{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T16:04:13Z","timestamp":1791561853165,"version":"4.3.4"},"reference-count":50,"publisher":"Elsevier BV","issue":"10","license":[{"start":{"date-parts":[[2023,10,1]],"date-time":"2023-10-01T00:00:00Z","timestamp":1696118400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,10,1]],"date-time":"2023-10-01T00:00:00Z","timestamp":1696118400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,9,1]],"date-time":"2023-09-01T00:00:00Z","timestamp":1693526400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100012166","name":"National Key Research and Development Program of China","doi-asserted-by":"publisher","award":["2022YFA0806302"],"award-info":[{"award-number":["2022YFA0806302"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100017287","name":"Special Funds for the Basic Research and Development Program in the Central Non-profit Research Institutes of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100017287","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014718","name":"Innovative Research Group Project of the National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82171646"],"award-info":[{"award-number":["82171646"]}],"id":[{"id":"10.13039\/100014718","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100023536","name":"Ferring Institute of Reproductive Medicine, Institute of Zoology, Chinese Academy of Sciences","doi-asserted-by":"publisher","award":["FIRMC200507"],"award-info":[{"award-number":["FIRMC200507"]}],"id":[{"id":"10.13039\/501100023536","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["iScience"],"published-print":{"date-parts":[[2023,10]]},"DOI":"10.1016\/j.isci.2023.107828","type":"journal-article","created":{"date-parts":[[2023,9,4]],"date-time":"2023-09-04T02:09:10Z","timestamp":1693793350000},"page":"107828","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":12,"title":["A heterozygous ZP2 mutation causes zona pellucida defects and female infertility in mouse and human"],"prefix":"10.1016","volume":"26","author":[{"given":"Sai-Li","family":"Liu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hai-Yang","family":"Zuo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bing-Wang","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia-Ni","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Bo","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wen-Long","family":"Lei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan-Yuan","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying-Chun","family":"Ouyang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Hou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhi-Ming","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei-Zhou","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qing-Yuan","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhen-Bo","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.isci.2023.107828_bib1","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1146\/annurev-biochem-011520-105310","article-title":"Zona Pellucida Proteins, Fibrils, and Matrix","volume":"89","author":"Litscher","year":"2020","journal-title":"Annu. Rev. Biochem."},{"key":"10.1016\/j.isci.2023.107828_bib2","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1093\/humupd\/dmm040","article-title":"Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality","volume":"14","author":"Gilchrist","year":"2008","journal-title":"Hum. Reprod. Update"},{"key":"10.1016\/j.isci.2023.107828_bib3","doi-asserted-by":"crossref","first-page":"2178","DOI":"10.1126\/science.1071965","article-title":"Intercellular communication in the mammalian ovary: oocytes carry the conversation","volume":"296","author":"Matzuk","year":"2002","journal-title":"Science (New York, N.Y.)"},{"key":"10.1016\/j.isci.2023.107828_bib4","doi-asserted-by":"crossref","first-page":"1761","DOI":"10.1126\/science.1207438","article-title":"Human Sperm Binding Is Mediated by the Sialyl-Lewis(x) Oligosaccharide on the Zona Pellucida","volume":"333","author":"Pang","year":"2011","journal-title":"Science (New York, N.Y.)"},{"key":"10.1016\/j.isci.2023.107828_bib5","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1016\/j.devcel.2018.07.020","article-title":"Glycan-Independent Gamete Recognition Triggers Egg Zinc Sparks and ZP2 Cleavage to Prevent Polyspermy","volume":"46","author":"Tokuhiro","year":"2018","journal-title":"Dev. Cell"},{"key":"10.1016\/j.isci.2023.107828_bib6","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1083\/jcb.201112094","article-title":"Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy","volume":"197","author":"Burkart","year":"2012","journal-title":"J.\u00a0Cell Biol."},{"key":"10.1016\/j.isci.2023.107828_bib7","doi-asserted-by":"crossref","first-page":"6730","DOI":"10.2741\/3185","article-title":"Structural changes of the zona pellucida during fertilization and embryo development","volume":"13","author":"Familiari","year":"2008","journal-title":"Front. Biosci."},{"key":"10.1016\/j.isci.2023.107828_bib8","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1111\/j.1439-0531.2006.00829.x","article-title":"Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis","volume":"42","author":"Michelmann","year":"2007","journal-title":"Reprod. Domest. Anim."},{"key":"10.1016\/j.isci.2023.107828_bib9","doi-asserted-by":"crossref","first-page":"619868","DOI":"10.3389\/fcell.2021.619868","article-title":"Human Zona Pellucida Glycoproteins: Binding Characteristics With Human Spermatozoa and Induction of Acrosome Reaction","volume":"9","author":"Gupta","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"10.1016\/j.isci.2023.107828_bib10","doi-asserted-by":"crossref","first-page":"626679","DOI":"10.3389\/fcell.2020.626679","article-title":"ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction","volume":"8","author":"Izquierdo-Rico","year":"2020","journal-title":"Front. Cell Dev. Biol."