Systemic administration of alcohol to adult rats inhibits Leydig cell activity: Time course of effect and role of nitric oxide

Alcoholism: Clinical and Experimental Research

Volumn 30, Issue 9, 2006, Pages 1479-1491

  Herman, Melissa ^a   Kang, Sang Soo ^a   Lee, Soon ^a   James, Peter ^a   Rivier, Catherine ^a,b  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Leydig Cells; Nitric Oxide; PBR; StAR; Testosterone

Indexed keywords

ALCOHOL; BENZODIAZEPINE RECEPTOR; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CHORIONIC GONADOTROPIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; LEYDIG CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; RAT; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE RELEASE; WESTERN BLOTTING;

ADMINISTRATION, INHALATION; ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL SEPARATION; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; CHORIONIC GONADOTROPIN; ENZYME INHIBITORS; ETHANOL; INDICATORS AND REAGENTS; INJECTIONS, INTRAVENOUS; LEYDIG CELLS; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; TESTOSTERONE; TIME FACTORS;

EID: 33747689017     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2006.00179.x     Document Type: Article

References (112)

1. Adams ML, Cicero TJ (1991) Effect of alcohol on β-endorphin and reproductive hormones in the male rat. Alcohol Clin Exp Res 15:685-692.
2. Adams ML, Forman JB, Kalicki JM, Meyer ER, Sewing B (1993) Antagonism of alcohol-induced suppression of rat testosterone secretion by an inhibitor of nitric oxide synthase. Alcohol Clin Exp Res 17:660-664.
3. Adams ML, Meyer ER, Sewing BN, Cicero TJ (1994) Effects of nitric oxide-related agents on rat testicular function. J Pharmacol Exp. Ther 269:230-237.
4. Akane A, Fukushima S, Shiono H, Fukui Y (1988) Effects of ethanol on testicular steroidogenesis in the rat. Alcohol Alcohol 23:203-209.
5. Andrew PJ, Mayer B (1999) Enzymatic function of nitric oxide synthases. Cardiovascular Res 43:521-531.
6. Anholt R, DeSouza E, Kuhar M, Snyder S (1985) Depletion of peripheral-type benzodiazepine receptors after hypophysectomy in rat adrenal and testis. Eur J Pharmacol 110:41-46.
7. Artmenko I, Zhao D, Hales D, Hales K, Jefcoate C (2001) Mitochondrial processing of newly synthesized steroidogenic acute regulatory protein, but not total StAR, mediates cholesterol transfer to cytochrome P-450 side chain cleavage enzyme in adrenal cells. J Bioclin Chem 276:46583-46596.
8. Belda X, Marquez C, Armario A (2004) Long-term effects of a single exposure to stress in adult rats on behavior and hypothalamic-pituitary-adrenal responsiveness: comparison of two outbred rat strains. Behav Brain Res 154:399-408.
9. Black S, Szklarz G, Harikrishna J, Lin D, Wolf C, Miller W (1993) Regulation of proteins in the cholesterol side-chain cleavage system in JEG-3 and Y-1 cells. Endocrinology 132:539-545.
10. Bose H, Lingappa V, Miller W (2002) Rapid regulation of steroidogenesis by mitochondrial protein import. Nature 417:87-91.
11. Bose HS, Whittal RM, Baldwin MA, Miller WL (1999) The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule. Proc Natl Acad Sci U S A 96:7250-7255.
12. Brown RC, Papadopoulos V (2001) Role of the peripheral-type benzodiazepine receptor in adrenal and brain steroidogenesis. Int Rev Neurobiol 46:117-143.
13. Burnett AL, Ricker DD, Chamness SL, Maguire MP, Crone JK, Bredt DS, Snyder SH, Chang TSK (1995) Localization of nitric oxide synthase in the reproductive organs of the male rat. Biol Reprod 52:1-7.
14. Canteros G, Rettori V, Franchi A, Genaro A, Cebral E, Faletti A, Gimeno M, McCann SM (1995) Ethanol inhibits luteinizing hormone-releasing hormone (LHRH) secretion by blocking the response of LHRH neuronal terminals to nitric oxide. Proc Natl Acad Sci U S A 92:3416-3420.
15. Chamness SL, Ricker DD, Crone JK, Dembeck CL, Maguire MP, Burnett AL, Change TSK (1995) The effect of androgen on nitric oxide synthase in the male reproductive tract of the rat. Fertil Steril 63:1101-1107.
16. Chiao YB, Johnston KE, Gavaler JS, VanThiel DH (1981) Effect of chronic ethanol feeding on testicular content of enzymis required for testosteronogenesis. Alcohol Clin Exp Res 5:230-236.
