Regulation of spermatogenesis: An evolutionary biologist's perspective

Seminars in Cell and Developmental Biology

Volumn 29, Issue , 2014, Pages 2-16

  Schlatt, Stefan ^a   Ehmcke, Jens ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Evolution; FSH; LH; Sperm; Spermatogenesis; Spermatogonia; Steroidogenesis; Testis; Testosterone

Indexed keywords

ANDROGEN; FOLLITROPIN; GONADORELIN; GONADOTROPIN; GROWTH FACTOR; HORMONE RECEPTOR; INHIBIN; INHIBIN B; LUTEINIZING HORMONE; STEROID HORMONE; TESTOSTERONE;

BLOOD TESTIS BARRIER; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; FEEDBACK SYSTEM; GAMETOGENESIS; GERM CELL; HORMONAL REGULATION; HUMAN; HYPOPHYSIS GONAD SYSTEM; LEYDIG CELL; MALE; MEIOSIS; NONHUMAN; ORGANOGENESIS; PARACRINE SIGNALING; PROPHASE; REVIEW; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; STEROIDOGENESIS; TESTIS; TESTIS FUNCTION; ANIMAL; BIOSYNTHESIS; CYTOLOGY; HAMSTER; MACACA; METABOLISM; MOUSE; PHYSIOLOGY; RAT; SPERMATOZOON;

CRICETINAE; PRIMATES; RODENTIA;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CRICETINAE; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; HUMANS; INHIBINS; LUTEINIZING HORMONE; MACACA; MALE; MICE; RATS; SPERMATOGENESIS; SPERMATOGONIA; SPERMATOZOA; TESTIS; TESTOSTERONE;

EID: 84901591375     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2014.03.007     Document Type: Review

References (138)

1. Clermont Y. Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972, 52:198-236.
2. de Kretser D.M., Kerr J.B. The cytology of the testis. The physiology of reproduction 1988, vol. 1:837-932. Raven Press, New York.
3. Russell L.D., Ettlin R.A., Sinha Hikim A.P., Clegg E.D. Histological and histopathological evaluation of the testis 1990, Cache River Press, Clearwater, FL.
4. Russell L. Role in spermiation. The Sertoli cell 1993, 269-302. Cache River Press, Clearwater, FL. L.D. Russell, M.D. Griswold (Eds.).
5. Awoniyi C.A., Santulli R., Sprando R.L., Ewing L.L., Zirkin B.R. Restoration of advanced spermatogenic cells in the experimentally regressed rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinology 1989, 124:1217-1223.
6. El Shennawy A., Gates R.J., Russell L.D. Hormonal regulation of spermatogenesis in the hypophysectomized rat: cell viability after hormonal replacement in adults after intermediate periods of hypophysectomy. J Androl 1998, 19:320-334.
7. Marshall G.R., Zorub D.S., Plant T.M. Follicle-stimulating hormone amplifies the population of differentiated spermatogonia in the hypophysectomized testosterone-replaced adult rhesus monkey (Macaca mulatta). Endocrinology 1995, 136:3504-3511.
8. McLachlan R.I., Wreford N.G., de Kretser D.M., Robertson D.M. The effects of recombinant follicle stimulating hormone on the restoration of spermatogenesis in the gonadotropin-releasing hormone-immunized adult rat. Endocrinology 1995, 136:4035-4043.
9. Meachem S.J., Wreford N.G., Stanton P.G., Robertson D.M., McLachlan R.I. Follicle-stimulating hormone is required for the initial phase of spermatogenic restoration in adult rats following gonadotropin suppression. J Androl 1998, 19:725-735.
10. Meachem S.J., McLachlan R.I., Stanton P.G., Robertson D.M., Wreford N.G. FSH immunoneutralization acutely impairs spermatogonial development in normal adult rats. J Androl 1999, 20:756-762.
