{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,19]],"date-time":"2026-03-19T04:34:30Z","timestamp":1773894870259,"version":"3.50.1"},"reference-count":41,"publisher":"Elsevier BV","issue":"11","license":[{"start":{"date-parts":[[2017,11,1]],"date-time":"2017-11-01T00:00:00Z","timestamp":1509494400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2017,11,1]],"date-time":"2017-11-01T00:00:00Z","timestamp":1509494400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2019,12,13]],"date-time":"2019-12-13T00:00:00Z","timestamp":1576195200000},"content-version":"vor","delay-in-days":772,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["8P20 GM103453-10"],"award-info":[{"award-number":["8P20 GM103453-10"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01-HD057501"],"award-info":[{"award-number":["R01-HD057501"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["5P20RR017702-10"],"award-info":[{"award-number":["5P20RR017702-10"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["ajp.amjpathol.org","clinicalkey.com","clinicalkey.com.au","clinicalkey.es","clinicalkey.fr","clinicalkey.jp","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["The American Journal of Pathology"],"published-print":{"date-parts":[[2017,11]]},"DOI":"10.1016\/j.ajpath.2017.07.016","type":"journal-article","created":{"date-parts":[[2017,8,18]],"date-time":"2017-08-18T06:23:00Z","timestamp":1503037380000},"page":"2508-2519","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":14,"title":["Ggnbp2-Null Mutation in Mice Leads to Male Infertility due to a Defect at the Spermiogenesis Stage"],"prefix":"10.1016","volume":"187","author":[{"given":"Lingyun","family":"Liu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yan","family":"He","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kaimin","family":"Guo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Linying","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xian","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michael","family":"Tseng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lu","family":"Cai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zi-Jian","family":"Lan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Junmei","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hongliang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhenmin","family":"Lei","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"78","reference":[{"key":"10.1016\/j.ajpath.2017.07.016_bib1","series-title":"The spermatozoon. Knobil and Neill's Physiology of Reproduction, ed 3","first-page":"3","author":"Eddy","year":"2006"},{"key":"10.1016\/j.ajpath.2017.07.016_bib2","first-page":"1","article-title":"Spermatogenesis and cycle of the seminiferous epithelium","volume":"636","author":"Hess","year":"2008","journal-title":"Adv Exp Med Biol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib3","doi-asserted-by":"crossref","first-page":"12201","DOI":"10.1073\/pnas.1635054100","article-title":"A multitude of genes expressed solely in meiotic or postmeiotic spermatogenic cells offers a myriad of contraceptive targets","volume":"100","author":"Schultz","year":"2003","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2017.07.016_bib4","doi-asserted-by":"crossref","first-page":"6852","DOI":"10.1073\/pnas.0701669104","article-title":"Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility","volume":"104","author":"Zheng","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2017.07.016_bib5","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1016\/j.mce.2009.03.003","article-title":"Male infertility caused by spermiogenic defects: lessons from gene knockouts","volume":"306","author":"Yan","year":"2009","journal-title":"Mol Cell Endocrinol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib6","doi-asserted-by":"crossref","first-page":"e2472","DOI":"10.1038\/cddis.2016.344","article-title":"The control of male fertility by spermatid-specific factors: searching for contraceptive targets from spermatozoon's head to tail","volume":"7","author":"Chen","year":"2016","journal-title":"Cell Death Dis"},{"key":"10.1016\/j.ajpath.2017.07.016_bib7","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/S0014-5793(01)03039-3","article-title":"Dioxin induces a novel nuclear factor, DIF-3, that is implicated in spermatogenesis","volume":"508","author":"Ohbayashi","year":"2001","journal-title":"FEBS Lett"},{"key":"10.1016\/j.ajpath.2017.07.016_bib8","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1016\/j.febslet.2004.10.112","article-title":"Yeast two-hybrid screens imply that GGNBP1, GGNBP2 and OAZ3 are potential interaction partners of testicular germ cell-specific protein GGN1","volume":"579","author":"Zhang","year":"2005","journal-title":"FEBS Lett"},{"key":"10.1016\/j.ajpath.2017.07.016_bib9","first-page":"468","volume":"33","author":"Duan","year":"2008","journal-title":"Zhong Nan Da Xue Xue Bao Yi Xue Ban"},{"key":"10.1016\/j.ajpath.2017.07.016_bib10","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1095\/biolreprod.115.136358","article-title":"Ggnbp2 is essential for pregnancy success via regulation of mouse trophoblast stem cell proliferation and differentiation","volume":"94","author":"Li","year":"2016","journal-title":"Biol Reprod"},{"key":"10.1016\/j.ajpath.2017.07.016_bib11","first-page":"315","article-title":"Cloning