{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,7,30]],"date-time":"2025-07-30T11:42:21Z","timestamp":1753875741299,"version":"3.41.2"},"reference-count":57,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2022,7,23]],"date-time":"2022-07-23T00:00:00Z","timestamp":1658534400000},"content-version":"am","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100004663","name":"Ministry of Science and Technology of Taiwan","doi-asserted-by":"publisher","award":["MOST 108-2314-B-195-011-MY3"],"award-info":[{"award-number":["MOST 108-2314-B-195-011-MY3"]}],"id":[{"id":"10.13039\/501100004663","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004861","name":"Mackay Memorial Hospital","doi-asserted-by":"publisher","award":["MMH-E 108001"],"award-info":[{"award-number":["MMH-E 108001"]}],"id":[{"id":"10.13039\/501100004861","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Junctional adhesion molecule 3 (JAM3) is involved in epithelial cell junction, cell polarity, and motility. The molecular mechanisms underlying the role of JAM3 in placental dysfunction remain unclear. We hypothesized that JAM3 expression regulates trophoblast fusion, differentiation, proliferation, and apoptosis. Our results revealed that JAM3 was expressed in the cytotrophoblasts and syncytiotrophoblasts of first-trimester and term placental villi. JAM3 expression in cell\u2013cell junctions decreased with the formation of syncytiotrophoblasts. Using trophoblasts as an in vitro model, we observed that forskolin and JAM3 knockdown significantly reduced JAM3 expression and increased syncytium formation. JAM3 knockdown additionally inhibited trophoblast proliferation and increased the number of trophoblasts in the sub-G1 and G2\/M phases, indicating cell-cycle disturbance and apoptosis. Cell-cycle arrest was associated with the engagement of checkpoint kinase 2-cell division cycle 25C-cyclin-dependent kinase 1\/cyclin B1 signaling. Increased expression of BIM, NOXA, XAF1, cytochrome c, and cleaved caspase-3 further indicated trophoblast apoptosis. Overexpression of JAM3 or recombinant JAM3 protein enhanced trophoblast adhesion and migration, which were inhibited by JAM3 knockdown. JAM3 knockdown induced reactive oxygen species and syncytin 2 expression in trophoblasts. Furthermore, H2O2-induced oxidative stress reduced JAM3 expression in trophoblasts and cell culture supernatants. H2O2 simultaneously induced trophoblast apoptosis. JAM3 expression was significantly decreased in the plasmas and placentas of patients with early-onset severe preeclampsia. Thus, our results show that JAM3 may not only be a structural component of trophoblast cell junctions but also regulates trophoblast fusion, differentiation, proliferation, apoptosis, and motility. Dysregulated trophoblast JAM3 expression is crucial in preeclampsia development.<\/jats:p>","DOI":"10.1093\/biolre\/ioac149","type":"journal-article","created":{"date-parts":[[2022,7,25]],"date-time":"2022-07-25T01:09:00Z","timestamp":1658711340000},"source":"Crossref","is-referenced-by-count":0,"title":["Decreased junctional adhesion molecule 3 expression induces reactive oxygen species production and apoptosis in trophoblasts"],"prefix":"10.1093","author":[{"given":"Chie-Pein","family":"Chen","sequence":"first","affiliation":[{"name":"Division of High Risk Pregnancy, MacKay Memorial Hospital , Taipei , Taiwan"},{"name":"Department of Medical Research, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liang-Kai","family":"Wang","sequence":"additional","affiliation":[{"name":"Division of High Risk Pregnancy, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chen-Yu","family":"Chen","sequence":"additional","affiliation":[{"name":"Division of High Risk Pregnancy, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chia-Yu","family":"Chen","sequence":"additional","affiliation":[{"name":"Department of Medical Research, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yi-Hsiu","family":"Kuo","sequence":"additional","affiliation":[{"name":"Department of Medical Research, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yi-Hsin","family":"Wu","sequence":"additional","affiliation":[{"name":"Department of Medical Research, MacKay Memorial Hospital , Taipei , Taiwan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2022,7,23]]},"reference":[{"key":"2022081806573048700_ref1","doi-asserted-by":"crossref","first-page":"183299","DOI":"10.1016\/j.bbamem.2020.183299","article-title":"Physiological