{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,17]],"date-time":"2026-05-17T07:58:06Z","timestamp":1779004686397,"version":"3.51.4"},"reference-count":54,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2020,2,26]],"date-time":"2020-02-26T00:00:00Z","timestamp":1582675200000},"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\/100009633","name":"Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["R01HD088412"],"award-info":[{"award-number":["R01HD088412"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000053","name":"National Eye Institute","doi-asserted-by":"publisher","award":["R01EY022356"],"award-info":[{"award-number":["R01EY022356"]}],"id":[{"id":"10.13039\/100000053","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32GM088129"],"award-info":[{"award-number":["T32GM088129"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"publisher","award":["T32GM120011"],"award-info":[{"award-number":["T32GM120011"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Promotion of Science Overseas Research"},{"DOI":"10.13039\/100000053","name":"National Eye Institute","doi-asserted-by":"publisher","award":["R01EY026545"],"award-info":[{"award-number":["R01EY026545"]}],"id":[{"id":"10.13039\/100000053","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,5,26]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Receptor accessory protein 6 (REEP6) is a member of the REEP\/Ypt-interacting protein family that we recently identified as essential for normal endoplasmic reticulum homeostasis and protein trafficking in the retina of mice and humans. Interestingly, in addition to the loss of REEP6 in our knockout (KO) mouse model recapitulating the retinal degeneration of humans with REEP6 mutations causing retinitis pigmentosa (RP), we also found that male mice are sterile. Herein, we characterize the infertility caused by loss of Reep6. Expression of both Reep6 mRNA transcripts is present in the testis; however, isoform 1 becomes overexpressed during spermiogenesis. In vitro fertilization assays reveal that Reep6 KO spermatozoa are able to bind the zona pellucida but are only able to fertilize oocytes lacking the zona pellucida. Although spermatogenesis appears normal in KO mice, cauda epididymal spermatozoa have severe motility defects and variable morphological abnormalities, including bent or absent tails. Immunofluorescent staining reveals that REEP6 expression first appears in stage IV tubules within step 15 spermatids, and REEP6 localizes to the connecting piece, midpiece, and annulus of mature spermatozoa. These data reveal an important role for REEP6 in sperm motility and morphology and is the first reported function for a REEP protein in reproductive processes. Additionally, this work identifies a new gene potentially responsible for human infertility and has implications for patients with RP harboring mutations in REEP6.<\/jats:p>","DOI":"10.1093\/biolre\/ioaa024","type":"journal-article","created":{"date-parts":[[2020,2,26]],"date-time":"2020-02-26T15:04:40Z","timestamp":1582729480000},"page":"1234-1247","source":"Crossref","is-referenced-by-count":18,"title":["Knockout of mouse receptor accessory protein 6 leads to sperm function and morphology defects\u2020"],"prefix":"10.1093","volume":"102","author":[{"given":"Darius J","family":"Devlin","sequence":"first","affiliation":[{"name":"Interdepartmental Program in Translational Biology & Molecular Medicine, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Pathology & Immunology, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Smriti","family":"Agrawal Zaneveld","sequence":"first","affiliation":[{"name":"Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kaori","family":"Nozawa","sequence":"first","affiliation":[{"name":"Department of Pathology & Immunology, Baylor College of Medicine, Houston, TX, USA"},{"name":"Center for Drug Discovery, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiao","family":"Han","sequence":"first","affiliation":[{"name":"Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"},{"name":"Reproductive Medical Center, People\u2019s Hospital of Zhengzhou University, Zhengzhou, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Abigail R","family":"Moye","sequence":"first","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qingnan","family":"Liang","sequence":"first","affiliation":[{"name":"Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacob Michael","family":"Harnish","sequence":"first","affiliation":[{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin M","family":"Matzuk","sequence":"first","affiliation":[{"name":"Department of Pathology & Immunology, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"},{"name":"Center for Drug Discovery, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rui","family":"Chen","sequence":"first","affiliation":[{"name":"Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA"},{"name":"Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2020,2,26]]},"reference":[{"key":"2020052802495427100_ref1","doi-asserted-by":"crossref","first-page":"191","DOI":"10.4103\/0974-1208.170370","article-title":"Trends of male factor infertility, an important cause of infertility: a review of literature","volume":"8","author":"Kumar","year":"2015","journal-title":"J