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Hormonal Regulation of Spermatogenesis international journal of andrology, 27:335–342 (2004) REVIEW Hormonal regulation of spermatogenesis ROBERT W. HOLDCRAFT and ROBERT E. BRAUN Department of Genome Sciences, School of Medicine, University of Washington, Seattle, WA 98195, USA Summary Proper functioning of the mammalian testis is dependent upon an array of hormonal messengers acting through endocrine, paracrine, and autocrine pathways. Within the testis, the primary messengers are the gonadotrophins, follicle stimulating hormone and luteinizing hormone, and the androgens. Abundant evidence indicates that the role of the gonadotrophins is to maintain proper functioning of testicular somatic cells. It is the androgens, primarily testosterone, which act through the somatic cells to regulate germ cell differentiation. Despite extensive research in this area, little is known about the cell- specific requirements for androgens and even less is understood about the downstream effectors of androgen signalling. However, recent work using cell-specific ablation of androgen receptor function has demonstrated a clear requirement for androgen signalling at multiple, discrete time points during spermatogenesis. These models also provide useful tools for identifying the targets of androgen receptor activity. The purpose of this review is to provide a brief overview of recent advances in our understanding of hormonal regulation of spermatogenesis, with an emphasis on the role of testosterone within the testis, and to pose important questions for future research in this field. Keywords: androgens, gonadotrophins, Sertoli, spermatogenesis Gonadotrophic regulation of spermatogenesis Spermatogenesis in mammals requires the actions of a cells, whose primary function appears to be production of complex assortment of peptide and steroid hormones, each testosterone (Mendis-Handagama, 1997); the myoid cells of which plays an important role in the normal functioning that surround the seminiferous tubules and provide physical of the seminiferous epithelium (Fig. 1 and Table 1). These support and contractile motion to these structures (Maekawa hormonal messengers are critical not only for regulation of et al., 1996); and the Sertoli cells, whose direct contact with male germ cell development, but also for the proliferation proliferating and differentiating germ cells within the and function of the somatic cell types required for proper seminiferous tubules makes them essential for providing development of the testis (Sharpe, 1994; McLachlan et al., both physical and nutritional support for spermatogenesis 2002). These include the interstitial steroidogenic Leydig (Griswold, 1998). Each of these cell types is a direct target for one or more of the hormones whose actions are essential for Correspondence: Robert E. Braun PhD, University of Washington unimpaired male fertility. School of Medicine, Department of Genome Sciences, 1959 NE Follicle-stimulating hormone (FSH) and luteinizing hor- Pacific Street, HSB – J259, Box 357730, Seattle, WA 98195-7730, mone (LH) are glycoprotein hormones secreted by the USA. anterior pituitary that act directly on the testis to stimulate E-mail: [email protected] somatic cell function in support of spermatogenesis. These This is a review article for the European Academy of Andrology hormones, part of the transforming growth factor (TGF) b International Symposium ÔGenetics of male infertility: from research superfamily of secreted growth factors, share a common to clinicÕ, Firenze, Italy. a-subunit and are distinguished by their hormone-specific Ó 2004 Blackwell Publishing Ltd. 336 R. W. Holdcraft and R. E. Braun able to fully rescue spermatogenesis in the absence of LH-R Hypothalamus function (Lei et al., 2001). Testosterone treatment also confers a qualitative recovery of spermatogenesis in hpg GnRH mice, which lack both FSH and LH because of an inactivating mutation at the GnRH locus (Singh et al., 1995). In the absence of T replacement, spermatogenesis is Pituitary arrested during meiosis in hpg males (Cattanach et al., 1977). It is also clear that this effect of T replacement is not T dependent upon stimulation of other Leydig cell products by Testis T or LH, as T alone completely rescues spermatogenesis in rats treated with the Leydig cell-specific cytotoxin ethane T LH Myoid dimethane sulphonate (EDS) (Kerr et al., 1993). FSH T Steroid function in spermatogenesis Testosterone and its metabolites, dihydrotestosterone Leydig Inhibin (DHT) and estradiol (E2), are collectively referred to as the sex hormones. This is because of their primary role in the T T regulation of gonadal and germ cell development in both males and females as well as in the sexual differentiation of Sertoli males. In the male, T assumes the lead role in