and expression analysis of a laryngeal carcinoma related gene, LCRG1","volume":"33","author":"Li","year":"2001","journal-title":"Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai)"},{"key":"10.1016\/j.ajpath.2017.07.016_bib12","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.canlet.2003.11.034","article-title":"Molecular cloning and characterization of LCRG1 a novel gene localized to the tumor suppressor locus D17S800-D17S930","volume":"209","author":"Li","year":"2004","journal-title":"Cancer Lett"},{"key":"10.1016\/j.ajpath.2017.07.016_bib13","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1097\/01.mlg.0000191470.71454.a1","article-title":"Comparative proteomics analysis of the proteins associated with laryngeal carcinoma-related gene 1","volume":"116","author":"Zhang","year":"2006","journal-title":"Laryngoscope"},{"key":"10.1016\/j.ajpath.2017.07.016_bib14","doi-asserted-by":"crossref","first-page":"362","DOI":"10.3892\/or.2014.3175","article-title":"Downregulation of tumor suppressor gene ribonuclease T2 and gametogenetin binding protein 2 is associated with drug resistance in ovarian cancer","volume":"32","author":"Yin","year":"2014","journal-title":"Oncol Rep"},{"key":"10.1016\/j.ajpath.2017.07.016_bib15","first-page":"147","article-title":"ZNF403, a novel cell cycle regulator","volume":"40","author":"Guan","year":"2013","journal-title":"Prog Biochem Biophys"},{"key":"10.1016\/j.ajpath.2017.07.016_bib16","doi-asserted-by":"crossref","first-page":"20435","DOI":"10.1038\/srep20435","article-title":"Transcription factor RFX2 is a key regulator of mouse spermiogenesis","volume":"6","author":"Wu","year":"2016","journal-title":"Sci Rep"},{"key":"10.1016\/j.ajpath.2017.07.016_bib17","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1095\/biolreprod.103.020628","article-title":"Mutations in a novel locus on mouse chromosome 11 resulting in male infertility associated with defects in microtubule assembly and sperm tail function","volume":"70","author":"Clark","year":"2004","journal-title":"Biol Reprod"},{"key":"10.1016\/j.ajpath.2017.07.016_bib18","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.mce.2017.01.043","article-title":"Selective deletion of Pten in theca-interstitial cells leads to androgen excess and ovarian dysfunction in mice","volume":"444","author":"Lan","year":"2017","journal-title":"Mol Cell Endocrinol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib19","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"10.1016\/j.ajpath.2017.07.016_bib20","series-title":"Staging for laboratory species. Histological and Histopathological Evaluation of the Testis, ed 1","first-page":"62","author":"Russell","year":"1990"},{"key":"10.1016\/j.ajpath.2017.07.016_bib21","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1369\/0022155414562045","article-title":"Quantitative analysis of the cellular composition in seminiferous tubules in normal and genetically modified infertile mice","volume":"63","author":"Nakata","year":"2015","journal-title":"J Histochem Cytochem"},{"key":"10.1016\/j.ajpath.2017.07.016_bib22","doi-asserted-by":"crossref","first-page":"16696","DOI":"10.1073\/pnas.0506084102","article-title":"Androgens regulate the permeability of the blood-testis barrier","volume":"102","author":"Meng","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2017.07.016_bib23","doi-asserted-by":"crossref","first-page":"2998","DOI":"10.1038\/s41598-017-03193-y","article-title":"GGNBP2 is necessary for testis morphology and sperm development","volume":"7","author":"Chen","year":"2017","journal-title":"Sci Rep"},{"key":"10.1016\/j.ajpath.2017.07.016_bib24","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1038\/nature19356","article-title":"High-throughput discovery of novel developmental phenotypes","volume":"537","author":"Dickinson","year":"2016","journal-title":"Nature"},{"key":"10.1016\/j.ajpath.2017.07.016_bib25","doi-asserted-by":"crossref","first-page":"398","DOI":"10.2741\/1537","article-title":"Cadherin-mediated cell-cell adhesion in the testis","volume":"10","author":"Goossens","year":"2005","journal-title":"Front Biosci"},{"key":"10.1016\/j.ajpath.2017.07.016_bib26","doi-asserted-by":"crossref","first-page":"6775","DOI":"10.2741\/3188","article-title":"Mechanisms of reorganization of cell-cell junctions in the testis","volume":"13","author":"Lui","year":"2008","journal-title":"Front Biosci"},{"key":"10.1016\/j.ajpath.2017.07.016_bib27","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1038\/nrendo.2010.71","article-title":"A local autocrine axis in the testes that regulates spermatogenesis","volume":"6","author":"Cheng","year":"2010","journal-title":"Nat Rev Endocrinol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib28","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/1477-7827-10-27","article-title":"Tubulobulbar complex: cytoskeletal remodeling to release spermatozoa","volume":"10","author":"Upadhyay","year":"2012","journal-title":"Reprod Biol Endocrinol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib29","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.semcdb.2016.01.034","article-title":"Nectins and nectin-like molecules (Necls): recent findings and their role and regulation in spermatogenesis","volume":"59","author":"Huang","year":"2016","journal-title":"Semin Cell Dev