FSH and testosterone signaling in Sertoli cells

Reproduction

Volumn 130, Issue 1, 2005, Pages 15-28

  Walker, William H ^a   Cheng, Jing ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FOLLITROPIN; FOLLITROPIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE A2; TESTOSTERONE; TRANSCRIPTION FACTOR;

CALCIUM CELL LEVEL; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DESENSITIZATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GERM CELL; HORMONE ACTION; HORMONE RECEPTOR INTERACTION; MALE; MALE FERTILITY; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REGULATORY MECHANISM; REVIEW; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOON MATURATION; TESTIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CALCIUM; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION; HUMANS; MALE; RECEPTORS, FSH; SERTOLI CELLS; SIGNAL TRANSDUCTION; TESTOSTERONE;

EID: 22544432534     PISSN: 14701626     EISSN: None     Source Type: Journal    
DOI: 10.1530/rep.1.00358     Document Type: Review

References (141)

1. Alam H, Maizels ET, Park Y, Ghaey S, Feiger ZJ, Chandel NS & Hunzicker-Dunn M 2004 Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT /Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. Journal of Biological Chemistry 279 19431-19440.
2. Allan CM, Garcia A, Spaliviero J, Zhang FP, Jimenez M, Huhtaniemi I & Handelsman DJ 2004 Complete Sertoli cell proliferation induced by follicle-stimulating hormone (FSH) independently of luteinizing hormone activity: evidence from genetic models of isolated FSH action. Endocrinology 145 1587-1593.
3. Bagchi MK, Tsai MJ, O'Malley BW & Tsai SY 1992 Analysis of the mechanism of steroid hormone receptor-dependent gene activation in cell-free systems. Endocrine Reviews 13 525-535.
4. Bagowski CP, Myers JW & Ferrell JE Jr 2001 The classical progesterone receptor associates with p42 MAPK and is involved in phosphatidylinositol 3-kinase signaling in Xenopus oocytes. Journal of Biological Chemistry 276 37708-37714.
5. Blok LJ, Mackenbach P, Trapman J, Themmen APN, Brinkman AO & Grootegoed A 1989 Follicle-stimulating hormone regulates androgen receptor mRNA in Sertoli cells. Molecular and Cellular Endocrinology 63 267-271.
6. Blok LJ, Hoogenbrugge JW, Themmen APN, Baarends WM, Post M & Grootegoed A 1992 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 1343-1349.
7. Bortolussi M, Zanchetta R, Belvedere P & Colombo L 1990 Sertoli and Leydig cell numbers and gonadotropin receptors in rat testis from birth to puberty. Cell Tissue Research 260 185-191.
8. 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.
9. Buzek SW & Sanborn BM 1988 Increase in testicular androgen receptor during sexual maturation in the rat. Biology of Reproduction 39 39-49.
10. Cato AC, Nestl A & Mink S 2002 Rapid actions of steroid receptors in cellular signaling pathways. Science's Signal Transduction Knowledge Environment RE9.
11. Chaudhary J & Skinner MK 1999 E-box and cyclic adenosine monophosphate response elements are both required for follicle-stimulating hormone-induced transferrin promoter activation in Sertoli cells. Endocrinology 140 1262-1271.
12. Chen JK & Heckert LL 2001 Dmrt1 expression is regulated by follicle-stimulating hormone and phorbol esters in postnatal Sertoli cells. Endocrinology 142 1167-1178.
13. Chen Y, Robles AI, Martinez LA, Liu F, Gimenez-Conti IB & Conti CJ 1996 Expression of G1 cyclins, cyclin-dependent kinases, and cyclin-dependent kinase inhibitors in androgen-induced prostate proliferation in castrated rats. Cell Growth and Differentiation 7 1571-1578.
14. Chowdhury M & Steinberger E 1976 Pituitary and plasma levels of gonadotrophins in foetal and newborn male and female rats. Journal of Endocrinology 69 381-384.
15. Claessens F, Celis L, De Vos P, Peeters B, Heyns W, Verhoeven G & Rombauts W 1993 Intronic androgen Response elements of prostatic binding protein genes. Biochemical and Biophysical Research Communications 191 688-694.
