SGK1 is essential for meiotic resumption in mammalian oocytes

In mammalian females, oocytes are stored in the ovary and meiosis is arrested at the diplotene stage of prophase I. When females reach puberty oocytes are selectively recruited in cycles to grow, overcome the meiotic arrest, complete the first meiotic division and become mature (ready for fertilizat...

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Main Authors: Edgar del Llano, Rajan Iyyappan, Daria Aleshkina, Tomas Masek, Michal Dvoran, Zongliang Jiang, Martin Pospisek, Michal Kubelka, Andrej Susor
Format: Article
Language:English
Published: Elsevier 2022-04-01
Series:European Journal of Cell Biology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0171933522000139
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author Edgar del Llano
Rajan Iyyappan
Daria Aleshkina
Tomas Masek
Michal Dvoran
Zongliang Jiang
Martin Pospisek
Michal Kubelka
Andrej Susor
author_facet Edgar del Llano
Rajan Iyyappan
Daria Aleshkina
Tomas Masek
Michal Dvoran
Zongliang Jiang
Martin Pospisek
Michal Kubelka
Andrej Susor
author_sort Edgar del Llano
collection DOAJ
description In mammalian females, oocytes are stored in the ovary and meiosis is arrested at the diplotene stage of prophase I. When females reach puberty oocytes are selectively recruited in cycles to grow, overcome the meiotic arrest, complete the first meiotic division and become mature (ready for fertilization). At a molecular level, the master regulator of prophase I arrest and meiotic resumption is the maturation-promoting factor (MPF) complex, formed by the active form of cyclin dependent kinase 1 (CDK1) and Cyclin B1. However, we still do not have complete information regarding the factors implicated in MPF activation.In this study we document that out of three mammalian serum-glucocorticoid kinase proteins (SGK1, SGK2, SGK3), mouse oocytes express only SGK1 with a phosphorylated (active) form dominantly localized in the nucleoplasm. Further, suppression of SGK1 activity in oocytes results in decreased CDK1 activation via the phosphatase cell division cycle 25B (CDC25B), consequently delaying or inhibiting nuclear envelope breakdown. Expression of exogenous constitutively active CDK1 can rescue the phenotype induced by SGK1 inhibition. These findings bring new insights into the molecular pathways acting upstream of MPF and a better understanding of meiotic resumption control by presenting a new key player SGK1 in mammalian oocytes.
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spelling doaj.art-7a74b538a21346588f6ae9f0b1c057142022-12-21T22:51:11ZengElsevierEuropean Journal of Cell Biology0171-93352022-04-011012151210SGK1 is essential for meiotic resumption in mammalian oocytesEdgar del Llano0Rajan Iyyappan1Daria Aleshkina2Tomas Masek3Michal Dvoran4Zongliang Jiang5Martin Pospisek6Michal Kubelka7Andrej Susor8Laboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech Republic; Corresponding authors.Laboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech RepublicLaboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech RepublicLaboratory of RNA Biochemistry, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, Prague 128 44, Czech RepublicLaboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech RepublicSchool of Animal Sciences, AgCenter, Louisiana State University, Baton Rouge, LA 70803, United StatesLaboratory of RNA Biochemistry, Department of Genetics and Microbiology, Faculty of Science, Charles University, Viničná 5, Prague 128 44, Czech RepublicLaboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech RepublicLaboratory of Biochemistry and Molecular Biology of Germ Cells, Institute of Animal Physiology and Genetics, CAS, Libechov, Czech Republic; Corresponding authors.In mammalian females, oocytes are stored in the ovary and meiosis is arrested at the diplotene stage of prophase I. When females reach puberty oocytes are selectively recruited in cycles to grow, overcome the meiotic arrest, complete the first meiotic division and become mature (ready for fertilization). At a molecular level, the master regulator of prophase I arrest and meiotic resumption is the maturation-promoting factor (MPF) complex, formed by the active form of cyclin dependent kinase 1 (CDK1) and Cyclin B1. However, we still do not have complete information regarding the factors implicated in MPF activation.In this study we document that out of three mammalian serum-glucocorticoid kinase proteins (SGK1, SGK2, SGK3), mouse oocytes express only SGK1 with a phosphorylated (active) form dominantly localized in the nucleoplasm. Further, suppression of SGK1 activity in oocytes results in decreased CDK1 activation via the phosphatase cell division cycle 25B (CDC25B), consequently delaying or inhibiting nuclear envelope breakdown. Expression of exogenous constitutively active CDK1 can rescue the phenotype induced by SGK1 inhibition. These findings bring new insights into the molecular pathways acting upstream of MPF and a better understanding of meiotic resumption control by presenting a new key player SGK1 in mammalian oocytes.http://www.sciencedirect.com/science/article/pii/S0171933522000139OocyteMPFCDK1SGK1MeiosisNuclear envelope breakdown
spellingShingle Edgar del Llano
Rajan Iyyappan
Daria Aleshkina
Tomas Masek
Michal Dvoran
Zongliang Jiang
Martin Pospisek
Michal Kubelka
Andrej Susor
SGK1 is essential for meiotic resumption in mammalian oocytes
European Journal of Cell Biology
Oocyte
MPF
CDK1
SGK1
Meiosis
Nuclear envelope breakdown
title SGK1 is essential for meiotic resumption in mammalian oocytes
title_full SGK1 is essential for meiotic resumption in mammalian oocytes
title_fullStr SGK1 is essential for meiotic resumption in mammalian oocytes
title_full_unstemmed SGK1 is essential for meiotic resumption in mammalian oocytes
title_short SGK1 is essential for meiotic resumption in mammalian oocytes
title_sort sgk1 is essential for meiotic resumption in mammalian oocytes
topic Oocyte
MPF
CDK1
SGK1
Meiosis
Nuclear envelope breakdown
url http://www.sciencedirect.com/science/article/pii/S0171933522000139
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