Hum Reprod Sci"},{"key":"2020052802495427100_ref2","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s12958-018-0334-1","article-title":"Proteomic profile of human spermatozoa in healthy and asthenozoospermic individuals","volume":"16","author":"Cao","year":"2018","journal-title":"Reprod Biol Endocrinol"},{"key":"2020052802495427100_ref3","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1093\/humupd\/dmw014","article-title":"Gamete activation: basic knowledge and clinical applications","volume":"22","author":"Tosti","year":"2016","journal-title":"Hum Reprod Update"},{"key":"2020052802495427100_ref4","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1093\/biolre\/iox096","article-title":"Formation and function of sperm tail structures in association with sperm motility defects","volume":"97","author":"Lehti","year":"2017","journal-title":"Biol Reprod"},{"key":"2020052802495427100_ref5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.28199","article-title":"Essential role for SUN5 in anchoring sperm head to the tail","volume":"6","author":"Shang","year":"2017","journal-title":"elife"},{"key":"2020052802495427100_ref6","doi-asserted-by":"crossref","first-page":"E5370","DOI":"10.1073\/pnas.1621279114","article-title":"TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa","volume":"114","author":"Castaneda","year":"2017","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020052802495427100_ref7","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1016\/j.bbagen.2017.12.005","article-title":"Disruption of Ssp411 causes impaired sperm head formation and male sterility in mice","volume":"1862","author":"Liu","year":"2018","journal-title":"Biochim Biophys Acta, Gen Subj"},{"key":"2020052802495427100_ref8","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.ajhg.2018.03.007","article-title":"Absence of CFAP69 causes male infertility due to multiple morphological abnormalities of the flagella in human and mouse","volume":"102","author":"Dong","year":"2018","journal-title":"Am J Hum Genet"},{"key":"2020052802495427100_ref9","doi-asserted-by":"crossref","first-page":"2667","DOI":"10.1093\/hmg\/ddx149","article-title":"REEP6 deficiency leads to retinal degeneration through disruption of ER homeostasis and protein trafficking","volume":"26","author":"Agrawal","year":"2017","journal-title":"Hum Mol Genet"},{"key":"2020052802495427100_ref10","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1016\/j.ajhg.2016.10.008","article-title":"Mutations in REEP6 cause autosomal-recessive retinitis pigmentosa","volume":"99","author":"Arno","year":"2016","journal-title":"Am J Hum Genet"},{"key":"2020052802495427100_ref11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0076366","article-title":"REEPs are membrane shaping adapter proteins that modulate specific G protein-coupled receptor trafficking by affecting ER cargo capacity","volume":"8","author":"Bj\u00f6rk","year":"2013","journal-title":"PLoS One"},{"key":"2020052802495427100_ref12","doi-asserted-by":"crossref","first-page":"4260","DOI":"10.1093\/hmg\/ddu143","article-title":"Regulation of a novel isoform of receptor expression enhancing protein REEP6 in rod photoreceptors by bZIP transcription factor NRL","volume":"23","author":"Hao","year":"2014","journal-title":"Hum Mol Genet"},{"key":"2020052802495427100_ref13","doi-asserted-by":"crossref","first-page":"17847","DOI":"10.1523\/JNEUROSCI.1373-13.2013","article-title":"Development and plasticity of outer retinal circuitry following genetic removal of horizontal cells","volume":"33","author":"Keeley","year":"2013","journal-title":"J Neurosci"},{"key":"2020052802495427100_ref14","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/978-1-4614-2364-5_7","article-title":"Ramp like proteins RTP and REEP family of proteins","volume":"744","author":"Mainland","year":"2012","journal-title":"Adv Exp Med Biol"},{"key":"2020052802495427100_ref15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep39041","article-title":"The accessory proteins REEP5 and REEP6 refine CXCR1-mediated cellular responses and lung cancer progression","volume":"6","author":"Park","year":"2016","journal-title":"Sci Rep"},{"key":"2020052802495427100_ref16","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1146\/annurev.cellbio.042308.113324","article-title":"Mechanisms shaping the membranes of cellular organelles","volume":"25","author":"Shibata","year":"2009","journal-title":"Annu Rev Cell Dev Biol"},{"key":"2020052802495427100_ref17","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1167\/iovs.04-0867","article-title":"Deleted in polyposis 1-like 1 gene (Dp1l1): a novel gene richly expressed in retinal ganglion cells","volume":"46","author":"Sato","year":"2005","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"2020052802495427100_ref18","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1083\/jcb.74.1.68","article-title":"Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization","volume":"74","author":"Bellv\u00e9","year":"1977","journal-title":"J Cell Biol"},{"key":"2020052802495427100_ref19","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/978-1-60761-103-5_16","article-title":"Staging of mouse seminiferous tubule cross-sections","volume":"558","author":"Ahmed","year":"2009","journal-title":"Methods