{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T15:07:55Z","timestamp":1790435275781,"version":"4.1.0"},"reference-count":53,"publisher":"CSIRO Publishing","issue":"12","license":[{"start":{"date-parts":[[2025,5,27]],"date-time":"2025-05-27T00:00:00Z","timestamp":1748304000000},"content-version":"vor","delay-in-days":3613,"URL":"https:\/\/doi.org\/10.1071\/journalslicense"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2016,10,11]]},"abstract":"<jats:p>The aim of the present study was to characterise receptors for LH and FSH (LHR and FSHR, respectively) and aromatase in epididymal and testicular tissue from stallions of different ages (prepubertal, young, mature and old). Gene and protein expression were assessed by real-time quantitative polymerase chain reaction (real-time qPCR), immunohistochemistry and multiple immunofluorescence labelling. There were no differences in LHR mRNA expression in epididymal and testicular parenchyma in stallions of different age. In contrast, expression of FSHR and CYP19A1 in caput, corpus and cauda epididymis and in testicular parenchyma increased with age (P &amp;lt; 0.001). Immunolabelling for LHR, FSHR and aromatase was influenced by puberty. In postpubertal stallions, positive staining for LHR and aromatase was detected in Leydig cells, whereas protein expression of FSHR was present in Sertoli cells and primary spermatocytes. In prepubertal colts, staining for LHR, FSHR and aromatase was detected in seminiferous tubules. In epididymal tissue, aromatase was present in the cauda epididymis only, regardless of age. In conclusion, the results highlight the significance of gonadotropin action and oestrogen production for the maturation of male reproductive tissue in the horse. The presence of FSHR in the seminiferous tubules suggests effects of FSH on spermatogenesis in this species. The importance of oestrogen production for maintenance of testicular function in stallions was confirmed.<\/jats:p>","DOI":"10.1071\/rd15027","type":"journal-article","created":{"date-parts":[[2015,7,6]],"date-time":"2015-07-06T00:16:57Z","timestamp":1436141817000},"page":"2016-2026","source":"Crossref","is-referenced-by-count":13,"title":["Effect of stallion age on the expression of LH and FSH receptors and aromatase P450 in equine male reproductive tissues"],"prefix":"10.1071","volume":"28","author":[{"given":"Carlos Vladimir","family":"Herrera-Luna","sequence":"first","affiliation":[{"name":"ACentre for Artificial Insemination and Embryo Transfer, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria."},{"name":"CAnimal Health Department, Faculty of Veterinary Medicine and Animal Science, National University of Colombia, Carrera 45, 26-85, Bogota, Colombia."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dragos","family":"Scarlet","sequence":"additional","affiliation":[{"name":"ACentre for Artificial Insemination and Embryo Transfer, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ingrid","family":"Walter","sequence":"additional","affiliation":[{"name":"BInstitute of Anatomy, Histology and Embryology, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Aurich","sequence":"additional","affiliation":[{"name":"ACentre for Artificial Insemination and Embryo Transfer, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria."},{"name":"DCorresponding author. Email: christine.aurich@vetmeduni.ac.at"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"67","published-online":{"date-parts":[[2015,7,6]]},"reference":[{"key":"2025102820190888900_R1","doi-asserted-by":"publisher","first-page":"291","DOI":"10.1677\/JME-08-0107","article-title":"Effects of FSH on testicular mRNA transcript levels in the hypogonadal mouse.","volume":"42","author":"Abel","year":"2009","journal-title":"J. Mol. Endocrinol."},{"key":"2025102820190888900_R2","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1530\/REP-10-0499","article-title":"Expression of steroidogenic enzymes during equine testicular development.","volume":"141","author":"Almeida","year":"2011","journal-title":"Reproduction"},{"key":"2025102820190888900_R3","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1210\/EDRV.23.2.0462","article-title":"The lutropin\/choriogonadotropin receptor, a 2002 perspective.","volume":"23","author":"Ascoli","year":"2002","journal-title":"Endocr. Rev."