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TRIM24 links a non-canonical histone signature to breast cancer

Author

Listed:
  • Wen-Wei Tsai

    (Program in Genes and Development, Graduate School of Biomedical Sciences, University of Texas M.D. Anderson Cancer Center)

  • Zhanxin Wang

    (Structural Biology Program, Memorial Sloan-Kettering Cancer Center)

  • Teresa T. Yiu

    (Program in Genes and Development, Graduate School of Biomedical Sciences, University of Texas M.D. Anderson Cancer Center
    Centers for Cancer Epigenetics and Stem Cell and Developmental Biology, University of Texas M.D. Anderson Cancer Center)

  • Kadir C. Akdemir

    (Centers for Cancer Epigenetics and Stem Cell and Developmental Biology, University of Texas M.D. Anderson Cancer Center
    University of Texas M.D. Anderson Cancer Center)

  • Weiya Xia

    (University of Texas M.D. Anderson Cancer Center)

  • Stefan Winter

    (Laboratory of Chromatin Biochemistry, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Goettingen, Germany)

  • Cheng-Yu Tsai

    (University of Texas M.D. Anderson Cancer Center)

  • Xiaobing Shi

    (Program in Genes and Development, Graduate School of Biomedical Sciences, University of Texas M.D. Anderson Cancer Center
    Centers for Cancer Epigenetics and Stem Cell and Developmental Biology, University of Texas M.D. Anderson Cancer Center)

  • Dirk Schwarzer

    (Leibniz-Institut für Molekulare Pharmakologie (FMP), Robert-Roessle-Strasse 10, 13125 Berlin, Germany)

  • William Plunkett

    (University of Texas M.D. Anderson Cancer Center)

  • Bruce Aronow

    (Computational Medicine Center, Cincinnati Children's Hospital Medical Center)

  • Or Gozani

    (Stanford University)

  • Wolfgang Fischle

    (Laboratory of Chromatin Biochemistry, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, 37077 Goettingen, Germany)

  • Mien-Chie Hung

    (University of Texas M.D. Anderson Cancer Center
    Center for Molecular Medicine and Graduate Institute of Cancer Biology, China Medical University and Hospital)

  • Dinshaw J. Patel

    (Structural Biology Program, Memorial Sloan-Kettering Cancer Center)

  • Michelle Craig Barton

    (Program in Genes and Development, Graduate School of Biomedical Sciences, University of Texas M.D. Anderson Cancer Center
    Centers for Cancer Epigenetics and Stem Cell and Developmental Biology, University of Texas M.D. Anderson Cancer Center)

Abstract

Recognition of modified histone species by distinct structural domains within ‘reader’ proteins plays a critical role in the regulation of gene expression. Readers that simultaneously recognize histones with multiple marks allow transduction of complex chromatin modification patterns into specific biological outcomes. Here we report that chromatin regulator tripartite motif-containing 24 (TRIM24) functions in humans as a reader of dual histone marks by means of tandem plant homeodomain (PHD) and bromodomain (Bromo) regions. The three-dimensional structure of the PHD-Bromo region of TRIM24 revealed a single functional unit for combinatorial recognition of unmodified H3K4 (that is, histone H3 unmodified at lysine 4, H3K4me0) and acetylated H3K23 (histone H3 acetylated at lysine 23, H3K23ac) within the same histone tail. TRIM24 binds chromatin and oestrogen receptor to activate oestrogen-dependent genes associated with cellular proliferation and tumour development. Aberrant expression of TRIM24 negatively correlates with survival of breast cancer patients. The PHD-Bromo of TRIM24 provides a structural rationale for chromatin activation through a non-canonical histone signature, establishing a new route by which chromatin readers may influence cancer pathogenesis.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:nature:v:468:y:2010:i:7326:d:10.1038_nature09542
    DOI: 10.1038/nature09542
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    Citations

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    Cited by:

    1. Dimitrios Spiliotopoulos & Andrea Spitaleri & Giovanna Musco, 2012. "Exploring PHD Fingers and H3K4me0 Interactions with Molecular Dynamics Simulations and Binding Free Energy Calculations: AIRE-PHD1, a Comparative Study," PLOS ONE, Public Library of Science, vol. 7(10), pages 1-13, October.
    2. Vanessa Rousseau & Elias Einig & Chao Jin & Julia Horn & Mathias Riebold & Tanja Poth & Mohamed-Ali Jarboui & Michael Flentje & Nikita Popov, 2023. "Trim33 masks a non-transcriptional function of E2f4 in replication fork progression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Wen Wei & Qiaoli Chen & Minjun Liu & Yang Sheng & Qian OuYang & Weikuan Feng & Xinyu Yang & Longfei Ding & Shu Su & Jingzi Zhang & Lei Fang & Antonio Vidal-Puig & Hong-Yu Wang & Shuai Chen, 2022. "TRIM24 is an insulin-responsive regulator of P-bodies," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. 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.
    5. Ciira wa Maina & Antti Honkela & Filomena Matarese & Korbinian Grote & Hendrik G Stunnenberg & George Reid & Neil D Lawrence & Magnus Rattray, 2014. "Inference of RNA Polymerase II Transcription Dynamics from Chromatin Immunoprecipitation Time Course Data," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-17, May.

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