Competition between kinesin-1 and myosin-V defines Drosophila posterior determination

  1. Wen Lu
  2. Margot Lakonishok
  3. Rong Liu
  4. Neil Billington
  5. Ashley Rich
  6. Michael Glotzer
  7. James R Sellers
  8. Vladimir I Gelfand  Is a corresponding author
  1. Northwestern University, United States
  2. National Heart, Lung and Blood Institute, National Institutes of Health, United States
  3. University of Chicago, United States

Abstract

Local accumulation of oskar (osk) mRNA in the Drosophila oocyte determines the posterior pole of the future embryo. Two major cytoskeletal components, microtubules and actin filaments, together with a microtubule motor, kinesin-1, and an actin motor, myosin-V, are essential for osk mRNA posterior localization. In this study, we use Staufen, an RNA-binding protein that colocalizes with osk mRNA, as a proxy for osk mRNA. We demonstrate that posterior localization of osk/Staufen is determined by competition between kinesin-1 and myosin-V. While kinesin-1 removes osk/Staufen from the cortex along microtubules, myosin-V anchors osk/Staufen at the cortex. Myosin-V wins over kinesin-1 at the posterior pole due to low microtubule density at this site, while kinesin-1 wins at anterior and lateral positions because they have high density of cortically-anchored microtubules. As a result, posterior determinants are removed from the anterior and lateral cortex but retained at the posterior pole. Thus, posterior determination of Drosophila oocytes is defined by kinesin-myosin competition, whose outcome is primarily determined by cortical microtubule density.

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

Article and author information

Author details

  1. Wen Lu

    Department of Cell and Molecular Biology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Margot Lakonishok

    Department of Cell and Developmental Biology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rong Liu

    Cell Biology and Physiology Center, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Neil Billington

    Cell Biology and Physiology Center, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2306-0228
  5. Ashley Rich

    Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Michael Glotzer

    Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8723-7232
  7. James R Sellers

    Cell Biology and Physiology Center, National Heart, Lung and Blood Institute, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6296-564X
  8. Vladimir I Gelfand

    Department of Cell and Developmental Biology, Feinberg School of Medicine, Northwestern University, Chicago, United States
    For correspondence
    vgelfand@northwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6361-2798

Funding

National Institute of General Medical Sciences (GM124029)

  • Vladimir I Gelfand

National Institute of General Medical Sciences (GM131752)

  • Vladimir I Gelfand

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

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Version history

  1. Received: December 5, 2019
  2. Accepted: February 14, 2020
  3. Accepted Manuscript published: February 14, 2020 (version 1)
  4. Version of Record published: April 1, 2020 (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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  1. Wen Lu
  2. Margot Lakonishok
  3. Rong Liu
  4. Neil Billington
  5. Ashley Rich
  6. Michael Glotzer
  7. James R Sellers
  8. Vladimir I Gelfand
(2020)
Competition between kinesin-1 and myosin-V defines Drosophila posterior determination
eLife 9:e54216.
https://doi.org/10.7554/eLife.54216

Share this article

https://doi.org/10.7554/eLife.54216

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