Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans

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 PA...

Full description

Bibliographic Details
Main Authors: Kerstin Klinkert, Nicolas Levernier, Peter Gross, Christian Gentili, Lukas von Tobel, Marie Pierron, Coralie Busso, Sarah Herrman, Stephan W Grill, Karsten Kruse, Pierre Gönczy
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-02-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/44552
id doaj-f761873501a34fd49a8a957932035da4
record_format Article
spelling doaj-f761873501a34fd49a8a957932035da42021-05-05T17:26:21ZengeLife Sciences Publications LtdeLife2050-084X2019-02-01810.7554/eLife.44552Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegansKerstin Klinkert0https://orcid.org/0000-0001-5268-3710Nicolas Levernier1Peter Gross2Christian Gentili3Lukas von Tobel4Marie Pierron5Coralie Busso6Sarah Herrman7Stephan W Grill8Karsten Kruse9Pierre Gönczy10https://orcid.org/0000-0002-6305-6883Swiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandDepartment of Biochemistry, University of Geneva, Geneva, Switzerland; Department of Theoretical Physics, University of Geneva, Geneva, SwitzerlandBIOTEC, TU Dresden, Dresden, GermanySwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandSwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandSwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandSwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandSwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandBIOTEC, TU Dresden, Dresden, Germany; Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany; Cluster of Excellence Physics of Life, TU Dresden, Dresden, GermanyDepartment of Biochemistry, University of Geneva, Geneva, Switzerland; Department of Theoretical Physics, University of Geneva, Geneva, Switzerland; National Center of Competence in Research Chemical Biology, University of Geneva, Geneva, SwitzerlandSwiss Institute for Experimental Cancer Research (ISREC), School of Life Sciences, Swiss Federal Institute of Technology Lausanne (EPFL), Lausanne, SwitzerlandHow 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.https://elifesciences.org/articles/44552symmetry breakingAurora Aanterior-posterior polarityphysical analysis
collection DOAJ
language English
format Article
sources DOAJ
author Kerstin Klinkert
Nicolas Levernier
Peter Gross
Christian Gentili
Lukas von Tobel
Marie Pierron
Coralie Busso
Sarah Herrman
Stephan W Grill
Karsten Kruse
Pierre Gönczy
spellingShingle Kerstin Klinkert
Nicolas Levernier
Peter Gross
Christian Gentili
Lukas von Tobel
Marie Pierron
Coralie Busso
Sarah Herrman
Stephan W Grill
Karsten Kruse
Pierre Gönczy
Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
eLife
symmetry breaking
Aurora A
anterior-posterior polarity
physical analysis
author_facet Kerstin Klinkert
Nicolas Levernier
Peter Gross
Christian Gentili
Lukas von Tobel
Marie Pierron
Coralie Busso
Sarah Herrman
Stephan W Grill
Karsten Kruse
Pierre Gönczy
author_sort Kerstin Klinkert
title Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
title_short Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
title_full Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
title_fullStr Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
title_full_unstemmed Aurora A depletion reveals centrosome-independent polarization mechanism in Caenorhabditis elegans
title_sort aurora a depletion reveals centrosome-independent polarization mechanism in caenorhabditis elegans
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-02-01
description 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.
topic symmetry breaking
Aurora A
anterior-posterior polarity
physical analysis
url https://elifesciences.org/articles/44552
work_keys_str_mv AT kerstinklinkert auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT nicolaslevernier auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT petergross auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT christiangentili auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT lukasvontobel auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT mariepierron auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT coraliebusso auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT sarahherrman auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT stephanwgrill auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT karstenkruse auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
AT pierregonczy auroraadepletionrevealscentrosomeindependentpolarizationmechanismincaenorhabditiselegans
_version_ 1721459263331631104