Functions of somatic cells for spermatogenesis in stallions
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Spermatogenesis and testis development are highly structured physiological processes responsible for post-pubertal fertility in stallions. Spermatogenesis comprises spermatocytogenesis, meiosis, and spermiogenesis. Although germ cell degeneration is a continuous process, its effects are more pronounced during spermatocytogenesis and meiosis. The productivity and efficiency of spermatogenesis are directly linked to pubertal development, degenerated germ cell populations, aging, nutrition, and season of the year in stallions. The multiplex interplay of germ cells with somatic cells, endocrine and paracrine factors, growth factors, and signaling molecules contributes to the regulation of spermatogenesis. A cell-tocell communication within the testes of these factors is a fundamental requirement of normal spermatogenesis. A noteworthy development has been made recently on discovering the effects of different somatic cells including Leydig, Sertoli, and peritubular myoid cells on manipulation the fate of spermatogonial stem cells. In this review, we discuss the self-renewal, differentiation, and apoptotic roles of somatic cells and the relationship between somatic and germ cells during normal spermatogenesis. We also summarize the roles of different growth factors, their paracrine/endocrine/autocrine pathways, and the different cytokines associated with spermatogenesis. Furthermore, we highlight important matters for further studies on the regulation of spermatogenesis. This review presents an insight into the mechanism of spermatogenesis, and helpful in developing better understanding of the functions of somatic cells, particularly in stallions and would offer new research goals for developing curative techniques to address infertility/subfertility in stallions.
Abstract
Spermatogenesis and testis development are highly structured physiological processes responsible for post-pubertal fertility in stallions. Spermatogenesis comprises spermatocytogenesis, meiosis, and spermiogenesis. Although germ cell degeneration is a continuous process, its effects are more pronounced during spermatocytogenesis and meiosis. The productivity and efficiency of spermatogenesis are directly linked to pubertal development, degenerated germ cell populations, aging, nutrition, and season of the year in stallions. The multiplex interplay of germ cells with somatic cells, endocrine and paracrine factors, growth factors, and signaling molecules contributes to the regulation of spermatogenesis. A cell-tocell communication within the testes of these factors is a fundamental requirement of normal spermatogenesis. A noteworthy development has been made recently on discovering the effects of different somatic cells including Leydig, Sertoli, and peritubular myoid cells on manipulation the fate of spermatogonial stem cells. In this review, we discuss the self-renewal, differentiation, and apoptotic roles of somatic cells and the relationship between somatic and germ cells during normal spermatogenesis. We also summarize the roles of different growth factors, their paracrine/endocrine/autocrine pathways, and the different cytokines associated with spermatogenesis. Furthermore, we highlight important matters for further studies on the regulation of spermatogenesis. This review presents an insight into the mechanism of spermatogenesis, and helpful in developing better understanding of the functions of somatic cells, particularly in stallions and would offer new research goals for developing curative techniques to address infertility/subfertility in stallions.
참고문헌 (113)
- Varner DD, "Stallion fertility : a focus on the spermatozoon", Equine Vet J, 47, pp.16~24 (2015)[DOI]
- Zhou R, "The roles and mechanisms of Leydig cells and myoid cells in regulating spermatogenesis", Cell Mol Life Sci, 76, pp.2681~2695 (2019)[DOI]
- Johnson L, "Temporal appearance of seasonal changes in numbers of Sertoli cells, Leydig cells, and germ cells in stallions", Biol Reprod, 40, pp.994~999 (1989)[DOI]
