.

Suggested Citation

  • Mitsuaki Fujimoto & Ryosuke Takii & Masaki Matsumoto & Mariko Okada & Keiich I. Nakayama & Ryuichiro Nakato & Katsunori Fujiki & Katsuhiko Shirahige & Akira Nakai, 2022. "HSF1 phosphorylation establishes an active chromatin state via the TRRAP–TIP60 complex and promotes tumorigenesis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32034-4
    DOI: 10.1038/s41467-022-32034-4
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    1. Wen-Wei Tsai & Zhanxin Wang & Teresa T. Yiu & Kadir C. Akdemir & Weiya Xia & Stefan Winter & Cheng-Yu Tsai & Xiaobing Shi & Dirk Schwarzer & William Plunkett & Bruce Aronow & Or Gozani & Wolfgang Fisc, 2010. "TRIM24 links a non-canonical histone signature to breast cancer," Nature, Nature, vol. 468(7326), pages 927-932, December.
    2. Han Xue & Tonghui Yao & Mi Cao & Guanjun Zhu & Yan Li & Guiyong Yuan & Yong Chen & Ming Lei & Jing Huang, 2019. "Structural basis of nucleosome recognition and modification by MLL methyltransferases," Nature, Nature, vol. 573(7774), pages 445-449, September.
    3. Sanchita Bhatnagar & Claude Gazin & Lynn Chamberlain & Jianhong Ou & Xiaochun Zhu & Jogender S. Tushir & Ching-Man Virbasius & Ling Lin & Lihua J. Zhu & Narendra Wajapeyee & Michael R. Green, 2014. "TRIM37 is a new histone H2A ubiquitin ligase and breast cancer oncoprotein," Nature, Nature, vol. 516(7529), pages 116-120, December.
    4. Patrick Cramer, 2019. "Organization and regulation of gene transcription," Nature, Nature, vol. 573(7772), pages 45-54, September.
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