1. Cell Biology
  2. Computational and Systems Biology
Download icon

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

  1. Renat N Khaliullin  Is a corresponding author
  2. Rebecca A Green
  3. Linda Z Shi
  4. J Sebastian Gomez-Cavazo
  5. Michael W Berns  Is a corresponding author
  6. Arshad Desai
  7. Karen Oegema  Is a corresponding author
  1. University of California, San Diego, United States
Research Article
  • Cited 6
  • Views 1,186
  • Annotations
Cite this article as: eLife 2018;7:e36073 doi: 10.7554/eLife.36073

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.

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

Publication 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.

Metrics

  • 1,186
    Page views
  • 235
    Downloads
  • 6
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Cell Biology
    Alison K Gillingham et al.
    Tools and Resources Updated
    1. Cell Biology
    2. Chromosomes and Gene Expression
    Konstadinos Moissoglu et al.
    Research Article Updated