16. Claessens F, Verrijdt G, Schoenmakers E, Haelens A, Peeters B, Verhoeven G & Rombauts W 2001 Selective DNA binding by the androgen receptor as a mechanism for hormone-specific gene regulation. Journal of Steroid Biochemistry and Molecular Biology 76 23-30.
17. Conti M, Toscano MV, Petrelli L, Geremia R & Stefanini M 1983 Involvement of phosphodiesterase in the refractoriness of the Sertoli cell. Endocrinology 113 1845-1853.
18. Cottom J, Salvador LM, Maizels ET, Reierstad S, Park Y, Carr DW, Davare MA, Hell JW, Palmer SS & Dent P et al. 2003 Follicle-stimulating hormone activates extracellular signal-regulated kinase but not extracellular signal-regulated kinase kinase through a 100-kDa phosphotyrosine phosphatase. Journal of Biological Chemistry 278 7167-7179.
19. Crepieux P, Martinat N, Marion S, Guillou F & Reiter E 2002 Cellular adhesion of primary Sertoli cells affects responsiveness of the extracellular signal-regulated kinases 1 and 2 to follicle-stimulating hormone but not to epidermal growth factor. Archives of Biochemistry and Biophysics 399 245-250.
20. Crepieux P, Marion S, Martinat N, Fafeur V, Vern YL, Kerboeuf D, Guillou F & Reiter E 2001 The ERK-dependent signalling is stage-specifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 20 4696-4709.
21. D'Agostino A, Mene P & Stefanini M 1992 Voltage-gated calcium channels in rat Sertoli cells. Biology of Reproduction 46 414-418.
22. Deenadayalu VP, White RE, Stallone JN, Gao X & Garcia AJ 2001 Testosterone relaxes coronary arteries by opening the large-conductance, calcium-activated potassium channel. American Journal of Physiology: Heart and Circulatory Physiology 281 H1720-H1727.
23. Delfino FJ & Walker WH 1998 Stage-specific nuclear expression of NF-κB in mammalian testis. Molecular Endocrinology 12 1696-1707.
24. Denison SH, Sands A & Tindall DJ 1989 A tyrosine aminotransferase glucocorticoid response element also mediates androgen enhancement of gene expression. Endocrinology 124 1091-1093.
25. Dias JA 2005 Endocrinology: fertility hormone in repose. Nature 433 203-204.
26. Fan QR & Hendrickson WA 2005 Structure of human follicle-stimulating hormone in complex with its receptor. Nature 433 269-277.
27. Finkbeiner S & Greenberg ME 1996 Ca(2+)-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16 233-236.
28. Fiorini S, Ferretti ME, Biondi C, Pavan B, Lunghi L, Paganetto G & Abelli L 2003 17Beta-eEstradiol stimulates arachidonate release from human amnion-like WISH cells through a rapid mechanism involving a membrane receptor. Endocrinology 144 3359-3367.
29. Fix C, Jordan C, Cano P & Walker WH 2004 Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells. PNAS 101 10919-10924.
30. Foulkes NS, Schlotter F, Pevet P & Sassone-Corsi P 1993 Pituitary hormone FSH directs the CREM functional switch during spermatogenesis. Nature 362 264-267.
31. Fragale A, Aguanno S, Kemp M, Reeves M, Price K, Beattie R, Craig P, Volsen S, Sher E & D'Agostino A 2000 Identification and cellular localisation of voltage-operated calcium channels in immature rat testis. Molecular and Cellular Endocrinology 162 25-33.
32. Franchi E & Camatini M 1985 Evidence that a Ca2 + chelator and a calmodulin blocker interfere with the structure of inter-Sertoli junctions. Tissue Cell 17 13-25.
33. Ghosh S & Baltimore D 1990 Activation in vitro of NF-κB by phosphorylation of its inhibitor IκB. Nature 344 678-682.
34. Goetz TL, Lloyd TL & Griswold MD 1996 Role of E box and initiator region in the expression of the rat follicle-stimulating hormone receptor (FSHR) gene in testicular Sertoli cells. Journal of Biological Chemistry 271 33317-33324.
