Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.

In mammalian oocytes, three actin binding proteins, Formin 2 (Fmn2), Spire, and profilin, synergistically organize a dynamic cytoplasmic actin meshwork that mediates translocation of the spindle toward the cortex and is required for successful fertilization. Here we characterize Fmn2 and elucidate t...

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Autores principales:	Pierre Montaville, Antoine Jégou, Julien Pernier, Christel Compper, Bérengère Guichard, Binyam Mogessie, Melina Schuh, Guillaume Romet-Lemonne, Marie-France Carlier
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/9860aee1054444d0928bc5248cce29f7
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spelling	oai:doaj.org-article:9860aee1054444d0928bc5248cce29f72021-11-18T05:37:34ZSpire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.1544-91731545-788510.1371/journal.pbio.1001795https://doaj.org/article/9860aee1054444d0928bc5248cce29f72014-02-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/24586110/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885In mammalian oocytes, three actin binding proteins, Formin 2 (Fmn2), Spire, and profilin, synergistically organize a dynamic cytoplasmic actin meshwork that mediates translocation of the spindle toward the cortex and is required for successful fertilization. Here we characterize Fmn2 and elucidate the molecular mechanism for this synergy, using bulk solution and individual filament kinetic measurements of actin assembly dynamics. We show that by capping filament barbed ends, Spire recruits Fmn2 and facilitates its association with barbed ends, followed by rapid processive assembly and release of Spire. In the presence of actin, profilin, Spire, and Fmn2, filaments display alternating phases of rapid processive assembly and arrested growth, driven by a "ping-pong" mechanism, in which Spire and Fmn2 alternately kick off each other from the barbed ends. The results are validated by the effects of injection of Spire, Fmn2, and their interacting moieties in mouse oocytes. This original mechanism of regulation of a Rho-GTPase-independent formin, recruited by Spire at Rab11a-positive vesicles, supports a model for modulation of a dynamic actin-vesicle meshwork in the oocyte at the origin of asymmetric positioning of the meiotic spindle.Pierre MontavilleAntoine JégouJulien PernierChristel CompperBérengère GuichardBinyam MogessieMelina SchuhGuillaume Romet-LemonneMarie-France CarlierPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 2, p e1001795 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Pierre Montaville Antoine Jégou Julien Pernier Christel Compper Bérengère Guichard Binyam Mogessie Melina Schuh Guillaume Romet-Lemonne Marie-France Carlier Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
description	In mammalian oocytes, three actin binding proteins, Formin 2 (Fmn2), Spire, and profilin, synergistically organize a dynamic cytoplasmic actin meshwork that mediates translocation of the spindle toward the cortex and is required for successful fertilization. Here we characterize Fmn2 and elucidate the molecular mechanism for this synergy, using bulk solution and individual filament kinetic measurements of actin assembly dynamics. We show that by capping filament barbed ends, Spire recruits Fmn2 and facilitates its association with barbed ends, followed by rapid processive assembly and release of Spire. In the presence of actin, profilin, Spire, and Fmn2, filaments display alternating phases of rapid processive assembly and arrested growth, driven by a "ping-pong" mechanism, in which Spire and Fmn2 alternately kick off each other from the barbed ends. The results are validated by the effects of injection of Spire, Fmn2, and their interacting moieties in mouse oocytes. This original mechanism of regulation of a Rho-GTPase-independent formin, recruited by Spire at Rab11a-positive vesicles, supports a model for modulation of a dynamic actin-vesicle meshwork in the oocyte at the origin of asymmetric positioning of the meiotic spindle.
format	article
author	Pierre Montaville Antoine Jégou Julien Pernier Christel Compper Bérengère Guichard Binyam Mogessie Melina Schuh Guillaume Romet-Lemonne Marie-France Carlier
author_facet	Pierre Montaville Antoine Jégou Julien Pernier Christel Compper Bérengère Guichard Binyam Mogessie Melina Schuh Guillaume Romet-Lemonne Marie-France Carlier
author_sort	Pierre Montaville
title	Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
title_short	Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
title_full	Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
title_fullStr	Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
title_full_unstemmed	Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
title_sort	spire and formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/9860aee1054444d0928bc5248cce29f7
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Spire and Formin 2 synergize and antagonize in regulating actin assembly in meiosis by a ping-pong mechanism.

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