Mol Biol"},{"key":"2020052802495427100_ref20","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/S0015-0282(16)48918-1","article-title":"Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid","volume":"44","author":"Quinn","year":"1985","journal-title":"Fertil Steril"},{"key":"2020052802495427100_ref21","doi-asserted-by":"crossref","first-page":"1207","DOI":"10.1095\/biolreprod.110.088989","article-title":"Classification of mouse sperm motility patterns using an automated multiclass support vector machines model","volume":"84","author":"Goodson","year":"2011","journal-title":"Biol Reprod"},{"key":"2020052802495427100_ref22","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1095\/biolreprod53.2.276","article-title":"Viability assessment of mammalian sperm using SYBR-14 and propidium iodide","volume":"53","author":"Garner","year":"1995","journal-title":"Biol Reprod"},{"key":"2020052802495427100_ref23","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1002\/mrd.20759","article-title":"Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice","volume":"75","author":"P\u00e9rez-Crespo","year":"2008","journal-title":"Mol Reprod Dev"},{"key":"2020052802495427100_ref24","first-page":"59","article-title":"Visualization of sperm accessory structures in the mammalian spermatids, spermatozoa, and zygotes by immunofluorescence, confocal, and immunoelectron microscopy","volume":"253","author":"Sutovsky","year":"2004","journal-title":"Methods Mol Biol"},{"key":"2020052802495427100_ref25","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/nmeth.2089","article-title":"NIH image to ImageJ: 25 years of image analysis","volume":"9","author":"Schneider","year":"2012","journal-title":"Nat Methods"},{"key":"2020052802495427100_ref26","doi-asserted-by":"crossref","first-page":"3850","DOI":"10.1073\/pnas.1117963109","article-title":"Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein ADAM3 and male fertility [corrected]","volume":"109","author":"Tokuhiro","year":"2012","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020052802495427100_ref27","doi-asserted-by":"crossref","first-page":"6794","DOI":"10.1128\/MCB.01029-07","article-title":"Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis","volume":"27","author":"Lin","year":"2007","journal-title":"Mol Cell Biol"},{"key":"2020052802495427100_ref28","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1274\/jmor.35.71","article-title":"The early history of the TYH medium for in vitro fertilization of mouse ova","volume":"35","author":"Toyoda","year":"2018","journal-title":"J Mamm Ova Res"},{"key":"2020052802495427100_ref29","doi-asserted-by":"crossref","first-page":"4892","DOI":"10.1073\/pnas.1018202108","article-title":"Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization","volume":"108","author":"Jin","year":"2011","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020052802495427100_ref30","doi-asserted-by":"crossref","first-page":"e979114","DOI":"10.4161\/21565562.2014.979114","article-title":"Interpreting histopathology in the epididymis","volume":"4","author":"De Grava","year":"2014","journal-title":"Spermatogenesis"},{"key":"2020052802495427100_ref31","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1242\/dev.121.4.1129","article-title":"Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation","volume":"121","author":"Visconti","year":"1995","journal-title":"Development"},{"key":"2020052802495427100_ref32","first-page":"245","article-title":"Signalling pathways involved in sperm capacitation","volume":"65","author":"Salicioni","year":"2007","journal-title":"Soc Reprod Fertil Suppl"},{"key":"2020052802495427100_ref33","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1530\/REP-11-0326","article-title":"The slower the better: how sperm capacitation and acrosome reaction is modified in the presence of estrogens","volume":"143","author":"Sebkova","year":"2012","journal-title":"Reproduction"},{"key":"2020052802495427100_ref34","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1073\/pnas.0811895106","article-title":"Understanding the molecular basis of sperm capacitation through kinase design","volume":"106","author":"Visconti","year":"2009","journal-title":"Proc Natl Acad Sci USA"},{"key":"2020052802495427100_ref35","doi-asserted-by":"crossref","first-page":"2868","DOI":"10.1093\/humrep\/del250","article-title":"Quantitative effects of male age on sperm motion","volume":"21","author":"Sloter","year":"2006","journal-title":"Hum Reprod"},{"key":"2020052802495427100_ref36","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":"2020052802495427100_ref37","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.fertnstert.2013.09.016","article-title":"Acetylated \u03b1-tubulin is reduced in individuals with poor sperm motility","volume":"101","author":"Bhagwat","year":"2014","journal-title":"Fertil Steril"},{"key":"2020052802495427100_ref38","volume-title":"Histological and Histopathological Evaluation of the Testis","author":"Russell","year":"1990","edition":"1st"},{"key":"2020052802495427100_ref39","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.semcdb.2014.01.003","article-title":"Microtubules and spermatogenesis","volume":"30","author":"O\u2019Donnell","year":"2014","journal-title":"Semin