{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T10:18:35Z","timestamp":1790849915635,"version":"4.1.0"},"reference-count":103,"publisher":"Elsevier BV","license":[{"start":{"date-parts":[[2021,3,1]],"date-time":"2021-03-01T00:00:00Z","timestamp":1614556800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2021,3,1]],"date-time":"2021-03-01T00:00:00Z","timestamp":1614556800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"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":["Differentiation"],"published-print":{"date-parts":[[2021,3]]},"DOI":"10.1016\/j.diff.2020.11.002","type":"journal-article","created":{"date-parts":[[2020,12,9]],"date-time":"2020-12-09T16:15:14Z","timestamp":1607530514000},"page":"24-33","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":21,"special_numbering":"C","title":["Role of nuclear and membrane estrogen signaling pathways in the male and female reproductive tract"],"prefix":"10.1016","volume":"118","author":[{"given":"Paul S.","family":"Cooke","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana M.","family":"Mesa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vijay K.","family":"Sirohi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ellis R.","family":"Levin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.diff.2020.11.002_bib1","doi-asserted-by":"crossref","first-page":"2143","DOI":"10.1161\/ATVBAHA.120.314159","article-title":"Mutation of arginine 264 on ER\u03b1 (Estrogen receptor alpha) selectively abrogates the rapid signaling of estradiol in the endothelium without altering fertility","volume":"40","author":"Adlanmerini","year":"2020","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib2","doi-asserted-by":"crossref","first-page":"E283","DOI":"10.1073\/pnas.1322057111","article-title":"Mutation of the palmitoylation site of estrogen receptor \u03b1 in vivo reveals tissue-specific roles for membrane versus nuclear actions","volume":"111","author":"Adlanmerini","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"issue":"11","key":"10.1016\/j.diff.2020.11.002_bib3","doi-asserted-by":"crossref","DOI":"10.1210\/endocr\/bqaa175","article-title":"Mechanisms by which membrane and nuclear ER alpha inhibit adipogenesis in cells isolated from female mice","volume":"161","author":"Ahluwalia","year":"2020","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib4","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."},{"key":"10.1016\/j.diff.2020.11.002_bib5","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1152\/physrev.00024.2016","article-title":"Membrane and nuclear estrogen receptor alpha actions: from tissue specificity to medical implications","volume":"97","author":"Arnal","year":"2017","journal-title":"Physiol. Rev."},{"key":"10.1016\/j.diff.2020.11.002_bib6","doi-asserted-by":"crossref","first-page":"3426","DOI":"10.1016\/j.jmb.2014.07.025","article-title":"Histone methyltransferase EZH2 is transcriptionally induced by estradiol as well as estrogenic endocrine disruptors bisphenol-A and diethylstilbestrol","volume":"426","author":"Bhan","year":"2014","journal-title":"J. Mol. Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib7","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1210\/endo-119-1-390","article-title":"Estrogen stimulation of deoxyribonucleic acid synthesis in uterine epithelial cells which lack estrogen receptors","volume":"119","author":"Bigsby","year":"1986","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib8","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/0090-8258(83)90111-7","article-title":"Two pathogenetic types of endometrial carcinoma","volume":"15","author":"Bokhman","year":"1983","journal-title":"Gynecol. Oncol."},{"key":"10.1016\/j.diff.2020.11.002_bib9","doi-asserted-by":"crossref","first-page":"2679","DOI":"10.1113\/JP270502","article-title":"Membrane glucocorticoid receptors are localised in the extracellular matrix and signal through the MAPK pathway in mammalian skeletal muscle fibres","volume":"593","author":"Boncompagni","year":"2015","journal-title":"J. Physiol."},{"key":"10.1016\/j.diff.2020.11.002_bib10","doi-asserted-by":"crossref","first-page":"286","DOI":"10.1016\/j.steroids.2005.09.018","article-title":"Plasma membrane requirements for 1\u03b1, 25 (OH) 2D3 dependent PKC signaling in chondrocytes and osteoblasts","volume":"71","author":"Boyan","year":"2006","journal-title":"Steroids"},{"key":"10.1016\/j.diff.2020.11.002_bib11","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1210\/me.2009-0438","article-title":"Xenoestrogen-induced regulation of EZH2 and histone methylation via estrogen receptor signaling to PI3K\/AKT","volume":"24","author":"Bredfeldt","year":"2010","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib12","doi-asserted-by":"crossref","first-page":"1491","DOI":"10.1007\/s00204-012-0868-5","article-title":"Estrogen receptors and human disease: an update","volume":"86","author":"Burns","year":"2012","journal-title":"Arch. Toxicol."