A positive feedback-based mechanism for constriction rate acceleration during cytokinesis in C. elegans

Abstract

To ensure timely cytokinesis, the equatorial actomyosin contractile ring constricts at a relatively constant rate despite its progressively decreasing size. Thus, the per-unit-length constriction rate increases as ring perimeter decreases. To understand this acceleration, we monitored cortical surface and ring component dynamics during the first cytokinesis of the C. elegans embryo. We found that, per-unit-length, the amount of ring components (myosin, anillin) and the constriction rate increase with parallel exponential kinetics. Quantitative analysis of cortical flow indicated that the cortex within the ring is compressed along the axis perpendicular to the ring, and the per-unit-length rate of cortical compression increases during constriction in proportion to ring myosin. We propose that positive feedback between ring myosin and compression-driven flow of cortex into the ring drives an exponential increase in the per-unit-length amount of ring myosin to maintain a high ring constriction rate and support this proposal with an analytical mathematical model.

Data availability

All data generated during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Renat N Khaliullin

    Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, United States
    For correspondence
    renatkh@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebecca A Green

    Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Linda Z Shi

    Department of Bioengineering and Institute of Engineering in Medicine, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. J Sebastian Gomez-Cavazo

    Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Michael W Berns

    Department of Bioengineering and Institute of Engineering in Medicine, University of California, San Diego, La Jolla, United States
    For correspondence
    mwberns17@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  6. Arshad Desai

    Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5410-1830
  7. Karen Oegema

    Department of Cellular and Molecular Medicine, Ludwig Institute for Cancer Research, University of California, San Diego, La Jolla, United States
    For correspondence
    koegema@ucsd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8515-7514

Funding

Ludwig Institute for Cancer Research

  • Arshad Desai
  • Karen Oegema

Beckman Laser Institute and Medical Clinic

  • Michael W Berns

Air Force Office of Scientific Research (FA9550-08-1-0284)

  • Michael W Berns

Jane Coffin Childs Memorial Fund for Medical Research

  • Renat N Khaliullin

National Institutes of Health (T32 CA067754)

  • J Sebastian Gomez-Cavazo

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

Reviewing Editor

  1. Mohan K Balasubramanian, University of Warwick, United Kingdom

Version history

  1. Received: February 20, 2018
  2. Accepted: July 1, 2018
  3. Accepted Manuscript published: July 2, 2018 (version 1)
  4. Accepted Manuscript updated: July 5, 2018 (version 2)
  5. Version of Record published: July 27, 2018 (version 3)

Copyright

© 2018, Khaliullin 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. Renat N Khaliullin
  2. Rebecca A Green
  3. Linda Z Shi
  4. J Sebastian Gomez-Cavazo
  5. Michael W Berns
  6. Arshad Desai
  7. Karen Oegema
(2018)
A positive feedback-based mechanism for constriction rate acceleration during cytokinesis in C. elegans
eLife 7:e36073.
https://doi.org/10.7554/eLife.36073

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https://doi.org/10.7554/eLife.36073

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