functions of junctional adhesion molecules (JAMs) in tight junctions","volume":"1862","author":"Hartmann","year":"2020","journal-title":"Biochim Biophys Acta Biomembr"},{"key":"2022081806573048700_ref2","doi-asserted-by":"crossref","DOI":"10.1101\/cshperspect.a029181","article-title":"Cell-Cell Junctions Organize Structural and Signaling Networks","volume":"10","author":"Garcia","year":"2018","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"2022081806573048700_ref3","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1038\/ni.2062","article-title":"The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo","volume":"12","author":"Woodfin","year":"2011","journal-title":"Nat Immunol"},{"key":"2022081806573048700_ref4","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1161\/ATVBAHA.107.141515","article-title":"Platelets recruit human dendritic cells via Mac-1\/JAM-C interaction and modulate dendritic cell function in vitro","volume":"27","author":"Langer","year":"2007","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"2022081806573048700_ref5","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1016\/S0143-4004(85)80066-7","article-title":"Linkage of human chorionic gonadotrophin and placental lactogen biosynthesis to trophoblast differentiation and tumorigenesis","volume":"6","author":"Hoshina","year":"1985","journal-title":"Placenta"},{"key":"2022081806573048700_ref6","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1093\/humupd\/6.5.485","article-title":"Villous sprouting: fundamental mechanisms of human placental development","volume":"6","author":"Castellucci","year":"2000","journal-title":"Hum Reprod Update"},{"key":"2022081806573048700_ref7","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1093\/humupd\/dmab015","article-title":"Cell dynamics in human villous trophoblast","volume":"27","author":"Aplin","year":"2021","journal-title":"Hum Reprod Update"},{"key":"2022081806573048700_ref8","doi-asserted-by":"crossref","first-page":"S745","DOI":"10.1016\/j.ajog.2017.11.577","article-title":"Pathophysiology of placental-derived fetal growth restriction","volume":"218","author":"Burton","year":"2018","journal-title":"Am J Obstet Gynecol"},{"key":"2022081806573048700_ref9","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.2215\/CJN.12081115","article-title":"Preeclampsia: updates in pathogenesis, definitions, and guidelines","volume":"11","author":"Phipps","year":"2016","journal-title":"Clin J Am Soc Nephrol"},{"issue":"Suppl","key":"2022081806573048700_ref10","doi-asserted-by":"crossref","first-page":"S48","DOI":"10.1016\/j.placenta.2011.12.006","article-title":"Review: does size matter? Placental debris and the pathophysiology of pre-eclampsia","volume":"33","author":"Redman","year":"2012","journal-title":"Placenta"},{"key":"2022081806573048700_ref11","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1016\/j.placenta.2009.05.006","article-title":"Interstitial trophoblastic cell fusion and E-cadherin immunostaining in the placental bed of normal and hypertensive pregnancies","volume":"30","author":"Al-Nasiry","year":"2009","journal-title":"Placenta"},{"key":"2022081806573048700_ref12","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1007\/s00418-002-0396-0","article-title":"Invasive depth of extravillous trophoblast correlates with cellular phenotype: a comparison of intra- and extrauterine implantation sites","volume":"117","author":"Kemp","year":"2002","journal-title":"Histochem Cell Biol"},{"key":"2022081806573048700_ref13","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.humpath.2011.03.012","article-title":"Sensitivity and specificity of finding of multinucleate trophoblastic giant cells in decidua in placentas from high-risk pregnancies","volume":"43","author":"Stanek","year":"2012","journal-title":"Hum Pathol"},{"key":"2022081806573048700_ref14","doi-asserted-by":"crossref","first-page":"158","DOI":"10.1067\/mob.2002.119176","article-title":"Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation","volume":"186","author":"Ishihara","year":"2002","journal-title":"Am J Obstet Gynecol"},{"issue":"Suppl A","key":"2022081806573048700_ref15","doi-asserted-by":"crossref","first-page":"S49","DOI":"10.1016\/j.placenta.2008.10.011","article-title":"Factors involved in regulating trophoblast fusion: potential role in the development of