Artigo Acesso aberto Revisado por pares

‘Paracrine’ control of spermatogenesis

2009; Wiley; Volume: 31; Issue: 5 Linguagem: Italiano

10.1111/j.1439-0272.1999.tb01421.x

ISSN

1439-0272

Autores

Gerhard F. Weinbauer, Jocelyn M. Wessels,

Tópico(s)

Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities

Resumo

AndrologiaVolume 31, Issue 5 p. 249-262 'Paracrine' control of spermatogenesis Dr G. F. Weinbauer, Corresponding Author Dr G. F. Weinbauer Institute of Reproductive Medicine of the University, Münster, GermanyInstitute of Reproductive Medicine of the University, Domagkstrasse 11, D-48129 Münster, GermanySearch for more papers by this authorJ. Wessels, J. Wessels Institute for Hormone and Fertility Research, Hamburg, GermanySearch for more papers by this author Dr G. F. Weinbauer, Corresponding Author Dr G. F. Weinbauer Institute of Reproductive Medicine of the University, Münster, GermanyInstitute of Reproductive Medicine of the University, Domagkstrasse 11, D-48129 Münster, GermanySearch for more papers by this authorJ. Wessels, J. Wessels Institute for Hormone and Fertility Research, Hamburg, GermanySearch for more papers by this author First published: 24 April 2009 https://doi.org/10.1111/j.1439-0272.1999.tb01421.xCitations: 9AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Summary. Spermatogenesis is a remarkably complex but precise process yielding highly differentiated haploid germ cells from diploid stem cells. Although many factors have been implicated in the paracrine control of spermatogenesis, functional proof is only available for a few regulators. Among those are androgens, growth factors and stem cell factor. Cell- and organ-specific gene-targeting will provide important insights into the relevance of local factors controlling male gameto-genesis. As testicular communication frequently occurs between rather remote cells and compartments, it is proposed that the term 'local' rather than 'paracrine' mediators/factors should be used, since the latter term refers to communication amongst neighbouring cells (and mainly via diffusion). References Aceitero J., Llanero M., Parrado R., Pena E., Lopez-Beltran A. (1998) Neonatal exposure of male rats to estradiol benzoate causes rete testis dilation and backflow impairment of spermatogenesis. Anat Rec 252: 17 – 33. Alastalo TP, Lonnstrom M., Leppa S., Kaarniranta K., Pelto-Huikko M., Sistonen L., Parvinen M. (1998) Stage-specific expression and cellular localization of the heat shock factor 2 isoforms in the rat seminiferous epithelium. Exp Cell Res 240: 16 – 27. Albanesi C., Geremia R., Giorgio M., Dolci S., Sette C., Rossi P. (1996) A cell- and developmental stage-specific promotor drives the expression of a truncated c-kit protein during mouse spermatid elongation. Development 122: 1291 – 1302. Anawalt BD, Bebb RA, Matsumoto AM, Groome NP, Illingworth PJ, McNeilly AS, Bremner WJ (1996) Serum inhibin B levels reflect Sertoli cell function in normal men and men with testicular dysfunction. J Clin Endocrinol Metab 81: 3341 – 3345. Anderson RA, Wallace EM, Groome NP, Bellis AJ, Wu FCW (1997) Physiological relationships between inhibin B, follicle stimulating hormone secretion and spermatogenesis in normal men and response to gonadotrophin suppression by exogenous testosterone. Hum Reprod 12: 746 – 751. Anderson RA, Irvine DS, Balfour C., Groome NP, Riley SC (1998) Inhibin B in seminal plasma: testicular origin and relationship to spermatogenesis. Hum Reprod 13: 920 – 926. Andersson AM, Juul A., Petersen JH, Muller J., Groome NP, Skakkebaek NE (1997) Serum inhibin B in healthy pubertal and adolescent boys: relation to age, stage of puberty, and follicle-stimulating hormone, luteinizing hormone, testosterone, and