11. Russell L.D., Clermont Y. Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anat Rec 1977, 187:347-366.
12. Sinha Hikim A.P., Swerdloff R.S. Temporal and stage-specific effects of recombinant human follicle-stimulating hormone on the maintenance of spermatogenesis in gonadotropin-releasing hormone antagonist-treated rat. Endocrinology 1995, 136:253-261.
13. Weinbauer G.F., Behre H.M., Fingscheidt U., Nieschlag E. Human follicle-stimulating hormone exerts a stimulatory effect on spermatogenesis, testicular size, and serum inhibin levels in the gonadotropin-releasing hormone antagonist-treated nonhuman primate (Macaca fascicularis). Endocrinology 1991, 129:1831-1839.
14. Weinbauer G.F., Gockeler E., Nieschlag E. Testosterone prevents complete suppression of spermatogenesis in the gonadotropin-releasing hormone antagonist-treated nonhuman primate (Macaca fascicularis). J Clin Endocrinol Metab 1988, 67:284-290.
15. Cooke H.J., Saunders P.T. Mouse models of male infertility. Nat Rev Genet 2002, 3:790-801.
16. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr Rev 1999, 20:358-417.
17. Weinbauer G.F., Gromoll J., Simoni M., Nieschlag E. Physiology of testicular function. Andrology, male reproductive health and dysfunction 1997, 25-57. [Chapter 3]. 1st ed. E. Nieschlag, H.M. Behre (Eds.).
18. Reuter K., Schlatt S., Ehmcke J., Wistuba J. Fact or fiction: in vitro spermatogenesis. Spermatogenesis 2012, 2:245-252.
19. Kanatsu-Shinohara M., Shinohara T. Culture and genetic modification of mouse germline stem cells. Ann N Y Acad Sci 2007, 1120:59-71.
20. Dym M., Fawcett D.W. The blood-testis barrier in the rat and the physiological compartmentation of the seminiferous epithelium. Biol Reprod 1970, 3:308-326.
21. Christensen A.K. Leydig cells. Handbook of physiology. Section 7 1975, vol. 5:57-94. American Physiological Society, Washington, DC.
22. Gondos B., Berndston W.E. Postnatal and pubertal development. The Sertoli cell 1994, 116-153. Cache River Press, Clearwater, FL. L.D. Russell, M.D. Griswold (Eds.).
23. Orth J.M. Proliferation of Sertoli cells in fetal and postnatal rats: a quantitative autoradiographic study. Anat Rec 1982, 203:485-492.
24. Meachem S.J., McLachlan R.I., de Kretser D.M., Robertson D.M., Wreford N.G. Neonatal exposure of rats to recombinant follicle stimulating hormone increases adult Sertoli and spermatogenic cell numbers. Biol Reprod 1996, 54:36-44.
25. Cooke P.S., Zhao Y.D., Bunick D. Triiodothyronine inhibits proliferation and stimulates differentiation of cultured neonatal Sertoli cells: possible mechanism for increased adult testis weight and sperm production induced by neonatal goitrogen treatment. Biol Reprod 1994, 51:1000-1005.
26. Huhtaniemi I.T., Nevo N., Amsterdam A., Naor Z. Effect of postnatal treatment with a gonadotropin-releasing hormone antagonist on sexual maturation of malerats. Biol Reprod 1986, 35:501-507.
27. Sharpe R.M., Atanassova N., McKinnell C., Parte P., Turner K.J., Fisher J.S., et al. Abnormalities in functional development of the Sertoli cells in rats treated neonatally with diethylstilbestrol: a possible role for estrogens in Sertoli cell development. Biol Reprod 1998, 59:1084-1094.
28. Janecki A., Steinberger A. Polarized Sertoli cell functions in a new two-compartment culture system. J Androl 1986, 7(1):69-71.
29. Handelsman D.J., Spaliviero J.A., Kidston E., Robertson D.M. Highly polarized secretion of inhibin by Sertoli cells in vitro. Endocrinology 1989, 125(2):721-729.
