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Reduced growth capacity of preimplantation mouse embryos in chronic unpredictable stress model
Psychological stress can affect female reproduction by deteriorating oocyte quality, but the molecular mechanism is unclear. In this study, we used the chronic unpredictable stress model to study the effect of psychological stress on mouse oocyte competence during preimplantation stage, and RNA sequ...
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Published in: | Molecular reproduction and development 2021-01, Vol.88 (1), p.80-95 |
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creator | Zhao, Xiaoli Ma, Ruihong Zhang, Xiaoyu Cheng, Rui Jiang, Nan Guo, Mengjia Rong, Beilei Liu, Yan Chen, Mingli Feng, Weihua Xia, Tian |
description | Psychological stress can affect female reproduction by deteriorating oocyte quality, but the molecular mechanism is unclear. In this study, we used the chronic unpredictable stress model to study the effect of psychological stress on mouse oocyte competence during preimplantation stage, and RNA sequencing in single oocytes to analyze differential gene expression at the transcription level. Stress changed the serum levels of glucocorticoids and reduced oocyte developmental potential, depending on the strength of the stress. Strong stress (two stressors per day) reduced the fertilization rate and induced significant apoptosis in blastocysts. Moderate stress (one stressor per day) reduced the cleavage rate and blastocyst formation rate. Weak stress (one stressor every 2 days) did not have any significant negative effect on the fertilization, cleavage, and blastocyst formation. Hatching rate was not affected by stress, but stress retarded the development of the expanded blastocysts and inhibited the embryo development at early stages. Transcriptome analysis revealed that stress disturbed the expression of cell cycle regulators and apoptotic genes. The hub genes identified through protein‐protein interaction analysis include Msln, Ceacam12, Psg16, Psg17, and Psg23, which are all carcinoembryonic or related genes involved in cell adhesion, proliferation, and migration. Thus, stress was inhibitory on fertilization and early embryo development in mice. |
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In this study, we used the chronic unpredictable stress model to study the effect of psychological stress on mouse oocyte competence during preimplantation stage, and RNA sequencing in single oocytes to analyze differential gene expression at the transcription level. Stress changed the serum levels of glucocorticoids and reduced oocyte developmental potential, depending on the strength of the stress. Strong stress (two stressors per day) reduced the fertilization rate and induced significant apoptosis in blastocysts. Moderate stress (one stressor per day) reduced the cleavage rate and blastocyst formation rate. Weak stress (one stressor every 2 days) did not have any significant negative effect on the fertilization, cleavage, and blastocyst formation. Hatching rate was not affected by stress, but stress retarded the development of the expanded blastocysts and inhibited the embryo development at early stages. Transcriptome analysis revealed that stress disturbed the expression of cell cycle regulators and apoptotic genes. The hub genes identified through protein‐protein interaction analysis include Msln, Ceacam12, Psg16, Psg17, and Psg23, which are all carcinoembryonic or related genes involved in cell adhesion, proliferation, and migration. Thus, stress was inhibitory on fertilization and early embryo development in mice.</description><identifier>ISSN: 1040-452X</identifier><identifier>EISSN: 1098-2795</identifier><identifier>DOI: 10.1002/mrd.23439</identifier><identifier>PMID: 33216405</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Apoptosis ; Blastocysts ; Cell adhesion ; Cell adhesion & migration ; Cell cycle ; Cell migration ; chronic unpredictable stress model ; Developmental stages ; differential gene expression ; Embryos ; Fertilization ; Gene expression ; Glucocorticoids ; Hatching ; hypothalamus‐pituitary‐adrenal axis ; Oocytes ; preimplantation embryos ; Ribonucleic acid ; RNA ; RNA sequencing ; Serum levels ; Transcription ; Transcriptomes</subject><ispartof>Molecular reproduction and development, 2021-01, Vol.88 (1), p.80-95</ispartof><rights>2020 Wiley Periodicals LLC</rights><rights>2020 Wiley Periodicals LLC.