},{"key":"2025102820190888900_R4","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1530\/REP.1.00768","article-title":"Postnatal changes in testicular gonadotropin receptors, serum gonadotropin, and testosterone concentrations and functional development of the testes in bulls.","volume":"132","author":"Bagu","year":"2006","journal-title":"Reproduction"},{"issue":"Suppl. 1","key":"2025102820190888900_R5","first-page":"43","article-title":"Hormonal status of male reproductive system: androgens and estrogens in the testis and epididymis. In vivo and in vitro approaches.","volume":"6","author":"Bilinska","year":"2006","journal-title":"Reprod. Biol."},{"key":"2025102820190888900_R6","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1007\/BF00331379","article-title":"Localization of follicle-stimulating hormone (FSH) immunoreactivity and hormone receptor mRNA in testicular tissue of infertile men.","volume":"278","author":"B\u00f6ckers","year":"1994","journal-title":"Cell Tissue Res."},{"key":"2025102820190888900_R7","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1054\/TICE.2001.0186","article-title":"Immunolocalization of cytochrome P450 aromatase in rat testis during postnatal development.","volume":"33","author":"Carpino","year":"2001","journal-title":"Tissue Cell"},{"key":"2025102820190888900_R8","doi-asserted-by":"publisher","first-page":"1517","DOI":"10.1098\/RSTB.2009.0235","article-title":"Oestrogens and spermatogenesis.","volume":"365","author":"Carreau","year":"2010","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"2025102820190888900_R9","first-page":"23","article-title":"The promoter(s) of the aromatase gene in male testicular cells.","volume":"4","author":"Carreau","year":"2004","journal-title":"Reprod. Biol."},{"key":"2025102820190888900_R10","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1262\/JRD.2011-025","article-title":"Circulating pituitary and gonadal hormones in spring-born thoroughbred fillies and colts from birth to puberty.","volume":"58","author":"Dhakal","year":"2012","journal-title":"J. Reprod. Dev."},{"key":"2025102820190888900_R11","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1002\/j.1939-4640.1995.tb01725.x","article-title":"Effects of lipoprotein, equine luteinizing hormone, equine follicle-stimulating hormone, and equine prolactin on equine testicular steroidogenesis in vitro.","volume":"16","author":"Eisenhauer","year":"1995","journal-title":"J. Androl."},{"key":"2025102820190888900_R12","doi-asserted-by":"publisher","first-page":"1376","DOI":"10.1016\/J.THERIOGENOLOGY.2005.08.013","article-title":"Aromatization and antioxidant capacity in the testis of seasonally breeding bank voles: Effects of LH, PRL and IGF-I.","volume":"65","author":"Gancarczyk","year":"2006","journal-title":"Theriogenology"},{"key":"2025102820190888900_R13","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1016\/S0303-7207(01)00409-9","article-title":"Regulation of the aromatase gene expression in mature rat Leydig cells.","volume":"178","author":"Genissel","year":"2001","journal-title":"Mol. Cell. Endocrinol."},{"key":"2025102820190888900_R14","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1139\/Y05-127","article-title":"G-Protein-coupled receptors signalling at the cell nucleus: an emerging paradigm.","volume":"84","author":"Gobeil","year":"2006","journal-title":"Can. J. Physiol. Pharmacol."},{"key":"2025102820190888900_R15","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/0960-0760(95)00049-6","article-title":"The molecular biology of the FSH receptor.","volume":"53","author":"Griswold","year":"1995","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"2025102820190888900_R16","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1016\/S0303-7207(96)03949-4","article-title":"Functional and clinical consequences of mutations in the FSH receptor.","volume":"125","author":"Gromoll","year":"1996","journal-title":"Mol. Cell. Endocrinol."