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

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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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Kerstin Klinkert

Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Nicolas Levernier

Department of Biochemistry, University of Geneva, Geneva, Switzerland

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The authors declare that no competing interests exist.
Peter Gross

Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany

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The authors declare that no competing interests exist.
Christian Gentili

Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Lukas von Tobel

Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Marie Pierron

Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Coralie Busso

Swiss Institute of Experimental Cancer Research, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Sarah Herrman

Swiss Institute for Experimental Cancer Research, School of Life Sciences, Swiss Federal Institute of Technology, Lausanne, Switzerland

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The authors declare that no competing interests exist.
Stephan W Grill

Biotechnology Center (BIOTEC), Technische Universität Dresden, Dresden, Germany

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The authors declare that no competing interests exist.
Karsten Kruse

Department of Biochemistry, University of Geneva, Geneva, Switzerland

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The authors declare that no competing interests exist.
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

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The authors declare that no competing interests exist.

"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.

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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.