Effect of stallion age on the expression of LH and FSH receptors and aromatase P450 in equine male reproductive tissues
Carlos Vladimir Herrera-Luna A C , Dragos Scarlet A , Ingrid Walter B and Christine Aurich A D
+ Author Affiliations
- Author Affiliations
A Centre for Artificial Insemination and Embryo Transfer, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria.
B Institute of Anatomy, Histology and Embryology, University for Veterinary Sciences Vienna, Veterinaerplatz 1, 1210 Vienna, Austria.
C Animal Health Department, Faculty of Veterinary Medicine and Animal Science, National University of Colombia, Carrera 45, 26-85, Bogota, Colombia.
D Corresponding author. Email: christine.aurich@vetmeduni.ac.at
Reproduction, Fertility and Development 28(12) 2016-2026 https://doi.org/10.1071/RD15027
Submitted: 20 January 2015 Accepted: 6 June 2015 Published: 6 July 2015
Abstract
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 < 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.
Additional keywords: epididymis, horse, testis.
References
Abel, M. H., Baban, D., Lee, S., Charlton, H. M., and O’Shaughnessy, P. J. (2009). Effects of FSH on testicular mRNA transcript levels in the hypogonadal mouse. J. Mol. Endocrinol. 42, 291–303.| Effects of FSH on testicular mRNA transcript levels in the hypogonadal mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFSjs7s%3D&md5=620a7b6979e907d9aed6af5565e7fee6CAS | 19136570PubMed |
Almeida, J., Conley, A. J., Mathewson, L., and Ball, B. A. (2011). Expression of steroidogenic enzymes during equine testicular development. Reproduction 141, 841–848.
| Expression of steroidogenic enzymes during equine testicular development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVCktbg%3D&md5=814f703454d93fa127b8a51151522f1cCAS | 21300693PubMed |
Ascoli, M., Fanelli, F., and Segaloff, D. L. (2002). The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr. Rev. 23, 141–174.
| The lutropin/choriogonadotropin receptor, a 2002 perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWjtr4%3D&md5=fa25dba1bd344b17888b6f1e6e59c333CAS | 11943741PubMed |
Bagu, E. T., Cook, S., Gratton, C. L., and Rawlings, N. C. (2006). Postnatal changes in testicular gonadotropin receptors, serum gonadotropin, and testosterone concentrations and functional development of the testes in bulls. Reproduction 132, 403–411.
| Postnatal changes in testicular gonadotropin receptors, serum gonadotropin, and testosterone concentrations and functional development of the testes in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt7%2FO&md5=9781248889e3e28cdeebcabf6c355bb8CAS | 16940281PubMed |
Bilińska, B., Wiszniewska, B., Kosiniak-Kamysz, K., Kotula-Balak, M., Gancarczyk, M., Hejmej, A., Sadowska, J., Marchlewicz, M., Kolasa, A., and Wenda-Rózewicka, L. (2006). Hormonal status of male reproductive system: androgens and estrogens in the testis and epididymis. In vivo and in vitro approaches. Reprod. Biol. 6, 43–58.
| 16967089PubMed |
Böckers, T. M., Nieschlag, E., Kreutz, M. R., and Bergmann, M. (1994). Localization of follicle-stimulating hormone (FSH) immunoreactivity and hormone receptor mRNA in testicular tissue of infertile men. Cell Tissue Res. 278, 595–600.
| Localization of follicle-stimulating hormone (FSH) immunoreactivity and hormone receptor mRNA in testicular tissue of infertile men.Crossref | GoogleScholarGoogle Scholar | 7850869PubMed |
Carpino, A., Pezzi, V., Rago, V., Bilinska, B., and Ando, S. (2001). Immunolocalization of cytochrome P450 aromatase in rat testis during postnatal development. Tissue Cell 33, 349–353.
| Immunolocalization of cytochrome P450 aromatase in rat testis during postnatal development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvnvVGluw%3D%3D&md5=fc79b73252464057eb6cf74ae412d137CAS | 11521950PubMed |
Carreau, S., and Hess, R. A. (2010). Oestrogens and spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1517–1535.
| Oestrogens and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVaisr3K&md5=c0e8e3aca08f21f04cb2be752791a18aCAS | 20403867PubMed |
Carreau, S., Bourguiba, S., Lambard, S., Silandre, D., and Delalande, C. (2004). The promoter(s) of the aromatase gene in male testicular cells. Reprod. Biol. 4, 23–34.
