Aurora A depletion reveals centrosome-independent polarization mechanism in C. elegans

  1. Kerstin Klinkert
  2. Nicolas Levernier
  3. Peter Gross
  4. Christian Gentili
  5. Lukas von Tobel
  6. Marie Pierron
  7. Coralie Busso
  8. Sarah Herrman
  9. Stephan W Grill
  10. Karsten Kruse
  11. Pierre Gönczy  Is a corresponding author
  1. Swiss Federal Institute of Technology, Switzerland
  2. University of Geneva, Switzerland
  3. Technische Universität Dresden, Germany

Abstract

How living systems break symmetry in an organized manner is a fundamental question in biology. In wild type Caenorhabditis elegans zygotes, symmetry breaking during anterior-posterior axis specification is guided by centrosomes, resulting in anterior-directed cortical flows and a single posterior PAR-2 domain. We uncover that C. elegans zygotes depleted of the Aurora A kinase AIR-1 or lacking centrosomes entirely usually establish two posterior PAR-2 domains, one at each pole. We demonstrate that AIR-1 prevents symmetry breaking early in the cell cycle, whereas centrosomal AIR-1 instructs polarity initiation thereafter. Using triangular microfabricated chambers, we establish that bipolarity of air-1(RNAi) embryos occurs effectively in a cell-shape and curvature-dependent manner. Furthermore, we develop an integrated physical description of symmetry breaking, wherein local PAR-2-dependent weakening of the actin cortex, together with mutual inhibition of anterior and posterior PAR proteins, provides a mechanism for spontaneous symmetry breaking without centrosomes.

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All data is available in the manuscript or the supplementary materials.

Article and author information

Author details

  1. Kerstin Klinkert

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  2. Nicolas Levernier

    Department of Biochemistry, University of Geneva, Geneva, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  3. Peter Gross

    Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Christian Gentili

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Lukas von Tobel

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  6. Marie Pierron

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  7. Coralie Busso

    Swiss Institute of Experimental Cancer Research, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  8. Sarah Herrman

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  9. Stephan W Grill

    Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Karsten Kruse

    Department of Biochemistry, University of Geneva, Geneva, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  11. Pierre Gönczy

    Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland
    For correspondence
    pierre.gonczy@epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6305-6883

Funding

European Molecular Biology Organization (ALTF 81-2017)

  • Kerstin Klinkert

European Molecular Biology Organization (ALTF 1426-2016)

  • Marie Pierron

Fondation Bettencourt Schueller

  • Nicolas Levernier

Swiss National Science Foundation (31003A_155942)

  • Pierre Gönczy

Swiss National Science Foundation (205321_175996)

  • Karsten Kruse

H2020 European Research Council (281903)

  • Stephan W Grill

H2020 European Research Council (742712)

  • Stephan W Grill

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

Reviewing Editor

  1. Yukiko M Yamashita, University of Michigan, United States

Version history

  1. Received: December 19, 2018
  2. Accepted: February 24, 2019
  3. Accepted Manuscript published: February 25, 2019 (version 1)
  4. Accepted Manuscript updated: February 26, 2019 (version 2)
  5. Version of Record published: March 14, 2019 (version 3)

Copyright

© 2019, Klinkert 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. Kerstin Klinkert
  2. Nicolas Levernier
  3. Peter Gross
  4. Christian Gentili
  5. Lukas von Tobel
  6. Marie Pierron
  7. Coralie Busso
  8. Sarah Herrman
  9. Stephan W Grill
  10. Karsten Kruse
  11. Pierre Gönczy
(2019)
Aurora A depletion reveals centrosome-independent polarization mechanism in C. elegans
eLife 8:e44552.
https://doi.org/10.7554/eLife.44552

Share this article

https://doi.org/10.7554/eLife.44552

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