35. Gonzalez-Robayna IJ, Falender AE, Ochsner S, Firestone GL & Richards JS 2000 Follicle-Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-Induced kinase (Sgk): evidence for A kinase-independent signaling by FSH in granulosa cells. Molecular Endocrinology 14 1283-1300.
36. Gorczynska E & Handelsman DJ 1991 The role of calcium in follicle-stimulating hormone signal transduction in Sertoli cells. Journal of Biological Chemistry 266 23739-23744.
37. Gorczynska E & Handelsman DJ 1995 Androgens rapidly increase the cytosolic calcium concentration in Sertoli cells. Endocrinology 136 2052-2059.
38. Gorczynska E, Spaliviero J & Handelsman DJ 1994 The relationship between 3′,5′-cyclic adenosine monophosphate and calcium in mediating follicle-stimulating hormone signal transduction in Sertoli cells. Endocrinology 134 293-300.
39. Grad JM, Dai JL, Wu S & Burnstein KL 1999 Multiple androgen response elements and a Myc consensus site in the androgen receptor (AR) coding region are involved in androgen-mediated up-regulation of AR messenger RNA. Molecular Endocrinology 13 1896-1911.
40. Grasso P & Reichert LE Jr 1989 Follicle-stimulating hormone receptor-mediated uptake of 45Ca2 + by proteoliposomes and cultured rat sertoli cells: evidence for involvement of voltage-activated and voltage-independent calcium channels. Endocrinology 125 3029-3036.
41. Griswold MD 1998 The central role of Sertoli cells in spermatogenesis. Seminars in Cell and Developmental Biology 9 411-416.
42. Griswold MD, Solari A, Tung PS & Fritz IB 1977 Stimulation by follicle-stimulating hormone of DNA synthesis and of mitosis in cultured Sertoli cells prepared from testes of immature rats. Molecular and Cellular Endocrinology 7 151-165.
43. Hamil KG, Conti M, Shimasaki S & Hall SH 1994 Follicle-stimulating hormone regulation of AP-1: inhibition of c-jun and stimulation of jun-B gene transcription in the rat Sertoli cell. Molecular and Cellular Endocrinology 99 269-277.
44. Haywood M, Spaliviero J, Jimemez M, King NJ, Handelsman DJ & Allan CM 2003 Sertoli and germ cell development in hypogonadal (hpg) mice expressing transgenic follicle-stimulating hormone alone or in combination with testosterone. Endocrinology 144 509-517.
45. He WW, Sciavolino PJ, Wing J, Augustus M, Hudson P, Meissner PS, Curtis RT, Shell BK, Bostwick DG & Tindall DJ et al. 1997 A novel human prostate-specific, androgen-regulated homeobox gene (NKX3.1) that maps to 8p21, a region frequently deleted in prostate cancer. Genomics 43 69-77.
46. Heckert LL & Griswold MD 1991 Expression of follicle-stimulating hormone receptor mRNA in rat testis and Sertoli cells. Molecular Endocrinology 5 670-677.
47. Heckert LL & Griswold MD 2002 The expression of the follicle-stimulating hormone receptor in spermatogenesis. Recent Progress in Hormonal Research 57 129-148.
48. Heckert LL, Daggett MAF & Chen J 1998 Multiple promoter elements contribute to activity of the follicle-stimulating hormone receptor (FSHR) gene in testicular Sertoli cells. Molecular Endocrinology 12 1499-1512.
49. Heinlein CA & Chang C 2002 The roles of androgen receptors and androgen-binding proteins in nongenomic androgen actions. Molecular Endocrinology 16 2181-2187.
50. Honda K, Shimohama S, Sawada H, Kihara T, Nakamizo T, Shibasaki H & Akaike A 2001 Nongenomic antiapoptotic signal transduction by estrogen in cultured cortical neurons. Journal of Neuroscience Research 64 466-475.
51. Jannini EA, Ulisse S, Cecconi S, Cironi L, Colonna R, D'Armiento M, Santoni A & Cifone MG 1994 Follicle-stimulating hormone-induced phospholipase A2 activity and eicosanoid generation in rat Sertoli cells. Biology of Reproduction 51 140-145.
52. Johnston H, Baker PJ, Abel M, Charlton HM, Jackson G, Fleming L, Kumar TR & O'Shaughnessy PJ 2004 Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology 145 318-329.