estradiol levels. J Clin Endocrinol Metab 82: 3976 – 3981. Andersson AM, Muller J., Skakkebaek NE (1998a) Different roles of prepubertal and postpubertal germ cells and Sertoli cells in the regulation of serum inhibin B levels. J Clin Endocrinol Metab 83: 4451 – 4458. Andersson AM, Toppari J., Haavisto AM, Petersen JH, Simell T., Simell O., Skakkebaek NE (1998b) Longitudinal reproductive hormone profiles in infants: peak of inhibin B levels in infant boys exceeds levels in adult men. J Clin Endocrinol Metab 83: 675 – 681. Aoki A., Fawcett DW (1978) Is there a local feedback from the seminiferous tubules affecting activity of the Leydig cells? Biol Reprod 19: 144 – 158. Behringer RR, Finegold MJ, Cate RL (1994) Muellerian-inhibiting substance function during mammalian sexual development. Cell 79: 415 – 423. Benahmed M. (1997) Role of tumor necrosis factor in the male gonad. Contracept Fertil Sex 25: 569 – 571. Berruti G. (1998) Signaling events during male germ cell differentiation: bases and perspectives. Front Biosci 3: 1097 – 1108. Blok LJ, Bartlett JMS, Bolt-de-Vries J., Themmen APN, Brinkmann AO, Weinbauer GF, Nieschlag E., Grootegoed JA (1992a). Effect of testosterone deprivation on expression of the androgen receptor in rat prostate, epididymis and testis. Int J Androl 15: 182 – 198. Blok LJ, Hoogerbrugge JW, Themmen JPN, Baarends WN, Post M., Grootegoed JA (1992b) Transient down-regulation of androgen receptor messenger ribonucleic acid (mRNA) expression in Sertoli cells by follicle-stimulating hormone is followed by up-regulation of androgen receptor mRNA and protein. Endocrinology 131: 1243 – 1349. Bremner WJ, Millar MR, Sharpe RM, Saunders PTK (1994) Immunohistochemical localization of androgen receptors in the rat testis: evidence for stage-dependent expression and regulation by androgens. Endocrinology 135: 1227 – 1234. Brinster RL, Avarbock MR (1994) Germline transmission of donor haplotype following spermatogonial transplantation. Proc Natl Acad Sci 91: 11303 – 11307. Cameron DF, Muffly KE, Nazian SJ (1993) Testosterone stimulates spermatid binding to competent Sertoli cells in vitro. J Endocrinol 1: 61 – 65. Carani C., Qin K., Simoni M., Faustini-Fustini M., Serpente S., Boyd J., Korach KS, Simpson ER (1997) Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337: 91 – 95. Cardone A., Angelini F., Varriale B. (1998) Autoregulation of estrogen and androgen receptor mRNAs and downregul-ation of androgen receptor mRNA by estrogen in primary cultures of lizard testis cells. Gen Comp Endocrinol 110: 227 – 236. Clouthier DE, Avarbock MR, Maika SD, Hammer RE, Brinster RL (1996) Rat spermatogenesis in mouse testis. Nature 381: 418 – 421. Cohen PE, Chisholm O., Arceci RJ, Stanley ER, Pollard JW (1996) Absence of colony-stimulating factor-1 in osteope-trotic (csfmop/csfmop) mice results in male fertility defects. Biol Reprod 55: 310 – 317. Cohen PE, Pollard JW (1998) Normal sexual function in male mice lacking a functional type 1 interleukin-1 (II-1) receptor. Endocrinology 139: 815 – 818. Danzo BJ, Eller BC (1985) The ontogeny of biologically active androgen-biding protein in rat plasma, testis and epididymis. Endocrinology 117: 1380 – 1388. Danzo BJ, Pavlou SN, Anthony HL (1990) Hormonal regulation of androgen-binding protein in the rat. Endocrinology 127: 2829 – 2838. De Franca LR, Hess RA, Cooke PS, Russell D. (1995) Neonatal hypthyroidism causes delayed Sertoli cell maturation in rats treated with propylthiouracil: evidence that the Sertoli cell controls testis growth. Anat Rec 242: 57 – 69. DeKretser DM, Loveland KL, Meinhardt A., Simorangkir D., Wreford N. (1998) Spermatogenesis. Hum Reprod 13: 1 – 8. Dym M. (1994) Basement membrane regulation of Sertoli cells. Endocr Rev 15: 102 – 115. Dym M., Jia MC, Dirami G., Price JM, Rabin SJ, Mocchetti I., Ravindranath N. (1995) Expression of c-kit receptor and its autophosphorylation in immature rat type A spermato-gonia. Biol Reprod 52: 8 – 19. