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RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes

Mammalian oocyte meiotic divisions are highly asymmetric and produce a large haploid gamete and 2 small polar bodies. This relies on the ability of the cell to break symmetry and position its spindle close to the cortex before anaphase occurs. In metaphase II–arrested mouse oocytes, the spindle is a...

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Autores principales: Dehapiot, Benoit, Clément, Raphaël, Bourdais, Anne, Carrière, Virginie, Huet, Sébastien, Halet, Guillaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8448345/
https://www.ncbi.nlm.nih.gov/pubmed/34491981
http://dx.doi.org/10.1371/journal.pbio.3001376
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author Dehapiot, Benoit
Clément, Raphaël
Bourdais, Anne
Carrière, Virginie
Huet, Sébastien
Halet, Guillaume
author_facet Dehapiot, Benoit
Clément, Raphaël
Bourdais, Anne
Carrière, Virginie
Huet, Sébastien
Halet, Guillaume
author_sort Dehapiot, Benoit
collection PubMed
description Mammalian oocyte meiotic divisions are highly asymmetric and produce a large haploid gamete and 2 small polar bodies. This relies on the ability of the cell to break symmetry and position its spindle close to the cortex before anaphase occurs. In metaphase II–arrested mouse oocytes, the spindle is actively maintained close and parallel to the cortex, until fertilization triggers sister chromatid segregation and the rotation of the spindle. The latter must indeed reorient perpendicular to the cortex to enable cytokinesis ring closure at the base of the polar body. However, the mechanisms underlying symmetry breaking and spindle rotation have remained elusive. In this study, we show that spindle rotation results from 2 antagonistic forces. First, an inward contraction of the cytokinesis furrow dependent on RhoA signaling, and second, an outward attraction exerted on both sets of chromatids by a Ran/Cdc42-dependent polarization of the actomyosin cortex. By combining live segmentation and tracking with numerical modeling, we demonstrate that this configuration becomes unstable as the ingression progresses. This leads to spontaneous symmetry breaking, which implies that neither the rotation direction nor the set of chromatids that eventually gets discarded are biologically predetermined.
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spelling pubmed-84483452021-09-18 RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes Dehapiot, Benoit Clément, Raphaël Bourdais, Anne Carrière, Virginie Huet, Sébastien Halet, Guillaume PLoS Biol Research Article Mammalian oocyte meiotic divisions are highly asymmetric and produce a large haploid gamete and 2 small polar bodies. This relies on the ability of the cell to break symmetry and position its spindle close to the cortex before anaphase occurs. In metaphase II–arrested mouse oocytes, the spindle is actively maintained close and parallel to the cortex, until fertilization triggers sister chromatid segregation and the rotation of the spindle. The latter must indeed reorient perpendicular to the cortex to enable cytokinesis ring closure at the base of the polar body. However, the mechanisms underlying symmetry breaking and spindle rotation have remained elusive. In this study, we show that spindle rotation results from 2 antagonistic forces. First, an inward contraction of the cytokinesis furrow dependent on RhoA signaling, and second, an outward attraction exerted on both sets of chromatids by a Ran/Cdc42-dependent polarization of the actomyosin cortex. By combining live segmentation and tracking with numerical modeling, we demonstrate that this configuration becomes unstable as the ingression progresses. This leads to spontaneous symmetry breaking, which implies that neither the rotation direction nor the set of chromatids that eventually gets discarded are biologically predetermined. Public Library of Science 2021-09-07 /pmc/articles/PMC8448345/ /pubmed/34491981 http://dx.doi.org/10.1371/journal.pbio.3001376 Text en © 2021 Dehapiot et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dehapiot, Benoit
Clément, Raphaël
Bourdais, Anne
Carrière, Virginie
Huet, Sébastien
Halet, Guillaume
RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title_full RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title_fullStr RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title_full_unstemmed RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title_short RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
title_sort rhoa- and cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8448345/
https://www.ncbi.nlm.nih.gov/pubmed/34491981
http://dx.doi.org/10.1371/journal.pbio.3001376
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