Physical basis of large microtubule aster growth

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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.

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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.

"This ORCID iD identifies the author of this article:" 0000-0002-8481-8680
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.
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.

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).

Copyright

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.