53. Jorgensen JS & Nilson JH 2001 AR suppresses transcription of the alpha glycoprotein hormone subunit gene through protein-protein interactions with cJun and activation transcription factor 2. Molecular Endocrinology 15 1496-1504.
54. Kangasniemi M, Kaipia A, Mali P, Toppari J, Huhtaniemi I & Parvinen M 1990 Modulation of basal and FSH-dependent cyclic AMP production in rat seminiferous tubules staged by an improved transillumination technique. The Anatomical Record 227 62-76.
55. Kerr JB, Millar M, Maddocks S & Sharpe RM 1993 Stage-dependent changes in spermatogenesis and Sertoli cells in relation to the onset of spermatogenic failure following withdrawal of testosterone. The Anatomical Record 235 547-559.
56. Ketelslegers JM, Hetzel WD, Sherins RJ & Catt KJ 1978 Developmental changes in testicular gonadotropin receptors: plasma gonadotropins and plasma testosterone in the rat. Endocrinology 103 212-222.
57. Kumar TR, Palapattu G, Wang P, Woodruff TK, Boime I, Byrne MC & Matzuk MM 1999 Transgenic models to study gonadotropin function: the role of follicle-stimulating hormone in gonadal growth and tumorigenesis. Molecular Endocrinology 13 851-865.
58. Lalevee N, Pluciennik F & Joffre M 1997 Voltage dependent calcium current with properties of T-type current in Sertoli cells from immature rat testis in primary cultures. Biology of Reproduction 56 680-687.
59. Lin B, White JT, Ferguson C, Bumgarner R, Friedman C, Trask B, Ellis W, Lange P, Hood L & Nelson PS 2000 PART-1: a novel human prostate-specific, androgen-regulated gene that maps to chromosome 5q12. Cancer Research 60 858-863.
60. Lindsey JS & Wilkinson MF 1996 Pem: a testosterone- and LH-regulated homeobox gene expressed in mouse Sertoli cells and epididymus. Developmental Biology 179 471-484.
61. Lu S, Tsai SY & Tsai MJ 1997 Regulation of androgen-dependent prostatic cancer cell growth: androgen regulation of CDK2, CDK4, and CKI p16 genes. Cancer Research 57 4511-4516.
62. Lu S, Liu M, Epner DE, Tsai SY & Tsai MJ 1999 Androgen regulation of the cyclin-dependent kinase inhibitor p21 gene through an androgen response element in the proximal promoter. Molecular Endocrinology 13 376-384.
63. Luke MC & Coffey DS 1994 Human androgen receptor binding to the androgen Response element of prostate specific antigen. Journal of Andrology 15 41-51.
64. Lyng FM, Jones GR & Rommerts FFG 2000 Rapid androgen actions on calcium signaling in rat Sertoli cells and two human prostatic cell lines: Similar biphasic responses between 1 picomolar and 100 nanomolar concentrations. Biology of Reproduction 63 736-747.
65. Lyon MF, Glenister PH & Lamoreux ML 1975 Normal spermatozoa from androgen-resistant germ cells of chimaeric mice and the role of androgen in spermatogenesis. Nature 258 620-622.
66. Maguire SM, Tribley WA & Griswold MD 1997 Follicle-stimulating hormone (FSH) regulates the expression of FSH receptor messenger ribonucleic acid in cultured Sertoli cells and in hypophysectomized rat testis. Biology of Reproduction 56 1106-1111.
67. Maizels ET, Cottom J, Jones JC & Hunzicker-Dunn M 1998 Follicle stimulating hormone (FSH) activates the p38 mitogen-activated protein kinase pathway, inducing small heat shock protein phosphorylation and cell rounding in immature rat ovarian granulosa cells. Endocrinology 139 3353-3356.
68. Marion S, Robert F, Crepieux P, Martinat N, Troispoux C, Guillou F & Reiter E 2002 G protein-coupled receptor kinases and beta arrestins are relocalized and attenuate cyclic 3′,5′-adenosine monophosphate Response to follicle-stimulating hormone in rat primary Sertoli cells. Biology of Reproduction 66 70-76.
69. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, De Kretser DM, Pratis K & Robertson DM 2002 Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Progress in Hormonal Research 57 149-179.