},{"key":"10.1016\/j.diff.2020.11.002_bib13","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1007\/BF01506919","article-title":"Uber progynon ein krytallisiertes weibliches exualhormon","volume":"17","author":"Butenandt","year":"1929","journal-title":"Naturwissenschaften"},{"key":"10.1016\/j.diff.2020.11.002_bib14","doi-asserted-by":"crossref","first-page":"63","DOI":"10.3389\/fendo.2019.00063","article-title":"Non-genomic actions of thyroid hormones regulate the growth and angiogenesis of T cell lymphomas","volume":"10","author":"Cayrol","year":"2019","journal-title":"Front. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib15","doi-asserted-by":"crossref","first-page":"35505","DOI":"10.1074\/jbc.274.50.35505","article-title":"1, 25-Dihydroxyvitamin D3 stimulates activator protein-1-dependent Caco-2 cell differentiation","volume":"274","author":"Chen","year":"1999","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.diff.2020.11.002_bib16","doi-asserted-by":"crossref","first-page":"2066","DOI":"10.1210\/en.2006-1465","article-title":"Testosterone activates mitogen-activated protein kinase via Src kinase and the epidermal growth factor receptor in sertoli cells","volume":"148","author":"Cheng","year":"2007","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib17","first-page":"640","article-title":"Conditional ablation of progesterone receptor membrane component 2 causes female premature reproductive senescence","volume":"158","author":"Clark","year":"2017","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib18","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."},{"key":"10.1016\/j.diff.2020.11.002_bib19","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"},{"key":"10.1016\/j.diff.2020.11.002_bib20","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"},{"key":"10.1016\/j.diff.2020.11.002_bib21","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1016\/j.ajpath.2019.02.016","article-title":"Enhancer of Zeste Polycomb repressive complex 2 subunit is required for uterine epithelial integrity","volume":"189","author":"Fang","year":"2019","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.diff.2020.11.002_bib22","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. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib23","doi-asserted-by":"crossref","DOI":"10.1242\/dev.182303","article-title":"Membrane expression of the estrogen receptor ER\u03b1 is required for intercellular communications in the mammary epithelium","volume":"147","author":"Gagniac","year":"2020","journal-title":"Development"},{"key":"10.1016\/j.diff.2020.11.002_bib24","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1158\/1541-7786.MCR-11-0605","article-title":"Environmental estrogens differentially engage the histone methyltransferase EZH2 to increase risk of uterine tumorigenesis","volume":"10","author":"Greathouse","year":"2012","journal-title":"Mol. Canc. Res."},{"key":"10.1016\/j.diff.2020.11.002_bib25","doi-asserted-by":"crossref","first-page":"29473","DOI":"10.1038\/srep29473","article-title":"The role of membrane ER\u03b1 signaling in bone and other major estrogen responsive tissues","volume":"6","author":"Gustafsson","year":"2016","journal-title":"Sci. Rep."},{"key":"10.1016\/j.diff.2020.11.002_bib26","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1016\/j.beem.2015.04.001","article-title":"Overlapping nongenomic and genomic actions of thyroid hormone and steroids","volume":"29","author":"Hammes","year":"2015","journal-title":"Best Pract. Res. Clin. Endocrinol. Metabol."},{"key":"10.1016\/j.diff.2020.11.002_bib27","doi-asserted-by":"crossref","first-page":"12729","DOI":"10.1073\/pnas.97.23.12729","article-title":"Increased adipose tissue in male and female estrogen receptor-\u03b1 knockout mice","volume":"97","author":"Heine","year":"2000","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib28","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"},{"key":"10.1016\/j.diff.2020.11.002_bib29","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."},{"key":"10.1016\/j.diff.2020.11.002_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.diff.2020.11.002_bib31","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1210\/er.2018-00087","article-title":"Estrogen receptors: new directions in the new millennium","volume":"39","author":"Hewitt","year":"2018","journal-title":"Endocr. Rev."