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Interplay between kinesin-1 and cortical dynein during axonal outgrowth and microtubule organization in Drosophila neurons

  1. Urko del Castillo
  2. Michael Winding
  3. Wen Lu
  4. Vladimir I Gelfand  Is a corresponding author
  1. Northwestern University, United States
Research Article
  • Cited 54
  • Views 3,546
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Cite this article as: eLife 2015;4:e10140 doi: 10.7554/eLife.10140

Abstract

In this study, we investigated how microtubule motors organize microtubules in Drosophila neurons. We showed that, during the initial stages of axon outgrowth, microtubules display mixed polarity and minus-end-out microtubules push the tip of the axon, consistent with kinesin-1 driving outgrowth by sliding antiparallel microtubules. At later stages, the microtubule orientation in the axon switches from mixed to uniform polarity with plus-end-out. Dynein knockdown prevents this rearrangement and results in microtubules of mixed orientation in axons and accumulation of microtubule minus-ends at axon tips. Microtubule reorganization requires recruitment of dynein to the actin cortex, as actin depolymerization phenocopies dynein depletion, and direct recruitment of dynein to the membrane bypasses the actin requirement. Our results show that cortical dynein slides 'minus-end-out' microtubules from the axon, generating uniform microtubule arrays. We speculate that differences in microtubule orientation between axons and dendrites could be dictated by differential activity of cortical dynein.

Article and author information

Author details

  1. Urko del Castillo

    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. Michael Winding

    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.
  3. 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.
  4. Vladimir I Gelfand

    Department of Cell and Molecular 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.

Reviewing Editor

  1. Viki Allan, University of Manchester, United Kingdom

Publication history

  1. Received: July 16, 2015
  2. Accepted: November 27, 2015
  3. Accepted Manuscript published: November 28, 2015 (version 1)
  4. Accepted Manuscript updated: December 7, 2015 (version 2)
  5. Version of Record published: January 22, 2016 (version 3)

Copyright

© 2015, del Castillo 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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