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Cold-induced FOXO1 nuclear transport aids cold survival and tissue storage

Author

Listed:
  • Xiaomei Zhang

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University
    Harvard Medical School)

  • Lihao Ge

    (Xinxiang Medical University)

  • Guanghui Jin

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University
    The First Affiliated Hospital of Guangzhou Medical University)

  • Yasong Liu

    (Sun Yat-sen University)

  • Qingfen Yu

    (The Third Affiliated Hospital of Sun Yat-sen University)

  • Weizhao Chen

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University)

  • Liang Chen

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University)

  • Tao Dong

    (Sun Yat-sen University
    University of Michigan)

  • Kiyoharu J. Miyagishima

    (National Institutes of Health)

  • Juan Shen

    (the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine)

  • Jinghong Yang

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University)

  • Guo Lv

    (Guangdong province engineering laboratory for transplantation medicine)

  • Yan Xu

    (the Third Affiliated Hospital of Sun Yat-sen University)

  • Qing Yang

    (Sun Yat-sen University)

  • Linsen Ye

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University)

  • Shuhong Yi

    (Sun Yat-sen University)

  • Hua Li

    (Sun Yat-sen University)

  • Qi Zhang

    (the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine
    the Third Affiliated Hospital of Sun Yat-sen University)

  • Guihua Chen

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine)

  • Wei Liu

    (the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine)

  • Yang Yang

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine)

  • Wei Li

    (National Institutes of Health)

  • Jingxing Ou

    (Sun Yat-sen University
    the Third Affiliated Hospital of Sun Yat-sen University
    Guangdong province engineering laboratory for transplantation medicine)

Abstract

Cold-induced injuries severely limit opportunities and outcomes of hypothermic therapies and organ preservation, calling for better understanding of cold adaptation. Here, by surveying cold-altered chromatin accessibility and integrated CUT&Tag/RNA-seq analyses in human stem cells, we reveal forkhead box O1 (FOXO1) as a key transcription factor for autonomous cold adaptation. Accordingly, we find a nonconventional, temperature-sensitive FOXO1 transport mechanism involving the nuclear pore complex protein RANBP2, SUMO-modification of transporter proteins Importin-7 and Exportin-1, and a SUMO-interacting motif on FOXO1. Our conclusions are supported by cold survival experiments with human cell models and zebrafish larvae. Promoting FOXO1 nuclear entry by the Exportin-1 inhibitor KPT-330 enhances cold tolerance in pre-diabetic obese mice, and greatly prolongs the shelf-life of human and mouse pancreatic tissues and islets. Transplantation of mouse islets cold-stored for 14 days reestablishes normoglycemia in diabetic mice. Our findings uncover a regulatory network and potential therapeutic targets to boost spontaneous cold adaptation.

Suggested Citation

  • Xiaomei Zhang & Lihao Ge & Guanghui Jin & Yasong Liu & Qingfen Yu & Weizhao Chen & Liang Chen & Tao Dong & Kiyoharu J. Miyagishima & Juan Shen & Jinghong Yang & Guo Lv & Yan Xu & Qing Yang & Linsen Ye, 2024. "Cold-induced FOXO1 nuclear transport aids cold survival and tissue storage," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47095-w
    DOI: 10.1038/s41467-024-47095-w
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    References listed on IDEAS

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