30. Russell L.D. Form, dimensions and cytology of mammalian Sertoli cells. The Sertoli cell 1993, 1-38. Cache River Press, Clearwater, FL. L.D. Russell, M.D. Griswold (Eds.).
31. Blüm V. Vergleichende Reproduktionsbiologie der Wirbeltiere 1985, 1-109. Springer Verlag, Berlin.
32. Penzlin H. Lehrbuch der Tierphysiologie 1970, 1-513. Gustav Fischer Verlag, Stuttgart.
33. Leblond C.P., Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 1952, 548-573.
34. Leblond C.P., Clermont Y. Spermiogenesis of rat, mouse and guinea pig as revealed by the 'periodic acid-fuchsin sulfurus acid' technique. Am J Anat 1952, 90:167-206.
35. de Rooij D.G., Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000, 21:776-798.
36. Meachem S., von Schönfeldt V., Schlatt S. Spermatogonia: stem cells with a great perspective. Reproduction 2001, 121:825-834.
37. McLean D.J., Johnston D.S., Russell L.D., Griswold M.D. Germ cell transplantation and the study of testicular function. Trends Endocrinol Metab 2001, 12:16-21.
38. Meistrich M.L., van Beek M.E. Spermatogonial stem cells. Cell and molecular biology of the testis 1993, 266-295. Oxford University Press, New York. C. Desjardins, L.L. Ewing (Eds.).
39. Schlatt S., Weinbauer G.F. Immunohistochemical localization of proliferating cell nuclear antigen as a tool to study cell proliferation in rodent and primate testes. Int J Androl 1994, 17:214-222.
40. Clermont Y. Two classes of spermatogonial stem cells in the monkey (Cercopithecus aethiops). Am J Anat 1969, 126:57-71.
41. van Alphen M.M., van de Kant H.J., de Rooij D.G. Depletion of the spermatogonia from the seminiferous epithelium of the rhesus monkey after X irradiation. Radiat Res 1988, 113:473-486.
42. van Alphen M.M., van de Kant H.J., de Rooij D.G. Repopulation of the seminiferous epithelium of the rhesus monkey after X irradiation. Radiat Res 1988, 113:487-500.
43. Schulze C. Morphological characteristics of the spermatogonial stem cells in man. Cell Tissue Res 1979, 198:191-199.
44. Schulze C. Survival of human spermatogonial stem cells in various clinical conditions. Fortschr Androl 1981, 7:58-68.
45. Fouquet J.P., Dadoune J.P. Renewal of spermatogonia in the monkey (Macaca fascicularis). Biol Reprod 1986, 35:199-207.
46. O'Donnell L., Narula A., Balourdos G., Gu Y.Q., Wreford N.G., Robertson D.M., et al. Impairment of spermatogonial development and spermiation after testosterone-induced gonadotropin suppression in adult monkeys (Macaca fascicularis). J Clin Endocrinol Metab 2001, 86:1814-1822.
47. Braun R.E. Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 1998, 9:483-489.
48. De Rooij D.G., Lok D., Weenk D. Feedback regulation of the proliferation of the undifferentiated spermatogonia in the Chinese hamster by the differentiating spermatogonia. Cell Tissue Kinet 1985, 18:71-81.
49. de Rooij D.G., van Alphen M.M., van de Kant H.J. Duration of the cycle of the seminiferous epithelium and its stages in the rhesus monkey (Macaca mulatta). Biol Reprod 1986, 35(3):587-591.
50. Schulze W., Rehder U. Organization and morphogenesis of the human seminiferous epithelium. Cell Tissue Res 1984, 237(3):395-407.
51. Schulze W., Riemer M., Rehder U., Hohne K.H. Computer-aided three-dimensional reconstructions of the arrangement of primary spermatocytes in human seminiferous tubules. Cell Tissue Res 1986, 244:1-7.