preeclampsia","volume":"30","author":"Gauster","year":"2009","journal-title":"Placenta"},{"key":"2022081806573048700_ref16","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1007\/s00418-005-0051-7","article-title":"E-cadherin in the assessment of aberrant placental cytotrophoblast turnover in pregnancies complicated by pre-eclampsia","volume":"124","author":"Brown","year":"2005","journal-title":"Histochem Cell Biol"},{"issue":"Suppl","key":"2022081806573048700_ref17","first-page":"OL713","article-title":"Junctions and adhesion molecules in first trimester and term human placentas","volume":"51","author":"Challier","year":"2005","journal-title":"Cell Mol Biol (Noisy-le-Grand)"},{"key":"2022081806573048700_ref18","first-page":"25","article-title":"Nationwide singleton birth weight percentiles by gestational age in Taiwan, 1998-2002","volume":"47","author":"Hsieh","year":"2006","journal-title":"Acta Paediatr Taiwan"},{"key":"2022081806573048700_ref19","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1016\/j.placenta.2013.06.311","article-title":"Human placental multipotent mesenchymal stromal cells modulate trophoblast migration via Rap1 activation","volume":"34","author":"Chen","year":"2013","journal-title":"Placenta"},{"key":"2022081806573048700_ref20","doi-asserted-by":"crossref","first-page":"465","DOI":"10.4103\/aja.aja_132_19","article-title":"Fluorescent probes for the detection of reactive oxygen species in human spermatozoa","volume":"22","author":"Escada-Rebelo","year":"2020","journal-title":"Asian J Androl"},{"issue":"Pt 7","key":"2022081806573048700_ref21","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1242\/jcs.111.7.995","article-title":"Cyclic AMP-dependent protein kinases and human trophoblast cell differentiation in vitro","volume":"111","author":"Keryer","year":"1998","journal-title":"J Cell Sci"},{"key":"2022081806573048700_ref22","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.ceb.2009.01.018","article-title":"Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2","volume":"21","author":"Reinhardt","year":"2009","journal-title":"Curr Opin Cell Biol"},{"key":"2022081806573048700_ref23","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1038\/sj.embor.embor887","article-title":"Regulating mammalian checkpoints through Cdc25 inactivation","volume":"4","author":"Donzelli","year":"2003","journal-title":"EMBO Rep"},{"key":"2022081806573048700_ref24","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.devcel.2010.02.013","article-title":"Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis","volume":"18","author":"Gavet","year":"2010","journal-title":"Dev Cell"},{"key":"2022081806573048700_ref25","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.semcdb.2020.03.009","article-title":"Mammalian cell cycle cyclins","volume":"107","author":"Martinez-Alonso","year":"2020","journal-title":"Semin Cell Dev Biol"},{"key":"2022081806573048700_ref26","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1146\/annurev.biochem.73.011303.073723","article-title":"Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints","volume":"73","author":"Sancar","year":"2004","journal-title":"Annu Rev Biochem"},{"key":"2022081806573048700_ref27","doi-asserted-by":"crossref","first-page":"1071","DOI":"10.1038\/cdd.2015.50","article-title":"The BCL-2 protein family, BH3-mimetics and cancer therapy","volume":"22","author":"Delbridge","year":"2015","journal-title":"Cell Death Differ"},{"key":"2022081806573048700_ref28","doi-asserted-by":"crossref","first-page":"1294","DOI":"10.1101\/gad.1304105","article-title":"Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins","volume":"19","author":"Willis","year":"2005","journal-title":"Genes Dev"},{"key":"2022081806573048700_ref29","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1038\/35055027","article-title":"Identification of XAF1 as an antagonist of XIAP anti-Caspase activity","volume":"3","author":"Liston","year":"2001","journal-title":"Nat Cell Biol"},{"key":"2022081806573048700_ref30","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1038\/nrm2308","article-title":"The BCL-2 protein family: opposing activities that mediate cell death","volume":"9","author":"Youle","year":"2008","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2022081806573048700_ref31","doi-asserted-by":"crossref","first-page":"1517","DOI":"10.1089\/ars.2010.3642","article-title":"Regulation of endothelial function by mitochondrial reactive