| 15094793PubMed |
Dhakal, P., Hirama, A., Nambo, Y., Harada, T., Sato, F., Nagaoka, K., Watanabe, G., and Taya, K. (2012). Circulating pituitary and gonadal hormones in spring-born thoroughbred fillies and colts from birth to puberty. J. Reprod. Dev. 58, 522–530.
| Circulating pituitary and gonadal hormones in spring-born thoroughbred fillies and colts from birth to puberty.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVClt7rJ&md5=516136569d788f0e9455ac3cc146a4e1CAS | 22673032PubMed |
Eisenhauer, K. M., and Roser, J. F. (1995). Effects of lipoprotein, equine luteinizing hormone, equine follicle-stimulating hormone, and equine prolactin on equine testicular steroidogenesis in vitro. J. Androl. 16, 18–27.
| 1:CAS:528:DyaK2MXkvF2ltLY%3D&md5=e8d5ccb944dc671eed0803608f91ca7aCAS | 7768749PubMed |
Gancarczyk, M., Kuklinska, M., Sadowska, J., Strzezek, J., and Bilinska, B. (2006). Aromatization and antioxidant capacity in the testis of seasonally breeding bank voles: Effects of LH, PRL and IGF-I. Theriogenology 65, 1376–1391.
| Aromatization and antioxidant capacity in the testis of seasonally breeding bank voles: Effects of LH, PRL and IGF-I.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Srsb8%3D&md5=2343d06afe2b81e591d108d75aaebb98CAS | 16226304PubMed |
Genissel, C., and Carreau, S. (2001). Regulation of the aromatase gene expression in mature rat Leydig cells. Mol. Cell. Endocrinol. 178, 141–146.
| Regulation of the aromatase gene expression in mature rat Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlWntb4%3D&md5=0ae92bf9587051e733d67834c49afc47CAS | 11403903PubMed |
Gobeil, F., Fortier, A., Zhu, T., Bossolasco, M., Leduc, M., Grandbois, M., Heveker, N., Bkaily, G., Chemtob, S., and Barbaz, D. (2006). G-Protein-coupled receptors signalling at the cell nucleus: an emerging paradigm. Can. J. Physiol. Pharmacol. 84, 287–297.
| G-Protein-coupled receptors signalling at the cell nucleus: an emerging paradigm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVOltLc%3D&md5=ebaa7fa204779225d435e88af69e95a6CAS | 16902576PubMed |
Griswold, M. D., Heckert, L., and Linder, C. (1995). The molecular biology of the FSH receptor. J. Steroid Biochem. Mol. Biol. 53, 215–218.
| The molecular biology of the FSH receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnt1GnsbY%3D&md5=41df4b172b242de9a97e207cca246a7bCAS | 7626457PubMed |
Gromoll, J., Simoni, M., Nordhoff, V., Behre, H. M., de Geyter, C., and Nieschlag, E. (1996). Functional and clinical consequences of mutations in the FSH receptor. Mol. Cell. Endocrinol. 125, 177–182.
| Functional and clinical consequences of mutations in the FSH receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSrsQ%3D%3D&md5=f7cf435140ee31a9876186eb65d04b72CAS | 9027356PubMed |
Heckert, L. L., and Griswold, M. D. (1991). Expression of follicle-stimulating hormone receptor mRNA in rat testes and Sertoli cells. Mol. Endocrinol. 5, 670–677.
| Expression of follicle-stimulating hormone receptor mRNA in rat testes and Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkt1altLY%3D&md5=68980e15a3ae8cd0d986931295fee6adCAS | 2072927PubMed |
Hejmej, A., Gorazd, M., Kosiniak-Kamysz, K., Wiszniewska, B., Sadowska, J., and Bilinska, B. (2005). Expression of aromatase and oestrogen receptors in reproductive tissues of the stallion and a single cryptorchid visualised by means of immunohistochemistry. Domest. Anim. Endocrinol. 29, 534–547.
| Expression of aromatase and oestrogen receptors in reproductive tissues of the stallion and a single cryptorchid visualised by means of immunohistochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpvV2msb4%3D&md5=ae75525adcb4518215005919363a14d3CAS | 16153502PubMed |
Herrera-Luna, C. V., Budik, S., and Aurich, C. (2012). Gene expression of ACTH, glucocorticoid receptors, 11βHSD enzymes, LH-, FSH-, GH receptors and aromatase in equine epididymal and testicular tissue. Reprod. Domest. Anim. 47, 928–935.