52. Millar M.R., Sharpe R.M., Weinbauer G.F., Fraser H.M., Saunders P.T. Marmoset spermatogenesis: organizational similarities to the human. Int J Androl 2000, 23:266-277.
53. Heller C.G., Clermont Y. Spermatogenesis in man: an estimation of its duration. Science 1963, 140:184-186.
54. Franca L.R., Ogawa T., Avarbock M.R., Brinster R.L., Russell L.D. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998, 59:1371-1377.
55. Dobrinski I. Transplantation of germ cells and testis tissue for the study and preservation of fertility. Soc Reprod Fertil Suppl 2007, 65:447-458.
56. Timmons P.M., Rigby P.W., Poirier F. The murine seminiferous epithelial cycle is pre-figured in the Sertoli cells of the embryonic testis. Development 2002, 129:635-647.
57. de Rooij D.G. The spermatogonial stem cell niche. Microsc Res Tech 2009, 72:580-585.
58. Stukenborg J.B., Wistuba J., Luetjens C.M., Elhija M.A., Huleihel M., Lunenfeld E., et al. Coculture of spermatogonia with somatic cells in a novel three-dimensional soft-agar-culture-system. J Androl 2008, 29:312-329.
59. Kanatsu-Shinohara M., Toyokuni S., Morimoto T., Matsui S., Honjo T., Shinohara T. Functional assessment of self-renewal activity of male germline stem cells following cytotoxic damage and serial transplantation. Biol Reprod 2003, 68:1801-1807.
60. Ogawa T., Ohmura M., Yumura Y., Sawada H., Kubota Y. Expansion of murine spermatogonial stem cells through serial transplantation. Biol Reprod 2003, 68:316-322.
61. Clermont Y., Leblond C.P. Differentiation and renewal of spermatogonia in the monkey, Macaca rhesus. Am J Anat 1959, 104:237-273.
62. Clermont Y. Renewal of spermatogonia in man. Am J Anat 1966, 118:509-524.
63. Luo J., Megee S., Dobrinski I. Asymmetric distribution of UCH-L1 in spermatogonia is associated with maintenance and differentiation of spermatogonial stem cells. J Cell Physiol 2009, 220:460-468.
64. Suzuki H., Sada A., Yoshida S., Saga Y. The heterogeneity of spermatogonia is revealed by their topology and expression of marker proteins including the germ cell-specific proteins Nanos2 and Nanos3. Dev Biol 2009, 336:222-231.
65. Schrans-Stassen B.H., van de Kant H.J., de Rooij D.G., van Pelt A.M. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999, 140:5894-5900.
66. Buaas F.W., Kirsh A.L., Sharma M., McLean D.J., Morris J.L., Griswold M.D., et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004, 36:647-652.
67. Wu X., Schmidt J.A., Avarbock M.R., Tobias J.W., Carlson C.A., Kolon T.F., et al. Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules. Proc Natl Acad Sci U S A 2009, 106:21672-21677.
68. Gassei K., Ehmcke J., Schlatt S. Efficient enrichment of undifferentiated GFR alpha 1+ spermatogonia from immature rat testis by magnetic activated cell sorting. Cell Tissue Res 2009, 337:177-183.
69. Gassei K., Ehmcke J., Dhir R., Schlatt S. Magnetic activated cell sorting allows isolation of spermatogonia from adult primate testes and reveals distinct GFRa1-positive subpopulations in men. J Med Primatol 2010, 39:83-91.
70. Hermann B.P., Sukhwani M., Simorangkir D.R., Chu T., Plant T.M., Orwig K.E. Molecular dissection of the male germ cell lineage identifies putative spermatogonial stem cells in rhesus macaques. Hum Reprod 2009, 24:1704-1716.
71. Hermo L., Pelletier R.M., Cyr D.G., Smith C.E. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: Background to spermatogenesis, spermatogonia, and spermatocytes. Microsc Res Tech 2010, 73:241-278.
