1. Physics of Living Systems
  2. Cell Biology

Physical basis of large microtubule aster growth

  1. Keisuke Ishihara  Is a corresponding author
  2. Kirill S Korolev  Is a corresponding author
  3. Timothy J Mitchison
  1. Center for Systems Biology Dresden, Germany
  2. Boston University, United States
  3. Harvard Medical School, United States
https://doi.org/10.7554/eLife.19145
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  1. Keisuke Ishihara
  2. Kirill S Korolev
  3. Timothy J Mitchison
(2016)
Physical basis of large microtubule aster growth
eLife 5:e19145.
https://doi.org/10.7554/eLife.19145
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Abstract

Microtubule asters - radial arrays of microtubules organized by centrosomes - play a fundamental role in the spatial coordination of animal cells. The standard model of aster growth assumes a fixed number of microtubules originating from the centrosomes. However, aster morphology in this model does not scale with cell size, and we recently found evidence for non-centrosomal microtubule nucleation. Here, we combine autocatalytic nucleation and polymerization dynamics to develop a biophysical model of aster growth. Our model predicts that asters expand as traveling waves and recapitulates all major aspects of aster growth. With increasing nucleation rate, the model predicts an explosive transition from stationary to growing asters with a discontinuous jump of the aster velocity to a nonzero value. Experiments in frog egg extract confirm the main theoretical predictions. Our results suggest that asters observed in large frog and amphibian eggs are a meshwork of short, unstable microtubules maintained by autocatalytic nucleation and provide a paradigm for the assembly of robust and evolvable polymer networks.

Article and author information

Author details

  1. Keisuke Ishihara

    Center for Systems Biology Dresden, Dresden, Germany
    For correspondence
    ishihara@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8481-8680

  2. Kirill S Korolev

    Department of Physics, Boston University, Boston, United States
    For correspondence
    korolev@bu.edu
    Competing interests
    The authors declare that no competing interests exist.

  3. Timothy J Mitchison

    Department of Systems Biology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (GM39565)

  • Keisuke Ishihara
  • Timothy J Mitchison

Marine Biological Laboratory (Whitman Center Award)

  • Timothy J Mitchison

Honjo International Scholarship Foundation (Graduate Student Fellowship)

  • Keisuke Ishihara

Boston University (Start up fund)

  • Kirill S Korolev

Simons Foundation (#409704)

  • Kirill S Korolev

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

Reviewing Editor

  1. Anthony A Hyman, Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (IS00000519) of Harvard Medical School. The protocol was approved by the HMA Standing Committee on Animals (SIRIUS/Procurement Number 2762).

Version history

  1. Received: June 27, 2016
  2. Accepted: November 21, 2016
  3. Accepted Manuscript published: November 28, 2016 (version 1)
  4. Version of Record published: January 3, 2017 (version 2)

Copyright

© 2016, Ishihara 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. Keisuke Ishihara
  2. Kirill S Korolev
  3. Timothy J Mitchison
(2016)
Physical basis of large microtubule aster growth
eLife 5:e19145.
https://doi.org/10.7554/eLife.19145

Share this article

https://doi.org/10.7554/eLife.19145

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