- Johnson L, "Efficiency of spermatogenesis", Microsc Res Tech, 32, pp.385~422 (1995)[DOI]
- Johnson L, "Age-related and seasonal variation in the Sertoli cell population, daily sperm production and serum concentrations of follicle-stimulating hormone, luteinizing hormone and testosterone in stallions", Biol Reprod, 29, pp.777~789 (1983)[DOI]
- Chamindrani Mendis-Handagama SML, "Differentiation of the adult Leydig cell population in the postnatal testis", Biol Reprod, 65, pp.660~671 (2001)[DOI]
- Tajima Y, "Insulin-like growth factor-I and transforming growth factor-α stimulate differentiation of type A spermatogonia in organ culture of adult mouse cryptorchid testes", Int J Androl, 18, pp.8~12 (1995)[DOI]
- Söder O, "Insulin-like growth factors selectively stimulate spermatogonial, but not meiotic, deoxyribonucleic acid synthesis during rat spermatogenesis", Endocrinology, 131, pp.2344~2350 (1992)[DOI]
- Hess MF, "The effects of age, season and fertility status on plasma and intratesticular insulin-like growth factor I concentration in stallions", Theriogenology, 56, pp.723~733 (2001)[DOI]
- Roser JF, "Endocrine and paracrine control of sperm production in stallions", Anim Reprod Sci, 68, pp.139~151 (2001)[DOI]
- Yoon MJ, "Localization of insulin-like growth factor-I(IGF-I)and IGF-I receptor(IGF-IR)in equine testes", Reprod Domest Anim, 46, pp.221~228 (2011)[DOI]
- Müller L, "Different expression of leptin and IGF1 in the adult and prepubertal testis in dogs", Reprod Domest Anim, 52, pp.187~192 (2017)[DOI]
- Yuan C, "Medaka igf1 identifies somatic cells and meiotic germ cells of both sexes", Gene, 642, pp.423~429 (2018)[DOI]
- Makanji Y, "Inhibin at 90 : from discovery to clinical application, a historical review", Endocr Rev, 35, pp.747~794 (2014)[DOI]
- McNeilly AS, "Production of inhibin A not B in rams : changes in plasma inhibin A during testis growth, and expression of inhibin", activin subunit mRNA and protein in adult testis, 2002, pp.123, 827~835
- Kaneko H, "Molecular weight forms of inhibin A and inhibin B in the bovine testis change with age", Biol Reprod, 68, pp.1918~1925 (2003)[DOI]
- Jin W, "Testicular secretion of inhibin in the male golden hamster : (Mesocricetus auratus)", J Androl, 22, pp.207~211 (2001)[DOI]
- Weng Q, "Immunolocalization of steroidogenic enzymes P450scc, 3βHSD, P450c17, and P450arom in Göttingen miniature pig testes", J Reprod Dev, 51, pp.299~304 (2005)[DOI]
- WoodruffTK, "Inhibin A and inhibin B are inversely correlated to follicle-stimulating hormone, yet are discordant during the follicular phase of the rat estrous cycle, and inhibin A is expressed in a sexually dimorphic manner", Endocrinology, 137, pp.5463~5467 (1996)[DOI]
- Nagata S, "Testicular inhibin in the stallion : cellular source and seasonal changes in its secretion", Biol Reprod, 59, pp.62~68 (1998)[DOI]
- Taya K, "Testicular secretion of inhibin in stallions", J Reprod Fertil Suppl, 56, pp.43~50 (2000)
- Pierik FH, "Serum inhibin B as a marker of spermatogenesis", J Clin Endocrinol Metab, 83, pp.3110~3114 (1998)[DOI]
- Kumanov P, "Inhibin B is a better marker of spermatogenesis than other hormones in the evaluation of male factor infertility", Fertil Steril, 86, pp.332~338 (2006)[DOI]
- Mabeck LM, "Fecundability according to male serum inhibin B—a prospective study among first pregnancy planners", Hum Reprod, 20, pp.2909~2915 (2005)[DOI]
- Stewart BL, "Effects of age, season, and fertility status on plasma and intratesticular immunoreactive(IR)inhibin concentrations in stallions", Domest Anim Endocrinol, 15, pp.129~139 (1998)[DOI]
- Roser JF, "Inhibin activity in the mare and stallion", Domest Anim Endocrinol, 11, pp.87~100 (1994)[DOI]
- Hedger MP, "Regulation of activin and inhibin in the adult testis and the evidence for functional roles in spermatogenesis and immunoregulation", Mol Cell Endocrinol, 359, pp.30~42 (2012)[DOI]
- Hakovirta H, "Effects of activin-A, inhibin-A, and transforming growth factor-beta 1 on stage-specific deoxyribonucleic acid synthesis during rat seminiferous epithelial cycle", Endocrinology, 133, pp.1664~1668 (1993)[DOI]