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB, Korach KS (1996) Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and fertility. Endocrinology 137: 4796 – 4805. El-Hafnawy T., Huthaniemi I. (1998) Progesterone can participate in down-regulation of the luteinizing hormone receptor gene expression and function in cultured murine. Leydig cells. Mol Cell Endocrinol 137: 127 – 138. Felden F., Gueant JL, Ennya A., Gerard A., Fremont S., Nicolas JP, Gerard H. (1992) Photoaffinity labelled rat androgen-binding protein and human sex hormone steroid-binding protein bind specifically to rat germ cells. Mol Endocrinol 9: 36 – 46. Fisher JS, Turner KJ, Fraser HM, Saunders PT, Brown D., Sharpe RM (1998) Immunoexpression of aquaporin-1 in the efferent ducts of the rat and marmoset monkey during development, its modulation by estrogens, and its possible role in fluid resorption. Endocrinology 139: 3935 – 3945. Franca LR, Ogawa T., Avarbock MR, Brinster RL, Russell LD (1998) Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 59: 1371 – 1377. Fujisawa M., Kanzaki M., Okuda Y., Okada H., Arakawa S., Kamidono S. (1998) Stem cell factor in human plasma as a marker for spermatogenesis. Urology 51: 460 – 463. Gerard A. (1995) Endocytosis of androgen-binding protein (ABP) by spermatogenic cells. J Steroid Biochem Mol Biol 53: 533 – 542. Gerard H., Gerard A., Ennya A., Felden F., Gueant JL (1994) Spermatogenic cells do internalize Sertoli androgen-binding protein: a transmission electron microscopy auto-radiographic study in the rat. Endocrinology 134: 1515 – 1527. Graf KM, Dias JA, Griswold MA (1997) Decreased spermatogenesis as the result of an induced autoimmune reaction directed against the gonadotropin receptors in male rats. J Androl 18: 174 – 185. Guo Q., Kumar TR, Woodruff T., Hadsell L., DeMayo FJ, Matzuk MM (1998) Overexpression of mouse follistatin causes reproductive defects in transgenic mice. Mol Endocrinol 12: 96 – 106. Haneji T., Koide SS, Tajima Y., Nishimune Y. (1991) Differential effects of epidermal growth factor on the differentiation of type A spermatogonia in adult mouse cryptorchid testes in vitro. J Endocrinol 128: 383 – 388. Hara T., Tamura K., De Miguel MP, Mukouyama Y., Kim HJ, Kogo H., Donovan PJ, Miyajima A. (1998) Distinct roles of oncostatin M and leukemia inhibitory factor in the development of primordial germ cells and Sertoli cells in mice. Dev Biol 201: 144 – 153. Hedger MP (1997) Testicular leukocytes: what are they doing? Rev Reprod 2: 38 – 47. Hess RA, Bunick D., Lee KH, Bahr J., Taylor JA, Korach KS, Lubahn DB (1997a) A role for oestrogens in the male reproductive system. Nature 390: 509 – 512. Hess RA, Gist DH, Bunick D., Lubahn DB, Farrell A., Bahr J., Cooke PS, Greene GL (1997b) Estrogen receptor (alpha and beta) expression in the excurrent ducts of the adult male rat reproductive tract. J Androl 18: 602 – 611. Hoeben E., Deboel L., Rombauts L., Heyns W., Verhoeven G. (1994) Different cells and cell lines produce factors that modulate Sertoli cell function. Mol Cell Endocrinol 101: 263 – 275. Holstein AF, Roosen-Runge EC (1981) Atlas of human spermatogenesis. Grosse-Verlag, Berlin . Huang HFS, Pogach LM, Nathan E., Giglio W., Seebode JJ (1991) Synergistic effects of follicle-stimulating hormone and testosterone on the maintenance of spermiogenesis in hypophysectomized rats: relationship with the androgen-binding protein status. Endocrinology 128: 3152 – 3161. Huang HFS, Pogach L., Giglio W., Nathan E., Seebode J. (1992) GnRH-A