},{"key":"10.1016\/j.diff.2020.11.002_bib32","doi-asserted-by":"crossref","first-page":"14104","DOI":"10.1073\/pnas.0601600103","article-title":"Rapid nongenomic actions of thyroid hormone","volume":"103","author":"Hiroi","year":"2006","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib33","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/S0021-9258(18)73338-3","article-title":"The isolation of \u03b1-dihydrotheelin from human placenta","volume":"133","author":"Huffman","year":"1940","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.diff.2020.11.002_bib34","doi-asserted-by":"crossref","first-page":"948","DOI":"10.1016\/S0022-5347(02)80307-X","article-title":"Studies on prostatic cancer. I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate","volume":"167","author":"Huggins","year":"1941","journal-title":"J. Urol."},{"key":"10.1016\/j.diff.2020.11.002_bib35","doi-asserted-by":"crossref","first-page":"2660","DOI":"10.1210\/me.2004-0116","article-title":"The vitamin D receptor is present in caveolae-enriched plasma membranes and binds 1\u03b1, 25 (OH) 2-vitamin D3 in vivo and in vitro","volume":"18","author":"Huhtakangas","year":"2004","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib36","first-page":"109","article-title":"Developmental pattern of estrogen receptor expression in male mouse genitalorgans","volume":"3","author":"Iguchi","year":"1991","journal-title":"Mol. Androl."},{"key":"10.1016\/j.diff.2020.11.002_bib37","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1126\/science.158.3800.529-c","article-title":"Estrogen-binding substances of target tissues","volume":"158","author":"Jensen","year":"1967","journal-title":"Science"},{"key":"10.1016\/j.diff.2020.11.002_bib38","series-title":"Fate of Steroid Estrogens in Target Tissues Biological Activities of Steroids in Relation to Cancer","author":"Jensen","year":"1960"},{"key":"10.1016\/j.diff.2020.11.002_bib39","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/0039-128X(69)90053-1","article-title":"Estrogen-binding substances of target tissues","volume":"13","author":"Jensen","year":"1969","journal-title":"Steroids"},{"key":"10.1016\/j.diff.2020.11.002_bib40","series-title":"Proceedings of the 1972 Laurentian Hormone Conference","first-page":"1","article-title":"Studies on sex differentiation in mammals","author":"Jost","year":"1973"},{"key":"10.1016\/j.diff.2020.11.002_bib41","doi-asserted-by":"crossref","DOI":"10.1126\/scisignal.2004911","article-title":"Nongenomic thyroid hormone signaling occurs through a plasma membrane\u2013localized receptor","volume":"7","author":"Kalyanaraman","year":"2014","journal-title":"Sci. Signal."},{"key":"10.1016\/j.diff.2020.11.002_bib42","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1016\/S0140-6736(02)08152-7","article-title":"Hypospadias in sons of women exposed to diethylstilbestrol in utero: a cohort study","volume":"359","author":"Klip","year":"2002","journal-title":"Lancet"},{"key":"10.1016\/j.diff.2020.11.002_bib43","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. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib44","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1210\/me.2002-0368","article-title":"Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor","volume":"17","author":"Levin","year":"2003","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib45","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."},{"key":"10.1016\/j.diff.2020.11.002_bib46","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. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib47","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1095\/biolreprod.107.063909","article-title":"17Beta-Estradiol induces the translocation of the estrogen receptors ESR1 and ESR2 to the cell membrane, MAPK3\/1 phosphorylation and proliferation of cultured immature rat sertoli cells","volume":"78","author":"Lucas","year":"2008","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.diff.2020.11.002_bib48","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2020.00148","article-title":"Does GPER really function as a G protein-coupled estrogen receptor in vivo?","volume":"11","author":"Luo","year":"2020","journal-title":"Front. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib49","doi-asserted-by":"crossref","first-page":"5743","DOI":"10.1073\/pnas.1700367114","article-title":"Regulation of the sperm calcium channel CatSper by endogenous steroids and plant triterpenoids","volume":"114","author":"Mannowetz","year":"2017","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib50","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.1210\/en.2016-1081","article-title":"Conditional ablation of progesterone receptor membrane component 1 results in subfertility in the female and development of endometrial cysts","volume":"157","author":"McCallum","year":"2016","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib51","first-page":"S1","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"},{"key":"10.1016\/j.diff.2020.11.002_bib52","doi-asserted-by":"crossref","first-page":"6856","DOI":"10.1158\/0008-5472.CAN-13-1197","article-title":"D538G mutation in estrogen receptor-\u03b1: a novel mechanism for acquired endocrine resistance in breast cancer","volume":"73","author":"Merenbakh-Lamin","year":"2013","journal-title":"Canc. Res."