Biol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib30","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.1016\/S0960-9822(02)00922-3","article-title":"Nectin couples cell-cell adhesion and the actin scaffold at heterotypic testicular junctions","volume":"12","author":"Ozaki-Kuroda","year":"2002","journal-title":"Curr Biol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib31","doi-asserted-by":"crossref","first-page":"2865","DOI":"10.1128\/MCB.20.8.2865-2873.2000","article-title":"Defects in nuclear and cytoskeletal morphology and mitochondrial localization in spermatozoa of mice lacking nectin-2, a component of cell-cell adherens junctions","volume":"20","author":"Bouchard","year":"2000","journal-title":"Mol Cell Biol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib32","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1111\/j.1745-7262.2008.00357.x","article-title":"Disruption of ectoplasmic specializations between Sertoli cells and maturing spermatids by anti-nectin-2 and anti-nectin-3 antibodies","volume":"10","author":"Toyama","year":"2008","journal-title":"Asian J Androl"},{"key":"10.1016\/j.ajpath.2017.07.016_bib33","doi-asserted-by":"crossref","first-page":"1330","DOI":"10.1095\/biolreprod.102.014670","article-title":"Loss of nectin-2 at Sertoli-spermatid junctions leads to male infertility and correlates with severe spermatozoan head and midpiece malformation, impaired binding to the zona pellucida, and oocyte penetration","volume":"69","author":"Mueller","year":"2003","journal-title":"Biol Reprod"},{"key":"10.1016\/j.ajpath.2017.07.016_bib34","doi-asserted-by":"crossref","first-page":"1125","DOI":"10.1111\/j.1365-2443.2006.01006.x","article-title":"Role of cell adhesion molecule nectin-3 in spermatid development","volume":"11","author":"Inagaki","year":"2006","journal-title":"Genes Cells"},{"key":"10.1016\/j.ajpath.2017.07.016_bib35","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1002\/aja.1001880106","article-title":"Immunofluorescence localization of vinculin in ectoplasmic (\u201cjunctional\u201d) specializations of rat Sertoli cells","volume":"188","author":"Grove","year":"1990","journal-title":"Am J Anat"},{"key":"10.1016\/j.ajpath.2017.07.016_bib36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ydbio.2005.08.001","article-title":"Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis: a review of recent data","volume":"286","author":"Wong","year":"2005","journal-title":"Dev Biol"},{"key":"10.1016\/j.ajpath.2017.07.016_bib37","doi-asserted-by":"crossref","first-page":"1813","DOI":"10.1242\/dev.032631","article-title":"The PGD2 pathway, independently of FGF9, amplifies SOX9 activity in Sertoli cells during male sexual differentiation","volume":"136","author":"Moniot","year":"2009","journal-title":"Development"},{"key":"10.1016\/j.ajpath.2017.07.016_bib38","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1002\/mrd.20313","article-title":"Germ-cell specific protein gametogenetin protein 2 (GGN2), expression in the testis, and association with intracellular membrane","volume":"72","author":"Zhao","year":"2005","journal-title":"Mol Reprod Dev"},{"key":"10.1016\/j.ajpath.2017.07.016_bib39","doi-asserted-by":"crossref","first-page":"e56955","DOI":"10.1371\/journal.pone.0056955","article-title":"Loss of GGN leads to pre-implantation embryonic lethality and compromised male meiotic DNA double strand break repair in the mouse","volume":"8","author":"Jamsai","year":"2013","journal-title":"PLoS One"},{"key":"10.1016\/j.ajpath.2017.07.016_bib40","doi-asserted-by":"crossref","first-page":"7793","DOI":"10.1073\/pnas.0308025101","article-title":"Haploinsufficiency of kelch-like protein homolog 10 causes infertility in male mice","volume":"101","author":"Yan","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.1016\/j.ajpath.2017.07.016_bib41","doi-asserted-by":"crossref","first-page":"e979623","DOI":"10.4161\/21565562.2014.979623","article-title":"Mechanisms of spermiogenesis and spermiation and how they are disturbed","volume":"4","author":"O'Donnell","year":"2014","journal-title":"Spermatogenesis"}],"container-title":["The American Journal of Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002944017305011?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0002944017305011?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,9,12]],"date-time":"2025-09-12T16:30:05Z","timestamp":1757694605000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0002944017305011"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,11]]},"references-count":41,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2017,11]]}},"alternative-id":["S0002944017305011"],"URL":"https:\/\/doi.org\/10.1016\/j.ajpath.2017.07.016","relation":{},"ISSN":["0002-9440"],"issn-type":[{"value":"0002-9440","type":"print"}],"subject":[],"published":{"date-parts":[[2017,11]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Ggnbp2-Null Mutation in Mice Leads to Male Infertility due to a Defect at the Spermiogenesis Stage","name":"articletitle","label":"Article Title"},{"value":"The American Journal of Pathology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ajpath.2017.07.016","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2017 American Society for Investigative Pathology. Published by Elsevier Inc.","name":"copyright","label":"Copyright"}]}}