{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T16:11:18Z","timestamp":1791389478339,"version":"4.3.3"},"reference-count":89,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,1,11]],"date-time":"2023-01-11T00:00:00Z","timestamp":1673395200000},"content-version":"am","delay-in-days":375,"URL":"http:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-017"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-012"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2022,1,1]],"date-time":"2022-01-01T00:00:00Z","timestamp":1640995200000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-004"}],"funder":[{"DOI":"10.13039\/100004897","name":"Pennsylvania Department of Health","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100004897","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01 PR015540"],"award-info":[{"award-number":["R01 PR015540"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Seminars in Cell &amp; Developmental Biology"],"published-print":{"date-parts":[[2022,1]]},"DOI":"10.1016\/j.semcdb.2021.05.032","type":"journal-article","created":{"date-parts":[[2021,6,9]],"date-time":"2021-06-09T09:49:39Z","timestamp":1623232179000},"page":"71-81","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":40,"special_numbering":"C","title":["Nonclassical androgen and estrogen signaling is essential for normal spermatogenesis"],"prefix":"10.1016","volume":"121","author":[{"given":"Paul S.","family":"Cooke","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William H.","family":"Walker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib1","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1210\/endo-30-3-437","article-title":"Correlations between the chemical structure and the pharmacological actions of the steroids","volume":"30","author":"Selye","year":"1942","journal-title":"Endocrinology"},{"issue":"5490","key":"10.1016\/j.semcdb.2021.05.032_bib2","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/253357a0","article-title":"Endometrial cell calcium and oestrogen action","volume":"253","author":"Pietras","year":"1975","journal-title":"Nature"},{"issue":"5589","key":"10.1016\/j.semcdb.2021.05.032_bib3","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1038\/265069a0","article-title":"Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells","volume":"265","author":"Pietras","year":"1977","journal-title":"Nature"},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib4","first-page":"355","article-title":"Early effects of estradiol and cortisol on water and electrolyte shifts in the uterus of the immature rat","volume":"197","author":"Spaziani","year":"1959","journal-title":"Am. J. Pathol."},{"issue":"4","key":"10.1016\/j.semcdb.2021.05.032_bib5","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1073\/pnas.58.4.1711","article-title":"Adenosine 3\u2019, 5\u2019-monophosphate in rat uterus: acute elevation by estrogen","volume":"58","author":"Szego","year":"1967","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib6","doi-asserted-by":"crossref","first-page":"E283","DOI":"10.1073\/pnas.1322057111","article-title":"Mutation of the palmitoylation site of estrogen receptor alpha in vivo reveals tissue-specific roles for membrane versus nuclear actions","volume":"111","author":"Adlanmerini","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"4","key":"10.1016\/j.semcdb.2021.05.032_bib7","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1016\/j.devcel.2014.04.016","article-title":"Membrane-localized estrogen receptor \u03b1 is required for normal organ development and function","volume":"29","author":"Pedram","year":"2014","journal-title":"Dev. Cell"},{"issue":"7","key":"10.1016\/j.semcdb.2021.05.032_bib8","doi-asserted-by":"crossref","first-page":"2909","DOI":"10.1210\/en.2016-1085","article-title":"Membrane-localized estrogen receptor 1 is required for normal male reproductive development and function in mice","volume":"157","author":"Nanjappa","year":"2016","journal-title":"Endocrinology"},{"issue":"12","key":"10.1016\/j.semcdb.2021.05.032_bib9","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1038\/nrm.2016.122","article-title":"Nuclear receptors outside the nucleus: extranuclear signalling by steroid receptors","volume":"17","author":"Levin","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"issue":"20","key":"10.1016\/j.semcdb.2021.05.032_bib10","first-page":"30074","article-title":"Role of nuclear and membrane estrogen signaling pathways in the male and female reproductive tract","volume":"S0301\u20134681","author":"Cooke","year":"2020","journal-title":"Differentiation"},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib11","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1083\/jcb.97.3.679","article-title":"Estrogen action at endometrial membranes: alterations in luminal surface detectable within seconds","volume":"97","author":"Rambo","year":"1983","journal-title":"J. Cell Biol."