72. von Kopylow K., Kirchhoff C., Jezek D., Schulze W., Feig C., Primig M., et al. Screening for biomarkers of spermatogonia within the human testis: a whole genome approach. Hum Reprod 2010, 25:1104-1112.
73. Phillips B.T., Gassei K., Orwig K.E. Spermatogonial stem cell regulation and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010, 365:1663-1678.
74. De Rooij D.G., Grootegoed J.A. Spermatogonial stem cells. Curr Opin Cell Biol 1998, 10:694-701.
75. de Rooij D.G. Stem cells in the testis. Int J Exp Pathol 1998, 79:67-80.
76. Buageaw A., Sukhwani M., Ben-Yehudah A., Ehmcke J., Rawe V.Y., Pholpramool C., et al. GDNF family receptor alpha1 phenotype of spermatogonial stem cells in immature mouse testes. Biol Reprod 2005, 73:1011-1016.
77. Ehmcke J., Luetjens C.M., Schlatt S. Clonal organization of proliferating spermatogonial stem cells in adult males of two species of non-human primates, Macaca mulatta and Callithrix jacchus. Biol Reprod 2005, 72:293-300.
78. Ehmcke J., Simorangkir D.R., Schlatt S. Identification of the starting point for spermatogenesis and characterization of the testicular stem cell in adult male rhesus monkeys. Hum Reprod 2005, 20:1185-1193.
79. Hermann B.P., Sukhwani M., Hansel M.C., Orwig K.E. Spermatogonial stem cells in higher primates: are there differences from those in rodents?. Reproduction 2010, 139:479-493.
80. Simorangkir D.R., Marshall G.R., Plant T.M. A re-examination of proliferation and differentiation of type A spermatogonia in the adult rhesus monkey (Macaca mulatta). Hum Reprod 2009, 24:1596-1604.
81. Day I.N., Thompson R.J. UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein. Prog Neurobiol 2010, 90:327-362.
82. Klein A.M., Nakagawa T., Ichikawa R., Yoshida S., Simons B.D. Mouse germ line stem cells undergo rapid and stochastic turnover. Cell Stem Cell 2010, 6:214-224.
83. Huckins C., Oakberg E.F. Morphological and quantitative analysis of spermatogonia in mouse testes using whole mounted seminiferous tubules. I: The normal testes. Anat Rec 1978, 192:519-528.
84. Lok D., Weenk D., de Rooij D.G. Morphology, proliferation and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat Rec 1982, 203:83-99.
85. Ehmcke J., Wistuba J., Schlatt S. Spermatogonial stem cells: questions, models and perspectives. Hum Reprod Update 2006, 12:275-282.
86. Clermont Y. The cycle of the seminiferous epithelium in man. Am J Anat 1963, 112:35-51.
87. Clermont Y. Stermatogenesis in man. A study of the spermatogonial population. Fertil Steril 1966, 17:705-721.
88. Clermont Y., Antar M. Duration of the cycle of the seminiferous epithelium and the spermatogonial renewal in the monkey, Macaca arctoides. Am J Anat 1973, 136:153-165.
89. Ehmcke J., Hübner K., Schöler H.R., Schlatt S. Spermatogonia: origin, physiology and prospects for conservation and manipulation of the male germ line. Reprod Fertil Dev 2006, 18:7-12.
90. Simorangkir D.R., Marshall G.R., Ehmcke J., Schlatt S., Plant T.M. Prepubertal expansion of dark and pale type A spermatogonia in the rhesus monkey (Macaca mulatta) results from proliferation during infantile and juvenile development in a relatively gonadotropin independent manner. Biol Reprod 2005, 73:1109-1115.
91. Ehmcke J., Schlatt S. A revised model for spermatogonial expansion in man: lessons from non-human primates. Reproduction 2006, 132:673-680.
92. Ogawa T., Ohmura M., Ohbo K. The niche for spermatogonial stem cells in the mammalian testis. Int J Hematol 2005, 82:381-388.