},{"key":"2025102820190888900_R17","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1210\/MEND-5-5-670","article-title":"Expression of follicle-stimulating hormone receptor mRNA in rat testes and Sertoli cells.","volume":"5","author":"Heckert","year":"1991","journal-title":"Mol. Endocrinol."},{"key":"2025102820190888900_R18","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1016\/J.DOMANIEND.2005.03.002","article-title":"Expression of aromatase and oestrogen receptors in reproductive tissues of the stallion and a single cryptorchid visualised by means of immunohistochemistry.","volume":"29","author":"Hejmej","year":"2005","journal-title":"Domest. Anim. Endocrinol."},{"key":"2025102820190888900_R19","doi-asserted-by":"publisher","first-page":"928","DOI":"10.1111\/J.1439-0531.2012.01993.X","article-title":"Gene expression of ACTH, glucocorticoid receptors, 11\u00dfHSD enzymes, LH-, FSH-, GH receptors and aromatase in equine epididymal and testicular tissue.","volume":"47","author":"Herrera-Luna","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"2025102820190888900_R20","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1111\/J.1439-0531.2012.02137.X","article-title":"Expression of 11\u00df-hydroxysteroid dehydrogenase type 1 and glucocorticoid receptors in reproductive tissue of male horses at different stages of sexual maturity.","volume":"48","author":"Herrera-Luna","year":"2013","journal-title":"Reprod. Domest. Anim."},{"key":"2025102820190888900_R21","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/S0093-691X(03)00237-1","article-title":"Immunocytochemical localization of cytochrome P450 aromatase in the testis of prepubertal, pubertal, and postpubertal horses.","volume":"61","author":"Hess","year":"2004","journal-title":"Theriogenology"},{"key":"2025102820190888900_R22","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1016\/J.ANIREPROSCI.2005.06.014","article-title":"A comparison of the effects of equine luteinizing hormone (eLH), equine growth hormone (eGH) and human recombinant insulin-like growth factor (hrIGF-I) on steroid production in cultured equine Leydig cells during sexual maturation.","volume":"89","author":"Hess","year":"2005","journal-title":"Anim. Reprod. Sci."},{"key":"2025102820190888900_R23","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/J.ANIREPROSCI.2008.11.011","article-title":"Suppression of testicular function and sexual behavior by vaccination against GnRH (Equity) in the adult stallion.","volume":"115","author":"Janett","year":"2009","journal-title":"Anim. Reprod. Sci."},{"key":"2025102820190888900_R24","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1095\/BIOLREPROD24.3.703","article-title":"Age-related changes in the Leydig cell population, seminiferous tubules, and sperm production in stallions.","volume":"24","author":"Johnson","year":"1981","journal-title":"Biol. Reprod."},{"key":"2025102820190888900_R25","first-page":"87","article-title":"Effect of age and season on the establishment of spermatogenesis in the horse.","volume":"44","author":"Johnson","year":"1991","journal-title":"J. Reprod. Fertil. Suppl."},{"key":"2025102820190888900_R26","doi-asserted-by":"publisher","first-page":"1199","DOI":"10.1016\/S0093-691X(97)00353-1","article-title":"Factors affecting spermatogenesis in the stallion.","volume":"48","author":"Johnson","year":"1997","journal-title":"Theriogenology"},{"key":"2025102820190888900_R27","doi-asserted-by":"publisher","first-page":"1147","DOI":"10.1016\/J.THERIOGENOLOGY.2008.06.037","article-title":"Embryo transfer induces a subclinical endometritis in recipient mares which can be prevented by treatment with non-steroid anti-inflammatory drugs.","volume":"70","author":"Koblischke","year":"2008","journal-title":"Theriogenology"},{"key":"2025102820190888900_R28","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/S0303-7207(01)00435-X","article-title":"Aromatase gene expression in the stallion.","volume":"178","author":"Lemazurier","year":"2001","journal-title":"Mol. Cell. Endocrinol."