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A FRET-based respirasome assembly screen identifies spleen tyrosine kinase as a target to improve muscle mitochondrial respiration and exercise performance in mice

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  • Ami Kobayashi

    (Tokyo Metropolitan Institute of Gerontology
    The University of Tokyo)

  • Kotaro Azuma

    (Tokyo Metropolitan Institute of Gerontology)

  • Toshihiko Takeiwa

    (Tokyo Metropolitan Institute of Gerontology)

  • Toshimori Kitami

    (RIKEN Center for Integrative Medical Sciences)

  • Kuniko Horie

    (Saitama Medical University)

  • Kazuhiro Ikeda

    (Saitama Medical University)

  • Satoshi Inoue

    (Tokyo Metropolitan Institute of Gerontology
    Saitama Medical University)

Abstract

Aerobic muscle activities predominantly depend on fuel energy supply by mitochondrial respiration, thus, mitochondrial activity enhancement may become a therapeutic intervention for muscle disturbances. The assembly of mitochondrial respiratory complexes into higher-order “supercomplex” structures has been proposed to be an efficient biological process for energy synthesis, although there is controversy in its physiological relevance. We here established Förster resonance energy transfer (FRET) phenomenon-based live imaging of mitochondrial respiratory complexes I and IV interactions using murine myoblastic cells, whose signals represent in vivo supercomplex assembly of complexes I, III, and IV, or respirasomes. The live FRET signals were well correlated with supercomplex assembly observed by blue native polyacrylamide gel electrophoresis (BN-PAGE) and oxygen consumption rates. FRET-based live cell screen defined that the inhibition of spleen tyrosine kinase (SYK), a non-receptor protein tyrosine kinase that belongs to the SYK/ zeta-chain-associated protein kinase 70 (ZAP-70) family, leads to an increase in supercomplex assembly in murine myoblastic cells. In parallel, SYK inhibition enhanced mitochondrial respiration in the cells. Notably, SYK inhibitor administration enhances exercise performance in mice. Overall, this study proves the feasibility of FRET-based respirasome assembly assay, which recapitulates in vivo mitochondrial respiration activities.

Suggested Citation

  • Ami Kobayashi & Kotaro Azuma & Toshihiko Takeiwa & Toshimori Kitami & Kuniko Horie & Kazuhiro Ikeda & Satoshi Inoue, 2023. "A FRET-based respirasome assembly screen identifies spleen tyrosine kinase as a target to improve muscle mitochondrial respiration and exercise performance in mice," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35865-x
    DOI: 10.1038/s41467-023-35865-x
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    1. Sara Cogliati & Enrique Calvo & Marta Loureiro & Adela M. Guaras & Rocio Nieto-Arellano & Carolina Garcia-Poyatos & Iakes Ezkurdia & Nadia Mercader & Jesús Vázquez & José Antonio Enriquez, 2016. "Mechanism of super-assembly of respiratory complexes III and IV," Nature, Nature, vol. 539(7630), pages 579-582, November.
    2. James A. Letts & Karol Fiedorczuk & Leonid A. Sazanov, 2016. "The architecture of respiratory supercomplexes," Nature, Nature, vol. 537(7622), pages 644-648, September.
    3. Irene Vercellino & Leonid A. Sazanov, 2021. "Structure and assembly of the mammalian mitochondrial supercomplex CIII2CIV," Nature, Nature, vol. 598(7880), pages 364-367, October.
    4. Kazuhiro Ikeda & Sachiko Shiba & Kuniko Horie-Inoue & Kunitoshi Shimokata & Satoshi Inoue, 2013. "A stabilizing factor for mitochondrial respiratory supercomplex assembly regulates energy metabolism in muscle," Nature Communications, Nature, vol. 4(1), pages 1-9, October.
    5. Michael T. Lin & M. Flint Beal, 2006. "Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases," Nature, Nature, vol. 443(7113), pages 787-795, October.
    6. Kazuhiro Ikeda & Kuniko Horie-Inoue & Takashi Suzuki & Rutsuko Hobo & Norie Nakasato & Satoru Takeda & Satoshi Inoue, 2019. "Mitochondrial supercomplex assembly promotes breast and endometrial tumorigenesis by metabolic alterations and enhanced hypoxia tolerance," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
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