Kinesin and dynein use distinct mechanisms to bypass obstacles

  1. Luke S Ferro
  2. Sinan Can
  3. Meghan A Turner
  4. Mohamed M ElShenawy
  5. Ahmet Yildiz  Is a corresponding author
  1. University of California, Berkeley, United States

Abstract

Kinesin-1 and cytoplasmic dynein are microtubule (MT) motors that transport intracellular cargos. It remains unclear how these motors move along MTs densely coated with obstacles of various sizes in the cytoplasm. Here, we tested the ability of single and multiple motors to bypass synthetic obstacles on MTs in vitro. Contrary to previous reports, we found that mammalian dynein is highly capable of bypassing obstacles. Human kinesin-1 motors fail to avoid obstacles, consistent with their inability to take sideways steps on to neighboring MT protofilaments. Kinesins overcome this limitation when working in teams, bypassing obstacles as effectively as multiple dyneins. Cargos driven by multiple kinesin or dyneins are also capable of rotating around the MT to bypass large obstacles. These results suggest that multiplicity of motors is required not only for transporting cargos over long distances and generating higher forces, but also for maneuvering of the cargos on obstacle-coated MT surfaces.

Data availability

All data generated or analyzed during this study will be included in the manuscript and supporting files.

Article and author information

Author details

  1. Luke S Ferro

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Sinan Can

    Department of Physics, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Meghan A Turner

    Biophysics Graduate Group, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Mohamed M ElShenawy

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ahmet Yildiz

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    yildiz@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4792-174X

Funding

National Institute of General Medical Sciences (GM094522)

  • Ahmet Yildiz

National Science Foundation (MCB-1055017)

  • Ahmet Yildiz

National Science Foundation (MCB-1617028)

  • Ahmet Yildiz

National Institute of General Medical Sciences (GM123655-03)

  • Luke S Ferro

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

Reviewing Editor

  1. Thomas Surrey, The Francis Crick Institute, United Kingdom

Publication history

  1. Received: May 21, 2019
  2. Accepted: September 7, 2019
  3. Accepted Manuscript published: September 9, 2019 (version 1)
  4. Version of Record published: October 8, 2019 (version 2)

Copyright

© 2019, Ferro 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. Luke S Ferro
  2. Sinan Can
  3. Meghan A Turner
  4. Mohamed M ElShenawy
  5. Ahmet Yildiz
(2019)
Kinesin and dynein use distinct mechanisms to bypass obstacles
eLife 8:e48629.
https://doi.org/10.7554/eLife.48629

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