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib12","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/S1097-2765(02)00471-9","article-title":"Formation of the androgen receptor transcription complex","volume":"9","author":"Shang","year":"2002","journal-title":"Mol. Cell"},{"issue":"30","key":"10.1016\/j.semcdb.2021.05.032_bib13","doi-asserted-by":"crossref","first-page":"10919","DOI":"10.1073\/pnas.0404278101","article-title":"Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells","volume":"101","author":"Fix","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"6322","key":"10.1016\/j.semcdb.2021.05.032_bib14","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1038\/351117a0","article-title":"Male development of chromosomally female mice transgenic for Sry","volume":"351","author":"Koopman","year":"1991","journal-title":"Nature"},{"issue":"23","key":"10.1016\/j.semcdb.2021.05.032_bib15","doi-asserted-by":"crossref","first-page":"3921","DOI":"10.1242\/dev.048983","article-title":"Sry: the master switch in mammalian sex determination","volume":"137","author":"Kashimada","year":"2010","journal-title":"Development"},{"key":"10.1016\/j.semcdb.2021.05.032_bib16","first-page":"1","article-title":"Studies on sex differentiation in mammals","volume":"29","author":"Jost","year":"1973","journal-title":"Recent Prog. Horm. Res."},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib17","first-page":"3","article-title":"Androgen receptor structure, function and biology: from bench to bedside","volume":"37","author":"Davey","year":"2016","journal-title":"Clin. Biochem. Rev."},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib18","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1073\/pnas.0308114100","article-title":"A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis","volume":"101","author":"De Gendt","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"9","key":"10.1016\/j.semcdb.2021.05.032_bib19","doi-asserted-by":"crossref","first-page":"2373","DOI":"10.1093\/nar\/19.9.2373","article-title":"A frame-shift mutation in the androgen receptor gene causes complete androgen insensitivity in the testicularfeminized mouse","volume":"19","author":"He","year":"1991","journal-title":"Nucleic Acids Res."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib20","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/S0022-3468(86)80830-2","article-title":"Testicular feminization: a model for testicular descent in mice and men","volume":"21","author":"Hutson","year":"1986","journal-title":"J. Pediatr. Surg."},{"issue":"7","key":"10.1016\/j.semcdb.2021.05.032_bib21","doi-asserted-by":"crossref","first-page":"3563","DOI":"10.1210\/en.2006-0159","article-title":"Spermatogonial differentiation in juvenile spermatogonial depletion (jsd) mice with androgen receptor or follicle-stimulating hormone mutations","volume":"147","author":"Shetty","year":"2006","journal-title":"Endocrinology"},{"issue":"18","key":"10.1016\/j.semcdb.2021.05.032_bib22","doi-asserted-by":"crossref","first-page":"6876","DOI":"10.1073\/pnas.0307306101","article-title":"Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells","volume":"101","author":"Chang","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"25","key":"10.1016\/j.semcdb.2021.05.032_bib23","doi-asserted-by":"crossref","first-page":"2841","DOI":"10.1091\/mbc.E20-05-0334","article-title":"Regulation of meiotic progression by Sertoli-cell androgen signaling","volume":"31","author":"Larose","year":"2020","journal-title":"Mol. Biol. Cell"},{"issue":"3354","key":"10.1016\/j.semcdb.2021.05.032_bib24","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1038\/133209a0","article-title":"Mass excretion of oestrogenic hormone in the urine of the stallion","volume":"133","author":"Zondek","year":"1934","journal-title":"Nature"},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib25","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1093\/biolre\/ioy043","article-title":"Estrogen in the male: a historical perspective","volume":"99","author":"Hess","year":"2018","journal-title":"Biol. Reprod."