oxygen species","volume":"15","author":"Widlansky","year":"2011","journal-title":"Antioxid Redox Signal"},{"key":"2022081806573048700_ref32","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1161\/ATVBAHA.109.187559","article-title":"Junctional adhesion molecule-C mediates leukocyte infiltration in response to ischemia reperfusion injury","volume":"29","author":"Scheiermann","year":"2009","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"2022081806573048700_ref33","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1016\/j.bbamcr.2018.01.008","article-title":"Junctional adhesion molecule C (JAM-C) dimerization aids cancer cell migration and metastasis","volume":"1865","author":"Garrido-Urbani","year":"2018","journal-title":"Biochim Biophys Acta Mol Cell Res"},{"key":"2022081806573048700_ref34","doi-asserted-by":"crossref","first-page":"731","DOI":"10.1042\/BCJ20160679","article-title":"Calcium-mediated oxidative stress: a common mechanism in tight junction disruption by different types of cellular stress","volume":"474","author":"Gangwar","year":"2017","journal-title":"Biochem J"},{"key":"2022081806573048700_ref35","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1016\/j.abb.2016.05.005","article-title":"What is the concentration of hydrogen peroxide in blood and plasma?","volume":"603","author":"Forman","year":"2016","journal-title":"Arch Biochem Biophys"},{"key":"2022081806573048700_ref36","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1016\/j.jsgi.2004.06.002","volume":"11","author":"Huppertz","year":"2004","journal-title":"J Soc Gynecol Investig"},{"key":"2022081806573048700_ref37","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1093\/molehr\/gaz061","article-title":"Transcriptomic profiling of trophoblast fusion using BeWo and JEG-3 cell lines","volume":"25","author":"Msheik","year":"2019","journal-title":"Mol Hum Reprod"},{"key":"2022081806573048700_ref38","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1111\/j.1471-0528.2005.00843.x","article-title":"Altered placental syncytin and its receptor ASCT2 expression in placental development and pre-eclampsia","volume":"113","author":"Chen","year":"2006","journal-title":"BJOG"},{"key":"2022081806573048700_ref39","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1095\/biolreprod.108.069765","article-title":"Functional characterization of the human placental fusogenic membrane protein syncytin 2","volume":"79","author":"Chen","year":"2008","journal-title":"Biol Reprod"},{"key":"2022081806573048700_ref40","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.placenta.2006.02.011","article-title":"The placenta in pre-eclampsia and intrauterine growth restriction: studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances","volume":"28","author":"Mayhew","year":"2007","journal-title":"Placenta"},{"key":"2022081806573048700_ref41","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1007\/BF02899568","article-title":"Proliferation of villous trophoblast of the human placenta in normal and abnormal pregnancies","volume":"60","author":"Arnholdt","year":"1991","journal-title":"Virchows Arch B Cell Pathol Incl Mol Pathol"},{"key":"2022081806573048700_ref42","doi-asserted-by":"crossref","first-page":"S907","DOI":"10.1016\/j.ajog.2020.09.047","article-title":"Syncytiotrophoblast stress in preeclampsia: the convergence point for multiple pathways","volume":"226","author":"Redman","year":"2022","journal-title":"Am J Obstet Gynecol"},{"key":"2022081806573048700_ref43","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.1038\/ajh.2008.289","article-title":"Serum uric acid levels correlate with plasma hydrogen peroxide and protein carbonyl levels in preeclampsia","volume":"21","author":"Tsukimori","year":"2008","journal-title":"Am J Hypertens"},{"key":"2022081806573048700_ref44","doi-asserted-by":"crossref","first-page":"3638","DOI":"10.1210\/endo.142.8.8329","article-title":"Overexpression of copper zinc superoxide dismutase impairs human trophoblast cell fusion and differentiation","volume":"142","author":"Frendo","year":"2001","journal-title":"Endocrinology"},{"key":"2022081806573048700_ref45","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.1016\/j.cellsig.2013.01.008","article-title":"Syncytin-1 modulates placental trophoblast cell proliferation by promoting G1\/S transition","volume":"25","author":"Huang","year":"2013","journal-title":"Cell