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Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis

Author

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  • Kei Yamamoto

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies))

  • Haruko Miura

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences)

  • Motohiko Ishida

    (University of Tokyo
    Universal Biology Institute, University of Tokyo)

  • Yusuke Mii

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies)
    Japan Science and Technology Agency (JST), PRESTO)

  • Noriyuki Kinoshita

    (National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies))

  • Shinji Takada

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies))

  • Naoto Ueno

    (National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies)
    National Institutes of Natural Sciences)

  • Satoshi Sawai

    (University of Tokyo
    Universal Biology Institute, University of Tokyo)

  • Yohei Kondo

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies))

  • Kazuhiro Aoki

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    SOKENDAI (The Graduate University for Advanced Studies)
    National Institutes of Natural Sciences)

Abstract

Actomyosin contractility generated cooperatively by nonmuscle myosin II and actin filaments plays essential roles in a wide range of biological processes, such as cell motility, cytokinesis, and tissue morphogenesis. However, subcellular dynamics of actomyosin contractility underlying such processes remains elusive. Here, we demonstrate an optogenetic method to induce relaxation of actomyosin contractility at the subcellular level. The system, named OptoMYPT, combines a protein phosphatase 1c (PP1c)-binding domain of MYPT1 with an optogenetic dimerizer, so that it allows light-dependent recruitment of endogenous PP1c to the plasma membrane. Blue-light illumination is sufficient to induce dephosphorylation of myosin regulatory light chains and a decrease in actomyosin contractile force in mammalian cells and Xenopus embryos. The OptoMYPT system is further employed to understand the mechanics of actomyosin-based cortical tension and contractile ring tension during cytokinesis. We find that the relaxation of cortical tension at both poles by OptoMYPT accelerated the furrow ingression rate, revealing that the cortical tension substantially antagonizes constriction of the cleavage furrow. Based on these results, the OptoMYPT system provides opportunities to understand cellular and tissue mechanics.

Suggested Citation

  • Kei Yamamoto & Haruko Miura & Motohiko Ishida & Yusuke Mii & Noriyuki Kinoshita & Shinji Takada & Naoto Ueno & Satoshi Sawai & Yohei Kondo & Kazuhiro Aoki, 2021. "Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27458-3
    DOI: 10.1038/s41467-021-27458-3
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    References listed on IDEAS

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    1. Emilie Montembault & Irène Deduyer & Marie-Charlotte Claverie & Lou Bouit & Nicolas J. Tourasse & Denis Dupuy & Derek McCusker & Anne Royou, 2023. "Two RhoGEF isoforms with distinct localisation control furrow position during asymmetric cell division," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Guillermo Martínez-Ara & Núria Taberner & Mami Takayama & Elissavet Sandaltzopoulou & Casandra E. Villava & Miquel Bosch-Padrós & Nozomu Takata & Xavier Trepat & Mototsugu Eiraku & Miki Ebisuya, 2022. "Optogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Özge Özgüç & Ludmilla de Plater & Varun Kapoor & Anna Francesca Tortorelli & Andrew G Clark & Jean-Léon Maître, 2022. "Cortical softening elicits zygotic contractility during mouse preimplantation development," PLOS Biology, Public Library of Science, vol. 20(3), pages 1-23, March.

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