induced arrest of spermiogenesis in rats is associated with altered androgen binding protein distribution in the testis and epididymis. J Androl 13: 153 – 159. Janulis L., Bahr JM, Hess RA, Bunick D. (1996) P450 aromat-ase messenger ribonucleic acid expression in male rat germ cells: detection by reverse transcription-polymerase chain reaction amplification. J Androl 17: 651 – 658. Jegou B. (1993) The Sertoli-germ cell communication network in mammals. Int Rev Cytol 147: 25 – 96. Jegou B., Syed V., Sourdaine P., Byers S., Gérard N., de la Calle Velez J., Pineau C., Ganier DH, Bauche F. (1992) The dialogue between late spermatids and Sertoli cells in vertebrates: a century of research. In: Spermatogenesis, fertilization, contraception molecular, cellular and endocrine events in male reproduction. E. Nieschlag, UF Habenicht (eds) Springer, Heidelberg , pp 57 – 97. Jensen TK, Andersson AM, Hjollund NH, Scheike T., Kolstad H., Giwercman A., Henriksen TB, Ernst E., Bonde JP, Olsen J., McNeilly A., Groome NP, Skakkebæk NE (1997) Inhibin B as a serum marker of spermatogenesis: correlation to differences in sperm concentration and follicle-stimulating hormone levels. A study of 349 Danish men. J Clin Endocrinol Metab 82: 4059 – 4063. Joseph DR, O'Brien DA, Sullivan PM, Bcchis M., Tsuruta JK, Petrusz P. (1997) Overexpression of androgen binding protein/sex hormone-binding globulin in male transgenic mice: tissue distribution and phenotypic disorders. Biol Reprod 56: 21 – 32. Klingmüller D., Haidl G. (1997) Inhibin B in men with normal and disturbed spermatogenesis. Hum Reprod 12: 2376 – 2378. Kondoh G., Yomogida K., Dohmae K., Nozawa M., Koga M., Nonomura N., Miki I., Okuyama A., Nishimune Y. (1997) Coexpression of multiple Sertoli cell and Leydig cell marker genes in the spontaneous testicular tumor of F344 rat: evidence for phenotypical bifurcation of the interstitial cell tumor. Jpn J Cancer Res 88: 839 – 845. Krege JH, Hodgin JB, Couse JF, Enmark E., Warner M., Mahler JF, Sar M., Korach KS, Gustafsson JA, Smithies O. (1998) Generation and reproductive phenotypes of mice lacking estrogen receptor. Med Sci 95: 15677 – 15682. Kremer H., Kraaij R., Toledo SPA, Psot M., Fridman JB, Hayashida CY, Van Reen M., Milgrom E., Ropers HH, Mariman E. (1995) Male pseudohermaphroditism due to a homozygous missense mutation of the luteinizing hormone receptor gene. Nat Genet 9: 160 – 164. Kuiper GG, Gustafsson JA (1997) The novel estrogen receptor-beta subtype: potential role in the cell- and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett 410: 87 – 90. Kula K. (1988) Induction of precocious maturation of spermatogenesis in infant rats by human menopausal gonadotropin and inhibition by simultaneous administration of gonado-tropins and testosterone. Endocrinology 122: 34 – 39. Kumar TR, Wang Y., Matzuk MM (1996) Gonadotropins are essential modifier factors for gonadal tumor development in inhibin-deficient mice. Endocrinology 137: 4210 – 4216. Larriba S., Esteban C., Toran N., Gerard A., Audi L., Gerard H., Reventos J. (1995) Androgen binding protein is tissue-specifically expressed and biologically active in transgenic mice. J Steroid Biochem Mol Biol 53: 573 – 578. Lejeune H., Chuzel F., Thomas T., Avallet O., Habert R., Durand P., Saez J. (1996) Paracrine regulation of Leydig cells. Ann Endocrinol 57: 55 – 63. Lejeune H., Chuzel F., Sanchez P., Durand P., Mather JP, Saez JM (1997) Stimulating effect of both human recombinant inhibin A and activin A on immature porcine Leydig cell functions in vitro. Endocrinology 138: 4783 – 4791. Lejeune H., Sanchez P., Saez JM (1998) Enhancement of long-term testosterone secretion and steroidogenic enzyme expression in human Leydig cells by co-culture with