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib26","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1152\/physrev.00018.2016","article-title":"Estrogens in male physiology","volume":"97","author":"Cooke","year":"2017","journal-title":"Physiol. Rev."},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib27","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1476-069X-8-37","article-title":"Urogenital abnormalities in men exposed to diethylstilbestrol in utero: a cohort study","volume":"8","author":"Palmer","year":"2009","journal-title":"Environ. Health"},{"issue":"S103","key":"10.1016\/j.semcdb.2021.05.032_bib28","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1111\/j.1600-0463.2001.tb05754.x","article-title":"From malformations to molecular mechanisms in the male: three decades of research on endocrine disrupters","volume":"109","author":"McLachlan","year":"2001","journal-title":"APMIS"},{"issue":"6","key":"10.1016\/j.semcdb.2021.05.032_bib29","doi-asserted-by":"crossref","first-page":"2874","DOI":"10.1210\/endo-128-6-2874","article-title":"Estrogen receptor expression in developing epididymis, efferent ductules, and other male reproductive organs","volume":"128","author":"Cooke","year":"1991","journal-title":"Endocrinology"},{"issue":"6","key":"10.1016\/j.semcdb.2021.05.032_bib30","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1002\/j.1939-4640.1997.tb02437.x","article-title":"Estrogen receptor (\u03b1 and \u03b2) expression in the excurrent ducts of the adult male rat reproductive tract","volume":"18","author":"Hess","year":"1997","journal-title":"J. Androl."},{"key":"10.1016\/j.semcdb.2021.05.032_bib31","first-page":"109","article-title":"Developmental pattern of estrogen receptor expression in male mouse genital organs","volume":"3","author":"Iguchi","year":"1991","journal-title":"Mol. Androl."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib32","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1210\/endo.132.3.8440194","article-title":"Germ cells of the mouse testis express P450 aromatase","volume":"132","author":"Nitta","year":"1993","journal-title":"Endocrinology"},{"issue":"23","key":"10.1016\/j.semcdb.2021.05.032_bib33","doi-asserted-by":"crossref","first-page":"11162","DOI":"10.1073\/pnas.90.23.11162","article-title":"Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene","volume":"90","author":"Lubahn","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"11","key":"10.1016\/j.semcdb.2021.05.032_bib34","doi-asserted-by":"crossref","first-page":"4796","DOI":"10.1210\/endo.137.11.8895349","article-title":"Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility","volume":"137","author":"Eddy","year":"1996","journal-title":"Endocrinology"},{"issue":"6659","key":"10.1016\/j.semcdb.2021.05.032_bib35","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1038\/37352","article-title":"A role for oestrogens in the male reproductive system","volume":"390","author":"Hess","year":"1997","journal-title":"Nature"},{"issue":"14","key":"10.1016\/j.semcdb.2021.05.032_bib36","doi-asserted-by":"crossref","first-page":"7986","DOI":"10.1073\/pnas.96.14.7986","article-title":"Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene","volume":"96","author":"Robertson","year":"1999","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"8","key":"10.1016\/j.semcdb.2021.05.032_bib37","doi-asserted-by":"crossref","first-page":"2913","DOI":"10.1210\/endo.143.8.8957","article-title":"The phenotype of the aromatase knockout mouse reveals dietary phytoestrogens impact significantly on testis function","volume":"143","author":"Robertson","year":"2002","journal-title":"Endocrinology"},{"issue":"12","key":"10.1016\/j.semcdb.2021.05.032_bib38","doi-asserted-by":"crossref","first-page":"5925","DOI":"10.1073\/pnas.93.12.5925","article-title":"Cloning of a novel receptor expressed in rat prostate and ovary","volume":"93","author":"Kuiper","year":"1996","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib39","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/j.bbrc.2020.06.063","article-title":"Generation of an all-exon Esr2 deleted mouse line: effects on fertility","volume":"529","author":"Antonson","year":"2020","journal-title":"Biochem. Biophys. Res. Commun."