70. McLean DJ, Friel PJ, Pouchnik D & Griswold MD 2002 Oligonucleotide microarray analysis of gene Expression in follicle-stimulating hormone-treated rat Sertoli cells. Molecular Endocrinology 16 2780-2792.
71. Meachem SJ, McLachlan RI, de Kretser DM, Robertson DM & Wreford NG 1996 Neonatal exposure of rats to recombinant follicle stimulating hormone increases adult Sertoli and spermatogenic cell numbers. Biology of Reproduction 54 36-44.
72. Meroni SB, Riera MF, Pellizzari EH & Cigorraga SB 2002 Regulation of rat Sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway. Journal of Endocrinology 174 195-204.
73. Mitchell SH, Murtha PE, Zhang S, Zhu W & Young CY 2000 An androgen Response element mediates LNCaP cell dependent androgen induction of the hK2 gene. Molecular and Cellular Endocrinology 168 89-99.
74. Molina CA, Foulkes NS, Lalli E & Sassone-Corsi P 1993 Inducibility and negative autoregulation of CREM: An alternative promoter directs the expression of ICER, an early response repressor. Cell 75 875-886.
75. Morris PL, Vale WW, Cappel S & Bardin CW 1988 Inhibin production by primary Sertoli cell-enriched cultures: regulation by follicle-stimulating hormone, androgens, and epidermal growth factor. Endocrinology 122 717-725.
76. Mruk DD & Cheng CY 2004 Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocrine Reviews 25 747-806.
77. Nakamura K, Hipkin RW & Ascoli M 1998a The agonist-induced phosphorylation of the rat follitropin receptor maps to the first and third intracellular loops. Molecular Endocrinology 12 580-591.
78. Nakamura K, Krupnick JG, Benovic JL & Ascoli M 1998b Signaling and phosphorylation-impaired mutants of the rat follitropin receptor reveal an activation- and phosphorylation-independent but arrestin-dependent pathway for internalization. Journal of Biological Chemistry 273 24346-24354.
79. Nalbandian A, Dettin L, Dym M & Ravindranath N 2003 Expression of vascular endothelial growth factor receptors during male germ cell differentiation in the mouse. Biology of Reproduction 69 985-994.
80. Nantel F, Monoco L, Foulkes NS, Masquillier D, LeMeur M, Henriksen K, Dierich M, Parvinen M & Sassone-Corsi P 1996 Spermiogenesis deficiency and germ cell apoptosis in CREM-mutant mice. Nature 380 159-162.
81. Nargolwalla C, McCabe D & Fritz IB 1990 Modulation of levels of messenger RNA for tissue-type plasminogen activator in rat Sertoli cells, and levels of messenger RNA for plasminogen activator inhibitor in testis peritubular cells. Molecular and Cellular Endocrinology 70 73-80.
82. Nechamen CA, Thomas RM, Cohen BD, Acevedo G, Poulikakos PI, Testa JR & Dias JA 2004 Human follicle-stimulating hormone (FSH) receptor interacts with the adaptor protein APPL1 in HEK 293 cells: potential involvement of the P13K pathway in FSH signaling. Biology of Reproduction 71 629-636.
83. Nelson PS, Gan L, Ferguson C, Moss P, Gelinas R, Hood L & Wang K 1999 Molecular cloning and characterization of prostase, an androgen-regulated serine protease with prostate-restricted expression. PNAS 96 3114-3119.
84. Orth JM 1984 The role of follicle-stimulating hormone in controlling Sertoli cell proliferation. Endocrinology 115 1248-1255.
85. Orth JM, Gunsalus GL & Lamperti AA 1988 Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122 787-794.
86. Pearson G, Robinson F, Gibson TB, Xu B-E, Karandikar M, Berman K & Cobb MH 2001 Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocrine Reviews 22 153-183.
87. Qi H, Labrie Y, Grenier J, Fournier A, Fillion C & Labrie C 2001 Androgens induce Expression of SPAK, a STE20/SPS1-related kinase, in LNCaP human prostate cancer cells. Molecular and Cellular Endocrinology 182 181-192.