- de Kretser DM, "The role of activin, follistatin and inhibin in testicular physiology", Mol Cell Endocrinol, 225, pp.57~64 (2004)[DOI]
- Lejeune H, "Stimulating effect of both human recombinant inhibin A and activin A on immature porcine Leydig cell functions in vitro", Endocrinology, 138, pp.4783~4791 (1997)[DOI]
- Beg MA, "Follicle selection in cattle and horses : role of intrafollicular factors", Reproduction, 132, pp.365~377 (2006)[DOI]
- Arai KY, "Expression of inhibins, activins, insulin-like growth factor-I and steroidogenic enzymes in the equine placenta", Domest Anim Endocrinol, 31, pp.19~34 (2006)[DOI]
- Roser JF, "Regulation of testicular function in the stallion : an intricate network of endocrine, paracrine and autocrine systems", Anim Reprod Sci, 107, pp.179~196 (2008)[DOI]
- Tsogtgerel M, "Serum concentrations and testicular expressions of insulin-like peptide 3 and anti-Müllerian hormone in normal and cryptorchid male horses", Theriogenology, 154, pp.135~142 (2020)[DOI]
- Caprio M, "Ontogenesis of leptin receptor in rat Leydig cells", Biol Reprod, 68, pp.1199~1207 (2003)[DOI]
- Hombach-Klonisch S, "Seasonal expression of INSL3 and Lgr8", Insl3 receptor transcripts indicates variable differentiation of Leydig cells in the roe deer testis, 2004, pp.71, 1079~1087
- Sadeghian H, "Constitutive regulation of the Insl3gene in rat Leydig cells", Mol Cell Endocrinol, 241, pp.10~20 (2005)[DOI]
- Klonisch T, "INSL3 ligandreceptor system in the equine testis", Biol Reprod, 68, pp.1975~1981 (2003)[DOI]
- Shima Y, "Contribution of Leydig and Sertoli cells to testosterone production in mouse fetal testes", Mol Endocrinol, 27, pp.63~73 (2013)[DOI]
- Parlevliet JM, "Immunolocalization of estrogen and androgen receptors and steroid concentrations in the stallion epididymis", Theriogenology, 66, pp.755~765 (2006)[DOI]
- Pearl CA, "Immunolocalization of estrogen receptor alpha, estrogen beta and androgen receptor in the pre-, peri-and post-pubertal stallion testis", Anim Reprod Sci, 125, pp.103~111 (2011)[DOI]
- Bilinska B, "Immunoexpression of androgen receptors in the reproductive tract of the stallion", Ann NY Acad Sci, 1040, pp.227~229 (2005)[DOI]
- Antonio-Cabrera E, "Effects of chronic estradiol or testosterone treatment upon sexual behavior in sexually sluggish male rats", Pharmacol Biochem Behav, 101, pp.336~341 (2012)[DOI]
- Jarow JP, "The androgen microenvironment of the human testis and hormonal control of spermatogenesis", Ann NY Acad Sci, 1061, pp.208~220 (2005)[DOI]
- Willems A, "Sertoli cell androgen receptor signalling in adulthood is essential for post-meiotic germ cell development", Mol Reprod Dev, 82, pp.626~627 (2015)[DOI]
- Welsh M, "Androgen action via testicular peritubular myoid cells is essential for male fertility", FASEB J, 23, pp.4218~4230 (2009)[DOI]
- Haider SG, "Cell biology of Leydig cells in the testis", Int Rev Cytol, 233, pp.181~241 (2004)[DOI]
- O’Donnell L, "Testosterone promotes the conversion of round spermatids between stages VII and VIII of the rat spermatogenic cycle", Endocrinology, 135, pp.2608~2614 (1994)[DOI]
- O’Donnell L, "Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium", Biol Reprod, 55, pp.895~901 (1996)[DOI]
- Bartlett JMS, "The effect of selective destruction and regeneration of rat Leydig cells on the intratesticular distribution of testosterone and morphology of the seminiferous epithelium", J Androl, 7, pp.240~253 (1986)[DOI]
- Stanton PG, "Proteomic changes in rat spermatogenesis in response to in vivo androgen manipulation; impact on meiotic cells", PLOS ONE, 7, pp.e41718~ (2012)[DOI]
- Haywood M, "Sertoli and germ cell development in hypogonadal(hpg)mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone", Endocrinology, 144, pp.509~517 (2003)[DOI]
- Ing NH, "Dexamethasone acutely down-regulates genes involved in steroidogenesis in stallion testes", J Steroid Biochem Mol Biol, 143, pp.451~459 (2014)[DOI]
- Pelletier RM, "The blood-testis barrier : the junctional permeability, the proteins and the lipids", Prog Histochem Cytochem, 46, pp.49~127 (2011)[DOI]
- Holdcraft RW, "Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids", Development, 131, pp.459~467 (2004)[DOI]