},{"key":"10.1016\/j.diff.2020.11.002_bib53","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1152\/physiolgenomics.00098.2019","article-title":"Mice lacking uterine enhancer of zeste homolog 2 have transcriptomic changes associated with uterine epithelial proliferation","volume":"52","author":"Mesa","year":"2020","journal-title":"Physiol. Genom."},{"key":"10.1016\/j.diff.2020.11.002_bib54","doi-asserted-by":"crossref","first-page":"165","DOI":"10.3389\/fendo.2017.00165","article-title":"Rodent models of non-classical progesterone action regulating ovulation","volume":"8","author":"Mittelman-Smith","year":"2017","journal-title":"Front. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib55","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":"78","key":"10.1016\/j.diff.2020.11.002_bib56","article-title":"Neonatal uterine and vaginal cell proliferation and adenogenesis are independent of estrogen receptor 1 (ESR1) in the mouse","volume":"92","author":"Nanjappa","year":"2015","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.diff.2020.11.002_bib57","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1093\/biolre\/ioz090","article-title":"Mice lacking membrane estrogen receptor 1 are protected from reproductive pathologies resulting from developmental estrogen exposure","volume":"101","author":"Nanjappa","year":"2019","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.diff.2020.11.002_bib58","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1093\/biolre\/ioz097","article-title":"The histone methyltransferase EZH2 is required for normal uterine development and function in mice","volume":"101","author":"Nanjappa","year":"2019","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.diff.2020.11.002_bib59","doi-asserted-by":"crossref","first-page":"7392","DOI":"10.1073\/pnas.0402207101","article-title":"Ribozyme knockdown functionally links a 1, 25 (OH) 2D3 membrane binding protein (1, 25D3-MARRS) and phosphate uptake in intestinal cells","volume":"101","author":"Nemere","year":"2004","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib60","doi-asserted-by":"crossref","first-page":"2882","DOI":"10.1096\/fj.201902521R","article-title":"Glucocorticoids rapidly activate cAMP production via G(\u03b1s) to initiate non-genomic signaling that contributes to one-third of their canonical genomic effects","volume":"34","author":"Nu\u00f1ez","year":"2020","journal-title":"Faseb. J."},{"key":"10.1016\/j.diff.2020.11.002_bib61","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.1210\/me.2012-1191","article-title":"Estrogen modulates metabolic pathway adaptation to available glucose in breast cancer cells","volume":"26","author":"O'Mahony","year":"2012","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib62","doi-asserted-by":"crossref","first-page":"1527","DOI":"10.1073\/pnas.60.4.1527","article-title":"Studies on the mechanism of estrogen-mediated tissue differentiation: regulation of nuclear transcription and induction of new RNA species","volume":"60","author":"O'Malley","year":"1968","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib63","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1095\/biolreprod.108.071175","article-title":"GPR30 does not mediate estrogenic responses in reproductive organs in mice","volume":"80","author":"Otto","year":"2009","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.diff.2020.11.002_bib64","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"},{"key":"10.1016\/j.diff.2020.11.002_bib65","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."},{"key":"10.1016\/j.diff.2020.11.002_bib66","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1096\/fj.15-274878","article-title":"Membrane and nuclear estrogen receptor a collaborate to suppress adipogenesis but not triglyceride content","volume":"30","author":"Pedram","year":"2016","journal-title":"Faseb. J."},{"key":"10.1016\/j.diff.2020.11.002_bib67","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1091\/mbc.e11-07-0638","article-title":"DHHC-7 and -21 are palmitoylacyltransferases for sex steroid receptors","volume":"23","author":"Pedram","year":"2012","journal-title":"Mol. Biol. Cell"},{"key":"10.1016\/j.diff.2020.11.002_bib68","doi-asserted-by":"crossref","first-page":"1996","DOI":"10.1210\/me.2005-0525","article-title":"Nature of functional estrogen receptors at the plasma membrane","volume":"20","author":"Pedram","year":"2006","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib69","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"},{"key":"10.1016\/j.diff.2020.11.002_bib70","doi-asserted-by":"crossref","DOI":"10.1126\/scisignal.2004013","article-title":"Estrogen reduces lipid content in the liver exclusively from membrane receptor signaling","volume":"6","author":"Pedram","year":"2013","journal-title":"Sci. Signal."