human Sertoli cell-enriched preparations. Int J Androl 21: 129 – 140. Lerchl A., Sotiriadu S., Behre HM, Pierce J., Weinbauer GF, Kliesch S., Nieschlag E. (1993) Restoration of spermato-genesis by follicle-stimulating hormone despite low intra-testicular testosterone in photoinhibited hypogonadotropic Djungarian hamsters (Phodopus sungorus). Biol Reprod 49: 1108 – 1116. Levallet J., Bilinska B., Mittre H., Genissel C., Fresnel J., Carreau S. (1998) Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat tes-ticular cells. Biol Reprod 58: 919 – 926. Li H., Papadopoulos V., Vidic B., Dym M., Culty M. (1997) Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol: identification of signaling mechanisms involved. Endocrinology 138: 1289 – 1298. Loveland KL, Schlatt S. (1997) Stem cell factor and c-kit in the mammalian testis: lessons originating from mother nature's gene knockouts. J Endocrinol 153: 337 – 344. Lubahn DB, Moyer JS, Golding TS, Couse JF, Korach KS, Smithies O. (1993) Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc Natl Acad Sci 90: 11162 – 11166. Lukyanenko YO, Carpenter AM, Brigham DE, Stocco DM (1998) Regulation of Leydig cells through a steriodogenic acute regulatory protein-independent pathway by a lipo-philic factor from macrophages. J Endocrinol 156: 267 – 275. Mather JP, Moore A., Li RH (1997) Activins, inhibins, and follistatins: further thoughts on a growing family of regulators. Proc Soc Exp Biol Med 215: 209 – 222. Matzuk MM, Finegold MJ, Mishina Y., Bradley A., Behringer RR (1995) Synergistic effects of inhibins and mullerian-inhibiting substance on testicular tumorigenesis. Mol Endocrinol 9: 1337 – 1345. Monaco L., Foulkes NS, Sassone-Corsi P. (1995) Pituitary follicle-stimulating hormone (FSH) induces CREM gene expression in Sertoli cells: involvement in long-term desen-sitization of the FSH receptor. Proc Natl Acad Sci 92: 10673 – 10677. Monsees TK, Göring M., Schill WB, Miska W. (1998) Possible roles of proteases in the regulation of spermatogenesis. Andrologia 30: 185 – 191. Morishima A., Grumbach MM, Simpson ER, Fischer C., Qin K. (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab 80: 3689 – 3698. Moudgal NR, Murthy GS, Kumar KMP, Martin F., Suresh R., Medhamurthy R., Patil S., Sehgal S., Saxena BN (1997) Responsiveness of human male volunteers to immunization with ovine follicle stimulating hormone vaccine: results of a pilot study. Hum Reprod 12: 457 – 463. Muffly KE, Nazian SJ, Cameron DF (1994) Effects of follicle-stimulating hormone on the junction-related Sertoli cell cytoskeleton and daily sperm production in testosterone-treated hypophysectomized rats. Biol Reprod 51: 158 – 166. Munsie M., Schlatt S., DeKretser DM, Loveland KL (1997) Expression of stem cell factor in the postnatal rat testis. Mol Reprod Dev 47: 19 – 25. Niklowitz P., Lerchl A., Nieschlag E. (1997) In vitro fertilizing capacity of sperm from FSH-treated photoinhibited Djungarian hamsters (Phodopus sungorus). J Endocrinol 154: 475 – 481. Orth JM, Qiu J., Jester WF, Pilder S. (1997) Expression of the c-kit gene critical for migration of neonatal rat gonocytes in vitro. Bio Reprod 57: 676 – 683. Parvinen M., Vihko KK, Toppari J. (1986) Cell interactions during the seminiferous epithelial cycle. Int Rev Cytol 104: 115 – 151. Payne AH, Hardy MP, Russell LD (1996) The Leydig cell Cache River Press, Vienna . Perryman KJ, Stanton PG, Loveland KL, McLachlan RI, Robertson DM (1996) Hormonal binding dependency of neural cadherin in the binding of round spermatids to Sertoli cells in vitro. Endocrinology 137: 3877 – 3883. Petersen MP, Andersson AM, Rørth M., Daugaard G., Skakkebaek NE (1999) Undetectable inhibin B serum levels in men after testicular irradiation. J Clin Endocrinol