{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T14:20:08Z","timestamp":1784557208447,"version":"3.55.0"},"reference-count":44,"publisher":"Bioscientifica","issue":"2","content-domain":{"domain":["jme.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2018,8]]},"abstract":"<jats:p>\n                    Boars exhibit high concentrations of sulfonated estrogens (SE) mainly originating from the testicular-epididymal compartment. Intriguingly, in porcine Leydig cells, sulfonation of estrogens is colocalized with aromatase and steroid sulfatase (STS), indicating that\n                    <jats:italic>de novo<\/jats:italic>\n                    synthesis of unconjugated estrogens (UE), their sulfonation and hydrolysis of SE occur within the same cell type. So far in boars no plausible concept concerning the role of SE has been put forward. To obtain new information on SE formation and hydrolysis, the porcine testicular-epididymal compartment was screened for the expression of the estrogen-specific sulfotransferase SULT1E1 and STS applying real-time RT-qPCR, Western blot and immunohistochemistry. The epididymal head was identified as the major site of SULT1E1 expression, whereas in the testis, it was virtually undetectable. However, SE tissue concentrations are clearly consistent with the testis as the predominant site of estrogen sulfonation. Results from measurements of estrogen sulfotransferase activity indicate that in the epididymis, SULT1E1 is the relevant enzyme, whereas in the testis, estrogens are sulfonated by a different sulfotransferase with a considerably lower affinity. STS expression and activity was high in the testis (Leydig cells, rete testis epithelium) but also present throughout the epididymis. In the epididymis, SULT1E1 and STS were colocalized in the ductal epithelium, and there was evidence for their apocrine secretion into the ductal lumen. The results suggest that in porcine Leydig cells, SE may be produced as a reservoir to support the levels of bioactive UE via the sulfatase pathway during periods of low activity of the pulsatile testicular steroidogenesis.\n                  <\/jats:p>","DOI":"10.1530\/jme-17-0245","type":"journal-article","created":{"date-parts":[[2018,2,21]],"date-time":"2018-02-21T20:45:23Z","timestamp":1519245923000},"page":"M13-M25","update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-6","source":"Crossref","is-referenced-by-count":14,"title":["SULFATION PATHWAYS: Formation and hydrolysis of sulfonated estrogens in the porcine testis and epididymis"],"prefix":"10.1530","volume":"61","author":[{"given":"G","family":"Schuler","sequence":"first","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Y","family":"Dezhkam","sequence":"additional","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"L","family":"Tenbusch","sequence":"additional","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"MC","family":"Klymiuk","sequence":"additional","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B","family":"Zimmer","sequence":"additional","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"B","family":"Hoffmann","sequence":"additional","affiliation":[{"name":"Veterinary Clinic for Obstetrics, Gynecology and Andrology, Faculty of Veterinary Medicine, Justus-Liebig-University, Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"416","reference":[{"key":"ref121","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1055\/s-2007-1010866","article-title":"A study of the source of estradiol-17\u03b2 beta in the bull","volume":"20","year":"1988","journal-title":"Hormone and Metabolic Research"},{"key":"ref141","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0303-7207(01)00412-9","article-title":"Oestrogen, its receptors and function in the male reproductive tract \u2013 a review","volume":"178","year":"2001","journal-title":"Molecular and Cellular Endocrinology"},{"key":"ref371","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1677\/jme.1.01847","article-title":"Molecular cloning and regulation of porcine SULT2A1: relationship between SULT2A1 expression and sulfoconjugation of androstenone","volume":"36","year":"2006","journal-title":"Journal of Molecular Endocrinology"},{"key":"ref241","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1210\/er.2010-0013","article-title":"The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders","volume":"32","year":"2011","journal-title":"Endocrine Reviews"},{"key":"ref161","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/S0378-4320(99)00050-0","article-title":"Testicular endocrine function, seasonality and semen quality of the stallion","volume":"57","year":"1999","journal-title":"Animal Reproduction Science"},{"key":"ref231","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1016\/j.theriogenology.2008.10.015","article-title":"Reversible downregulation of endocrine and germinative testicular function (hormonal castration) in the dog with the GnRH-agonist azagly-nafarelin as a removable implant \u201cGonazon\u201d; a preclinical trial","volume":"71","year":"2009","journal-title":"Theriogenology"},{"key":"ref111","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1111\/j.1365-2605.2011.01203.x","article-title":"GirouardJFrenetteGSullivanR Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis of https org","year":"2011","journal-title":"International Journal Andrology"},{"key":"ref131","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1002\/mrd.90023","article-title":"Nature\u2019s ingenuity: bypassing the classical secretory route via apocrine secretion","volume":"63","year":"2002","journal-title":"Molecular Reproduction and Development"},{"key":"ref281","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1439-0531.2007.00983.x","article-title":"Expression and activity of steroid sulphatase in the boar testis","volume":"44","year":"2009","journal-title":"Reproduction in Domestic Animals"},{"key":"ref341","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jsbmb.2017.10.006","article-title":"Simultaneous profiles of sulfonated androgens, sulfonated estrogens and sulfonated progestogens in postpubertal boars (Sus scrofa domestica) measured by LC\u2013MS\/MS","volume":"179","year":"2018","journal-title":"Journal of Steroid Biochemistry and Molecular Biology"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"995","DOI":"10.1152\/physrev.00018.2016","article-title":"Estrogens in male physiology","volume":"97","year":"2017","journal-title":"Physiological Reviews"},{"key":"ref171","first-page":"717","article-title":"Investigations into the course of progesterone-, oestrogen- and eCG-concentrations during normal and impaired pregnancy in the mare","volume":"32","year":"1996","journal-title":"Reproduction in Domestic Animals"},{"key":"ref291","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1111\/j.1749-6632.2009.04113.x","article-title":"Estrogen sulfotransferases in breast and endometrial cancers","volume":"1155","year":"2009","journal-title":"Annals of the New York Academy of Sciences"},{"key":"ref321","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1210\/jcem-59-1-29","article-title":"In situ estrogen production via the estrone sulfatase pathway in breast tumors: relative importance versus the aromatase pathway","volume":"59","year":"1984","journal-title":"Journal of Clinical Endocrinology and Metabolism"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1530\/acta.0.0940404","article-title":"Oestrogens, compared to other steroids of testicular origin, in blood plasma of boars","volume":"94","year":"1980","journal-title":"Acta Endocrinologica"},{"key":"ref301","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1095\/biolreprod28.3.727","article-title":"Estrogen and androgen production by purified Leydig cells of mature boars","volume":"28","year":"1983","journal-title":"Biology of Reproduction"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1515\/bchm3.1989.370.2.1093","article-title":"Human placental sterylsulfatase: immunocytochemical and biochemical localization","volume":"370","year":"1989","journal-title":"Biological Chemistry Hoppe-Seyler"},{"key":"ref181","first-page":"296","article-title":"Determination of free and conjugated oestrogens in peripheral blood plasma, feces and urine of cattle throughout pregnancy","volume":"105","year":"1997","journal-title":"Experimental and Clinical Endocrinology and Diabetes"},{"key":"ref251","doi-asserted-by":"crossref","first-page":"3361","DOI":"10.1210\/en.2002-220329","article-title":"Regulation of microsomal P450, redox partner proteins, and steroidogenesis in the developing testes of the neonatal pig","volume":"143","year":"2002","journal-title":"Endocrinology"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1515\/bchm3.1986.367.2.1223","article-title":"Human placental steryl-sulfatase. Enzyme purification, production of antisera, and immunoblotting reactions with normal and sulfatase-deficient placentas","volume":"367","year":"1986","journal-title":"Biological Chemistry Hoppe-Seyler"},{"key":"ref431","doi-asserted-by":"crossref","first-page":"10888","DOI":"10.1074\/jbc.273.18.10888","article-title":"Sulfuryl transfer: the catalytic mechanism of human estrogen sulfotransferase","volume":"273","year":"1998","journal-title":"Journal of Biological Chemistry"},{"key":"ref81","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1749-6632.1995.tb17372.x","article-title":"Human dehydroepiandrosterone sulfotransferase. Purification, molecular cloning, and characterization","volume":"774","year":"1995b","journal-title":"Annals of the New York Academy of Sciences"},{"key":"ref361","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1677\/joe.0.0960127","article-title":"Transport of free and conjugated steroids from the boar testis in lymph, venous blood and rete testis fluid","volume":"96","year":"1983","journal-title":"Journal of Endocrinology"},{"key":"ref411","doi-asserted-by":"crossref","first-page":"3144","DOI":"10.1210\/endo.143.8.8943","article-title":"Estrogen sulfotransferase: discrete and androgen-dependent expression in the male reproductive tract and demonstration of an in vivo function in the mouse epididymis","volume":"143","year":"2002","journal-title":"Endocrinology"},{"key":"ref71","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/0960-0760(95)00015-R","article-title":"Bacterial expression and characterization of a cDNA for human liver estrogen sulfotransferase","volume":"52","year":"1995a","journal-title":"Journal of Steroid