Curvature-induced expulsion of actomyosin bundles during cytokinetic ring contraction

  1. Junqi Huang  Is a corresponding author
  2. Ting Gang Chew  Is a corresponding author
  3. Ying Gu
  4. Saravanan Palani
  5. Anton Kamnev
  6. Douglas S Martin
  7. Nicholas J Carter
  8. Robert Anthony Cross
  9. Snezhana Oliferenko
  10. Mohan K Balasubramanian  Is a corresponding author
  1. University of Warwick, United Kingdom
  2. King's College London, United Kingdom
  3. Lawrence University, United States

Abstract

Many eukaryotes assemble a ring-shaped actomyosin network that contracts to drive cytokinesis. Unlike actomyosin in sarcomeres, which cycles through contraction and relaxation, the cytokinetic ring disassembles during contraction through an unknown mechanism. Here we find in Schizosaccharomyces japonicus and Schizosaccharomyces pombe that, during actomyosin ring contraction, actin filaments associated with actomyosin rings are expelled as micron-scale bundles containing multiple actomyosin ring proteins. Using functional isolated actomyosin rings we show that expulsion of actin bundles does not require continuous presence of cytoplasm. Strikingly, mechanical compression of actomyosin rings results in expulsion of bundles predominantly at regions of high curvature. Our work unprecedentedly reveals that the increased curvature of the ring itself promotes its disassembly. It is likely that such a curvature-induced mechanism may operate in disassembly of other contractile networks.

Article and author information

Author details

  1. Junqi Huang

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    For correspondence
    junqi.huang@warwick.ac.uk
    Competing interests
    No competing interests declared.
  2. Ting Gang Chew

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    For correspondence
    t.g.chew@warwick.ac.uk
    Competing interests
    No competing interests declared.
  3. Ying Gu

    Randall Division of Cell and Molecular Biophysics, King's College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  4. Saravanan Palani

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  5. Anton Kamnev

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  6. Douglas S Martin

    Department of Physics, Lawrence University, Appleton, United States
    Competing interests
    No competing interests declared.
  7. Nicholas J Carter

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
  8. Robert Anthony Cross

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0004-7832
  9. Snezhana Oliferenko

    Randall Division of Cell and Molecular Biophysics, King's College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  10. Mohan K Balasubramanian

    Division of Biomedical Sciences, Warwick Medical School, University of Warwick, Coventry, United Kingdom
    For correspondence
    m.k.balasubramanian@warwick.ac.uk
    Competing interests
    Mohan K Balasubramanian, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1292-8602

Funding

Wellcome (WT101885MA)

  • Mohan K Balasubramanian

Royal Society

  • Mohan K Balasubramanian

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Anthony A Hyman, Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Publication history

  1. Received: September 9, 2016
  2. Accepted: October 12, 2016
  3. Accepted Manuscript published: October 13, 2016 (version 1)
  4. Version of Record published: October 24, 2016 (version 2)
  5. Version of Record updated: October 25, 2016 (version 3)

Copyright

© 2016, Huang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Junqi Huang
  2. Ting Gang Chew
  3. Ying Gu
  4. Saravanan Palani
  5. Anton Kamnev
  6. Douglas S Martin
  7. Nicholas J Carter
  8. Robert Anthony Cross
  9. Snezhana Oliferenko
  10. Mohan K Balasubramanian
(2016)
Curvature-induced expulsion of actomyosin bundles during cytokinetic ring contraction
eLife 5:e21383.
https://doi.org/10.7554/eLife.21383

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