Cell Dev Biol"},{"key":"2020052802495427100_ref40","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.gene.2018.03.059","article-title":"The acroframosome-acroplaxome-manchette axis may function in sperm head shaping and male fertility","volume":"660","author":"Wei","year":"2018","journal-title":"Gene"},{"key":"2020052802495427100_ref41","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1159\/000086378","article-title":"Transcriptomic analyses support the similarity of gene expression between brain and testis in human as well as mouse","volume":"111","author":"Guo","year":"2005","journal-title":"Cytogenet Genome Res"},{"key":"2020052802495427100_ref42","doi-asserted-by":"crossref","DOI":"10.1007\/978-1-62703-038-0_27","volume-title":"Assessment of Spermatogenesis Through Staging of Seminiferous Tubules","author":"Meistrich","year":"2013"},{"key":"2020052802495427100_ref43","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\u2019Donnell","year":"2014","journal-title":"Spermatogenesis"},{"key":"2020052802495427100_ref44","doi-asserted-by":"crossref","first-page":"40S","DOI":"10.1177\/0192623312454337","article-title":"Proliferative and nonproliferative lesions of the rat and mouse male reproductive system","volume":"40","author":"Creasy","year":"2012","journal-title":"Toxicol Pathol"},{"key":"2020052802495427100_ref45","doi-asserted-by":"crossref","first-page":"39318","DOI":"10.1038\/srep39318","article-title":"Deficiency of Mkrn2 causes abnormal spermiogenesis and spermiation, and impairs male fertility","volume":"6","author":"Qian","year":"2016","journal-title":"Sci Rep"},{"key":"2020052802495427100_ref46","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.devcel.2005.01.021","article-title":"The Sept4 septin locus is required for sperm terminal differentiation in mice","volume":"8","author":"Kissel","year":"2005","journal-title":"Dev Cell"},{"key":"2020052802495427100_ref47","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1242\/jcs.158998","article-title":"SEPT12 orchestrates the formation of mammalian sperm annulus by organizing core octameric complexes with other SEPT proteins","volume":"128","author":"Kuo","year":"2015","journal-title":"J Cell Sci"},{"key":"2020052802495427100_ref48","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1007\/s11248-015-9886-4","article-title":"Ultrastructural study of spermatogenesis in KSR2 deficient mice","volume":"24","author":"Moretti","year":"2015","journal-title":"Transgenic Res"},{"key":"2020052802495427100_ref49","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1091\/mbc.e12-11-0801","article-title":"The N-DRC forms a conserved biochemical complex that maintains outer doublet\u00a0alignment and limits microtubule sliding in motile axonemes","volume":"24","author":"Bower","year":"2013","journal-title":"Mol Biol Cell"},{"key":"2020052802495427100_ref50","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1679\/aohc.66.383","article-title":"Formation and organization of the mammalian sperm head","volume":"66","author":"Toshimori","year":"2003","journal-title":"Arch Histol Cytol"},{"key":"2020052802495427100_ref51","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1002\/dvdy.22563","article-title":"GMAP210 and IFT88 are present in the spermatid golgi apparatus and participate in the development of the acrosome-acroplaxome complex, head-tail coupling apparatus and tail","volume":"240","author":"Kierszenbaum","year":"2011","journal-title":"Dev Dyn"},{"key":"2020052802495427100_ref52","doi-asserted-by":"crossref","first-page":"4358","DOI":"10.1091\/mbc.E15-08-0578","article-title":"Intraflagellar transport is essential for mammalian spermiogenesis but is absent in mature sperm","volume":"26","author":"San Agustin","year":"2015","journal-title":"Mol Biol Cell"},{"key":"2020052802495427100_ref53","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep32255","article-title":"Characterization of non-olfactory GPCRs in human sperm with a focus on GPR18","volume":"6","author":"Flegel","year":"2016","journal-title":"Sci Rep"},{"key":"2020052802495427100_ref54","doi-asserted-by":"crossref","first-page":"238","DOI":"10.2174\/138920211795860107","article-title":"Retinitis pigmentosa: genes and disease mechanisms","volume":"12","author":"Ferrari","year":"2011","journal-title":"Curr Genomics"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioaa024\/33014619\/ioaa024.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/102\/6\/1234\/33317759\/ioaa024.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/biolreprod\/article-pdf\/102\/6\/1234\/33317759\/ioaa024.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,16]],"date-time":"2022-10-16T17:21:51Z","timestamp":1665940911000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/article\/102\/6\/1234\/5758288"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,26]]},"references-count":54,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,2,26]]},"published-print":{"date-parts":[[2020,5,26]]}},"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioaa024","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"value":"0006-3363","type":"print"},{"value":"1529-7268","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,6]]},"published":{"date-parts":[[2020,2,26]]}}}