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Fibroblast-specific PRMT5 deficiency suppresses cardiac fibrosis and left ventricular dysfunction in male mice

Author

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  • Yasufumi Katanasaka

    (University of Shizuoka
    National Hospital Organization Kyoto Medical Center
    Shizuoka General Hospital)

  • Harumi Yabe

    (University of Shizuoka)

  • Noriyuki Murata

    (University of Shizuoka)

  • Minori Sobukawa

    (University of Shizuoka)

  • Yuga Sugiyama

    (University of Shizuoka)

  • Hikaru Sato

    (University of Shizuoka)

  • Hiroki Honda

    (University of Shizuoka)

  • Yoichi Sunagawa

    (University of Shizuoka
    National Hospital Organization Kyoto Medical Center
    Shizuoka General Hospital)

  • Masafumi Funamoto

    (University of Shizuoka)

  • Satoshi Shimizu

    (University of Shizuoka)

  • Kana Shimizu

    (University of Shizuoka)

  • Toshihide Hamabe-Horiike

    (University of Shizuoka
    National Hospital Organization Kyoto Medical Center
    Shizuoka General Hospital)

  • Philip Hawke

    (University of Shizuoka)

  • Maki Komiyama

    (National Hospital Organization Kyoto Medical Center)

  • Kiyoshi Mori

    (Shizuoka General Hospital
    Shizuoka Graduate University of Public Health
    University of Shizuoka)

  • Koji Hasegawa

    (University of Shizuoka
    National Hospital Organization Kyoto Medical Center)

  • Tatsuya Morimoto

    (University of Shizuoka
    National Hospital Organization Kyoto Medical Center
    Shizuoka General Hospital)

Abstract

Protein arginine methyltransferase 5 (PRMT5) is a well-known epigenetic regulatory enzyme. However, the role of PRMT5-mediated arginine methylation in gene transcription related to cardiac fibrosis is unknown. Here we show that fibroblast-specific deletion of PRMT5 significantly reduces pressure overload-induced cardiac fibrosis and improves cardiac dysfunction in male mice. Both the PRMT5-selective inhibitor EPZ015666 and knockdown of PRMT5 suppress α-smooth muscle actin (α-SMA) expression induced by transforming growth factor-β (TGF-β) in cultured cardiac fibroblasts. TGF-β stimulation promotes the recruitment of the PRMT5/Smad3 complex to the promoter site of α-SMA. It also increases PRMT5-mediated H3R2 symmetric dimethylation, and this increase is inhibited by Smad3 knockdown. TGF-β stimulation increases H3K4 tri-methylation mediated by the WDR5/MLL1 methyltransferase complex, which recognizes H3R2 dimethylation. Finally, treatment with EPZ015666 significantly improves pressure overload-induced cardiac fibrosis and dysfunction. These findings suggest that PRMT5 regulates TGF-β/Smad3-dependent fibrotic gene transcription, possibly through histone methylation crosstalk, and plays a critical role in cardiac fibrosis and dysfunction.

Suggested Citation

  • Yasufumi Katanasaka & Harumi Yabe & Noriyuki Murata & Minori Sobukawa & Yuga Sugiyama & Hikaru Sato & Hiroki Honda & Yoichi Sunagawa & Masafumi Funamoto & Satoshi Shimizu & Kana Shimizu & Toshihide Ha, 2024. "Fibroblast-specific PRMT5 deficiency suppresses cardiac fibrosis and left ventricular dysfunction in male mice," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46711-z
    DOI: 10.1038/s41467-024-46711-z
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    1. Sebastian Schafer & Sivakumar Viswanathan & Anissa A. Widjaja & Wei-Wen Lim & Aida Moreno-Moral & Daniel M. DeLaughter & Benjamin Ng & Giannino Patone & Kingsley Chow & Ester Khin & Jessie Tan & Sonia, 2017. "IL-11 is a crucial determinant of cardiovascular fibrosis," Nature, Nature, vol. 552(7683), pages 110-115, December.
    2. Shasha Yin & Liu Liu & Charles Brobbey & Viswanathan Palanisamy & Lauren E. Ball & Shaun K. Olsen & Michael C. Ostrowski & Wenjian Gan, 2021. "PRMT5-mediated arginine methylation activates AKT kinase to govern tumorigenesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Alessandro Bertero & Stephanie Brown & Pedro Madrigal & Anna Osnato & Daniel Ortmann & Loukia Yiangou & Juned Kadiwala & Nina C. Hubner & Igor Ruiz de los Mozos & Christoph Sadée & An-Sofie Lenaerts &, 2018. "The SMAD2/3 interactome reveals that TGFβ controls m6A mRNA methylation in pluripotency," Nature, Nature, vol. 555(7695), pages 256-259, March.
    4. Neil C. Henderson & Florian Rieder & Thomas A. Wynn, 2020. "Fibrosis: from mechanisms to medicines," Nature, Nature, vol. 587(7835), pages 555-566, November.
    5. Ting Zhang & Stefan Günther & Mario Looso & Carsten Künne & Marcus Krüger & Johnny Kim & Yonggang Zhou & Thomas Braun, 2015. "Prmt5 is a regulator of muscle stem cell expansion in adult mice," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
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