},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib40","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1096\/fasebj.9.5.7896011","article-title":"Membrane estrogen receptors identified by multiple antibody labeling and impeded\u2010ligand binding","volume":"9","author":"Pappas","year":"1995","journal-title":"FASEB J."},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib41","first-page":"307","article-title":"Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ER\u03b1 and ER\u03b2 expressed in Chinese hamster ovary cells","volume":"13","author":"Razandi","year":"1999","journal-title":"Mol. Endocrinol."},{"issue":"31","key":"10.1016\/j.semcdb.2021.05.032_bib42","doi-asserted-by":"crossref","first-page":"22278","DOI":"10.1074\/jbc.M611877200","article-title":"A conserved mechanism for steroid receptor translocation to the plasma membrane","volume":"282","author":"Pedram","year":"2007","journal-title":"J. Biol. Chem."},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-75631-3","article-title":"Transportin-2 plays a critical role in nucleocytoplasmic shuttling of oestrogen receptor-\u03b1","volume":"10","author":"Moriyama","year":"2020","journal-title":"Sci. Rep."},{"issue":"9","key":"10.1016\/j.semcdb.2021.05.032_bib44","doi-asserted-by":"crossref","first-page":"3615","DOI":"10.1073\/pnas.0611421104","article-title":"Male fetal germ cells are targets for androgens that physiologically inhibit their proliferation","volume":"104","author":"Merlet","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"18","key":"10.1016\/j.semcdb.2021.05.032_bib45","doi-asserted-by":"crossref","first-page":"2258","DOI":"10.4161\/cc.6.18.4654","article-title":"Development of fetal testicular cells in androgen receptor deficient mice","volume":"6","author":"Merlet","year":"2007","journal-title":"Cell Cycle"},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib46","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1177\/41.5.8468448","article-title":"Immunocytochemical localization of androgen receptor with polyclonal antibody in paraffin-embedded human tissues","volume":"41","author":"Kimura","year":"1993","journal-title":"J. Histochem. Cytochem."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib47","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1002\/(SICI)1097-0185(199607)245:3<509::AID-AR7>3.0.CO;2-M","article-title":"Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development","volume":"245","author":"Zhou","year":"1996","journal-title":"Anat. Rec."},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib48","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1046\/j.1439-0272.2002.00465.x","article-title":"Post-natal development of the rat testis: steroid hormone receptor distribution and extracellular matrix deposition","volume":"34","author":"Weber","year":"2002","journal-title":"Andrologia"},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib49","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1210\/endo.135.3.8070367","article-title":"Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens","volume":"135","author":"Bremner","year":"1994","journal-title":"Endocrinology"},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib50","first-page":"350","article-title":"Androgen receptor distribution in adult human testis","volume":"84","author":"Suarez-Quian","year":"1999","journal-title":"J. Clin. Endocrinol. Metab."},{"issue":"6","key":"10.1016\/j.semcdb.2021.05.032_bib51","doi-asserted-by":"crossref","first-page":"2405","DOI":"10.1210\/endo.142.6.8317","article-title":"Murine germ cells do not require functional androgen receptors to complete spermatogenesis following spermatogonial stem cell transplantation","volume":"142","author":"Johnston","year":"2001","journal-title":"Endocrinology"},{"issue":"50","key":"10.1016\/j.semcdb.2021.05.032_bib52","doi-asserted-by":"crossref","first-page":"18975","DOI":"10.1073\/pnas.0608565103","article-title":"Differential effects of spermatogenesis and fertility in mice lacking androgen receptor in individual testis cells","volume":"103","author":"Tsai","year":"2006","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"5536","key":"10.1016\/j.semcdb.2021.05.032_bib53","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1038\/258620a0","article-title":"Normal