17. Ching M, Valenca M, Negro-Vilar A (1988) Acute ethanol treatment lowers hypophyseal portal plasma luteinizing hormone-releasing hormone (LH-RH) and systemic plasma LH levels in orchidectomized rats. Brain Res 443:325-328.
18. Cicero TJ, Badger TM (1977) Effects of alcohol on the hypothalamic-pituitary-gonadal axis in the male rat. J Pharmacol Exp Ther 201:427-433.
19. Cicero TJ, Bell RD, Meyer ER, Badger TM (1980) Ethanol and adetaldehyde directly inhibit testicular steroidogenesis. J Pharmacol Exp Ther 213:228-233.
20. Cobb C, Ennis M, Thiel DV, Gavaler J, Lester R (1978) Acetaldehyde and ethanol are testicular toxins. Gastroenterology 75:958-965.
21. Dees WL, McArthur NH, Farr KL, Culler MD, Harms PG (1983) Effects of ethanol on rat hypothalamic luteinizing hormone releasing hormone: a study utilizing radioimmunoassay. Biol Reprod 28:1066-1070.
22. Del Punta K, Charreau EH, Pignataro OP (1996) Nitric oxide inhibits Leydig cell steroidogenesis. Endocrinology 137:5337-5343.
23. Desjardins C (1981) Endocrine signaling and male reproduction. Biol Reprod 24:1-21.
24. Dissen GA, Dearth RK, Scott HM, Ojeda SR, Dees WL (2004) Alcohol alters luteinizing hormone secretion in immature female rhesus monkeys by a hypothalamic action. Endocrinology 145:4558-4564.
25. Ellis GB, Desjardins C (1982) Male rats secrete luteinizing hormone and testosterone episodically. Endocrinology 110:1618-1627.
26. Emanuele M, Emanuele E (2001) Alcohol and the male reproductive system. Alcohol Res Health 25:282-287.
27. Emanuele MA, Tentler J, Reda D, Kirsteins L, Emanuele NV, Lawrence AM (1989) In vivo effect of ethanol on release of LH-release hormone and LH in rats. J Endocrinol 121:37-41.
28. Emanuele N, LaPaglia N, Kovacs E, Emanuele M (2005) The impact of burn injury and ethanol on the cytokine network of the mouse hypothalamus: reproductive implications. Cytokines 30:109-115.
29. Frias J, Rodriguez R, Torres J, Ruiz E, Ortega E (2000) Effects of acute alcohol intoxication on pituitary gonadal axis hormones, pituitary adrenal axis hormones, beta-endorphin and prolactin in human adolescents of both sexes. Life Sci 67:1081-1086.
30. Frias J, Torres JM, Miranda MT, Ruiz E, Ortega E (2002) Effects of acute alcohol intoxication on pituitary-gonadal axis hormones, pituitary-adrenal axis hormones, beta-endorphin and prolactin in human adults of both sexes. Alcohol Alcohol 37:169-173.
31. Gerendai I, Toth IE, Boldogkoi Z, Medveczky I, Halasz B (2000) Central nervous system structures labelled from the testis using the transsynaptic viral tracing technique. J Neuroendocrinol 12:1087-1095.
32. Gill K, France C, Amit Z (1986) Voluntary ethanol consumption in rats: an examination of blood/brain ethanol levels and behavior. Alcohol Clin Exp Res 10:457-462.
33. Granot Z, Geiss-Friendlander R, Melamed-Book N, Eimerl S, Timberg R, Weiss A, Hales K, Hales D, Stocco D, Orly J (2003) Proteolysis of normal and mutated steroidogenic acute regulatory proteins in the mitochondria: the fate of unwanted proteins. Mol Endocrinol 17:2461-2476.
34. Granot Z, Silverman E, Friedlander R, Melamed-Book N, Eimeri S, Timberg R, Hales K, Hales D, Stocco D, Orly J (2002) The life cylce of the steroidogenic acute regulatory (StAR) protein: from transcription through proteolysis. Endocrine Rev 28:375-386.
35. Hales DB, Diemer T, Hales KH (1999) Role of cytokines in testicular function. Endocrine 10:201-217.
36. Hales KH, Diemer T, Ginde S, Shankar BK, Roberts M, Bosmann HB, Hales DB (2000) Diametric effects of bacterial endotoxin lipopolysaccharide on adrenal and Leydig cell steroidogenic acute regulatory protein. Endocrinology 141:4000-4012.
37. Hauet T, Yao ZX, Bose HS, Wall CT, Han Z, Li W, Hales DB, Miller WL, Culty M, Papadopoulos V (2005) Peripheral-type benzodiazepine receptor-mediated action of steroidogenic acute regulatory protein on cholesterol entry into leydig cell mitochondria. Mol Endocrinol 19:540-554.
38. Hayley S, Wall P, Anisman H (2002) Sensitization to the neuroendocrine, central monoamine and behavioural effects of murine tumor necrosis factor-alpha: peripheral and central mechanisms. Eur J Neurosci 15:1061-1076.
39. Herman M, Rivier C (2006) Activation of a neural brain-testicular pathways lowers Leydic cell levels of the steroidogenic acute regulatory protein and the peripheral-type benzodiazepine receptor while increasing levels of neural nitric oxide synthase. Endocrinology 147:624-633.
