Multiple kinesins induce tension for smooth cargo transport

  1. Marco Tjioe
  2. Saurabh Shukla
  3. Rohit Vaidya
  4. Alice Troitskaia
  5. Carol S Bookwalter
  6. Kathleen M Trybus
  7. Yann R Chemla
  8. Paul R Selvin  Is a corresponding author
  1. University of Illinois at Urbana-Champaign, United States
  2. University of Vermont, United States

Abstract

How cargoes move within a crowded cell—over long distances and at speeds nearly the same as when moving on unimpeded pathway—has long been mysterious. Through an in vitro force-gliding assay, which involves measuring nanometer displacement and piconewtons of force, we show that multiple mammalian kinesin-1 (from 2-8) communicate in a team by inducing tension (up to 4 pN) on the cargo. Kinesins adopt two distinct states, with one-third slowing down the microtubule and two-thirds speeding it up. Resisting kinesins tend to come off more rapidly than, and speed up when pulled by driving kinesins, implying an asymmetric tug-of-war. Furthermore, kinesins dynamically interact to overcome roadblocks, occasionally combining their forces. Consequently, multiple kinesins acting as a team may play a significant role in facilitating smooth cargo motion in a dense environment. This is one of few cases in which single molecule behavior can be connected to ensemble behavior of multiple motors.

Data availability

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

Article and author information

Author details

  1. Marco Tjioe

    Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Saurabh Shukla

    Center for the Physics of Living Cells, University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Rohit Vaidya

    Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Alice Troitskaia

    Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Carol S Bookwalter

    Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kathleen M Trybus

    Department of Molecular Physiology and Biophysics, University of Vermont, Burlington, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5583-8500
  7. Yann R Chemla

    Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9167-0234
  8. Paul R Selvin

    Center for Biophysics and Quantitative Biology, University of Illinois at Urbana-Champaign, Champaign, United States
    For correspondence
    selvin@illinois.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3658-4218

Funding

National Institutes of Health (GM108578)

  • Paul R Selvin

National Science Foundation (1430124)

  • Paul R Selvin

National Institutes of Health (GM078097)

  • Kathleen M Trybus

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

Reviewing Editor

  1. Taekjip Ha, Johns Hopkins University, United States

Publication history

  1. Received: August 9, 2019
  2. Accepted: October 31, 2019
  3. Accepted Manuscript published: October 31, 2019 (version 1)
  4. Version of Record published: December 10, 2019 (version 2)
  5. Version of Record updated: March 13, 2020 (version 3)

Copyright

© 2019, Tjioe 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. Marco Tjioe
  2. Saurabh Shukla
  3. Rohit Vaidya
  4. Alice Troitskaia
  5. Carol S Bookwalter
  6. Kathleen M Trybus
  7. Yann R Chemla
  8. Paul R Selvin
(2019)
Multiple kinesins induce tension for smooth cargo transport
eLife 8:e50974.
https://doi.org/10.7554/eLife.50974

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