93. Chuma S., Kanatsu-Shinohara M., Inoue K., Ogonuki N., Miki H., Toyokuni S., et al. Spermatogenesis from epiblast and primordial germ cells following transplantation into postnatal mouse testis. Development 2005, 132:117-122.
94. Nayernia K., Drabent B., Meinhardt A., Adham I.M., Schwandt I., Müller C., et al. Triple knockouts reveal gene interactions affecting fertility of male mice. Mol Reprod Dev 2005, 70:406-416.
95. Chiarini-Garcia H., Raymer A.M., Russell L.D. Non-random distribution of spermatogonia in rats: evidence of niches in the seminiferous tubules. Reproduction 2003, 126:669-680.
96. Yoshida S., Sukeno M., Nabeshima Y. A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 2007, 317:1722-1726.
97. Niklowitz P., Lerchl A., Nieschlag E. Photoperiodic responses in Djungarian hamsters (Phodopus sungorus): importance of light history for pineal and serum melatonin profiles. Biol Reprod 1994, 51:714-724.
98. Ramaswamy S., Marshall G.R., McNeilly A.S., Plant T.M. Evidence that in a physiological setting Sertoli cell number is the major determinant of circulating concentrations of inhibin B in the adult male rhesus monkey (Macaca mulatta). J Androl 1999, 20:430-434.
99. Schlatt S., Gassei K., Westernströer B., Ehmcke J. Modulating testicular mass in xenografting: a model to explore testis development and endocrine function. Endocrinology 2010, 151:4018-4023.
100. Schlatt S., Westernströer B., Gassei K., Ehmcke J. Donor-host involvement in immature rat testis xenografting into nude mouse hosts. Biol Reprod 2010, 82(5):888-895.
101. Schlatt S., Kim S.S., Gosden R. Spermatogenesis and steroidogenesis in mouse, hamster and monkey testicular tissue after cryopreservation and heterotopic grafting to castrated hosts. Reproduction 2002, 124:339-346.
102. Wreford N.G., Rajendra Kumar T., Matzuk M.M., de Kretser D.M. Analysis of the testicular phenotype of the follicle-stimulating hormone beta-subunit knockout and the activin type II receptor knockout mice by stereological analysis. Endocrinology 2001, 142:2916-2920.
103. Kumar T.R., Wang Y., Lu N., Matzuk M.M. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997, 15:201-204.
104. Johnston H., Baker P.J., Abel M., Charlton H.M., Jackson G., Fleming L., et al. Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology 2004, 145:318-329.
105. Baker P.J., Pakarinen P., Huhtaniemi I.T., Abel M.H., Charlton H.M., Kumar T.R., et al. Failure of normal Leydig cell development in follicle-stimulating hormone (FSH) receptor-deficient mice, but not FSHbeta-deficient mice: role for constitutive FSH receptor activity. Endocrinology 2003, 144:138-145.
106. Allan C.M., Haywood M., Swaraj S., Spaliviero J., Koch A., Jimenz M., et al. A novel transgenic model to characterize the specific effects of follicle-stimulating hormone on gonadal physiology in the absence of lutenizing hormone actions. Endocrinology 2001, 142:2200-2213.
107. Dierich A., Sairam M.R., Monoco L., Fimia G.M., Gansmuller A., Lemeur M., et al. Impaired follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci U S A 1998, 95:13612-13617.
108. Abel M.H., Wootton A.N., Wilkins V., Huhtaniemi I., Knight P.G., Charlton H.M. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 2000, 141:1795-1803.
109. Krishnamurthy H., Kats R., Danilovich N., Javeshghani D., Sairam M.R. Intercellular communication between Sertoli cells and Leydig cells in the absence of follicle-stimulating hormone-receptor signaling. Biol Reprod 2001, 65:1201-1207.