},{"key":"10.1016\/j.isci.2023.107828_bib11","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."},{"key":"10.1016\/j.isci.2023.107828_bib12","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/ncb802","article-title":"The ZP domain is a conserved module for polymerization of extracellular proteins","volume":"4","author":"Jovine","year":"2002","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.isci.2023.107828_bib13","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/0014-5793(92)80853-9","article-title":"A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor","volume":"300","author":"Bork","year":"1992","journal-title":"FEBS Lett."},{"key":"10.1016\/j.isci.2023.107828_bib14","doi-asserted-by":"crossref","first-page":"5922","DOI":"10.1073\/pnas.0401600101","article-title":"A duplicated motif controls assembly of zona pellucida domain proteins","volume":"101","author":"Jovine","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.isci.2023.107828_bib15","doi-asserted-by":"crossref","first-page":"940","DOI":"10.1242\/jcs.079988","article-title":"ZP2 and ZP3 cytoplasmic tails prevent premature interactions and ensure incorporation into the zona pellucida","volume":"124","author":"Jimenez-Movilla","year":"2011","journal-title":"J.\u00a0Cell Sci."},{"key":"10.1016\/j.isci.2023.107828_bib16","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":"10.1016\/j.isci.2023.107828_bib17","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"},{"key":"10.1016\/j.isci.2023.107828_bib18","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"},{"key":"10.1016\/j.isci.2023.107828_bib19","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"},{"key":"10.1016\/j.isci.2023.107828_bib20","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.\u00a0Engl. J. Med."},{"key":"10.1016\/j.isci.2023.107828_bib21","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1093\/biolre\/ioab025","article-title":"Mutant Zp1 impedes incorporation of ZP3 and ZP4 in the zona pellucida, resulting in zona absence and female infertility in ratsdagger","volume":"104","author":"Lv","year":"2021","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib22","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1136\/jclinpath-2020-207170","article-title":"Mutations in ZP4 are associated with abnormal zona pellucida and female infertility","volume":"75","author":"Wei","year":"2022","journal-title":"J.\u00a0Clin. Pathol."},{"key":"10.1016\/j.isci.2023.107828_bib23","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."},{"key":"10.1016\/j.isci.2023.107828_bib24","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1186\/s12958-022-01046-6","article-title":"Can successful pregnancy be achieved and predicted from patients with identified ZP mutations? A literature review","volume":"20","author":"Zhou","year":"2022","journal-title":"Reprod. Biol. Endocrinol."},{"key":"10.1016\/j.isci.2023.107828_bib25","first-page":"21","article-title":"Zona pellucida genes and proteins and human fertility","volume":"13","author":"Litscher","year":"2020","journal-title":"Trends Dev. Biol."},{"key":"10.1016\/j.isci.2023.107828_bib26","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1038\/s41436-018-0064-y","article-title":"ZP2 pathogenic variants cause in\u00a0vitro fertilization failure and female infertility","volume":"21","author":"Dai","year":"2019","journal-title":"Genet. Med."},{"key":"10.1016\/j.isci.2023.107828_bib27","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1016\/j.fertnstert.2017.03.029","article-title":"Novel zona pellucida gene variants identified in patients with oocyte anomalies","volume":"107","author":"Yang","year":"2017","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.isci.2023.107828_bib28","doi-asserted-by":"crossref","first-page":"1239","DOI":"10.1007\/s10815-021-02107-2","article-title":"A novel homozygous variant in ZP2 causes abnormal zona pellucida formation and female infertility","volume":"38","author":"Sun","year":"2021","journal-title":"J.\u00a0Assist. Reprod. Genet."},{"key":"10.1016\/j.isci.2023.107828_bib29","first-page":"65","article-title":"Evolution, structure, and synthesis of vertebrate egg-coat proteins","volume":"8","author":"Litscher","year":"2014","journal-title":"Trends Dev. Biol."},{"key":"10.1016\/j.isci.2023.107828_bib30","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1093\/humupd\/dmq029","article-title":"Predictive value of oocyte morphology in human IVF: a systematic review of the literature","volume":"17","author":"Rienzi","year":"2011","journal-title":"Hum. Reprod. Update"},{"key":"10.1016\/j.isci.2023.107828_bib31","doi-asserted-by":"crossref","first-page":"3431","DOI":"10.1093\/humrep\/13.12.3431","article-title":"Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate after intracytoplasmic sperm injection","volume":"13","author":"Balaban","year":"1998","journal-title":"Hum. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib32","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.\u00a0Ovarian Res."},{"key":"10.1016\/j.isci.2023.107828_bib33","doi-asserted-by":"crossref","first-page":"e76106","DOI":"10.7554\/eLife.76106","article-title":"Female fertility and the zona pellucida","volume":"11","author":"Wassarman","year":"2022","journal-title":"Elife"},{"key":"10.1016\/j.isci.2023.107828_bib34","doi-asserted-by":"crossref","first-page":"e1269","DOI":"10.1002\/mgg3.1269","article-title":"A novel homozygous nonsense ZP1 variant causes human female infertility associated with empty follicle syndrome (EFS)","volume":"8","author":"Xu","year":"2020","journal-title":"Mol. Genet. Genomic Med."