Signal"},{"key":"2022081806573048700_ref46","doi-asserted-by":"crossref","first-page":"3151","DOI":"10.1007\/s00018-013-1533-8","article-title":"Reduced syncytin-1 expression in choriocarcinoma BeWo cells activates the calpain1-AIF-mediated apoptosis, implication for preeclampsia","volume":"71","author":"Huang","year":"2014","journal-title":"Cell Mol Life Sci"},{"key":"2022081806573048700_ref47","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1091\/mbc.e10-08-0677","article-title":"Tight function zonula occludens-3 regulates cyclin D1-dependent cell proliferation","volume":"22","author":"Capaldo","year":"2011","journal-title":"Mol Biol Cell"},{"key":"2022081806573048700_ref48","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1160\/TH16-11-0885","article-title":"JAM-C maintains VEGR2 expression to promote retinal pigment epithelium cell survival under oxidative stress","volume":"117","author":"Jia","year":"2017","journal-title":"Thromb Haemost"},{"key":"2022081806573048700_ref49","doi-asserted-by":"crossref","first-page":"1737","DOI":"10.1172\/JCI93198","article-title":"JAM3 maintains leukemia-initiating cell self-renewal through LRP5\/AKT\/beta-catenin\/CCND1 signaling","volume":"128","author":"Zhang","year":"2018","journal-title":"J Clin Invest"},{"key":"2022081806573048700_ref50","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1038\/35103059","article-title":"CHK2 kinase\u2013a busy messenger","volume":"2","author":"Bartek","year":"2001","journal-title":"Nat Rev Mol Cell Biol"},{"key":"2022081806573048700_ref51","doi-asserted-by":"crossref","first-page":"1507","DOI":"10.1093\/carcin\/bgp155","article-title":"Identification of XAF1 as a novel cell cycle regulator through modulating G(2)\/M checkpoint and interaction with checkpoint kinase 1 in gastrointestinal cancer","volume":"30","author":"Wang","year":"2009","journal-title":"Carcinogenesis"},{"key":"2022081806573048700_ref52","first-page":"2923","article-title":"Jam3 promotes migration and suppresses apoptosis of renal carcinoma cell lines","volume":"42","author":"Li","year":"2018","journal-title":"Int J Mol Med"},{"key":"2022081806573048700_ref53","doi-asserted-by":"crossref","first-page":"4096","DOI":"10.1158\/0008-5472.CAN-10-2794","article-title":"A novel function of junctional adhesion molecule-C in mediating melanoma cell metastasis","volume":"71","author":"Langer","year":"2011","journal-title":"Cancer Res"},{"key":"2022081806573048700_ref54","doi-asserted-by":"crossref","first-page":"55602","DOI":"10.1074\/jbc.M404676200","article-title":"The junctional adhesion molecule-C promotes neutrophil transendothelial migration in vitro and in vivo","volume":"279","author":"Chavakis","year":"2004","journal-title":"J Biol Chem"},{"key":"2022081806573048700_ref55","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.4049\/jimmunol.1000556","article-title":"Junctional adhesion molecule-C is a soluble mediator of angiogenesis","volume":"185","author":"Rabquer","year":"2010","journal-title":"J Immunol"},{"key":"2022081806573048700_ref56","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1002\/art.37712","article-title":"Differential expression of junctional adhesion molecules in different stages of systemic sclerosis","volume":"65","author":"Manetti","year":"2013","journal-title":"Arthritis Rheum"},{"key":"2022081806573048700_ref57","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ejogrb.2013.05.005","article-title":"Global and regional estimates of preeclampsia and eclampsia: a systematic review","volume":"170","author":"Abalos","year":"2013","journal-title":"Eur J Obstet Gynecol Reprod Biol"}],"container-title":["Biology of Reproduction"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioac149\/45460172\/ioac149.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article-pdf\/doi\/10.1093\/biolre\/ioac149\/45460172\/ioac149.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,18]],"date-time":"2022-08-18T06:58:24Z","timestamp":1660805904000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/biolreprod\/advance-article\/doi\/10.1093\/biolre\/ioac149\/6649115"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,23]]},"references-count":57,"URL":"https:\/\/doi.org\/10.1093\/biolre\/ioac149","relation":{},"ISSN":["0006-3363","1529-7268"],"issn-type":[{"type":"print","value":"0006-3363"},{"type":"electronic","value":"1529-7268"}],"subject":[],"published":{"date-parts":[[2022,7,23]]},"article-number":"ioac149"}}