Metab 84: 213 – 215. Pierik FH, Vreeburg JT, Stijnen T., De Jong FH, Weber RF (1998) Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab 83: 3110 – 3114. Pogach L., Giglio W., Nathan E., Huang HFS (1993) Maintenance of spermiogenesis by exogenous testosterone in rats treated with a GnRH antagonist: relationship with androgen-binding protein status. J Reprod Fertil 98: 415 – 422. Pollard JW, Dominguez MG, Mocci S., Cohen PE, Stanley SR (1997) Effect of the colony-stimulating factor-1 null mutation, osteopetrotic (csfm (op)), on the distribution of macrophages in the male mouse reproductive tract. Biol Reprod 56: 1290 – 1300. Quigley CA (1998) The androgen receptor. Physiology and pathophysiology. In: Testosterone: action, deficiency substitution. E. Nieschlag, HM Behre (eds) Springer Verlag, Berlin , pp. 33 – 107. Racine C., Rey R., Forest MG, Louis F., Ferre A., Huhtaniemi I., Josso N., di Clemente N. (1998) Receptors for anti-Mullerian hormone on Leydig cells are responsible for its effects on steroidogenesis and cell differentiation. Proc Natl Acad Sci 95: 594 – 599. Rajpert-De-Meyts E., Skakkebaek NE (1994) Expression of the c-kit protein product in carcinoma-in-situ and invasive testicular germ cell tumours. Int J Androl 17: 85 – 92. Rannikko A., Penttila TL, Zhang FP, Toppari J., Parvinen M., Huhtaniemi I. (1996) Stage-specific expression of the FSH receptor gene in the prepubertal and adult rat seminiferous epithelium. J Endocrinol 151: 29 – 35. Reventos J., Hammond GL, Crozat A., Brooks DE, Gunsalus GL, Bardin CW, Musto NA (1988) Hormonal regulation of rat androgen-binding protein (ABP) messenger ribo-nucleic acid and homology of human testosterone-estradiol-binding globulin and ABP complementary deoxyribo-nucleic acids. Mol Endocrinol 2: 125 – 132. Rey R. (1998) Endocrine, paracrine and cellular regulation of postnatal anti-Müllerian hormone secretion by Sertoli cells. Trend Endocrinol Metab 9: 271 – 276. Rommerts FF (1998) Testosterone: an overview of biosynthesis, transport, metabolism and action. In: Testosterone: action, deficiency, substitution. E. Nieschlag, HM Behre (eds) Springer Verlag, Berlin , pp 1 – 33. Rossi P., Dolci S., Albanesi C., Grimaldi P., Ricca R., Geremia R. (1993) Follicle-stimulating hormone induction of steel factor (SLF) mRNA in mouse Sertoli cells and stimulation of DNA synthesis in spermatogonia by soluble SLF. Dev Biol 155: 68 – 74. Rouiller-Fabre V., Carmona S., Merhi RA, Cate R., Habert R., Vigier B. (1998) Effect of anti-Mullerian hormone on Sertoli and Leydig cell functions in fetal and immature rats. Endocrinology 139: 1213 – 1220. Russell LD, Brinster RL (1996) Ultrastructural observations of spermatogenesis following transplantation of rat testis cells into mouse seminiferous tubules. J Androl 17: 615 – 627. Russell LD, Griswold MD (1993) The Sertoli cell. Cache River Press, Clearwater . Russell LD, Ettlin RA, Hikim Sinha AP, Clegg ED (1990) Histological and histopathological evaluation of the testis. Cache River Press, Clearwater . Saez JM (1994) Leydig cells: endocrine, paracrine, and auto- crine regulation. Endocr Rev 15: 574 – 594. Sandlow JI, Feng HL, Sandra A. (1997) Localization and expression of the c-kit receptor protein in human and rodent testis and sperm. Urology 49: 494 – 500. Saunders PTK (1998) Oestrogen receptor beta (ERβ). Rev Reprod 3: 164 – 171. Schlatt S., Weinbauer GF, Arslan M., Nieschlag E. (1993) Appearance of a smooth muscle actin in peritubular cells of monkey testes is induced by androgens, modulated by follicle-stimulating hormone, and maintained after hormonal withdrawal. J Androl 14: 340 – 350. Schlatt S., Arslan M., Weinbauer GF, Behre HM, Nieschlag E. (1995) Endocrine control of testicular somatic