both morphological development and reproductive function, although E2 and its receptor estrogen receptor (ER)a, but Figure 1. Hormonal regulation of spermatogenesis Most hormones shown not ERb, clearly play some role in the maintenance of male can have both positive and negative effects, either at the level of receptor fertility. However, these effects appear to be indirect and activation/desensitization or through activation and repression of down- secondary. Disruption of Erb has no apparent effect in males, stream targets. GnRH, gonadotrophin releasing hormone; LH, luteinizing as XY animals are morphologically normal and fertile (Krege hormone; FSH, follicle stimulating hormone; T, testosterone. et al., 1998). Initial observations of Era null male mice suggested a primary role for this gene in regulating b-subunit (Pierce & Parsons, 1981). In males, FSH receptor spermatogenesis, as animals presented with reduced fertility expression (FSH-R) is limited to the testicular Sertoli cells and dramatically decreased epididymal sperm counts (Lubahn (Rannikki et al., 1995), while LH receptors (LH-R) are et al., 1993). However, it is now clear that the primary found primarily in the Leydig cells, although receptor function of ERa in the male reproductive tract is the staining is also observed in spermatogenic cells (Eblen et al., regulation of luminal fluid reabsorption in the rete testis and 2001; Lei et al., 2001). efferent ducts linking the testis and epididymis (Hess et al., Genetic and pharmacological studies in rodents indicate 2000; Lee et al., 2000). As might be expected, males that the primary role of FSH in spermatogenesis is homozygous for mutations in both Era and b have a similar ) ) stimulation of Sertoli cell proliferation during prepubertal phenotype to Era / males (Couse et al., 1999). development (Heckert & Griswold, 2002). Sertoli cell Targeted disruption of Cyp19, whose gene product number largely determines the number of germ cells (Sharpe, converts T to E2, results in progressive loss of fertility and 1994). Targeted mutations in the murine FSH-R and FSHb disruption of spermatogenesis, although males are initially subunit genes lead to dramatically reduced testis weights and fertile. It is unclear why loss of E2 synthesis via mutation of epididymal sperm numbers, although males are fertile in Cyp19 has a less severe reproductive phenotype than disrup- both cases (Kumar et al., 1997; Dierich et al., 1998). These tion of Era. However, it is suggestive of the existence of an as results are consistent with hormone depletion-replacement yet unidentified Cyp19 paralog or an E2 independent function ) ) studies in human males (Matsumoto & Bremner, 1985; of ER within the Cyp19 / male. Surprisingly, despite the Matsumoto et al., 1986), although unlike in rodents, FSH complete absence of measurable aromatase activity from ) ) can also rescue spermatogenesis in gonadotrophin-suppressed Cyp19 / ovaries, there appears to be no difference in serum men independently of T (Matsumoto et al., 1983). How- concentrations of E2 between wild-type and Cyp19 mutant ever, the authors of this study suggest this effect is because of animals of either sex (Fisher et al., 1998). increased FSH-induced Sertoli cell sensitivity to residual T In contrast to the role of estrogens in males, androgens production within the testis. and androgen receptor (AR) function are essential for proper Regulation of testosterone (T) synthesis seems to be the sexual differentiation and the maintenance of normal only indispensable function of LH within the adult testis. spermatogenesis. AR activity is regulated by T and DHT, Treatment of LH-R knockout mice with exogenous T is whose binding initiates nuclear translocation and the Ó 2004 Blackwell Publishing Ltd, International Journal of Andrology, 27, 335–342 Hormonal regulation of spermatogenesis 337 Table 1. Animal models of hormonal regulation of spermatogenesis Model Organism Phenotype References Gnrhhpg/hpg Mouse Loss of LH, FSH, and T secondary to GnRH deficiency; cryptorchid; Cattanach et al. (1977), spermatogenic arrest at pachytene, rescued by LH and T Singh et al. (1995) ) ) Fsh-r / Mouse Loss of FSH-R signalling in Sertoli cells; decreased testis weight and Dierich et al. (1998) sperm output because of reduced Sertoli cell proliferation; fertile ) ) Fshb / Mouse Loss of FSH; decreased testis weight and sperm output as for Kumar et al. (1997) ) ) Fsh-r / ; fertile ) ) Lh-r / Mouse T deficiency because of loss of LH-R function in Leydig cells; T still Lei et al. (2001) detectable in serum; failure of postnatal male sexual development, cryptorchid; spermatogenic arrest at round spermatid stage, rescued by T Hypo-physectomy Rat Loss of LH, FSH, and T because of removal of pituitary; regression Elkington & Blackshaw
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