},{"key":"10.1016\/j.diff.2020.11.002_bib71","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."},{"key":"10.1016\/j.diff.2020.11.002_bib72","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"},{"key":"10.1016\/j.diff.2020.11.002_bib73","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"},{"key":"10.1016\/j.diff.2020.11.002_bib74","doi-asserted-by":"crossref","first-page":"684","DOI":"10.1177\/1933719111431000","article-title":"G protein-coupled estrogen receptor (GPER) expression in normal and abnormal endometrium","volume":"19","author":"Plante","year":"2012","journal-title":"Reprod. Sci."},{"key":"10.1016\/j.diff.2020.11.002_bib75","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1146\/annurev.physiol.70.113006.100518","article-title":"Estrogen signaling through the transmembrane G protein\u2013coupled receptor GPR30","volume":"70","author":"Prossnitz","year":"2008","journal-title":"Annu. Rev. Physiol."},{"key":"10.1016\/j.diff.2020.11.002_bib76","doi-asserted-by":"crossref","first-page":"168","DOI":"10.3389\/fnins.2013.00168","article-title":"PGRMC1 and PGRMC2 in uterine physiology and disease","volume":"7","author":"Pru","year":"2013","journal-title":"Front. Neurosci."},{"key":"10.1016\/j.diff.2020.11.002_bib77","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."},{"key":"10.1016\/j.diff.2020.11.002_bib78","doi-asserted-by":"crossref","first-page":"1633","DOI":"10.1128\/MCB.23.5.1633-1646.2003","article-title":"Identification of a structural determinant necessary for the localization and function of estrogen receptor \u03b1 at the plasma membrane","volume":"23","author":"Razandi","year":"2003","journal-title":"Mol. Cell Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib79","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1210\/mend.16.1.0757","article-title":"ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions","volume":"16","author":"Razandi","year":"2002","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib80","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."},{"key":"10.1016\/j.diff.2020.11.002_bib81","doi-asserted-by":"crossref","first-page":"3249","DOI":"10.1128\/MCB.01354-09","article-title":"Heat shock protein 27 is required for sex steroid receptor trafficking to and functioning at the plasma membrane","volume":"30","author":"Razandi","year":"2010","journal-title":"Mol. Cell Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib82","doi-asserted-by":"crossref","first-page":"2701","DOI":"10.1074\/jbc.M205692200","article-title":"Proximal events in signaling by plasma membrane estrogen receptors","volume":"278","author":"Razandi","year":"2003","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.diff.2020.11.002_bib83","doi-asserted-by":"crossref","DOI":"10.3389\/fendo.2017.00016","article-title":"New insights in glucocorticoid receptor signaling \u2013 more than just a ligand binding receptor","volume":"8","author":"Scheschowitsch","year":"2017","journal-title":"Front. Endocrinol."},{"key":"10.1016\/j.diff.2020.11.002_bib84","doi-asserted-by":"crossref","first-page":"2775","DOI":"10.1210\/endo.143.7.8889","article-title":"1alpha,25-dihydroxyvitamin D(3) and 24R,25-dihydroxyvitamin D(3) modulate growth plate chondrocyte physiology via protein kinase C-dependent phosphorylation of extracellular signal-regulated kinase 1\/2 mitogen-activated protein kinase","volume":"143","author":"Schwartz","year":"2002","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib85","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"},{"key":"10.1016\/j.diff.2020.11.002_bib86","doi-asserted-by":"crossref","DOI":"10.1126\/scitranslmed.aau5956","article-title":"Preclinical efficacy of the GPER-selective agonist G-1 in mouse models of obesity and diabetes","volume":"12","author":"Sharma","year":"2020","journal-title":"Sci. Transl. Med."},{"key":"10.1016\/j.diff.2020.11.002_bib87","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1016\/0140-6736(93)90953-E","article-title":"Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract?","volume":"341","author":"Sharpe","year":"1993","journal-title":"Lancet"},{"key":"10.1016\/j.diff.2020.11.002_bib88","doi-asserted-by":"crossref","first-page":"5105","DOI":"10.1128\/MCB.00162-07","article-title":"Integration of estrogen and Wnt signaling circuits by the polycomb group protein EZH2 in breast cancer cells","volume":"27","author":"Shi","year":"2007","journal-title":"Mol. Cell Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib89","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."},{"key":"10.1016\/j.diff.2020.11.002_bib90","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."