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Oxidation of F-actin controls the terminal steps of cytokinesis

Author

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  • Stéphane Frémont

    (Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department Institut Pasteur
    Centre National de la Recherche Scientifique UMR3691)

  • Hussein Hammich

    (Structural Motility, Institut Curie, PSL Research University,)

  • Jian Bai

    (Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department Institut Pasteur
    Centre National de la Recherche Scientifique UMR3691
    Sorbonne Universités)

  • Hugo Wioland

    (Institut Jacques Monod, CNRS, Université Paris Diderot, Université Sorbonne Paris Cité)

  • Kerstin Klinkert

    (Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department Institut Pasteur
    Centre National de la Recherche Scientifique UMR3691
    Sorbonne Universités)

  • Murielle Rocancourt

    (Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department Institut Pasteur
    Centre National de la Recherche Scientifique UMR3691)

  • Carlos Kikuti

    (Structural Motility, Institut Curie, PSL Research University,)

  • David Stroebel

    (Ecole Normale Supérieure, PSL Research University, CNRS, INSERM, Institut de Biologie de l'École Normale Supérieure (IBENS))

  • Guillaume Romet-Lemonne

    (Institut Jacques Monod, CNRS, Université Paris Diderot, Université Sorbonne Paris Cité)

  • Olena Pylypenko

    (Structural Motility, Institut Curie, PSL Research University,)

  • Anne Houdusse

    (Structural Motility, Institut Curie, PSL Research University,)

  • Arnaud Echard

    (Membrane Traffic and Cell Division Lab, Cell Biology and Infection Department Institut Pasteur
    Centre National de la Recherche Scientifique UMR3691)

Abstract

Cytokinetic abscission, the terminal step of cell division, crucially depends on the local constriction of ESCRT-III helices after cytoskeleton disassembly. While the microtubules of the intercellular bridge are cut by the ESCRT-associated enzyme Spastin, the mechanism that clears F-actin at the abscission site is unknown. Here we show that oxidation-mediated depolymerization of actin by the redox enzyme MICAL1 is key for ESCRT-III recruitment and successful abscission. MICAL1 is recruited to the abscission site by the Rab35 GTPase through a direct interaction with a flat three-helix domain found in MICAL1 C terminus. Mechanistically, in vitro assays on single actin filaments demonstrate that MICAL1 is activated by Rab35. Moreover, in our experimental conditions, MICAL1 does not act as a severing enzyme, as initially thought, but instead induces F-actin depolymerization from both ends. Our work reveals an unexpected role for oxidoreduction in triggering local actin depolymerization to control a fundamental step of cell division.

Suggested Citation

  • Stéphane Frémont & Hussein Hammich & Jian Bai & Hugo Wioland & Kerstin Klinkert & Murielle Rocancourt & Carlos Kikuti & David Stroebel & Guillaume Romet-Lemonne & Olena Pylypenko & Anne Houdusse & Arn, 2017. "Oxidation of F-actin controls the terminal steps of cytokinesis," Nature Communications, Nature, vol. 8(1), pages 1-16, April.
  • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms14528
    DOI: 10.1038/ncomms14528
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    Cited by:

    1. Daan M. K. Soest & Paulien E. Polderman & Wytze T. F. Toom & Janneke P. Keijer & Markus J. Roosmalen & Tim M. F. Leyten & Johannes Lehmann & Susan Zwakenberg & Sasha Henau & Ruben Boxtel & Boudewijn M, 2024. "Mitochondrial H2O2 release does not directly cause damage to chromosomal DNA," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    2. Tamara Advedissian & Stéphane Frémont & Arnaud Echard, 2024. "Cytokinetic abscission requires actin-dependent microtubule severing," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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