1. Biophysics and Structural Biology
  2. Cell Biology
Download icon

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
0
Views
479
Comments
0
Cite 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

    1. 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

    1. 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

    1. 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

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

    1. Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    1. casbury@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon 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, Reviewing Editor, Utrecht University, Netherlands

Publication history

  1. Received: May 7, 2017
  2. Accepted: June 18, 2017
  3. Accepted Manuscript published: June 19, 2017 (version 1)

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.

Metrics

  • 479
    Page views
  • 115
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: PubMed Central, Scopus, Crossref.

Comments

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Biochemistry
    2. Neuroscience
    Hansen Wang et al.
    Research Article