88. Qi H, Fillion C, Labrie Y, Grenier J, Fournier A, Berger L, El-Alfy M & Labrie C 2002 AlbZIP, a novel bZIP gene located on chromosome 1q21.3 that is highly expressed in prostate tumors and of which the expression is up-regulated by androgens in LNCaP human prostate cancer cells. Cancer Research 62 721-733.
89. Razandi M, Pedram A, Park ST & Levin ER 2003 Proximal events in signaling by plasma membrane estrogen receptors. Journal of Biological Chemistry 278 2701-2712.
90. Rennie PS, Bruchovsky N, Leco KJ, Sheppard PC, McQueen SA, Cheng H, Snoek R, Hamel A, Bock ME & MacDonald BS et al. 1993 Characterization of two cis-acting DNA elements involved in the androgen regulation of the probasin gene. Molecular Endocrinology 7 23-36.
91. Rommerts FFG 1988 How much androgen is required for maintenance of spermatogenesis? Journal of Endocrinology 116 7-9.
92. Rosini P, Bonaccorsi L, Baldi E, Chiasserini C, Forti G, De Chiara G, Lucibello M, Mongiat M, Iozzo RV & Garaci E et al. 2002 Androgen receptor expression induces FGF2, FGF-binding protein production, and FGF2 release in prostate carcinoma cells: role of FGF2 in growth, survival, and androgen receptor down-modulation. Prostate 33 310-321.
93. Sadate-Ngatchou PI, Pouchnik DJ & Griswold MD 2004a Follicle-stimulating hormone induced changes in gene Expression of murine testis. Molecular Endocrinology 18 2805-2816.
94. Sadate-Ngatchou PI, Pouchnik DJ & Griswold MD 2004b Identification of testosterone-regulated genes in testes of hypogonadal mice using oligonucleotide microarray. Molecular Endocrinology 18 422-433.
95. Sanborn BM, Caston LA, Chang C, Liao S, Speller R, Porter LD & Ku CY 1991 Regulation of androgen receptor mRNA in rat Sertoli and peritubular cells. Biology of Reproduction 45 634-641.
96. Saxena D, Safi R, Little-Ihrig L & Zeleznik AJ 2004 Liver receptor homolog-1 stimulates the progesterone biosynthetic pathway during follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 145 3821-3829.
97. Schteingart HF, Meroni SB, Pellizzari EH, Perez AL & Cigorraga SB 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. Journal of Steroid Biochemistry and Molecular Biology 52 375-381.
98. Scobey MJ, Bertera S, Somers JP, Watkins SC, Zeleznik AJ & Walker WH 2001 Delivery of a cyclic adenosine 3′,5′-monophosphate Response element binding protein (CREB) to seminiferous tubules results in impaired spermatogenesis. Endocrinology 142 948-954.
99. Scobey MJ, Fix CA & Walker WH 2004 The Id2 transcriptional repressor is induced by follicle-stimulating hormone and cAMP. Journal of Biological Chemistry 279 16064-16070.
100. Shan L-X, KZhu L-J, 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.
101. Shang Y, Hu X, DiRenzo J, Lazar MA & Brown M 2000 Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103 843-852.
102. Shang Y, Myers M & Brown M 2002 Formation of the androgen receptor transcription complex. Molecular Cell 9 601-610.
103. Sharma OP, Flores JA, Leong DA & Veldhuis JD 1994 Cellular basis for follicle-stimulating hormone-stimulated calcium signaling in single rat Sertoli cells: possible dissociation from effects of adenosine 3′,5′-monophosphate. Endocrinology 134 1915-1923.
104. Sharpe RM 1994 Regulation of spermatogenesis. In The Physiology of Reproduction, pp 1363-1434. Eds E Knobil & JD Neil. New York: Raven Press.
105. Shen R, Sumitomo M, Dai J, Hardy DO, Navarro D, Usmani B, Papandreou CN, Hersh LB, Shipp MA & Freedman LP et al. 2000 Identification and characterization of two androgen response regions in the human neutral endopeptidase gene. Molecular and Cellular Endocrinology 170 131-142.
106. Shirakawa F & Mizel S 1989 In vitro activation and nuclear translocation of NF-κB catalyzed cyclic AMP-dependent protein kinase and protein kinase C. Molecular Cell Biology 9 2424-2430.