110. Grover A., Sairam M.R., Smith C.E., Hermo L. Structural and functional modifications of sertoli cells in the testis of adult follicle-stimulating hormone receptor knockout mice. Biol Reprod 2004, 71:117-129.
111. Abel M.H., Baker P.J., Charlton H.M., Monteiro A., Verhoeven G., De Gendt K., et al. Spermatogenesis and sertoli cell activity in mice lacking sertoli cell receptors for follicle-stimulating hormone and androgen. Endocrinology 2008, 149:3279-3285.
112. Haywood M., Spaliviero J., Jimemez M., King N.J., Handelsman D.J., Allan C.M. Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 2003, 144:509-517.
113. O'Shaughnessy P.J., Monteiro A., Verhoeven G., De Gendt K., Abel M.H. Effect of FSH on testicular morphology and spermatogenesis in gonadotrophin-deficient hypogonadal mice lacking androgen receptors. Reproduction 2010, 139:177-184.
114. Singh J., Handelsman D.J. The effects of recombinant FSH on testosterone-induced spermatogenesis in gonadotropin deficient (hpg) mice. J Androl 1996, 17:382-393.
115. Siegel E.T., Kim H.G., Nishimoto H.K., Layman L.C. The molecular basis of impaired follicle-stimulating hormone action: evidence from human mutations and mouse models. Reprod Sci 2013, 20(3):211-233.
116. Niklowitz P., Khan S., Bergmann M., Hoffmann K., Nieschlag E. Differential effects of follicle-stimulating hormone and luteinizing hormone on Leydig cell function and restoration of spermatogenesis in hypophysectomized and photoinhibited Djungarian hamsters (Phodopus sungorus). Biol Reprod 1989, 41:871-880.
117. Schlatt S., de Geyter M., Kliesch S., Nieschlag E., Bergmann M. Spontaneous recrudescence of spermatogenesis in the photoinhibited male Djungarian hamster, Phodopus sungorus. Biol Reprod 1995, 53:169-1177.
118. Lerchl A., Sotiriadou S., Behre H.M., Pierce J., Weinbauer G.F., Kliesch S., et al. Restoration of spermatogenesis by follicle-stimulating hormone despite low intratesticular testosterone in photoinhibited hypogonadotropic Djungarian hamsters (Phodopus sungorus). Biol Reprod 1993, 49:1108-1116.
119. Niklowitz P., Lerchl A., Nieschlag E. In vitro fertilizing capacity of sperm from FSH-treated photoinhibited Djungarian hamsters (Phodopus sungorus). J Endocrinol 1997, 154:475-481.
120. Tarulli G.A., Stanton P.G., Lerchl A., Meachem S.J. Adult Sertoli cells are not terminally differentiated in the Djungarian hamster: effect of FSH on proliferation and junction protein organization. Biol Reprod 2006, 74:798-806.
121. Dankbar B., Brinkworth M.H., Schlatt S., Weinbauer G.F., Nieschlag E., Gromoll J. Ubiquitous expression of the androgen receptor and testis-specific expression of the FSH receptor in the cynomolgus monkey (Macaca fascicularis) revealed by a ribonuclease protection assay. J Steroid Biochem Mol Biol 1995, 55:35-41.
122. Plant T.M., Marshall G.R. The functional significance of FSH in spermatogenesis and the control of its secretion in male primates. Endocr Rev 2001, 22:764-786.
123. Phillip M., Arbelle J.E., Segev Y., Parvari R. Male hypogonadism due to a mutation in the gene for the β-subunit of follicle-stimulating hormone. N Engl J Med 1998, 338:1729-1732.
124. Lindstedt G., Nystrom E., Mathews C., Ernest I., Janson P.O., Chatterjee K. Follitropin (FSH) deficiency in an infertile male due to FSH-beta gene mutation: a syndrome of normal puberty and virulization but underdeveloped testicles with azoospermia, low FSH but high lutropin and normal serum testosterone concentrations. Clin Chem Lab Med 1998, 36:663-665.