},{"key":"10.1016\/j.isci.2023.107828_bib35","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1111\/cge.13921","article-title":"Novel mutations in ZP1: Expanding the mutational spectrum associated with empty follicle syndrome in infertile women","volume":"99","author":"Wu","year":"2021","journal-title":"Clin. Genet."},{"key":"10.1016\/j.isci.2023.107828_bib36","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."},{"key":"10.1016\/j.isci.2023.107828_bib37","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1093\/humrep\/deac026","article-title":"Identification of a heterozygous variant of ZP2 as a novel cause of empty follicle syndrome in humans and mice","volume":"37","author":"Shen","year":"2022","journal-title":"Hum. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib38","doi-asserted-by":"crossref","first-page":"690070","DOI":"10.3389\/fgene.2021.690070","article-title":"Case Report: A Novel Heterozygous ZP3 Deletion Associated With Empty Follicle Syndrome and Abnormal Follicular Development","volume":"12","author":"Chen","year":"2021","journal-title":"Front. Genet."},{"key":"10.1016\/j.isci.2023.107828_bib39","first-page":"2201","article-title":"ZP1 mutations are associated with empty follicle syndrome: evidence for the existence of an intact oocyte and a zona pellucida in follicles up to the early antral stage. A case report","volume":"34","author":"Dai","year":"2019","journal-title":"Hum. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib40","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/s10815-020-01995-0","article-title":"A novel mutation in ZP3 causes empty follicle syndrome and abnormal zona pellucida formation","volume":"38","author":"Zhang","year":"2021","journal-title":"J.\u00a0Assist. Reprod. Genet."},{"key":"10.1016\/j.isci.2023.107828_bib41","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/bs.ctdb.2018.02.007","article-title":"Structure of Zona Pellucida Module Proteins","volume":"130","author":"Bokhove","year":"2018","journal-title":"Curr. Top. Dev. Biol."},{"key":"10.1016\/j.isci.2023.107828_bib42","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1093\/biolre\/ioz093","article-title":"Influence of mouse defective zona pellucida in folliculogenesis on apoptosis of granulosa cells and developmental competence of oocytes","volume":"101","author":"Wang","year":"2019","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib43","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1002\/jemt.20301","article-title":"Three-dimensional structure of the zona pellucida at ovulation","volume":"69","author":"Familiari","year":"2006","journal-title":"Microsc. Res. Tech."},{"key":"10.1016\/j.isci.2023.107828_bib44","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1095\/biolreprod66.2.407","article-title":"Proteolytic processing of human zona pellucida proteins","volume":"66","author":"Kiefer","year":"2002","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.isci.2023.107828_bib45","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."},{"key":"10.1016\/j.isci.2023.107828_bib46","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1038\/nrm3531","article-title":"The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte","volume":"14","author":"Li","year":"2013","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"10.1016\/j.isci.2023.107828_bib47","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1530\/rep.0.1210647","article-title":"Cellular basis for paracrine regulation of ovarian follicle development","volume":"121","author":"Albertini","year":"2001","journal-title":"Reproduction"},{"key":"10.1016\/j.isci.2023.107828_bib48","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."},{"key":"10.1016\/j.isci.2023.107828_bib49","doi-asserted-by":"crossref","first-page":"2523","DOI":"10.1038\/s41467-021-22829-2","article-title":"Oocyte-derived microvilli control female fertility by optimizing ovarian follicle selection in mice","volume":"12","author":"Zhang","year":"2021","journal-title":"Nat. Commun."},{"key":"10.1016\/j.isci.2023.107828_bib50","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1530\/jrf.0.0170555","article-title":"Proposal for a classification of oocytes and follicles in the mouse ovary","volume":"17","author":"Pedersen","year":"1968","journal-title":"J.\u00a0Reprod. Fertil."}],"container-title":["iScience"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2589004223019053?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2589004223019053?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,8,5]],"date-time":"2025-08-05T15:03:32Z","timestamp":1754406212000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2589004223019053"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10]]},"references-count":50,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2023,10]]}},"alternative-id":["S2589004223019053"],"URL":"https:\/\/doi.org\/10.1016\/j.isci.2023.107828","relation":{},"ISSN":["2589-0042"],"issn-type":[{"value":"2589-0042","type":"print"}],"subject":[],"published":{"date-parts":[[2023,10]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"A heterozygous ZP2 mutation causes zona pellucida defects and female infertility in mouse and human","name":"articletitle","label":"Article Title"},{"value":"iScience","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.isci.2023.107828","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 The Authors.","name":"copyright","label":"Copyright"}],"article-number":"107828"}}