107. Short ML, Huang D, Milkowski DM, Short S, Kunstman K, Soong CJ, Chung KC & Jungmann RA 1994 Analysis of the rat lactate dehydrogenase A subunit gene promoter/regulatory region. Biochemical Journal 304 391-398.
108. Silva FRMB, Leite LD & Wassermann GF 2002 Rapid signal transduction in Sertoli cells. European Journal of Endocrinology 147 425-433.
109. Simoni M, Gromoli J & Niesclag E 1997 The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocrine Reviews 18 739-773.
110. Skinner MK 2005 Sertoli cell secreted regulatory factors. In Sertoli Cell Biology, pp 107-120. Eds MK Skinner & MD Griswold. San Diego: Elsevier Science.
111. Spady TJ, Shayya R, Thackray VG, Ehrensberger L, Bailey JS & Mellon PL 2004 Androgen regulates follicle-stimulating hormone beta gene Expression in an activin-dependent manner in immortalized gonadotropes. Molecular Endocrinology 18 925-940.
112. Spruill WA, Zysk JR, Tres LL & Kierszenbaum AL 1983 Calcium/calmodulin-dependent phosphorylation of vimentin in rat sertoli cells. PNAS 80 760-764.
113. Steinsapir J, Socci R & Reinach P 1991 Effects of androgen on intracellular calcium of LNCaP cells. Biochemical and Biophysical Research Communications 179 90-96.
114. Suire S, Fontaine I & Guillou F 1995 Follicle stimulating hormone (FSH) stimulates transferrin gene transcription in rat Sertoli cells: cis and trans-acting elements involved in FSH action via cyclic adenosine 3′,5′-monophosphate on the transferrin gene. Molecular Endocrinology. 9 756-766.
115. Sun Z, Pan J & Balk SP 1997 Androgen receptor-associated protein complex binds upstream of the androgen-responsive elements in the promoters of human prostate-specific antigen and kallikrein 2 genes. Nucleic Acids Research 25 3318-3325.
116. Suwanichkul A, DePaolis LA, Lee PD & Powell DR 1993 Identification of a promoter element which participates in cAMP-stimulated expression of human insulin-like growth factor-binding protein-1. Journal of Biological Chemistry 268 9730-9736.
117. Swinnen JV, Esquenet M, Goossens K, Heyns W & Verhoeven G 1997 Androgens stimulate fatty acid synthase in the human prostate cancer cell line LNCaP. Cancer Research 57 1086-1090.
118. Tadokoro Y, Yomogida K, Ohta H, Tohda A & Nishimune Y 2002 Homeostatic regulation of germinal stem cell proliferation by the GDNF/FSH pathway. Mechinisms of Development 113 29-39.
119. Tan J, Marschke KB, Ho KC, Perry ST, Wilson EM & French FS 1992 Response elements of the androgen-regulated C3 gene. Journal of Biological Chemistry 267 4456-4466.
120. Taylor WE, Najmabadi H, Strathearn M, Jou NT, Liebling M, Rajavashisth T, Chanani N, Phung L & Bhasin S 1996 Human stem cell factor promoter deoxyribonucleic acid sequence and regulation by cyclic 3′,5′-adenosine monophosphate in a Sertoli cell line. Endocrinology 137 5407-5414.
121. Themmen APN, Blok LJ, Post M, Baarends WM, Hoogerbrugge JW, Vassart G, Anton J & Grootengoed JA 1991 Follitropin receptor down-regulation involves a cAMP-dependent post-transcriptional decrease of receptor mRNA Expression. Molecular and Cellular Endocinology 78 R7-R13.
122. Troispoux C, Guillou F, Elalouf JM, Firsov D, Iacovelli L, De Blasi A, Combarnous Y & Reiter E 1999 Involvement of G protein-coupled receptor kinases and arrestins in desensitization to follicle-stimulating hormone action. Molecular Endocrinology 13 1599-1614.
123. Tsai MJ & O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Reviews of Biochemistry 63 451-486.
124. Unni E, Sun S, Nan B, McPhaul MJ, Cheskis B, Mancini MA & Marcelli M 2004 Changes in androgen receptor nongenotropic signaling correlate with transition of LNCaP cells to androgen independence. Cancer Research 64 7156-7168.
