1. Cell Biology

A disassembly-driven mechanism explains F-actin-mediated chromosome transport in starfish oocytes

  1. Philippe Bun
  2. Serge Dmitrieff
  3. Julio M Belmonte
  4. François J Nédélec  Is a corresponding author
  5. Péter Lénárt  Is a corresponding author
  1. European Molecular Biology Laboratory, Germany
https://doi.org/10.7554/eLife.31469
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  1. Philippe Bun
  2. Serge Dmitrieff
  3. Julio M Belmonte
  4. François J Nédélec
  5. Péter Lénárt
(2018)
A disassembly-driven mechanism explains F-actin-mediated chromosome transport in starfish oocytes
eLife 7:e31469.
https://doi.org/10.7554/eLife.31469
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Abstract

While contraction of sarcomeric actomyosin assemblies is well understood, this is not the case for disordered networks of actin filaments (F-actin) driving diverse essential processes in animal cells. For example, at the onset of meiosis in starfish oocytes a contractile F-actin network forms in the nuclear region transporting embedded chromosomes to the assembling microtubule spindle. Here, we addressed the mechanism driving contraction of this 3D disordered F-actin network by comparing quantitative observations to computational models. We analyzed 3D chromosome trajectories and imaged filament dynamics to monitor network behavior under various physical and chemical perturbations. We found no evidence of myosin activity driving network contractility. Instead, our observations are well explained by models based on a disassembly-driven contractile mechanism. We reconstitute this disassembly-based contractile system in silico revealing a simple architecture that robustly drives chromosome transport to prevent aneuploidy in the large oocyte, a prerequisite for normal embryonic development.

Article and author information

Author details

  1. Philippe Bun

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  2. Serge Dmitrieff

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Julio M Belmonte

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4315-9631

  4. François J Nédélec

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    For correspondence
    nedelec@embl.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8141-5288

  5. Péter Lénárt

    Cell Biology and Biophysics Unit, European Molecular Biology Laboratory, Heidelberg, Germany
    For correspondence
    lenart@embl.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3927-248X

Funding

European Molecular Biology Laboratory

  • Serge Dmitrieff
  • François J Nédélec
  • Péter Lénárt

EU Marie Curie Actions Cofund grant

  • Philippe Bun
  • Julio M Belmonte

Center for Modelling and Simulation in the Biosciences

  • Serge Dmitrieff

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

Reviewing Editor

  1. Pekka Lappalainen, University of Helsinki, Finland

Version history

  1. Received: August 23, 2017
  2. Accepted: January 18, 2018
  3. Accepted Manuscript published: January 19, 2018 (version 1)
  4. Version of Record published: January 29, 2018 (version 2)

Copyright

© 2018, Bun 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. Philippe Bun
  2. Serge Dmitrieff
  3. Julio M Belmonte
  4. François J Nédélec
  5. Péter Lénárt
(2018)
A disassembly-driven mechanism explains F-actin-mediated chromosome transport in starfish oocytes
eLife 7:e31469.
https://doi.org/10.7554/eLife.31469

Share this article

https://doi.org/10.7554/eLife.31469

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