Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.

Casein kinase I alpha (CK1α) is a member of serine/threonine protein kinase, generally present in all eukaryotes. In mammals, CK1α regulates the transition from interphase to metaphase in mitosis. However, little is known about its role in meiosis. Here we examined Ck1α mRNA and protein expression,...

Full description

Bibliographic Details
Main Authors: Lu Wang, Angeleem Lu, Hong-Xia Zhou, Ran Sun, Jie Zhao, Cheng-Jie Zhou, Jiang-Peng Shen, Sha-Na Wu, Cheng-Guang Liang
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3655170?pdf=render
_version_ 1818048394050928640
author Lu Wang
Angeleem Lu
Hong-Xia Zhou
Ran Sun
Jie Zhao
Cheng-Jie Zhou
Jiang-Peng Shen
Sha-Na Wu
Cheng-Guang Liang
author_facet Lu Wang
Angeleem Lu
Hong-Xia Zhou
Ran Sun
Jie Zhao
Cheng-Jie Zhou
Jiang-Peng Shen
Sha-Na Wu
Cheng-Guang Liang
author_sort Lu Wang
collection DOAJ
description Casein kinase I alpha (CK1α) is a member of serine/threonine protein kinase, generally present in all eukaryotes. In mammals, CK1α regulates the transition from interphase to metaphase in mitosis. However, little is known about its role in meiosis. Here we examined Ck1α mRNA and protein expression, as well as its subcellular localization in mouse oocytes from germinal vesicle to the late 1-cell stage. Our results showed that the expression level of CK1α was increased in metaphase. Immunostaining results showed that CK1α colocalized with condensed chromosomes during oocyte meiotic maturation and early embryo development. We used the loss-of-function approach by employing CK1α specific morpholino injection to block the function of CK1α. This functional blocking leads to failure of polar body 1 (PB1) extrusion, chromosome misalignment and MII plate incrassation. We further found that D4476, a specific and efficient CK1 inhibitor, decreased the rate of PB1 extrusion. Moreover, D4476 resulted in giant polar body extrusion, oocyte pro-MI arrest, chromosome congression failure and impairment of embryo developmental potential. In addition, we employed pyrvinium pamoate (PP), an allosteric activator of CK1α, to enhance CK1α activity in oocytes. Supplementation of PP induced oocyte meiotic maturation failure, severe congression abnormalities and misalignment of chromosomes. Taken together, our study for the first time demonstrates that CK1α is required for chromosome alignment and segregation during oocyte meiotic maturation and early embryo development.
first_indexed 2024-12-10T10:20:59Z
format Article
id doaj.art-27e2ce567cf74199adef39f05fc664a2
institution Directory Open Access Journal
issn 1932-6203
language English
last_indexed 2024-12-10T10:20:59Z
publishDate 2013-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj.art-27e2ce567cf74199adef39f05fc664a22022-12-22T01:52:51ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0185e6317310.1371/journal.pone.0063173Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.Lu WangAngeleem LuHong-Xia ZhouRan SunJie ZhaoCheng-Jie ZhouJiang-Peng ShenSha-Na WuCheng-Guang LiangCasein kinase I alpha (CK1α) is a member of serine/threonine protein kinase, generally present in all eukaryotes. In mammals, CK1α regulates the transition from interphase to metaphase in mitosis. However, little is known about its role in meiosis. Here we examined Ck1α mRNA and protein expression, as well as its subcellular localization in mouse oocytes from germinal vesicle to the late 1-cell stage. Our results showed that the expression level of CK1α was increased in metaphase. Immunostaining results showed that CK1α colocalized with condensed chromosomes during oocyte meiotic maturation and early embryo development. We used the loss-of-function approach by employing CK1α specific morpholino injection to block the function of CK1α. This functional blocking leads to failure of polar body 1 (PB1) extrusion, chromosome misalignment and MII plate incrassation. We further found that D4476, a specific and efficient CK1 inhibitor, decreased the rate of PB1 extrusion. Moreover, D4476 resulted in giant polar body extrusion, oocyte pro-MI arrest, chromosome congression failure and impairment of embryo developmental potential. In addition, we employed pyrvinium pamoate (PP), an allosteric activator of CK1α, to enhance CK1α activity in oocytes. Supplementation of PP induced oocyte meiotic maturation failure, severe congression abnormalities and misalignment of chromosomes. Taken together, our study for the first time demonstrates that CK1α is required for chromosome alignment and segregation during oocyte meiotic maturation and early embryo development.http://europepmc.org/articles/PMC3655170?pdf=render
spellingShingle Lu Wang
Angeleem Lu
Hong-Xia Zhou
Ran Sun
Jie Zhao
Cheng-Jie Zhou
Jiang-Peng Shen
Sha-Na Wu
Cheng-Guang Liang
Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
PLoS ONE
title Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
title_full Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
title_fullStr Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
title_full_unstemmed Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
title_short Casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development.
title_sort casein kinase 1 alpha regulates chromosome congression and separation during mouse oocyte meiotic maturation and early embryo development
url http://europepmc.org/articles/PMC3655170?pdf=render
work_keys_str_mv AT luwang caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT angeleemlu caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT hongxiazhou caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT ransun caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT jiezhao caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT chengjiezhou caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT jiangpengshen caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT shanawu caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment
AT chengguangliang caseinkinase1alpharegulateschromosomecongressionandseparationduringmouseoocytemeioticmaturationandearlyembryodevelopment