125. Veldscholte J, Berrevoets CA, Ris-Stalpers C, Kuiper GG, Jenster G, Trapman J, Brinkmann AO & Mulder E 1992 The androgen receptor in LNCaP cells contains a mutation in the ligand binding domain which affects steroid binding characteristics and Response to antiandrogens. Journal of Steroid Biochemistry and Molecular Biology 41 665-669.
126. Verhoeven G, Cailleau J & de Moor P 1980 Desensitization of cultured rat Sertoli cells by follicle-stimulating hormone and by L-isoproterenol. Molecular and Cellular Endocrinology 20 113-126.
127. Verhoven G & Cailleau J 1988 Follicle-stimulating hormone and androgens increase the concentration of the androgen receptor in Sertoli cells. Endocrinology 122 1541-1550.
128. Verrijdt G, Schoenmakers E, Haelens A, Peeters B, Verhoeven G, Rombauts W & Claessens F 2000 Change of specificity mutations in androgen-selective enhancers. Evidence for a role of differential DNA binding by the androgen receptor. Journal of Biological Chemistry 275 12298-12305.
129. Vornberger W, Prins G, Musto NA & Suarez-Quian CA 1994 Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology 134 2307-2316.
130. Walker WH & Habener JF 1996 Role of transcription factors CREB and CREM in cAMP-regulated transcription during spermatogenesis. Trends in Endocrinology and Metabolism 7 133-138.
131. Walker WH, Fucci L & Habener JF 1995 Expression of the gene encoding transcription factor adenosine 3′, 5′-monophosphate (cAMP) Response element-binding protein: regulation by follicle-stimulating hormone-induced cAMP signaling in primary rat Sertoli cells. Endocrinology 136 3534-3545.
132. Walker WH, Daniel PB & Habener JF 1998 Inducible cAMP early repressor ICER down-regulation of CREB gene Expression in Sertoli cells. Molecular and Cellular Endocrinology 143 167-178.
133. Warren DW, Huhtaniemi IT, Tapanainen J, Dufau ML & Catt KJ 1984 Ontogeny of gonadotropin receptors in the fetal and neo-natal rat testis. Endocrinology 114 470-476.
134. Wong CW, McNally C, Nickbarg E, Komm BS & Cheskis BJ 2002 Estrogen receptor-interacting protein that modulates its non-genomic activity-crosstalk with Src/Erk phosphorylation cascade. PNAS 99 14783-14788.
135. Wu G-Y, Deisseroth K & Tsien RW 2001 Activity-dependent CREB phosphorylation: Convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. PNAS 98 2808-2813.
136. Xia L, Robinson D, Ma AH, Chen HC, Wu F, Qiu Y & Kung HJ 2002 Identification of human male germ cell-associated kinase, a kinase transcriptionally activated by androgen in prostate cancer cells. Journal of Biological Chemistry 277 35422-35433.
137. Xu J, Kalos M, Stolk JA, Zasloff EJ, Zhang X, Houghton RL, Filho AM, Nolasco M, Badaro R & Reed SG 2001 Identification and characterization of prostein, a novel prostate-specific protein. Cancer Research 61 1563-1568.
138. Zhang J, Gao N, Kasper S, Reid K, Nelson C & Matusik RJ 2004 An androgen-dependent upstream enhancer is essential for high levels of probasin gene expression. Endocrinology 145 134-148.
139. Zhang SB, Dattatreyamurty B & Reichert LE Jr 1991 Differential roles of high and low affinity guanosine 5′-triphosphate binding sites in the regulation of follicle-stimulating hormone binding to receptor and signal transduction in bovine calf testis membranes. Endocrinology 128 295-302.
140. Zhou X, Kudo A, Kawakami H & Hirano H 1996 Immunohistochemical localization of androgen receptor in mouse testicular germ cells during fetal and postnatal development. The Anatomical Record 245 509-518.
141. Zirkin BR, Santulli R, Awoniyi CA & Ewing LL 1989 Maintenance of advanced spermatogenic cells in the adult rat testis: quantitative relationship to testosterone concentration within the testis. Endocrinology 124 3043-3049.