{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T11:47:34Z","timestamp":1784288854203,"version":"3.55.0"},"reference-count":27,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2019,6,4]],"date-time":"2019-06-04T00:00:00Z","timestamp":1559606400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"publisher","award":["2016YFC1201805"],"award-info":[{"award-number":["2016YFC1201805"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100012166","name":"National Key R&D Program of China","doi-asserted-by":"publisher","award":["2017YFC1001100"],"award-info":[{"award-number":["2017YFC1001100"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81471453"],"award-info":[{"award-number":["81471453"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["81501248"],"award-info":[{"award-number":["81501248"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004761","name":"Natural Science Foundation of Hunan Province of China","doi-asserted-by":"crossref","award":["2015JJ2166"],"award-info":[{"award-number":["2015JJ2166"]}],"id":[{"id":"10.13039\/501100004761","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100004761","name":"Natural Science Foundation of Hunan Province of China","doi-asserted-by":"crossref","award":["2017JJ3425"],"award-info":[{"award-number":["2017JJ3425"]}],"id":[{"id":"10.13039\/501100004761","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100002822","name":"Central South University","doi-asserted-by":"publisher","award":["164990007"],"award-info":[{"award-number":["164990007"]}],"id":[{"id":"10.13039\/501100002822","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Zona pellucida (ZP), which enwraps the oocyte during folliculogenesis, initially forms in the primary follicle and plays an important role in female fertility. Here, we investigated a mouse strain (\u201cmutant mice\u201d for short) carrying two types of ZP defects in folliculogenesis, i.e., ZP thinned (but intact) and ZP cracked, caused by targeted mutation in the Zp1 gene. Using this mutant mouse strain and wild-type mouse as control, we studied the effects of the ZP defects on the development of oocytes and granulosa cells during folliculogenesis. For each ZP defect, we examined the morphology of transzonal projections and apoptosis of granulosa cells in the corresponding growing follicles, as well as the morphology of corresponding ovulated eggs and their abilities to develop into viable individuals. Our results suggested that ZP integrity rather than thickness or porosity is crucial for preventing the ectopia of granulosa cells, maintaining adequate routine bilateral signaling between oocyte and surrounding granulosa cells, and thus for ensuring the survival of granulosa cells and the establishment of the full developmental competence of oocytes. This is the first study to elucidate the effects of different degrees of ZP defects caused by the same gene mutation, on the apoptosis of granulosa cells and developmental competence of oocytes, and to explore the potential mechanisms underlying these effects.<\/jats:p>","DOI":"10.1093\/biolre\/ioz093","type":"journal-article","created":{"date-parts":[[2019,6,4]],"date-time":"2019-06-04T17:16:10Z","timestamp":1559668570000},"page":"457-465","source":"Crossref","is-referenced-by-count":16,"title":["Influence of mouse defective zona pellucida in folliculogenesis on apoptosis of granulosa cells and developmental competence of oocytes\u2020"],"prefix":"10.1093","volume":"101","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4754-5759","authenticated-orcid":false,"given":"Yan","family":"Wang","sequence":"first","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chao","family":"Lv","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua-Lin","family":"Huang","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming-Hua","family":"Zeng","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Da-Jing","family":"Yi","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hang-Jing","family":"Tan","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tian-Liu","family":"Peng","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Xian","family":"Yu","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hong-Wen","family":"Deng","sequence":"additional","affiliation":[{"name":"Center of System Biology and Data Science, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Tulane Center for Bioinformatics and Genomics, Department of Global Biostatistics and Data Science, School of Public Health and Tropical Medicine, Tulane University, New