- Kopera IA, "Sertoli–germ cell junctions in the testis : a review of recent data", Philos Trans R Soc B Biol Sci, 365, pp.1593~1605 (2010)[DOI]
- Jung Y, "Oxytocin receptor expression in stallion testes and epididymides", Domest Anim Endocrinol, 74, pp.106562~ (2021)[DOI]
- Frayne J, "Effect of oxytocin on testosterone production by isolated rat Leydig cells is mediated via a specific oxytocin receptor", Biol Reprod, 52, pp.1268~1273 (1995)[DOI]
- Nicholson HD, "Function of somatic cells in the testis", pp.278~285 (1994), Springer
- Tahri-Joutei A, "Time-related effects of arginine vasopressin on steroidogenesis in cultured mouse Leydig cells", J Reprod Fertil, 82, pp.247~254 (1988)[DOI]
- Inaba T, "Oxytocin gene expression and action in goat testis", Theriogenology, 52, pp.425~434 (1999)[DOI]
- Assinder SJ, "Regulation of 5α-reductase isoforms by oxytocin in the rat ventral prostate", Endocrinology, 145, pp.5767~5773 (2004)[DOI]
- Hess MF, "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, pp.7~19 (2005)[DOI]
- O’Shaughnessy PJ, "Effects of FSH on Leydig cell morphology and function in the hypogonadal mouse", J Endocrinol, 135, pp.517~525 (1992)[DOI]
- Sipahutar H, "Immunolocalization of aromatase in stallion Leydig cells and seminiferous tubules", J Histochem Cytochem, 51, pp.311~318 (2003)[DOI]
- Hejmej A, "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, pp.534~547 (2005)[DOI]
- Hess MF, "Immunocytochemical localization of cytochrome P450 aromatase in the testis of prepubertal, pubertal, and postpubertal horses", Theriogenology, 61, pp.293~299 (2004)[DOI]
- Oatley JM, "The germline stem cell niche unit in mammalian testes", Physiol Rev, 92, pp.577~595 (2012)[DOI]
- Chui K, "Characterization and functionality of proliferative human Sertoli cells", Cell Transplant, 20, pp.619~635 (2011)[DOI]
- Li Y, "In vitro effects of cannabidiol and its main metabolites in mouse and human Sertoli cells", Food Chem Toxicol, 159, pp.112722~ (2022)[DOI]
- Costa GMJ, "Spermatogonial stem cell markers and niche in equids", PLOS ONE, 7, pp.e44091~ (2012)[DOI]
- Hai Y, "The roles and regulation of Sertoli cells in fate determinations of spermatogonial stem cells and spermatogenesis", Semin Cell Dev Biol, 29, pp.66~75 (2014)[DOI]
- Koubova J, "Retinoic acid regulates sex-specific timing of meiotic initiation in mice", Proc Natl Acad Sci USA, 103, pp.2474~2479 (2006)[DOI]
- Pellegrini M, "ATRA and KL promote differentiation toward the meiotic program of male germ cells", Cell Cycle, 7, pp.3878~3888 (2008)[DOI]
- van Pelt AMM, "Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice", Biol Reprod, 43, pp.363~367 (1990)[DOI]
- Harman D, "Aging : phenomena and theories", Ann NY Acad Sci, 854, pp.1~7 (1998)[DOI]
- Jiang H, "Quantitative histological analysis and ultrastructure of the aging human testis", Int Urol Nephrol, 46, pp.879~885 (2014)[DOI]
- Hellstrom WJG, "Semen and sperm reference ranges for men 45 years of age and older", J Androl, 27, pp.421~428 (2006)[DOI]
- Sayed RKA, "Lack of retinoid acid receptor-related orphan receptor alpha accelerates and melatonin supplementation prevents testicular aging", Aging, 12, pp.12648~12668 (2020)[DOI]
- Sayed RKA, "Retinoid-related orphan nuclear receptor alpha(RORα)-deficient mice display morphological testicular defects", Lab Invest, 99, pp.1835~1849 (2019)[DOI]
- Pellegrini M, "Developmental expression of BMP4", ALK3, J Cell Sci, pp.2003, 116[DOI]
- Yang Y, "BMP4 cooperates with retinoic acid to induce the expression of differentiation markers in cultured mouse spermatogonia", Stem Cells Int, 2016, pp.9536192~ (2016)[DOI]
- Jung H, "The KIT is a putative marker for differentiating spermatogonia in stallions", Anim Reprod Sci, 152, pp.39~46 (2015)[DOI]
- Feng LX, "Stem cell factor", c-kit up-regulates cyclin D3 and promotes cell cycle progression via the phosphoinositide 3-kinase, J Biol Chem, pp.2000, 275[DOI]
- Feng LX, "Generation and in vitro differentiation of a spermatogonial cell line", Science, 297, pp.392~395 (2002)[DOI]