125. Layman L.C., Porto A.L., Xie J., da Motta L.A., da Motta L.D., Weiser W., et al. FSH beta gene mutations in a female with partial breast development and a male sibling with normal puberty and azoospermia. J Clin Endocrinol Metab 2002, 87:3702-3707.
126. Mantovani G., Borgato S., Beck-Peccoz P., Romoli R., Borretta G., Persani L. Isolated follicle-stimulating hormone (FSH) deficiency in a young man with normal virilization who did not have mutations in the FSHbeta gene. Fertil Steril 2003, 79:434-436.
127. Giltay J.C., Deege M., Blankenstein R.A., Kastrop P.M., Wijmenga C., Lock T.T. Apparent primary follicle-stimulating hormone deficiency is a rare cause of treatable male infertility. Fertil Steril 2004, 81:693-696.
128. Gromoll J., Simoni M., Nieschlag E. An activating mutation of the follicle-stimulating hormone receptor autonomously sustains spermatogenesis in a hypophysectomized man. J Clin Endocrinol Metab 1996, 81:1367-1370.
129. Aravindan G.R., Gopalakrishnan K., Ravindranath N., Moudgal N.R. Effect of altering endogenous gonadotrophin concentrations on the kinetics of testicular germ cell turnover in the bonnet monkey (Macaca radiata). J Endocrinol 1993, 137:485-495.
130. van Alphen M.M.A., van de Kant H.J.G., de Rooij D.G. Follicle-stimulating hormone stimulates spermatogenesis in the adult monkey. Endocrinology 1988, 129:1831-1839.
131. Simorangkir D.R., Ramaswamy S., Marshall G.R., Pohl C.R., Plant T.M. A selective monotropic elevation of FSH, but not that of LH, amplifies the proliferation and differentiation of spermatogonia in the adult rhesus monkey (Macaca mulatta). Hum Reprod 2009, 24:1584-1595.
132. Arslan M., Weinbauer G.F., Schlatt S., Shahab M., Nieschlag E. FSH and testosterone, alone or in combination, initiate testicular growth and increase the number of spermatogonia and Sertoli cells in a juvenile non-human primate (Macaca mulatta). J Endocrinol 1993, 136:235-243.
133. Schlatt S., Arslan M., Weinbauer G.F., Behre H.M., Nieschlag E. Endocrine control of somatic cell and premeiotic germ cell development in the male rhesus monkey (Macaca mulatta). Eur J Endocrinol 1995, 133:235-247.
134. Ramaswamy S., Plant T.M., Marshall G.R. Pulsatile stimulation with recombinant single chain human lutenizing hormone elicits precocious Sertoli cell proliferation in the juvenile male rhesus monkey. Biol Reprod 2000, 63:82-88.
135. Ramaswamy S., Marshall G.R., McNeilly A.S., Plant T.M. Dynamics of the follicle-stimulating hormone (FSH)-inhibin B feedback loop and its role in regulating spermatogenesis in the adult male rhesus monkey (Macaca mulatta) as revealed by unilateral orchidectomy. Endocrinology 2000, 141:18-27.
136. Ramaswamy S., Marshall G.R., Pohl C.R., Friedman R.L., Plant T.M. Inhibitory and stimulatory regulation of testicular inhibin B secretion by luteinizing hormone and follicle-stimulating hormone, respectively, in the rhesus monkey (Macaca mulatta). Endocrinology 2003, 144:1175-1185.
137. Foppiani L., Schlatt S., Simoni M., Weinbauer G.F., Hacker-Klom U., Nieschlag Inhibin B is a more sensitive marker of spermatogenetic damage than FSH in the irradiated non-human primate model. J Endocrinol 1999, 162:393-400.
138. Schlatt S., Foppiani L., Rolf C., Weinbauer G.F., Nieschlag E. Germ cell transplantation into X-irradiated monkey testes. Hum Reprod 2002, 17:55-62.