},{"key":"2025102820190888900_R29","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1006\/GCEN.2001.7747","article-title":"Free and conjugated estrogens and androgens in stallion semen.","volume":"125","author":"Lemazurier","year":"2002","journal-title":"Gen. Comp. Endocrinol."},{"key":"2025102820190888900_R30","doi-asserted-by":"publisher","first-page":"3973","DOI":"10.1210\/JCEM.83.11.5177","article-title":"Recombinant human follicle-stimulating hormone administration increases testosterone production in men, possibly by a Sertoli cell-secreted nonsteroid factor.","volume":"83","author":"Levalle","year":"1998","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"2025102820190888900_R31","doi-asserted-by":"publisher","first-page":"402","DOI":"10.1006\/METH.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(t)) method.","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"2025102820190888900_R32","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1016\/S0960-0760(02)00041-9","article-title":"Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction.","volume":"80","author":"Luconi","year":"2002","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"2025102820190888900_R33","doi-asserted-by":"publisher","first-page":"145","DOI":"10.1095\/BIOLREPROD34.1.145","article-title":"Changes in Leydig cell ultrastructure and function during pubertal development in the boar.","volume":"34","author":"Lunstra","year":"1986","journal-title":"Biol. Reprod."},{"key":"2025102820190888900_R34","doi-asserted-by":"publisher","first-page":"1721","DOI":"10.4238\/2012.JUNE.29.4","article-title":"Luteinizing hormone receptor splicing variants in bovine Leydig cells.","volume":"11","author":"Ma","year":"2012","journal-title":"Genet. Mol. Res."},{"key":"2025102820190888900_R35","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1046\/J.1365-2265.1999.00846.X","article-title":"Role of FSH in the regulation of spermatogenesis: clinical aspects.","volume":"51","author":"Nieschlag","year":"1999","journal-title":"Clin. Endocrinol. (Oxf.)"},{"key":"2025102820190888900_R36","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1210\/edrv.22.3.0431","article-title":"Estrogen and spermatogenesis.","volume":"22","author":"O\u2019Donnell","year":"2001","journal-title":"Endocr. Rev."},{"key":"2025102820190888900_R37","doi-asserted-by":"publisher","first-page":"278","DOI":"10.1053\/J.CTEP.2007.09.006","article-title":"Pathogenesis, diagnosis, and management of testicular degeneration in stallions.","volume":"6","author":"Oristaglio Turner","year":"2007","journal-title":"Clin. Tech. Equine Pract."},{"key":"2025102820190888900_R38","doi-asserted-by":"publisher","first-page":"517","DOI":"10.1677\/JOE.0.1350517","article-title":"Effects of FSH on Leydig cell morphology and function in the hypogonadal mouse.","volume":"135","author":"O\u2019Shaughnessy","year":"1992","journal-title":"J. Endocrinol."},{"key":"2025102820190888900_R39","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/S0303-7207(96)03957-3","article-title":"Expression of follicle stimulating hormone-receptor mRNA during gonadal development.","volume":"125","author":"O\u2019Shaughnessy","year":"1996","journal-title":"Mol. Cell. Endocrinol."},{"key":"2025102820190888900_R40","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1186\/1471-2164-9-246","article-title":"Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate.","volume":"9","author":"Pascal","year":"2008","journal-title":"BMC Genomics"},{"key":"2025102820190888900_R41","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/J.ANIREPROSCI.2011.03.007","article-title":"Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri- and post-pubertal stallion testis.","volume":"125","author":"Pearl","year":"2011","journal-title":"Anim. Reprod. Sci."},{"key":"2025102820190888900_R42","doi-asserted-by":"publisher","first-page":"777","DOI":"10.1016\/J.THERIOGENOLOGY.2012.03.025","article-title":"Expression of luteinizing hormone and follicle-stimulating hormone receptor in the dog prostate.","volume":"78","author":"Ponglowhapan","year":"2012","journal-title":"Theriogenology"},{"key":"2025102820190888900_R43","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/S0378-4320(97)00045-6","article-title":"Estrogen concentrations in semen of the stallion.","volume":"48","author":"Raeside","year":"1997","journal-title":"Anim. Reprod. Sci."