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A FRET biosensor for necroptosis uncovers two different modes of the release of DAMPs

Author

Listed:
  • Shin Murai

    (Toho University School of Medicine)

  • Yoshifumi Yamaguchi

    (Hokkaido University)

  • Yoshitaka Shirasaki

    (Japan Science and Technology Agency
    The University of Tokyo)

  • Mai Yamagishi

    (The University of Tokyo)

  • Ryodai Shindo

    (Toho University School of Medicine)

  • Joanne M. Hildebrand

    (The Walter and Eliza Hall Institute of Medical Research
    University of Melbourne)

  • Ryosuke Miura

    (Toho University School of Medicine
    Tokyo University of Science)

  • Osamu Nakabayashi

    (Toho University School of Medicine)

  • Mamoru Totsuka

    (Nippon Veterinary and Life Science University)

  • Taichiro Tomida

    (Toho University School of Medicine)

  • Satomi Adachi-Akahane

    (Toho University School of Medicine)

  • Sotaro Uemura

    (The University of Tokyo)

  • John Silke

    (The Walter and Eliza Hall Institute of Medical Research
    University of Melbourne)

  • Hideo Yagita

    (Juntendo University Graduate School of Medicine)

  • Masayuki Miura

    (The University of Tokyo)

  • Hiroyasu Nakano

    (Toho University School of Medicine
    Toho University School of Medicine)

Abstract

Necroptosis is a regulated form of necrosis that depends on receptor-interacting protein kinase (RIPK)3 and mixed lineage kinase domain-like (MLKL). While danger-associated molecular pattern (DAMP)s are involved in various pathological conditions and released from dead cells, the underlying mechanisms are not fully understood. Here we develop a fluorescence resonance energy transfer (FRET) biosensor, termed SMART (a sensor for MLKL activation by RIPK3 based on FRET). SMART is composed of a fragment of MLKL and monitors necroptosis, but not apoptosis or necrosis. Mechanistically, SMART monitors plasma membrane translocation of oligomerized MLKL, which is induced by RIPK3 or mutational activation. SMART in combination with imaging of the release of nuclear DAMPs and Live-Cell Imaging for Secretion activity (LCI-S) reveals two different modes of the release of High Mobility Group Box 1 from necroptotic cells. Thus, SMART and LCI-S uncover novel regulation of the release of DAMPs during necroptosis.

Suggested Citation

  • Shin Murai & Yoshifumi Yamaguchi & Yoshitaka Shirasaki & Mai Yamagishi & Ryodai Shindo & Joanne M. Hildebrand & Ryosuke Miura & Osamu Nakabayashi & Mamoru Totsuka & Taichiro Tomida & Satomi Adachi-Aka, 2018. "A FRET biosensor for necroptosis uncovers two different modes of the release of DAMPs," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-06985-6
    DOI: 10.1038/s41467-018-06985-6
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    Cited by:

    1. Yanxiang Meng & Katherine A. Davies & Cheree Fitzgibbon & Samuel N. Young & Sarah E. Garnish & Christopher R. Horne & Cindy Luo & Jean-Marc Garnier & Lung-Yu Liang & Angus D. Cowan & Andre L. Samson &, 2021. "Human RIPK3 maintains MLKL in an inactive conformation prior to cell death by necroptosis," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Yuka Inaba & Emi Hashiuchi & Hitoshi Watanabe & Kumi Kimura & Yu Oshima & Kohsuke Tsuchiya & Shin Murai & Chiaki Takahashi & Michihiro Matsumoto & Shigetaka Kitajima & Yasuhiko Yamamoto & Masao Honda , 2023. "The transcription factor ATF3 switches cell death from apoptosis to necroptosis in hepatic steatosis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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