Orleans, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8121-9498","authenticated-orcid":false,"given":"Hong-Mei","family":"Xiao","sequence":"additional","affiliation":[{"name":"Institute of Reproductive and Stem Cell Engineering, School of Basic Medical Science, Central South University, Changsha, China"},{"name":"Center of Reproductive Health, School of Basic Medical Science, Central South University, Changsha, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,6,4]]},"reference":[{"key":"2021031608401626700_bib1","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/bs.ctdb.2018.01.003","article-title":"The mouse egg's zona pellucida","volume":"130","author":"Wassarman","year":"2018","journal-title":"Curr Top Dev Biol"},{"key":"2021031608401626700_bib2","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1016\/bs.ctdb.2018.01.001","article-title":"The human egg's zona pellucida","volume":"130","author":"Gupta","year":"2018","journal-title":"Curr Top Dev Biol"},{"issue":"10-12","key":"2021031608401626700_bib3","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1387\/ijdb.120136pw","article-title":"Influence of the zona pellucida of the mouse egg on folliculogenesis and fertility","volume":"56","author":"Wassarman","year":"2012","journal-title":"Int J Dev Biol"},{"issue":"7","key":"2021031608401626700_bib4","doi-asserted-by":"crossref","first-page":"1580","DOI":"10.1093\/humrep\/deh301","article-title":"Four zona pellucida glycoproteins are expressed in the human","volume":"19","author":"Lefievre","year":"2004","journal-title":"Hum Reprod"},{"key":"2021031608401626700_bib5","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s13048-014-0111-5","article-title":"Oocyte zona pellucida dysmorphology is associated with diminished in-vitro fertilization success","volume":"8","author":"Sauerbrun-Cutler","year":"2015","journal-title":"J Ovarian Res"},{"issue":"13","key":"2021031608401626700_bib6","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1056\/NEJMoa1308851","article-title":"Mutant ZP1 in familial infertility","volume":"370","author":"Huang","year":"2014","journal-title":"N Engl J Med"},{"issue":"3","key":"2021031608401626700_bib7","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1016\/j.ajhg.2017.08.001","article-title":"A recurrent missense mutation in ZP3 causes empty follicle syndrome and female infertility","volume":"101","author":"Chen","year":"2017","journal-title":"Am J Hum Genet"},{"issue":"8","key":"2021031608401626700_bib8","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1007\/s00439-017-1822-7","article-title":"Dosage effects of ZP2 and ZP3 heterozygous mutations cause human infertility","volume":"136","author":"Liu","year":"2017","journal-title":"Hum Genet"},{"issue":"11-12","key":"2021031608401626700_bib9","doi-asserted-by":"crossref","first-page":"1493","DOI":"10.1007\/s00439-017-1848-x","article-title":"Additive-effect pattern of both ZP2 and ZP3 in human and mouse","volume":"136","author":"Liu","year":"2017","journal-title":"Hum Genet"},{"issue":"2","key":"2021031608401626700_bib10","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/s41436-018-0064-y","article-title":"ZP2 pathogenic variants cause in vitro fertilization failure and female infertility","volume":"21","author":"Dai","year":"2019","journal-title":"Genet Med"},{"issue":"17","key":"2021031608401626700_bib11","doi-asserted-by":"crossref","first-page":"3847","DOI":"10.1242\/dev.126.17.3847","article-title":"Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss","volume":"126","author":"Rankin","year":"1999","journal-title":"Development"},{"issue":"7","key":"2021031608401626700_bib12","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1242\/dev.128.7.1119","article-title":"Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development","volume":"128","author":"Rankin","year":"2001","journal-title":"Development"},{"issue":"11","key":"2021031608401626700_bib13","doi-asserted-by":"crossref","first-page":"5431","DOI":"10.1073\/pnas.93.11.5431","article-title":"Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice","volume":"93","author":"Liu","year":"1996","journal-title":"Proc Natl Acad Sci USA"},{"issue":"4","key":"2021031608401626700_bib14","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1139\/Y10-009","article-title":"Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence","volume":"88","author":"Kidder","year":"2010","journal-title":"Can J Physiol Pharmacol"},{"issue":"22","key":"2021031608401626700_bib15","doi-asserted-by":"crossref","first-page":"5257","DOI":"10.1242\/jcs.02644","article-title":"Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins","volume":"118","author":"Hussein","year":"2005","journal-title":"J