},{"key":"2025102820190888900_R44","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1016\/J.ANIREPROSCI.2008.05.004","article-title":"Regulation of testicular function in the stallion: an intricate network of endocrine, paracrine and autocrine systems.","volume":"107","author":"Roser","year":"2008","journal-title":"Anim. Reprod. Sci."},{"key":"2025102820190888900_R45","doi-asserted-by":"publisher","first-page":"1615","DOI":"10.1210\/ENDO-120-4-1615","article-title":"Hormonal control of pubertal spermatogenesis.","volume":"120","author":"Russell","year":"1987","journal-title":"Endocrinology"},{"key":"2025102820190888900_R46","doi-asserted-by":"publisher","DOI":"10.1071\/RD14392","article-title":"Expression and immunolocalisation of follicle-stimulating hormone receptors in gonads of newborn and adult female horses.","author":"Scarlet","year":"2015","journal-title":"Reprod. Fertil. Dev."},{"key":"2025102820190888900_R47","doi-asserted-by":"publisher","first-page":"375","DOI":"10.1016\/0960-0760(94)00181-K","article-title":"Regulation of Sertoli cell aromatase activity by cell density and prolonged stimulation with FSH, EGF, insulin and IGF-I at different moments of pubertal development.","volume":"52","author":"Schteingart","year":"1995","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"2025102820190888900_R48","doi-asserted-by":"crossref","first-page":"2179","DOI":"10.1210\/endo.137.5.8612566","article-title":"Specific immunoneutralization of FSH leads to apoptotic cell death of the pachytene spermatocytes and spermatogonial cells in the rat.","volume":"137","author":"Shetty","year":"1996","journal-title":"Endocrinology"},{"key":"2025102820190888900_R49","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1177\/002215540305100306","article-title":"Immunolocalization of aromatase in stallion Leydig cells and seminiferous tubules.","volume":"51","author":"Sipahutar","year":"2003","journal-title":"J. Histochem. Cytochem."},{"key":"2025102820190888900_R50","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1530\/REP.1.00358","article-title":"FSH and testosterone signaling in Sertoli cells.","volume":"130","author":"Walker","year":"2005","journal-title":"Reproduction"},{"key":"2025102820190888900_R51","doi-asserted-by":"crossref","first-page":"2206","DOI":"10.1210\/endo.134.5.8156923","article-title":"Ontogeny of luteinizing hormone receptor gene expression in the rat testis.","volume":"134","author":"Zhang","year":"1994","journal-title":"Endocrinology"},{"key":"2025102820190888900_R52","doi-asserted-by":"publisher","first-page":"1453","DOI":"10.1210\/EN.2003-1049","article-title":"Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice.","volume":"145","author":"Zhang","year":"2004","journal-title":"Endocrinology"},{"key":"2025102820190888900_R53","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1006\/SCDB.1998.0253","article-title":"Spermatogenesis: its regulation by testosterone and FSH.","volume":"9","author":"Zirkin","year":"1998","journal-title":"Semin. Cell Dev. Biol."}],"container-title":["Reproduction, Fertility and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/28\/12\/2016\/317937\/rd15027.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/28\/12\/2016\/317937\/rd15027.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,29]],"date-time":"2025-10-29T00:19:13Z","timestamp":1761697153000},"score":1,"resource":{"primary":{"URL":"https:\/\/connectsci.au\/rd\/article\/28\/12\/2016\/50806\/Effect-of-stallion-age-on-the-expression-of-LH-and"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,7,6]]},"references-count":53,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2016,10,11]]}},"URL":"https:\/\/doi.org\/10.1071\/rd15027","relation":{},"ISSN":["1031-3613","1448-5990"],"issn-type":[{"value":"1031-3613","type":"print"},{"value":"1448-5990","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,7,6]]}}}