</rights><rights>2021 Wiley Periodicals LLC</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3539-1cb9b956b8b7905a1a920bc5fc70b5189438d99c7bb241549009ce217f2c96373</citedby><cites>FETCH-LOGICAL-c3539-1cb9b956b8b7905a1a920bc5fc70b5189438d99c7bb241549009ce217f2c96373</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33216405$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhao, Xiaoli</creatorcontrib><creatorcontrib>Ma, Ruihong</creatorcontrib><creatorcontrib>Zhang, Xiaoyu</creatorcontrib><creatorcontrib>Cheng, Rui</creatorcontrib><creatorcontrib>Jiang, Nan</creatorcontrib><creatorcontrib>Guo, Mengjia</creatorcontrib><creatorcontrib>Rong, Beilei</creatorcontrib><creatorcontrib>Liu, Yan</creatorcontrib><creatorcontrib>Chen, Mingli</creatorcontrib><creatorcontrib>Feng, Weihua</creatorcontrib><creatorcontrib>Xia, Tian</creatorcontrib><title>Reduced growth capacity of preimplantation mouse embryos in chronic unpredictable stress model</title><title>Molecular reproduction and development</title><addtitle>Mol Reprod Dev</addtitle><description>Psychological stress can affect female reproduction by deteriorating oocyte quality, but the molecular mechanism is unclear. In this study, we used the chronic unpredictable stress model to study the effect of psychological stress on mouse oocyte competence during preimplantation stage, and RNA sequencing in single oocytes to analyze differential gene expression at the transcription level. Stress changed the serum levels of glucocorticoids and reduced oocyte developmental potential, depending on the strength of the stress. Strong stress (two stressors per day) reduced the fertilization rate and induced significant apoptosis in blastocysts. Moderate stress (one stressor per day) reduced the cleavage rate and blastocyst formation rate. Weak stress (one stressor every 2 days) did not have any significant negative effect on the fertilization, cleavage, and blastocyst formation. Hatching rate was not affected by stress, but stress retarded the development of the expanded blastocysts and inhibited the embryo development at early stages. Transcriptome analysis revealed that stress disturbed the expression of cell cycle regulators and apoptotic genes. The hub genes identified through protein‐protein interaction analysis include Msln, Ceacam12, Psg16, Psg17, and Psg23, which are all carcinoembryonic or related genes involved in cell adhesion, proliferation, and migration. Thus, stress was inhibitory on fertilization and early embryo development in mice.</description><subject>Apoptosis</subject><subject>Blastocysts</subject><subject>Cell adhesion</subject><subject>Cell adhesion & migration</subject><subject>Cell cycle</subject><subject>Cell migration</subject><subject>chronic unpredictable stress model</subject><subject>Developmental stages</subject><subject>differential gene expression</subject><subject>Embryos</subject><subject>Fertilization</subject><subject>Gene expression</subject><subject>Glucocorticoids</subject><subject>Hatching</subject><subject>hypothalamus‐pituitary‐adrenal axis</subject><subject>Oocytes</subject><subject>preimplantation embryos</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA sequencing</subject><subject>Serum levels</subject><subject>Transcription</subject><subject>Transcriptomes</subject><issn>1040-452X</issn><issn>1098-2795</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNp10E1LwzAABuAgipvTg39AAl700C0fzdocZX6CIgwFT5YkTV1G29SkZfTfm9npQfCUHB7evHkBOMVoihEis8rlU0JjyvfAGCOeRiThbH97j1EUM_I2AkferxFCnKfoEIwoJXgeIzYG70udd0rn8MPZTbuCSjRCmbaHtoCN06ZqSlG3ojW2hpXtvIa6kq63HpoaqpWztVGwqwPNjWqFLDX0rdPeB53r8hgcFKL0-mR3TsDr7c3L4j56fL57WFw9RooyyiOsJJeczWUqE46YwIITJBUrVIIkwymPaZpzrhIpSYxZzMNPlCY4KYjic5rQCbgYchtnPzvt26wyXukylNehdUbiOcUYpRQHev6Hrm3n6tAuqDS8RUhKgroclHLWe6eLrHGmEq7PMMq2o2dh9Ox79GDPdomdrHT-K39WDmA2gI0pdf9_Uva0vB4ivwBloYtE</recordid><startdate>202101</startdate><enddate>202101</enddate><creator>Zhao, Xiaoli</creator><creator>Ma, Ruihong</creator><creator>Zhang, Xiaoyu</creator><creator>Cheng, Rui</creator><creator>Jiang, Nan</creator><creator>Guo, Mengjia</creator><creator>Rong, Beilei</creator><creator>Liu, Yan</creator><creator>Chen, Mingli</creator><creator>Feng, Weihua</creator><creator>Xia, Tian</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>202101</creationdate><title>Reduced growth capacity of preimplantation mouse embryos in chronic unpredictable stress model</title><author>Zhao, Xiaoli ; Ma, Ruihong ; Zhang, Xiaoyu ; Cheng, Rui ; Jiang, Nan ; Guo, Mengjia ; Rong, Beilei ; Liu, Yan ; Chen, Mingli ; Feng, Weihua ; Xia, Tian</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3539-1cb9b956b8b7905a1a920bc5fc70b5189438d99c7bb241549009ce217f2c96373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Apoptosis</topic><topic>Blastocysts</topic><topic>Cell adhesion</topic><topic>Cell adhesion & migration</topic><topic>Cell cycle</topic><topic>Cell migration</topic><topic>chronic unpredictable stress model</topic><topic>Developmental stages</topic><topic>differential gene expression</topic><topic>Embryos</topic><topic>Fertilization</topic><topic>Gene expression</topic><topic>Glucocorticoids</topic><topic>Hatching</topic><topic>hypothalamus‐pituitary‐adrenal axis</topic><topic>Oocytes</topic><topic>preimplantation embryos</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>RNA sequencing</topic><topic>Serum levels</topic><topic>Transcription</topic><topic>Transcriptomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhao, Xiaoli</creatorcontrib><creatorcontrib>Ma, Ruihong</creatorcontrib><creatorcontrib>Zhang, Xiaoyu</creatorcontrib><creatorcontrib>Cheng, Rui</creatorcontrib><creatorcontrib>Jiang, Nan</creatorcontrib><creatorcontrib>Guo, Mengjia</creatorcontrib><creatorcontrib>Rong, Beilei</creatorcontrib><creatorcontrib>Liu, Yan</creatorcontrib><creatorcontrib>Chen, Mingli</creatorcontrib><creatorcontrib>Feng, Weihua</creatorcontrib><creatorcontrib>Xia, Tian</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular reproduction and development</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhao, Xiaoli</au><au>Ma, Ruihong</au><au>Zhang, Xiaoyu</au><au>Cheng, Rui</au><au>Jiang, Nan</au><au>Guo, Mengjia</au><au>Rong, Beilei</au><au>Liu, Yan</au><au>Chen, Mingli</au><au>Feng, Weihua</au><au>Xia, Tian</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reduced growth capacity of preimplantation mouse embryos in chronic unpredictable stress model</atitle><jtitle>Molecular reproduction and development</jtitle><addtitle>Mol Reprod Dev</addtitle><date>2021-01</date><risdate>2021</risdate><volume>88</volume><issue>1</issue><spage>80</spage><epage>95</epage><pages>80-95</pages><issn>1040-452X</issn><eissn>1098-2795</eissn><abstract>Psychological stress can affect female reproduction by deteriorating oocyte quality, but the molecular mechanism is unclear. In this study, we used the chronic unpredictable stress model to study the effect of psychological stress on mouse oocyte competence during preimplantation stage, and RNA sequencing in single oocytes to analyze differential gene expression at the transcription level. Stress changed the serum levels of glucocorticoids and reduced oocyte developmental potential, depending on the strength of the stress. Strong stress (two stressors per day) reduced the fertilization rate and induced significant apoptosis in blastocysts. Moderate stress (one stressor per day) reduced the cleavage rate and blastocyst formation rate. Weak stress (one stressor every 2 days) did not have any significant negative effect on the fertilization, cleavage, and blastocyst formation. Hatching rate was not affected by stress, but stress retarded the development of the expanded blastocysts and inhibited the embryo development at early stages. Transcriptome analysis revealed that stress disturbed the expression of cell cycle regulators and apoptotic genes. The hub genes identified through protein‐protein interaction analysis include Msln, Ceacam12, Psg16, Psg17, and Psg23, which are all carcinoembryonic or related genes involved in cell adhesion, proliferation, and migration. Thus, stress was inhibitory on fertilization and early embryo development in mice.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33216405</pmid><doi>10.1002/mrd.23439</doi><tpages>16</tpages></addata></record> |
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subjects | Apoptosis Blastocysts Cell adhesion Cell adhesion & migration Cell cycle Cell migration chronic unpredictable stress model Developmental stages differential gene expression Embryos Fertilization Gene expression Glucocorticoids Hatching hypothalamus‐pituitary‐adrenal axis Oocytes preimplantation embryos Ribonucleic acid RNA RNA sequencing Serum levels Transcription Transcriptomes |
title | Reduced growth capacity of preimplantation mouse embryos in chronic unpredictable stress model |
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