Cell Sci"},{"issue":"3","key":"2021031608401626700_bib16","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/S0015-0282(01)03006-0","article-title":"Apoptosis in human cumulus cells in relation to zona pellucida thickness variation, maturation stage, and cleavage of the corresponding oocyte after intracytoplasmic sperm injection","volume":"77","author":"Host","year":"2002","journal-title":"Fertil Steril"},{"issue":"5","key":"2021031608401626700_bib17","doi-asserted-by":"crossref","first-page":"613","DOI":"10.1530\/rep.0.1230613","article-title":"Gap junctions and ovarian folliculogenesis","volume":"123","author":"Kidder","year":"2002","journal-title":"Reproduction"},{"issue":"1","key":"2021031608401626700_bib18","doi-asserted-by":"crossref","DOI":"10.1002\/wdev.294","article-title":"Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle","volume":"7","author":"Clarke","year":"2018","journal-title":"Wiley Interdiscip Rev Dev Biol"},{"issue":"6616","key":"2021031608401626700_bib19","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/385525a0","article-title":"Female infertility in mice lacking connexin 37","volume":"385","author":"Simon","year":"1997","journal-title":"Nature"},{"issue":"3","key":"2021031608401626700_bib20","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1093\/biolre\/ioy072","article-title":"Mouse oocytes connect with granulosa cells by fusing with cell membranes and form a large complex during follicle development","volume":"99","author":"Komatsu","year":"2018","journal-title":"Biol Reprod"},{"issue":"2","key":"2021031608401626700_bib21","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1006\/dbio.1998.9087","article-title":"Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice","volume":"204","author":"Carabatsos","year":"1998","journal-title":"Dev Biol"},{"issue":"2","key":"2021031608401626700_bib22","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1093\/humrep\/dem373","article-title":"Detection of zona pellucida proteins during human folliculogenesis","volume":"23","author":"Gook","year":"2008","journal-title":"Hum Reprod"},{"issue":"1","key":"2021031608401626700_bib23","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1095\/biolreprod.107.061366","article-title":"Proteolytic activity of the 26S proteasome is required for the meiotic resumption, germinal vesicle breakdown, and cumulus expansion of porcine cumulus-oocyte complexes matured in vitro","volume":"78","author":"Yi","year":"2008","journal-title":"Biol Reprod"},{"issue":"6","key":"2021031608401626700_bib24","doi-asserted-by":"crossref","first-page":"1661","DOI":"10.1095\/biolreprod63.6.1661","article-title":"Gap junction communication and connexin 43 gene expression in a rat granulosa cell line: regulation by follicle-stimulating hormone","volume":"63","author":"Sommersberg","year":"2000","journal-title":"Biol Reprod"},{"issue":"2","key":"2021031608401626700_bib25","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1006\/dbio.2001.0216","article-title":"Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse","volume":"233","author":"Ackert","year":"2001","journal-title":"Dev Biol"},{"issue":"4","key":"2021031608401626700_bib26","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1007\/s00439-019-01990-1","article-title":"Novel mutations in ZP1, ZP2, and ZP3 cause female infertility due to abnormal zona pellucida formation","volume":"138","author":"Zhou","year":"2019","journal-title":"Hum Genet"},{"issue":"1380","key":"2021031608401626700_bib27","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1098\/rspb.1997.0046","article-title":"Mutant female mice carrying a single mZP3 allele produce eggs with a thin zona pellucida, but reproduce normally","volume":"264","author":"Wassarman","year":"1997","journal-title":"Proc Biol Sci"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioz093\/28905703\/ioz093.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/101\/2\/457\/36614358\/biolreprod_101_2_457.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/101\/2\/457\/36614358\/biolreprod_101_2_457.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,9,19]],"date-time":"2022-09-19T12:51:45Z","timestamp":1663591905000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/101\/2\/457\/5511265"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,6,4]]},"references-count":27,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2019,6,4]]},"published-print":{"date-parts":[[2019,8,1]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioz093","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2019,8]]},"published":{"date-parts":[[2019,6,4]]}}}