spermatozoa from androgen-resistant germ cells of chimaeric mice and the role of androgen in spermatogenesis","volume":"258","author":"Lyon","year":"1975","journal-title":"Nature"},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib54","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1242\/dev.00957","article-title":"Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids","volume":"131","author":"Holdcraft","year":"2004","journal-title":"Development"},{"key":"10.1016\/j.semcdb.2021.05.032_bib55","doi-asserted-by":"crossref","first-page":"4117","DOI":"10.1210\/en.2005-0300","article-title":"Development and function of the adult generation of Leydig cells in mice with Sertoli cell-selective (SCARKO) or total (ARKO) ablation of the androgen receptor","volume":"146","author":"De Gendt","year":"2005","journal-title":"Endocrinology"},{"issue":"11","key":"10.1016\/j.semcdb.2021.05.032_bib56","doi-asserted-by":"crossref","first-page":"14168","DOI":"10.1371\/journal.pone.0014168","article-title":"Selective ablation of the androgen receptor in mouse sertoli cells affects sertoli cell maturation, barrier formation and cytoskeletal development","volume":"5","author":"Willems","year":"2010","journal-title":"PLoS One"},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib57","doi-asserted-by":"crossref","first-page":"2307","DOI":"10.1210\/endo.134.5.8156934","article-title":"Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis","volume":"134","author":"Vornberger","year":"1994","journal-title":"Endocrinology"},{"issue":"9","key":"10.1016\/j.semcdb.2021.05.032_bib58","doi-asserted-by":"crossref","first-page":"3856","DOI":"10.1210\/endo.136.9.7649092","article-title":"Quantitative analysis of androgen receptor messenger ribonucleic acid in developing Leydig cells and Sertoli cells by in situ hybridization","volume":"136","author":"Shan","year":"1995","journal-title":"Endocrinology"},{"key":"10.1016\/j.semcdb.2021.05.032_bib59","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.steroids.2019.01.006","article-title":"Membrane androgen receptors (OXER1, GPRC6A and ZIP9) in prostate and breast cancer: a comparative study of their expression","volume":"142","author":"Kalyvianaki","year":"2019","journal-title":"Steroids"},{"issue":"21","key":"10.1016\/j.semcdb.2021.05.032_bib60","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21218275","article-title":"Crosstalk between androgen-ZIP9 signaling and notch pathway in rodent Sertoli cells","volume":"21","author":"Kaminska","year":"2020","journal-title":"Int. J. Mol. Sci."},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib61","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1111\/andr.12691","article-title":"Notch signaling regulates nuclear androgen receptor AR and membrane androgen receptor ZIP9 in mouse Sertoli cells","volume":"8","author":"Kami\u0144ska","year":"2020","journal-title":"Andrology"},{"issue":"18","key":"10.1016\/j.semcdb.2021.05.032_bib62","doi-asserted-by":"crossref","DOI":"10.3390\/ijms21186888","article-title":"Implication of membrane androgen receptor (ZIP9) in cell senescence in regressed testes of the bank vole","volume":"21","author":"Profaska-Szymik","year":"2020","journal-title":"Int. J. Mol. Sci."},{"issue":"15\u201316","key":"10.1016\/j.semcdb.2021.05.032_bib63","doi-asserted-by":"crossref","first-page":"577","DOI":"10.1016\/j.lfs.2011.05.017","article-title":"Rapid signaling responses in Sertoli cell membranes induced by follicle stimulating hormone and testosterone: calcium inflow and electrophysiological changes","volume":"89","author":"Loss","year":"2011","journal-title":"Life Sci."},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib64","doi-asserted-by":"crossref","first-page":"2052","DOI":"10.1210\/endo.136.5.7720654","article-title":"Androgens rapidly increase the cytosolic calcium concentration in Sertoli cells","volume":"136","author":"Gorczynska","year":"1995","journal-title":"Endocrinology"},{"key":"10.1016\/j.semcdb.2021.05.032_bib65","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1095\/biolreprod63.3.736","article-title":"Rapid androgen actions on calcium signaling in rat Sertoli cells and two human prostatic cell lines: similar biphasic responses between 1 picomolar and 100 nanomolar concentrations","volume":"63","author":"Lyng","year":"2000","journal-title":"Biol. Reprod."