- Donnelly CL, "The effects of growth factor on testicular germ cell apoptosis in the stallion", J Equine Vet Sci, 27, pp.212~216 (2007)[DOI]
- Meng X, "Regulation of cell fate decision of undifferentiated spermatogonia by GDNF", Science, 287, pp.1489~1493 (2000)[DOI]
- He Z, "Gdnf upregulates c-Fos transcription via the Ras", Erk1, Stem Cells, pp.2008, 26[DOI]
- Hofmann MC, "Isolation of male germ-line stem cells; influence of GDNF", Dev Biol, 279, pp.114~124 (2005)[DOI]
- Teubner A, "Effects of an anabolic steroid(Durateston)on testicular angiogenesis in peripubertal stallions", Theriogenology, 84, pp.323~332 (2015)[DOI]
- Kubota H, "Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells", Proc Natl Acad Sci USA, 101, pp.16489~16494 (2004)[DOI]
- Allan DJ, "Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat", Cell Prolif, 25, pp.241~250 (1992)[DOI]
- Welt C, "Activins, inhibins, and follistatins : from endocrinology to signaling. A paradigm for the new millennium", Exp Biol Med, 227, pp.724~752 (2002)[DOI]
- Gao T, "Transferrin receptor(TFRC)is essential for meiotic progression during mouse spermatogenesis", Zygote, 29, pp.169~175 (2021)[DOI]
- Zhang Z, "Direct transdifferentiation of spermatogonial stem cells to morphological, phenotypic and functional hepatocyte-like cells via the ERK1", 2 and Smad2, Cell Commun Signal, pp.2013, 11[DOI]
- Sharpe RM, "Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood", Reproduction, 125, pp.769~784 (2003)[DOI]
- Salian S, "Neonatal exposure of male rats to bisphenol A impairs fertility and expression of sertoli cell junctional proteins in the testis", Toxicology, 265, pp.56~67 (2009)[DOI]
- Abel MH, "Spermatogenesis and sertoli cell activity in mice lacking sertoli cell receptors for folliclestimulating hormone and androgen", Endocrinology, 149, pp.3279~3285 (2008)[DOI]
- Skinner MK, "Sertoli cell biology" (2004), Elsevier
- Losinno AD, "Peritubular myoid cells from rat seminiferous tubules contain actin and myosin filaments distributed in two independent layers", Biol Reprod, 86, pp.150~ (2012)[DOI]
- Skinner MK, "Cooperativity between Sertoli cells and testicular peritubular cells in the production and deposition of extracellular matrix components", J Cell Biol, 100, pp.1941~1947 (1985)[DOI]
- Nurmio M, "Peritubular myoid cells have a role in postnatal testicular growth", Spermatogenesis, 2, pp.79~87 (2012)[DOI]
- Chen LY, "Targeting the Gdnf gene in peritubular myoid cells disrupts undifferentiated spermatogonial cell development", Proc Natl Acad Sci USA, 113, pp.1829~1834 (2016)[DOI]
- Chen LY, "Peritubular myoid cells participate in male mouse spermatogonial stem cell maintenance", Endocrinology, 155, pp.4964~4974 (2014)[DOI]
- Quigley CA, "Androgen receptor defects : historical, clinical, and molecular perspectives", Endocr Rev, 16, pp.271~321 (1995)[DOI]
- Welsh M, "Androgen receptor signalling in peritubular myoid cells is essential for normal differentiation and function of adult Leydig cells", Int J Androl, 35, pp.25~40 (2012)[DOI]
- Skinner MK, "Identification of a non-mitogenic paracrine factor involved in mesenchymal-epithelial cell interactions between testicular peritubular cells and Sertoli cells", Mol Cell Endocrinol, 44, pp.85~97 (1986)[DOI]
- Piquet-Pellorce C, "Leukemia inhibitory factor expression and regulation within the testis", Endocrinology, 141, pp.1136~1141 (2000)[DOI]
- Maekawa M, "Peritubular myoid cells in the testis : their structure and function", Arch Histol Cytol, 59, pp.1~13 (1996)[DOI]
- Oatley JM, "Colony stimulating factor 1 is an extrinsic stimulator of mouse spermatogonial stem cell self-renewal", Development, 136, pp.1191~1199 (2009)[DOI]
- Virtanen I, "Peritubular myoid cells of human and rat testis are smooth muscle cells that contain desmin-type intermediate filaments", Anat Rec, 215, pp.10~20 (1986)[DOI]
- Lydka M, "Vimentin expression in testes of Arabian stallions", Equine Vet J, 43, pp.184~189 (2011)[DOI]
- Show MD, "Reduced intratesticular testosterone concentration alters the polymerization state of the Sertoli cell intermediate filament cytoskeleton by degradation of vimentin", Endocrinology, 144, pp.5530~5536 (2003)[DOI]
