The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice

Cumulus cells are a group of closely associated granulosa cells that surround and nourish oocytes. Previous studies have shown that cumulus cells contribute to oocyte maturation and fertilization through gap junction communication. However, it is not known how this gap junction signaling affects in...

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Main Authors: Cheng-Jie Zhou, Sha-Na Wu, Jiang-Peng Shen, Dong-Hui Wang, Xiang-Wei Kong, Angeleem Lu, Yan-Jiao Li, Hong-Xia Zhou, Yue-Fang Zhao, Cheng-Guang Liang
Format: Article
Language:English
Published: PeerJ Inc. 2016-03-01
Series:PeerJ
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Online Access:https://peerj.com/articles/1761.pdf
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author Cheng-Jie Zhou
Sha-Na Wu
Jiang-Peng Shen
Dong-Hui Wang
Xiang-Wei Kong
Angeleem Lu
Yan-Jiao Li
Hong-Xia Zhou
Yue-Fang Zhao
Cheng-Guang Liang
author_facet Cheng-Jie Zhou
Sha-Na Wu
Jiang-Peng Shen
Dong-Hui Wang
Xiang-Wei Kong
Angeleem Lu
Yan-Jiao Li
Hong-Xia Zhou
Yue-Fang Zhao
Cheng-Guang Liang
author_sort Cheng-Jie Zhou
collection DOAJ
description Cumulus cells are a group of closely associated granulosa cells that surround and nourish oocytes. Previous studies have shown that cumulus cells contribute to oocyte maturation and fertilization through gap junction communication. However, it is not known how this gap junction signaling affects in vivo versus in vitro maturation of oocytes, and their subsequent fertilization and embryonic development following insemination. Therefore, in our study, we performed mouse oocyte maturation and insemination using in vivo- or in vitro-matured oocyte-cumulus complexes (OCCs, which retain gap junctions between the cumulus cells and the oocytes), in vitro-matured, denuded oocytes co-cultured with cumulus cells (DCs, which lack gap junctions between the cumulus cells and the oocytes), and in vitro-matured, denuded oocytes without cumulus cells (DOs). Using these models, we were able to analyze the effects of gap junction signaling on oocyte maturation, fertilization, and early embryo development. We found that gap junctions were necessary for both in vivo and in vitro oocyte maturation. In addition, for oocytes matured in vivo, the presence of cumulus cells during insemination improved fertilization and blastocyst formation, and this improvement was strengthened by gap junctions. Moreover, for oocytes matured in vitro, the presence of cumulus cells during insemination improved fertilization, but not blastocyst formation, and this improvement was independent of gap junctions. Our results demonstrate, for the first time, that the beneficial effect of gap junction signaling from cumulus cells depends on oocyte maturation and fertilization methods.
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spelling doaj.art-444c009bda4c4dcca6f6cab3652e44df2023-12-02T21:54:09ZengPeerJ Inc.PeerJ2167-83592016-03-014e176110.7717/peerj.1761The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in miceCheng-Jie Zhou0Sha-Na Wu1Jiang-Peng Shen2Dong-Hui Wang3Xiang-Wei Kong4Angeleem Lu5Yan-Jiao Li6Hong-Xia Zhou7Yue-Fang Zhao8Cheng-Guang Liang9The Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaThe Research Center for Laboratory Animal Science, College of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, ChinaCumulus cells are a group of closely associated granulosa cells that surround and nourish oocytes. Previous studies have shown that cumulus cells contribute to oocyte maturation and fertilization through gap junction communication. However, it is not known how this gap junction signaling affects in vivo versus in vitro maturation of oocytes, and their subsequent fertilization and embryonic development following insemination. Therefore, in our study, we performed mouse oocyte maturation and insemination using in vivo- or in vitro-matured oocyte-cumulus complexes (OCCs, which retain gap junctions between the cumulus cells and the oocytes), in vitro-matured, denuded oocytes co-cultured with cumulus cells (DCs, which lack gap junctions between the cumulus cells and the oocytes), and in vitro-matured, denuded oocytes without cumulus cells (DOs). Using these models, we were able to analyze the effects of gap junction signaling on oocyte maturation, fertilization, and early embryo development. We found that gap junctions were necessary for both in vivo and in vitro oocyte maturation. In addition, for oocytes matured in vivo, the presence of cumulus cells during insemination improved fertilization and blastocyst formation, and this improvement was strengthened by gap junctions. Moreover, for oocytes matured in vitro, the presence of cumulus cells during insemination improved fertilization, but not blastocyst formation, and this improvement was independent of gap junctions. Our results demonstrate, for the first time, that the beneficial effect of gap junction signaling from cumulus cells depends on oocyte maturation and fertilization methods.https://peerj.com/articles/1761.pdfOocyteCumulus cellsGap junctionMaturationFertilizationEarly embryo development
spellingShingle Cheng-Jie Zhou
Sha-Na Wu
Jiang-Peng Shen
Dong-Hui Wang
Xiang-Wei Kong
Angeleem Lu
Yan-Jiao Li
Hong-Xia Zhou
Yue-Fang Zhao
Cheng-Guang Liang
The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
PeerJ
Oocyte
Cumulus cells
Gap junction
Maturation
Fertilization
Early embryo development
title The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
title_full The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
title_fullStr The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
title_full_unstemmed The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
title_short The beneficial effects of cumulus cells and oocyte-cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
title_sort beneficial effects of cumulus cells and oocyte cumulus cell gap junctions depends on oocyte maturation and fertilization methods in mice
topic Oocyte
Cumulus cells
Gap junction
Maturation
Fertilization
Early embryo development
url https://peerj.com/articles/1761.pdf
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