},{"issue":"10","key":"10.1016\/j.semcdb.2021.05.032_bib66","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1055\/s-2002-35426","article-title":"Rapid effect of testosterone on rat Sertoli cell membrane potential. Relationship with K+ATP channels","volume":"34","author":"Von Ledebur","year":"2002","journal-title":"Horm. Metab. Res."},{"issue":"8","key":"10.1016\/j.semcdb.2021.05.032_bib67","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1055\/s-2004-825753","article-title":"Testosterone modulates K(+)ATP channels in Sertoli cell membrane via the PLC-PIP2 pathway","volume":"36","author":"Loss","year":"2004","journal-title":"Horm. Metab. Res."},{"issue":"19","key":"10.1016\/j.semcdb.2021.05.032_bib68","doi-asserted-by":"crossref","first-page":"7156","DOI":"10.1158\/0008-5472.CAN-04-1121","article-title":"Changes in androgen receptor nongenotropic signaling correlate with transition of LNCaP cells to androgen independence","volume":"64","author":"Unni","year":"2004","journal-title":"Cancer Res."},{"key":"10.1016\/j.semcdb.2021.05.032_bib69","first-page":"719","article-title":"Nongenotropic, Sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity","volume":"104","author":"Kousteni","year":"2001","journal-title":"Cell"},{"key":"10.1016\/j.semcdb.2021.05.032_bib70","doi-asserted-by":"crossref","first-page":"5406","DOI":"10.1093\/emboj\/19.20.5406","article-title":"Steroid-induced androgen receptor-oestradial receptor beta-Src complex triggers prostate cancer cell proliferation","volume":"20","author":"Migliaccio","year":"2000","journal-title":"EMBO J."},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib71","doi-asserted-by":"crossref","first-page":"2066","DOI":"10.1210\/en.2006-1465","article-title":"Testosterone activates MAP kinase via Src kinase and the EGF receptor in Sertoli cells","volume":"148","author":"Cheng","year":"2007","journal-title":"Endocrinology"},{"issue":"2","key":"10.1016\/j.semcdb.2021.05.032_bib72","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1210\/me.2010-0030","article-title":"Regulation of Sertoli-germ cell adhesion and sperm release by FSH and nonclassical testosterone signaling","volume":"25","author":"Shupe","year":"2011","journal-title":"Mol. Endocrinol."},{"issue":"1","key":"10.1016\/j.semcdb.2021.05.032_bib73","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1095\/biolreprod.115.132068","article-title":"Mouse spermatogenesis requires classical and nonclassical testosterone signaling","volume":"94","author":"Toocheck","year":"2016","journal-title":"Biol. Reprod."},{"issue":"6","key":"10.1016\/j.semcdb.2021.05.032_bib74","doi-asserted-by":"crossref","first-page":"592","DOI":"10.2164\/jandrol.111.014266","article-title":"Androgen action in the epididymis","volume":"32","author":"Robaire","year":"2011","journal-title":"J. Androl."},{"key":"10.1016\/j.semcdb.2021.05.032_bib75","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3389\/fendo.2017.00002","article-title":"Non-Genomic actions of the androgen receptor in prostate cancer","volume":"8","author":"Leung","year":"2017","journal-title":"Front. Endocrinol."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib76","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.pharmthera.2013.07.003","article-title":"Androgen receptors in hormone-dependent and castration-resistant prostate cancer","volume":"140","author":"Shafi","year":"2013","journal-title":"Pharmacol. Ther."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib77","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0120783","article-title":"Restoration of spermatogenesis and male fertility using an androgen receptor transgene","volume":"10","author":"Walker","year":"2015","journal-title":"PLoS One"},{"key":"10.1016\/j.semcdb.2021.05.032_bib78","unstructured":"Cooke P., Walker W., Male fertility requires classical and nonclassical androgen signaling, Submitted."