A novel mechanism of bulk cytoplasmic transport by cortical dynein in Drosophila ovary

  1. Wen Lu
  2. Margot Lakonishok
  3. Anna S Serpinskaya
  4. Vladimir I Gelfand  Is a corresponding author
  1. Northwestern University, United States
  2. Feinberg School of Medicine, Northwestern University, United States

Abstract

Cytoplasmic dynein, a major minus-end directed microtubule motor, plays essential roles in eukaryotic cells. Drosophila oocyte growth is mainly dependent on the contribution of cytoplasmic contents from the interconnected sister cells, nurse cells. We have previously shown that cytoplasmic dynein is required for Drosophila oocyte growth and assumed that it simply transports cargoes along microtubule tracks from nurse cells to the oocyte. Here we report that instead of transporting individual cargoes along stationary microtubules into the oocyte, cortical dynein actively moves microtubules within nurse cells and from nurse cells to the oocyte via the cytoplasmic bridges, the ring canals. This robust microtubule movement is sufficient to drag even inert cytoplasmic particles through the ring canals to the oocyte. Furthermore, replacing dynein with a minus-end directed plant kinesin linked to the actin cortex is sufficient for transporting organelles and cytoplasm to the oocyte and driving its growth. These experiments show that cortical dynein performs bulk cytoplasmic transport by gliding microtubules along the cell cortex and through the ring canals to the oocyte. We propose that the dynein-driven microtubule flow could serve as a novel mode of fast cytoplasmic transport.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figure 5.

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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8849-8100
  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. Anna S Serpinskaya

    Department of Cell and Molecular Biology, Feinberg School of Medicine, Feinberg School of Medicine, Northwestern University, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. 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 (R35 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. Kassandra M Ori-McKenney, University of California, United States

Publication history

  1. Preprint posted: November 13, 2021 (view preprint)
  2. Received: November 13, 2021
  3. Accepted: February 16, 2022
  4. Accepted Manuscript published: February 16, 2022 (version 1)
  5. Version of Record published: March 4, 2022 (version 2)

Copyright

© 2022, Lu 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. Wen Lu
  2. Margot Lakonishok
  3. Anna S Serpinskaya
  4. Vladimir I Gelfand
(2022)
A novel mechanism of bulk cytoplasmic transport by cortical dynein in Drosophila ovary
eLife 11:e75538.
https://doi.org/10.7554/eLife.75538
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