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CYK-4 functions independently of its centralspindlin partner ZEN-4 to cellularize oocytes in germline syncytia

  1. Kian-Yong Lee
  2. Rebecca A Green
  3. Edgar Gutierrez
  4. J Sebastian Gomez-Cavazos
  5. Irina Kolotuev
  6. Shaohe Wang
  7. Arshad Desai
  8. Alex Groisman
  9. Karen Oegema  Is a corresponding author
  1. University of California, San Diego, United States
  2. University of Lausanne, Switzerland
Research Article
  • Cited 5
  • Views 940
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Cite this article as: eLife 2018;7:e36919 doi: 10.7554/eLife.36919

Abstract

Throughout metazoans, germ cells undergo incomplete cytokinesis to form syncytia connected by intercellular bridges. Gamete formation ultimately requires bridge closure, yet how bridges are reactivated to close is not known. The most conserved bridge component is centralspindlin, a complex of the Rho family GTPase-activating protein (GAP) CYK-4/MgcRacGAP and the microtubule motor ZEN-4/kinesin-6. Here, we show that oocyte production by the syncytial C. elegans germline requires CYK-4 but not ZEN-4, which contrasts with cytokinesis, where both are essential. Longitudinal imaging after conditional inactivation revealed that CYK-4 activity is important for oocyte cellularization, but not for the cytokinesis-like events that generate syncytial compartments. CYK-4's lipid-binding C1 domain and the GTPase-binding interface of its GAP domain were both required to target CYK-4 to intercellular bridges and to cellularize oocytes. These results suggest that the conserved C1-GAP region of CYK-4 constitutes a targeting module required for closure of intercellular bridges in germline syncytia.

Article and author information

Author details

  1. Kian-Yong Lee

    Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, 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:" 0000-0003-0946-1703
  2. Rebecca A Green

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

    Department of Physics, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. J Sebastian Gomez-Cavazos

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

    EM Facility, University of Lausanne, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1433-8048
  6. Shaohe Wang

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

    Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, 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
  8. Alex Groisman

    Department of Physics, University of California, San Diego, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Karen Oegema

    Ludwig Institute for Cancer Research, Department of Cellular and Molecular Medicine, 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

National Institutes of Health (T32 CA067754)

  • J Sebastian Gomez-Cavazos

National Science Foundation (PHY-14113130)

  • Alex Groisman

Ludwig Institute for Cancer Research

  • Arshad Desai
  • Karen Oegema

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: March 23, 2018
  2. Accepted: July 9, 2018
  3. Accepted Manuscript published: July 10, 2018 (version 1)
  4. Version of Record published: July 23, 2018 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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