},{"key":"10.1016\/j.diff.2020.11.002_bib91","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/ncprheum0898","article-title":"Genomic and nongenomic effects of glucocorticoids","volume":"4","author":"Stahn","year":"2008","journal-title":"Nat. Clin. Pract. Rheumatol."},{"key":"10.1016\/j.diff.2020.11.002_bib92","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1073\/pnas.58.4.1711","article-title":"Adenosine 3', 5'-monophosphate in rat uterus: acute elevation by estrogen","volume":"58","author":"Szego","year":"1967","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib93","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.fertnstert.2012.09.011","article-title":"Differential expression of G-protein-coupled estrogen receptor-30 in human myometrial and uterine leiomyoma smooth muscle","volume":"99","author":"Tian","year":"2013","journal-title":"Fertil. Steril."},{"key":"10.1016\/j.diff.2020.11.002_bib94","doi-asserted-by":"crossref","first-page":"1574","DOI":"10.1073\/pnas.55.6.1574","article-title":"A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization","volume":"55","author":"Toft","year":"1966","journal-title":"Proc. Natl. Acad. Sci. U. S. A"},{"key":"10.1016\/j.diff.2020.11.002_bib95","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."},{"key":"10.1016\/j.diff.2020.11.002_bib96","doi-asserted-by":"crossref","DOI":"10.1155\/2020\/2196024","article-title":"Expression of membrane progesterone receptors in eutopic and ectopic endometrium of women with endometriosis","author":"Vazquez-Martinez","year":"2020","journal-title":"BioMed Res. Int."},{"key":"10.1016\/j.diff.2020.11.002_bib97","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0021-9258(18)76871-3","article-title":"The preparation of the crystalline follicular ovarian hormone: theelin","volume":"87","author":"Veler","year":"1930","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.diff.2020.11.002_bib98","doi-asserted-by":"crossref","first-page":"2533","DOI":"10.1210\/en.2015-1994","article-title":"Role of ER\u03b1 in the effect of estradiol on cancellous and cortical femoral bone in growing female mice","volume":"157","author":"Vinel","year":"2016","journal-title":"Endocrinology"},{"key":"10.1016\/j.diff.2020.11.002_bib99","series-title":"Non-classical and Classical Testosterone Signaling Are Required for Fully Efficient Spermatogenesis and Development of the Prostate and Epididymis","author":"Walker","year":"2020"},{"key":"10.1016\/j.diff.2020.11.002_bib100","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1098\/rstb.2009.0258","article-title":"Non-classical actions of testosterone and spermatogenesis","volume":"365","author":"Walker","year":"2010","journal-title":"Phil. Trans. Biol. Sci."},{"key":"10.1016\/j.diff.2020.11.002_bib101","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.jsbmb.2017.01.016","article-title":"Rapid actions of aldosterone revisited: receptors in the limelight","volume":"176","author":"Wehling","year":"2018","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"10.1016\/j.diff.2020.11.002_bib102","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1385\/ENDO:12:3:207","article-title":"Normal development of thymus in male and female mice requires estrogen\/estrogen receptor-\u03b1 signaling pathway","volume":"12","author":"Yellayi","year":"2000","journal-title":"Endocrine"},{"key":"10.1016\/j.diff.2020.11.002_bib103","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1042\/CS20160114","article-title":"GPER\u2013novel membrane oestrogen receptor","volume":"130","author":"Zimmerman","year":"2016","journal-title":"Clin. Sci."}],"container-title":["Differentiation"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0301468120300748?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0301468120300748?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,10,4]],"date-time":"2025-10-04T08:07:01Z","timestamp":1759565221000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0301468120300748"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3]]},"references-count":103,"alternative-id":["S0301468120300748"],"URL":"https:\/\/doi.org\/10.1016\/j.diff.2020.11.002","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.739210338.793581797","asserted-by":"object"}]},"ISSN":["0301-4681"],"issn-type":[{"value":"0301-4681","type":"print"}],"subject":[],"published":{"date-parts":[[2021,3]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Role of nuclear and membrane estrogen signaling pathways in the male and female reproductive tract","name":"articletitle","label":"Article Title"},{"value":"Differentiation","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.diff.2020.11.002","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2020 Published by Elsevier B.V. on behalf of International Society of Differentiation.","name":"copyright","label":"Copyright"}]}}