| Gene expression of ACTH, glucocorticoid receptors, 11βHSD enzymes, LH-, FSH-, GH receptors and aromatase in equine epididymal and testicular tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFKgt70%3D&md5=a6ba3caa79e23691f55d6b9ff9e5edc6CAS | 22335522PubMed |
Herrera-Luna, C. V., Budik, S., Helmreich, M., Walter, I., and Aurich, C. (2013). Expression of 11β-hydroxysteroid dehydrogenase type 1 and glucocorticoid receptors in reproductive tissue of male horses at different stages of sexual maturity. Reprod. Domest. Anim. 48, 231–239.
| Expression of 11β-hydroxysteroid dehydrogenase type 1 and glucocorticoid receptors in reproductive tissue of male horses at different stages of sexual maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlWqtbk%3D&md5=60abda100811f47459e4a0516f9cd0bcCAS | 22734562PubMed |
Hess, M. F., and Roser, J. F. (2004). Immunocytochemical localization of cytochrome P450 aromatase in the testis of prepubertal, pubertal, and postpubertal horses. Theriogenology 61, 293–299.
| Immunocytochemical localization of cytochrome P450 aromatase in the testis of prepubertal, pubertal, and postpubertal horses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXps1Oks7k%3D&md5=1530884d2422f737aba763a71263faf4CAS | 14662129PubMed |
Hess, M. F., and Roser, J. F. (2005). 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. Anim. Reprod. Sci. 89, 7–19.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVart7%2FK&md5=ee71dec4030a4ac7ac001cd1a1b7d1d7CAS | 16085376PubMed |
Janett, F., Stump, R., Burger, D., and Thun, R. (2009). Suppression of testicular function and sexual behavior by vaccination against GnRH (Equity) in the adult stallion. Anim. Reprod. Sci. 115, 88–102.
| Suppression of testicular function and sexual behavior by vaccination against GnRH (Equity) in the adult stallion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2hsrk%3D&md5=eb409ab585eb2e4cf33e4889ad5bde92CAS | 19128902PubMed |
Johnson, L., and Neaves, W. B. (1981). Age-related changes in the Leydig cell population, seminiferous tubules, and sperm production in stallions. Biol. Reprod. 24, 703–712.
| Age-related changes in the Leydig cell population, seminiferous tubules, and sperm production in stallions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3gvVGmsw%3D%3D&md5=8373d67e2f85582dc92fadc8360624b9CAS | 7236827PubMed |
Johnson, L., Varner, D. D., and Thompson, D. L. (1991). Effect of age and season on the establishment of spermatogenesis in the horse. J. Reprod. Fertil. Suppl. 44, 87–97.
| 1:STN:280:DyaK387nslaktA%3D%3D&md5=5f3d424a84dedd2cffa2c759cc2242e1CAS | 1795306PubMed |
Johnson, L., Blanchard, T. L., Varner, D. D., and Scrutchfield, W. L. (1997). Factors affecting spermatogenesis in the stallion. Theriogenology 48, 1199–1216.
| Factors affecting spermatogenesis in the stallion.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28zgtV2lsg%3D%3D&md5=ed1d2ec276dacbc3c0dfedce745a43afCAS | 16728209PubMed |
Koblischke, P., Kindahl, H., Budik, S., Aurich, J., Palm, F., Walter, I., Kolodziejek, J., Nowotny, N., Hoppen, H.-O., and Aurich, C. (2008). Embryo transfer induces a subclinical endometritis in recipient mares which can be prevented by treatment with non-steroid anti-inflammatory drugs. Theriogenology 70, 1147–1158.
| Embryo transfer induces a subclinical endometritis in recipient mares which can be prevented by treatment with non-steroid anti-inflammatory drugs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFajurnL&md5=92d39ae0ade5b5883f3322c3393bbc87CAS | 18657311PubMed |
Lemazurier, E., Sourdaine, P., Nativelle, C., Plainfosse, B., and Seralini, G. (2001). Aromatase gene expression in the stallion. Mol. Cell. Endocrinol. 178, 133–139.
| Aromatase gene expression in the stallion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlWntLc%3D&md5=2882759a1310428563d6ac85e2ad6dc9CAS | 11403902PubMed |
Lemazurier, E., Moslemi, S., Sourdaine, P., Desjardins, I., Plainfosse, B., and Seralini, G.-E. (2002). Free and conjugated estrogens and androgens in stallion semen. Gen. Comp. Endocrinol. 125, 272–282.