Biochemistry and Molecular Biology"},{"key":"ref91","first-page":"51","article-title":"Cytochrome P450 aromatase in the testis of immature and mature pigs","volume":"1","year":"2001","journal-title":"Reproductive Biology"},{"key":"ref351","first-page":"57","article-title":"Gonadotrophin and steroid concentrations in jugular and testicular venous plasma in stallions before and after GnRH injection","volume":"44","year":"1991","journal-title":"Journal of Reproduction and Fertility Supplement"},{"key":"ref421","doi-asserted-by":"crossref","first-page":"880","DOI":"10.2164\/jandrol.106.000448","article-title":"Effects of estradiol infusion in GnRH immunized boars on spermatogenesis","volume":"27","year":"2006","journal-title":"Journal of Andrology"},{"key":"ref401","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/0378-4320(80)90032-9","article-title":"Developmental patterns of plasma dehydroepiandrosterone sulfate and testosterone in male pigs","volume":"3","year":"1980","journal-title":"Animal Reproduction Science"},{"key":"ref191","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1055\/s-2001-16350","article-title":"Investigations on the activity of bovine placental oestrogen sulfotransferase and -sulfatase from midgestation to parturition","volume":"109","year":"2001","journal-title":"Experimental and Clinical Endocrinology and Diabetes"},{"key":"ref01","doi-asserted-by":"crossref","first-page":"552","DOI":"10.2164\/jandrol.05195","article-title":"Reducing estrogen synthesis in developing boars increases testis size and total sperm production","volume":"27","year":"2006","journal-title":"Journal of Andrology"},{"key":"ref151","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/0022-4731(89)90211-2","article-title":"Partial characterization of steroid sulfohydrolase and steroid sulfotransferase activities in purified porcine Leydig cells","volume":"32","year":"1989","journal-title":"Journal of Steroid Biochemistry"},{"key":"ref391","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1530\/REP-13-0058","article-title":"prostasomes liposomes their roles in mammalian male reproductive physiology https org","author":"SullivanRSaezF","year":"2013","journal-title":"Reproduction"},{"key":"ref271","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1111\/j.1439-0531.2005.00586.x","article-title":"Expression of oestrogen receptors alpha and beta and of aromatase in the testis of immature and mature boars","volume":"40","year":"2005","journal-title":"Reproduction in Domestic Animals"},{"key":"ref311","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1210\/er.2004-0003","article-title":"Steroid sulfatase: molecular biology, regulation, and inhibition","volume":"26","year":"2005","journal-title":"Endocrine Reviews"},{"key":"ref381","doi-asserted-by":"crossref","first-page":"5006","DOI":"10.1210\/endo.138.11.5512","article-title":"Cellular localization and regulation of expression of testicular estrogen sulfotransferase","volume":"138","year":"1997","journal-title":"Endocrinology"},{"key":"ref331","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1530\/REP-14-0193","article-title":"Free and sulfated steroids secretion in postpubertal boars (Sus scrofa domestica)","volume":"148","year":"2014","journal-title":"Reproduction"},{"key":"ref101","doi-asserted-by":"crossref","first-page":"580","DOI":"10.2164\/jandrol.108.006668","article-title":"Estrogen sulfotransferase is highly expressed along the bovine epididymis and is secreted into the intraluminal environment","volume":"30","year":"2009","journal-title":"Journal of Andrology"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/S0940-9602(99)80020-X","article-title":"Apocrine secretion \u2013 fact or artifact?","volume":"181","year":"1999","journal-title":"Annals of Anatomy"},{"key":"ref211","doi-asserted-by":"crossref","first-page":"e0126848","DOI":"10.1371\/journal.pone.0126848","article-title":"Development of apical blebbing in the boar epididymis","volume":"10","year":"2015","journal-title":"PLoS ONE"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.mce.2012.11.011","article-title":"Increased testicular Sertoli cell population induced by an estrogen receptor antagonist","volume":"366","year":"2013","journal-title":"Molecular and Cellular Endocrinology"},{"key":"ref201","first-page":"274","article-title":"Testicular steroid hormone secretion in the boar and expression of testicular and epididymal steroid sulphatase and estrogen sulphotransferase activity","volume":"118","year":"2010","journal-title":"Experimental and Clinical Endocrinology and Diabetes"},{"key":"ref261","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1210\/er.2015-1036","article-title":"The regulation of steroid action by sulfation and desulfation","volume":"36","year":"2015","journal-title":"Endocrine Reviews"},{"key":"ref221","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1007\/s00335-002-2318-4","article-title":"Molecular cloning and functional analysis of porcine SULT1A1 gene and its variant: a single mutation SULT1A1 causes a significant decrease in sulfation activity","volume":"15","year":"2004","journal-title":"Mammalian Genome"}],"container-title":["Journal of Molecular 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