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:	Benoit Dehapiot, Raphaël Clément, Anne Bourdais, Virginie Carrière, Sébastien Huet, Guillaume Halet
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/f47342eb8aac4d47b454515302406523
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spelling	oai:doaj.org-article:f47342eb8aac4d47b4545153024065232021-12-02T19:54:37ZRhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes.1544-91731545-788510.1371/journal.pbio.3001376https://doaj.org/article/f47342eb8aac4d47b4545153024065232021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001376https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Mammalian 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.Benoit DehapiotRaphaël ClémentAnne BourdaisVirginie CarrièreSébastien HuetGuillaume HaletPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 9, p e3001376 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Benoit Dehapiot Raphaël Clément Anne Bourdais Virginie Carrière Sébastien Huet Guillaume Halet RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes.
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.
format	article
author	Benoit Dehapiot Raphaël Clément Anne Bourdais Virginie Carrière Sébastien Huet Guillaume Halet
author_facet	Benoit Dehapiot Raphaël Clément Anne Bourdais Virginie Carrière Sébastien Huet Guillaume Halet
author_sort	Benoit Dehapiot
title	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_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_sort	rhoa- and cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/f47342eb8aac4d47b454515302406523
work_keys_str_mv	AT benoitdehapiot rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes AT raphaelclement rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes AT annebourdais rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes AT virginiecarriere rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes AT sebastienhuet rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes AT guillaumehalet rhoaandcdc42inducedantagonisticforcesunderliesymmetrybreakingandspindlerotationinmouseoocytes
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RhoA- and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes.

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