| Free and conjugated estrogens and androgens in stallion semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhs1yrt74%3D&md5=53f565487765857d673fe96877311a97CAS | 11884073PubMed |
Levalle, O., Zylbersztein, C., Aszpis, S., Aquilano, D., Terradas, C., Colombani, M., Aranda, C., and Scaglia, H. (1998). Recombinant human follicle-stimulating hormone administration increases testosterone production in men, possibly by a Sertoli cell-secreted nonsteroid factor. J. Clin. Endocrinol. Metab. 83, 3973–3976.
| Recombinant human follicle-stimulating hormone administration increases testosterone production in men, possibly by a Sertoli cell-secreted nonsteroid factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntlOit7Y%3D&md5=d0cf039afe2cb9df2f65ce6d0e67b452CAS | 9814477PubMed |
Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(t)) method. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(t)) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=6db539426b70529f14f65734e4c1d0f6CAS | 11846609PubMed |
Luconi, M., Forti, G., and Baldi, E. (2002). Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction. J. Steroid Biochem. Mol. Biol. 80, 369–381.
| Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Cru7Y%3D&md5=53fee0a0dc6184321f5f85029efc899aCAS | 11983484PubMed |
Lunstra, D. D., Ford, J. J., Christenson, R. K., and Allrich, R. D. (1986). Changes in Leydig cell ultrastructure and function during pubertal development in the boar. Biol. Reprod. 34, 145–158.
| Changes in Leydig cell ultrastructure and function during pubertal development in the boar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xht1egur0%3D&md5=ace34b9bfddc44471e175d7c943cfe76CAS | 3006806PubMed |
Ma, T. H., Xiong, Q. H., Yuan, B., Jiang, H., Gao, Y., Xu, J. B., Liu, S. Y., Ding, Y., Zhang, G. L., Zhao, Y. M., and Zhang, J. B. (2012). Luteinizing hormone receptor splicing variants in bovine Leydig cells. Genet. Mol. Res. 11, 1721–1730.
| Luteinizing hormone receptor splicing variants in bovine Leydig cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVarsr%2FN&md5=05d97b62be21727801f1dc455738a969CAS | 22843048PubMed |
Nieschlag, E., Simoni, M., Gromoll, J., and Weinbauer, G. F. (1999). Role of FSH in the regulation of spermatogenesis: clinical aspects. Clin. Endocrinol. (Oxf.) 51, 139–146.
| Role of FSH in the regulation of spermatogenesis: clinical aspects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFGlsrw%3D&md5=59db1d55d08fe191b03b053816e99344CAS | 10468980PubMed |
O’Donnell, L., Robertson, K. M., Jones, M. E., and Simpson, E. R. (2001). Estrogen and spermatogenesis. Endocr. Rev. 22, 289–318.
| 1:CAS:528:DC%2BD3MXltVOgurw%3D&md5=cc9a092b816805bef572fe7f4f589116CAS | 11399746PubMed |
Oristaglio Turner, R. M. (2007). Pathogenesis, diagnosis, and management of testicular degeneration in stallions. Clin. Tech. Equine Pract. 6, 278–284.
| Pathogenesis, diagnosis, and management of testicular degeneration in stallions.Crossref | GoogleScholarGoogle Scholar |
O’Shaughnessy, P. J., Bennett, M. K., Scott, I. S., and Charlton, H. M. (1992). Effects of FSH on Leydig cell morphology and function in the hypogonadal mouse. J. Endocrinol. 135, 517–525.
| Effects of FSH on Leydig cell morphology and function in the hypogonadal mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjtlajtg%3D%3D&md5=c193036dc1fe08bc3b0b8071f1549144CAS | 1487704PubMed |
O’Shaughnessy, P. J., Dudley, K., and Rajapaksha, W. R. (1996). Expression of follicle stimulating hormone-receptor mRNA during gonadal development. Mol. Cell. Endocrinol. 125, 169–175.
| Expression of follicle stimulating hormone-receptor mRNA during gonadal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXksVSrsA%3D%3D&md5=4310ba5eecd4b80dec26d6d8a33cbd1bCAS | 9027355PubMed |
Pascal, L. E., True, L. D., Campbell, D. S., Deutsch, E. W., Risk, M., Coleman, I. M., Eichner, L. J., Nelson, P. S., and Liu, A. Y. (2008). Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate. BMC Genomics 9, 246.
| Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate.Crossref | GoogleScholarGoogle Scholar | 18501003PubMed |
Pearl, C. A., Mason, H., and Roser, J. F. (2011). Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri- and post-pubertal stallion testis. Anim. Reprod. Sci. 125, 103–111.
| Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri- and post-pubertal stallion testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVyrtLc%3D&md5=3e9ae5648b510b0922d2f59f87abb14eCAS | 21497463PubMed |
Ponglowhapan, S., Church, D. B., and Khalid, M. (2012). Expression of luteinizing hormone and follicle-stimulating hormone receptor in the dog prostate. Theriogenology 78, 777–783.
| Expression of luteinizing hormone and follicle-stimulating hormone receptor in the dog prostate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1GrsLk%3D&md5=1d501c64737d2f287974c3aaec15cb2aCAS | 22541321PubMed |
Raeside, J. I., and Christie, H. L. (1997). Estrogen concentrations in semen of the stallion. Anim. Reprod. Sci. 48, 293–300.
| Estrogen concentrations in semen of the stallion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns1Wmsbg%3D&md5=09e13c71289ed456407580a931483f0dCAS | 9452881PubMed |
Roser, J. F. (2008). Regulation of testicular function in the stallion: an intricate network of endocrine, paracrine and autocrine systems. Anim. Reprod. Sci. 107, 179–196.
| Regulation of testicular function in the stallion: an intricate network of endocrine, paracrine and autocrine systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXoslWkt70%3D&md5=efb72099dbe39c947b1cc50612e55a9eCAS | 18571346PubMed |
Russell, L. D., Alger, L. E., and Nequin, L. G. (1987). Hormonal control of pubertal spermatogenesis. Endocrinology 120, 1615–1632.
| Hormonal control of pubertal spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhs12nsbc%3D&md5=8bbc21f3ad77b3106deeb387e9eec873CAS | 3104013PubMed |
Scarlet, D., Walter, I., Hlavaty, J., and Aurich, C. (2015). Expression and immunolocalisation of follicle-stimulating hormone receptors in gonads of newborn and adult female horses. Reprod. Fertil. Dev. , .
| Expression and immunolocalisation of follicle-stimulating hormone receptors in gonads of newborn and adult female horses.Crossref | GoogleScholarGoogle Scholar | 25693905PubMed |
Schteingart, H. F., Meroni, S. B., Pellizzari, E. H., Perez, A. L., and Cigorraga, S. B. (1995). 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. J. Steroid Biochem. Mol. Biol. 52, 375–381.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltF2isbw%3D&md5=c89b96560909b6b1b600921fb65a5fe8CAS | 7734406PubMed |
Shetty, J., Marathe, G. K., and Dighe, R. R. (1996). Specific immunoneutralization of FSH leads to apoptotic cell death of the pachytene spermatocytes and spermatogonial cells in the rat. Endocrinology 137, 2179–2182.
| 1:CAS:528:DyaK28XisFCqt7w%3D&md5=093d66b85cf08578d0a6c66c02755a3dCAS | 8612566PubMed |
Sipahutar, H., Sourdaine, P., Moslemi, S., Plainfosse, B., and Seralini, G.-E. (2003). Immunolocalization of aromatase in stallion Leydig cells and seminiferous tubules. J. Histochem. Cytochem. 51, 311–318.
| Immunolocalization of aromatase in stallion Leydig cells and seminiferous tubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslCqtLw%3D&md5=90c7bf045557d4e0f437bfcc3a0d2edbCAS | 12588959PubMed |
Walker, W. H., and Cheng, J. (2005). FSH and testosterone signaling in Sertoli cells. Reproduction 130, 15–28.
| FSH and testosterone signaling in Sertoli cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1ynsrk%3D&md5=b96ae9bcc93148e3e116eab854836717CAS | 15985628PubMed |
Zhang, F. P., Hamalainen, T., Kaipia, A., Pakarinen, P., and Huhtaniemi, I. (1994). Ontogeny of luteinizing hormone receptor gene expression in the rat testis. Endocrinology 134, 2206–2213.
| 1:CAS:528:DyaK2cXivFSnsL4%3D&md5=692819853026a7d172eb0ea9d6b4c38bCAS | 8156923PubMed |
Zhang, F.-P., Pakarainen, T., Zhu, F., Poutanen, M., and Huhtaniemi, I. (2004). Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145, 1453–1463.
| Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1WitLo%3D&md5=35f1c27468adbe6b697c84b8ff4c6b9eCAS | 14645113PubMed |
Zirkin, B. R. (1998). Spermatogenesis: its regulation by testosterone and FSH. Semin. Cell Dev. Biol. 9, 417–421.
| Spermatogenesis: its regulation by testosterone and FSH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvFyk&md5=62a4d907821fb804696b493d6decb823CAS | 9813188PubMed |
