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Cyclin B3 promotes anaphase I onset in oocyte meiosis

Meiosis poses unique challenges because two rounds of chromosome segregation must be executed without intervening DNA replication. Mammalian cells express numerous temporally regulated cyclins, but how these proteins collaborate to control meiosis remains poorly understood. Here, we show that female...

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Autores principales: Karasu, Mehmet E., Bouftas, Nora, Keeney, Scott, Wassmann, Katja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446836/
https://www.ncbi.nlm.nih.gov/pubmed/30723090
http://dx.doi.org/10.1083/jcb.201808091
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author Karasu, Mehmet E.
Bouftas, Nora
Keeney, Scott
Wassmann, Katja
author_facet Karasu, Mehmet E.
Bouftas, Nora
Keeney, Scott
Wassmann, Katja
author_sort Karasu, Mehmet E.
collection PubMed
description Meiosis poses unique challenges because two rounds of chromosome segregation must be executed without intervening DNA replication. Mammalian cells express numerous temporally regulated cyclins, but how these proteins collaborate to control meiosis remains poorly understood. Here, we show that female mice genetically ablated for cyclin B3 are viable—indicating that the protein is dispensable for mitotic divisions—but are sterile. Mutant oocytes appear normal until metaphase I but then display a highly penetrant failure to transition to anaphase I. They arrest with hallmarks of defective anaphase-promoting complex/cyclosome (APC/C) activation, including no separase activity, high CDK1 activity, and high cyclin B1 and securin levels. Partial APC/C activation occurs, however, as exogenously expressed APC/C substrates can be degraded. Cyclin B3 forms active kinase complexes with CDK1, and meiotic progression requires cyclin B3–associated kinase activity. Cyclin B3 homologues from frog, zebrafish, and fruit fly rescue meiotic progression in cyclin B3–deficient mouse oocytes, indicating conservation of the biochemical properties and possibly cellular functions of this germline-critical cyclin.
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spelling pubmed-64468362019-10-01 Cyclin B3 promotes anaphase I onset in oocyte meiosis Karasu, Mehmet E. Bouftas, Nora Keeney, Scott Wassmann, Katja J Cell Biol Research Articles Meiosis poses unique challenges because two rounds of chromosome segregation must be executed without intervening DNA replication. Mammalian cells express numerous temporally regulated cyclins, but how these proteins collaborate to control meiosis remains poorly understood. Here, we show that female mice genetically ablated for cyclin B3 are viable—indicating that the protein is dispensable for mitotic divisions—but are sterile. Mutant oocytes appear normal until metaphase I but then display a highly penetrant failure to transition to anaphase I. They arrest with hallmarks of defective anaphase-promoting complex/cyclosome (APC/C) activation, including no separase activity, high CDK1 activity, and high cyclin B1 and securin levels. Partial APC/C activation occurs, however, as exogenously expressed APC/C substrates can be degraded. Cyclin B3 forms active kinase complexes with CDK1, and meiotic progression requires cyclin B3–associated kinase activity. Cyclin B3 homologues from frog, zebrafish, and fruit fly rescue meiotic progression in cyclin B3–deficient mouse oocytes, indicating conservation of the biochemical properties and possibly cellular functions of this germline-critical cyclin. Rockefeller University Press 2019-04-01 2019-02-05 /pmc/articles/PMC6446836/ /pubmed/30723090 http://dx.doi.org/10.1083/jcb.201808091 Text en © 2019 Karasu et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Research Articles
Karasu, Mehmet E.
Bouftas, Nora
Keeney, Scott
Wassmann, Katja
Cyclin B3 promotes anaphase I onset in oocyte meiosis
title Cyclin B3 promotes anaphase I onset in oocyte meiosis
title_full Cyclin B3 promotes anaphase I onset in oocyte meiosis
title_fullStr Cyclin B3 promotes anaphase I onset in oocyte meiosis
title_full_unstemmed Cyclin B3 promotes anaphase I onset in oocyte meiosis
title_short Cyclin B3 promotes anaphase I onset in oocyte meiosis
title_sort cyclin b3 promotes anaphase i onset in oocyte meiosis
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6446836/
https://www.ncbi.nlm.nih.gov/pubmed/30723090
http://dx.doi.org/10.1083/jcb.201808091
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