and premei-otic germ cell development in the immature testis of the primate Macaco mulatto. Eur J Endocrinol 133: 235 – 247. Schlatt S., Meinhardt A., Nieschlag E. (1997) Paracrine regulation of cellular interactions in the testis: factors in search of a function. Eur J Endocrinol 137: 107 – 117. Sette C., Bevilacqua A., Bianchini A., Mangia F., Geremia R., Rossi P. (1997) Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit kinase present in spermatozoa. Development 124: 2267 – 2274. Sette C., Bevilacqua A., Geremia R., Rossi P. (1998) Involvement of phospholipase C-gamma-1 in mouse egg activation induced by a truncated form of the c-kit tyrosine kinase present in spermatozoa. J Cell Biol 142: 1063 – 1074. Shan LX, Zhu LJ, Bardin CW, Hardy MP (1995) Quantitative analysis of androgen receptor messenger ribonucleic acid in developing Leydig cells and Sertoli cells by in situ hybridization. Endocrinology 136: 3856 – 3862. Shan LX, Bardin CW, Hardy MP (1997) Immuno-histochemical analysis of androgen effects on androgen receptor expression in developing Leydig and Sertoli cells. Endocrinology 138: 1259 – 1266. Sharpe RM (1994) Regulation of spermatogenesis. In: The physiology of reproduction. 2nd edn. E. Knobil, JD Neill (eds) Raven Press, New York , pp 1363 – 1436. Sharpe RM, McKinnell C., McLaren T., Millar M., West TP, Maguire S., Gaughan J., Syed V., Jégou B., Kerr JB, Saunders PTK (1994) Interactions between androgens, Sertoli cells and germ cells in the control of spermatogenesis. In: Molecular, cellular endocrinology of the testis. G. Verhoeven, UF Habenicht (eds) Springer, Heidelberg , pp 115 – 143. Shetty G., Krishnamurthy H., Krishnamurthy HN, Bhatnagar S., Mouggal RN (1997) Effect of estrogen deprivation on the reproductive physiology of male and female primates. J Steroid Biochem Mol Biol 61: 157 – 166. Shetty G., Krishnamurthy H., Krishnamurthy HN, Bhatnagar AS, Moudgal NR (1998) Effect of long-term treatment with aromatase inhibitor on testicular function of adult male bonnet monkeys (M. radiata). Steroids 63: 414 – 420. Shikone T., Matzuk MM, Perlas E., Finegold MJ, Lewis KA, Vale W., Bradles A., Hsueh AJ (1994) Characterization of gonadal sex cord-stromal tumor cell lines from inhibin-alpha and p53-deficient mice: the role of activin as an autocrine growth factor. Mol Endocrinol 8: 983 – 995. Shou W., Woodruff TK, Matzuk MM (1997) Role of androgens in testicular tumor development in inhibin-deficient mice. Endocrinology 138: 5000 – 5005. Simoni M., Gromoll J., Nieschlag E. (1997) The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr Rev 18: 739 – 773. Singh J., O'Neill C., Handelsman DJ (1995) Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology 136: 5311 – 5321. Skinner MK (1991) Cell-cell interactions in the testis. Endocr Rev 12: 45 – 77. Smith EP, Boyd J., Frank GR, Takahashi H., Cohen RM, Specker B., Williams T., Lubahn D., Korach KS (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. New Engl J Med 331: 1056 – 1061. Spiteri-Grech J., Nieschlag E. (1993) Paracrine factors relevant to the regulation of spermatogenesis—a review. J Reprod Fertil 98: 1 – 14. Strohmeyer T., Reese D., Press M., Ackermann R., Hartmann M., Slamon D. (1995) Expression of the c-kit proto-oncogene and its ligand stem cell factor (SCF) in normal and malignant human testicular tissue. J Urol 153: 511 – 515. Suarez-Quian CA, Martinez-Garcia F., Nistal M., Regadera J. (1999) Androgen receptor distribution in adult human testis. J Clin Endocrinol Metab 84: 350 – 358. Suresh R., Medhamurthy R., Moudal NR (1995) Comparative studies on the effects of specific immunoneutralization of endogenous FSH or LH on testicular germ cell transformations in the adult bonnet monkey (Macaca radiata). AJPJ 