1. Structural Biology and Molecular Biophysics
  2. Cell Biology
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Direct measurement of conformational strain energy in protofilaments curling outward from disassembling microtubule tips

  1. Jonathan W Driver
  2. Elisabeth A Geyer
  3. Megan E Bailey
  4. Luke M Rice  Is a corresponding author
  5. Charles L Asbury  Is a corresponding author
  1. University of Washington, United States
  2. University of Texas Southwestern Medical Center, United States
Research Article
  • Cited 24
  • Views 1,668
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Cite this article as: eLife 2017;6:e28433 doi: 10.7554/eLife.28433

Abstract

Disassembling microtubules can generate movement independently of motor enzymes, especially at kinetochores where they drive chromosome motility. A popular explanation is the 'conformational wave' model, in which protofilaments pull on the kinetochore as they curl outward from a disassembling tip. But whether protofilaments can work efficiently via this spring-like mechanism has been unclear. By modifying a previous assay to use recombinant tubulin and feedback-controlled laser trapping, we directly demonstrate the spring-like elasticity of curling protofilaments. Measuring their mechanical work output suggests they carry ~25% of the energy of GTP hydrolysis as bending strain, enabling them to drive movement with efficiency similar to conventional motors. Surprisingly, a β-tubulin mutant that dramatically slows disassembly has no effect on work output, indicating an uncoupling of disassembly speed from protofilament strain. These results show the wave mechanism can make a major contribution to kinetochore motility and establish a direct approach for measuring tubulin mechano-chemistry.

Article and author information

Author details

  1. Jonathan W Driver

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Elisabeth A Geyer

    Department of Biophysics and Biochemistry, University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Megan E Bailey

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Luke M Rice

    Department of Biophysics and Biochemistry, University of Texas Southwestern Medical Center, Dallas, United States
    For correspondence
    Luke.Rice@UTSouthwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
  5. Charles L Asbury

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    casbury@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0143-5394

Funding

Sackler Scholars Program in Integrative Biophysics

  • Jonathan W Driver

Leukemia and Lymphoma Society

  • Jonathan W Driver

National Institutes of Health (T32CA080416)

  • Megan E Bailey

Packard Foundation (2006‐30521)

  • Charles L Asbury

NSF Graduate Research Fellowship (2014177758)

  • Elisabeth A Geyer

National Institutes of Health (RO1GM098543)

  • Luke M Rice

NSF Career Award (MCB1054947)

  • Luke M Rice

National Institutes of Health (RO1GM079373)

  • Charles L Asbury

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

Reviewing Editor

  1. Anna Akhmanova, Utrecht University, Netherlands

Publication history

  1. Received: May 7, 2017
  2. Accepted: June 18, 2017
  3. Accepted Manuscript published: June 19, 2017 (version 1)
  4. Version of Record published: July 18, 2017 (version 2)

Copyright

© 2017, Driver 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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