},{"issue":"10","key":"10.1016\/j.semcdb.2021.05.032_bib79","doi-asserted-by":"crossref","first-page":"4755","DOI":"10.1210\/en.2009-0416","article-title":"Sertoli cell androgen receptor DNA binding domain is essential for the completion of spermatogenesis","volume":"150","author":"Lim","year":"2009","journal-title":"Endocrinology"},{"issue":"12","key":"10.1016\/j.semcdb.2021.05.032_bib80","doi-asserted-by":"crossref","first-page":"4961","DOI":"10.1073\/pnas.0610814104","article-title":"Loss of androgen receptor binding to selective androgen response elements causes a reproductive phenotype in a knockin mouse model","volume":"104","author":"Schauwaers","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"issue":"1546","key":"10.1016\/j.semcdb.2021.05.032_bib81","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1098\/rstb.2009.0117","article-title":"Androgens and spermatogenesis: lessons from transgenic mouse models","volume":"365","author":"Verhoeven","year":"2010","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"10.1016\/j.semcdb.2021.05.032_bib82","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.semcdb.2014.02.012","article-title":"The regulation of spermatogenesis by androgens","volume":"30","author":"Smith","year":"2014","journal-title":"Semin. Cell Dev. Biol."},{"issue":"4","key":"10.1016\/j.semcdb.2021.05.032_bib83","doi-asserted-by":"crossref","DOI":"10.1080\/21688370.2016.1265042","article-title":"Transport of germ cells across the seminiferous epithelium during spermatogenesis-the involvement of both actin- and microtubule-based cytoskeletons","volume":"4","author":"Wen","year":"2016","journal-title":"Tissue Barriers"},{"issue":"4","key":"10.1016\/j.semcdb.2021.05.032_bib84","first-page":"1644","article-title":"Coordination of actin- and microtubule-based cytoskeletons supports transport of spermatids and residual bodies\/phagosomes during spermatogenesis in the rat testis","volume":"157","author":"Tang","year":"2016","journal-title":"Endocrinology"},{"issue":"9","key":"10.1016\/j.semcdb.2021.05.032_bib85","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.tem.2004.09.009","article-title":"Cell-cell interactions at the ectoplasmic specialization in the testis","volume":"15","author":"Mruk","year":"2004","journal-title":"Trends Endocrinol. Metab."},{"issue":"5","key":"10.1016\/j.semcdb.2021.05.032_bib86","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1210\/er.2003-0022","article-title":"Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis","volume":"25","author":"Mruk","year":"2004","journal-title":"Endocr. Rev."},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib87","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/0040-8166(77)90007-6","article-title":"Observations on rat Sertoli ectoplasmic (\u2019junctional\u2019) specializations in their association with germ cells of the rat testis","volume":"9","author":"Russell","year":"1977","journal-title":"Tissue Cell"},{"issue":"3","key":"10.1016\/j.semcdb.2021.05.032_bib88","doi-asserted-by":"crossref","first-page":"692","DOI":"10.1016\/j.bbamem.2007.11.006","article-title":"Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis","volume":"1778","author":"Wong","year":"2008","journal-title":"Biochim. Biophys. Acta"},{"issue":"14","key":"10.1016\/j.semcdb.2021.05.032_bib89","doi-asserted-by":"crossref","first-page":"18722","DOI":"10.18632\/oncotarget.7916","article-title":"Androgen receptor in Sertoli cells regulates DNA double-strand break repair and chromosomal synapsis of spermatocytes partially through intercellular EGF-EGFR signaling","volume":"7","author":"Chen","year":"2016","journal-title":"Oncotarget"}],"container-title":["Seminars in Cell &amp; Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1084952121001476?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S1084952121001476?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T17:06:54Z","timestamp":1761066414000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S1084952121001476"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1]]},"references-count":89,"alternative-id":["S1084952121001476"],"URL":"https:\/\/doi.org\/10.1016\/j.semcdb.2021.05.032","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.740285409.793587168","asserted-by":"object"}]},"ISSN":["1084-9521"],"issn-type":[{"value":"1084-9521","type":"print"}],"subject":[],"published":{"date-parts":[[2022,1]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Nonclassical androgen and estrogen signaling is essential for normal spermatogenesis","name":"articletitle","label":"Article Title"},{"value":"Seminars in Cell & Developmental Biology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.semcdb.2021.05.032","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2021 Published by Elsevier Ltd.","name":"copyright","label":"Copyright"}]}}