34: 35 – 43. Syed V., Khan SA, Nieschlag E. (1991) Epidermal growth factor stimulates testosterone production of human Leydig cells in vitro. J Endocrinol Invest 14: 93 – 97. Tajima Y., Sawada K., Morimoto T., Nishimune Y. (1994) Switching of mouse spermatogonial proliferation from the c-kit receptor-independent type to the receptor-dependent type during differentiation. J Reprod Fertil 102: 117 – 122. Takaimya K., Yamamoto A., Furukawa K., Zhao J., Fukumoto S., Yamashiro S., Okada M., Haraguchi M., Shin M., Kishikawa M., Shiku H., Aizawa S., Furukawa K. (1998) Complex gangliosides are essential in spermatogenesis of mice: possible roles in the transport of testosterone. Proc Natl Acad Sci 95: 12147 – 12152. Tapanainen JS, Aittomäki K., Min J., Vaskivuo T., Huhtaniemi IT (1997) Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nature Gen 15: 205 – 206. Teerds KJ, Veldhuizen-Tsoerkan MB, Rommerts FFG, De Rooij DG, Dorrington DJ (1994) Proliferation and differentiation of testicular interstitial cells: aspects of Leydig cell development in the prepubertal and adult testis. In: Molecular and cellular endocrinology of the testis. G. Verhoeven, UF Habenicht (eds) Springer, Berlin , Heidelberg , New York , Tokyo , pp 37 – 66. Toppari J., Kaipia A., Kaleva M., Laato M., De Kretser DM, Krummen LA, Mather JP, Salmi TT (1998) Inhibin gene expression in a large cell calcifying tumour and serum inhibin and activin levels. APMIS 106: 101 – 112. Van Roijen JH, Van Assen S., Van der Kwast TH, De Rooij DG, Boersma JA, Vreeburg JTM, Weber RFA (1995) Androgen receptor immunoexpression in the testis of infertile men. J Androl 16: 510 – 516. Vassalli A., Matzk MM, Gardner HA, Lee KF, Jaenisch R. (1994) Activin/inhibin beta B subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev 8: 414 – 427. Verhoeven G., Cailleau J. (1988) Follicle-stimulating hormone and androgens increase the concentration of the androgen receptor in Sertoli cells. Endocrinology 122: 1541 – 1550. Vliegen M., Schlatt S., Weinbauer GF, Bergmann M., Groome NP, Nieschlag E. (1993) Localization of inhibin/activin subunits in the testis of adult nonhuman primates and men. Cell Tissue Res 273: 261 – 268. Vornberger W., Prins G., Musto NA, Suarez-Quian CA (1994) Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology 123: 2307 – 2316. Weinbauer GF, Nieschlag E. (1993) Hormonal control of spermatogenesis. In: Molecular biology of the male reproductive system. DM Kretser (ed) Academic Press, San Diego , pp 99 – 142. Weinbauer GF, Nieschlag E. (1996) The Leydig cell as a target for male contraception. In: The Leydig cell. AH Payne, MP Hardy, LD Russell (eds) Cache River Press, Clearwater , pp 629 – 662. Weinbauer GF, Nieschlag E. (1998) The role of testosterone in spermatogenesis. In: Testosterone: action, deficiency substitution. E. Nieschlag, HM Behre (eds) Springer, Heidelberg , pp 143 – 169. Yoshinaga K., Nishikawa S., Ogawa M., Hayashi S., Kunisada T., Fujimoto T., Nishikawa S. (1991) Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113: 689 – 699. Zhang FP, El-Hafnawy T., Huthaniemi I. (1998) Regulation of luteinizing hormone receptor gene expression by insulin-like growth factor-I in an immortalized murine Leydig tumor cell line (BLT-1). Biol Reprod 59: 1116 – 1123. Zhao GQ, Deng K., Labosky PA, Liaw L., Hogan BL (1996) The gene encoding bone morphogentic protein 8B is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev 10: 1657 – 1669. Zhao GQ, Liaw L., Hogan BL (1998) Bone morphogenetic protein 8A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 125: 1103 – 1112. Citing Literature Volume31, Issue5September 1999Pages 249-262 ReferencesRelatedInformation

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