40. Johnson JD, O'Connor KA, Deak T, Spencer RL, Watkins LR, Maier SF (2002) Prior stressor exposure primes the HPA axis. Psychoneuroendocrinology 27:353-365.
41. Kim C, Rivier C (2000) Nitric oxide and carbon monoxide have a stimulatory role in the hypothalamic-pituitary-adrenal response to physico-emotional stressors in rats. Endocrinology 141:2244-2253.
42. Kim CK, Rivier C (1998) Influence of nitric oxide synthase inhibitors on the ACTH and cytokine responses to peripheral immune signals. J Neuroendocrinol 10:353-362.
43. Kim JH, Kim HJ, Noh HS, Roh GS, Kang SS, Cho GJ, Park SK, Lee BJ, Choi WS (2003) Suppression by ethanol of male reproductive activity. Brain Res 989:91-98.
44. Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298 (part 2): 249-258.
45. Kostic T, Andric S, Maric D, Kovacevic R (2000) Inhibitory effects of stress-activated nitric oxide on antioxidant enzymes and testicular steroidogenesis. J Steroid Biochem Mol Biol 31:299-306.
46. Kostic TS, Andric SA, Maric D, Stojilkovic SS, Kovacevic R (1999) Involvement of inducible nitric oxide synthase in stress-impaired testicular steroidogenesis. J Endocrinol 163:409-416.
47. Krueger R, Orme-Johnson N (1983) Acute adrenocorticotropic hormone stimulation of adrenal corticosteroidogenesis. J Biol Chem 258:10159-10167.
48. Lacapere JJ, Papadopoulos V (2003) Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis. Steroids 68:569-585.
49. LaPaglia N, Steiner J, Kirsteins L, Emanuele MA, Emanuele N (1997) The impact of acute ethanol on reproductive hormone synthesis, processing, and secretion in female rats at proestrous. Alcohol Clin Exp Res 21:1567-1572.
50. Lee JJ, Eisenberg P, Papadopoulos V, Wang J, Widmaier EP (2004) Reversible changes in adrenocorticotropin (ACTH)-induced adrenocortical steroidogenesis and expression of the peripheral-type benzodiazepine receptor during the ACTH-insensitive period in young rats. Endocrinology 145:2165-2173.
51. Lee S, Blanton C, Rivier C (2003) Prenatal ethanol exposure alters the responsiveness of the rat hypothalamic-pituitary-adrenal axis to nitric oxide. Alcohol Clin Exp Res 27:962-969.
52. Lee S, Kim C, Rivier C (1999) Nitric oxide stimulates ACTH secretion and the transcription of the genes encoding for NGFI-B, corticotropin-releasing factor, corticotropin-releasing factor receptor type 1 and vasopressin in the hypothalamus of the intact rat. J Neurosci 19:7640-7647.
53. Lee S, Miselis R, Rivier C (2002) Anatomical and functional evidence for a neural hypothalamic-testicular pathway that is independent of the pituitary. Endocrinology 143:4447-4454.
54. Lee S, Rivier C (1993) Effect of exposure to an alcohol diet for ten days on the ability of interleukin-1β to release ACTH and corticosterone in the adult ovariectomized female rat. Alcohol Clin Exp Res 17:1009-1013.
55. Lee S, Rivier C (1994) Prenatal alcohol exposure alters the hypothalamic-pituitary-adrenal axis response of offspring to interleukin-1: is nitric oxide involved? Alcohol Clin Exp Res 18:1242-1247.
56. Lee S, Rivier C (1997) An initial, three-day long treatment with alcohol induces a long-lasting phenomenon of selective tolerance in the activity of the rat hypothalamic-pituitary-adrenal axis. J Neurosci 17:8856-8866.
57. Lee S, Rivier C (2003) Long-term influence of an initial exposure to alcohol on the rat hypothalamic-pituitary axis. Alcohol Clin Exp Res 27:1463-1470.
58. Lee S, Schmidt D, Tilders F, Cole M, Smith A, Rivier C (2000) Prolonged exposure to intermittent alcohol vapors blunts hypothalamic responsiveness to immune and non-immune signals. Alcohol Clin Exp Res 24:110-122.
59. Lin D, Sugawara T, Strauss JF III, Clark BJ, Stocco DM, Saenger P, Rogol A, Miller WL (1995) Role of steroidogenesis acute regulatory protein in adrenal and gonadal steroidogenesis. Science 267:1828-1831.
60. Lin T, Wang D, Nagpal ML, Calkins JH, Chang W, Chi R (1991) Interleukin-1 inhibits cholesterol side-chain cleavage cytochrome P450 expression in primary cultures of Leydig cells. Endocrinology 129:1305-1311.
61. Liu J, Li H, Papadopoulos V (2003) PAP7, a PBR/PKA-RIalpha-associated protein: a new element in the relay of the hormonal induction of steroidogenesis. J Steroid Biochem Mol Biol 85:275-283.
62. Luo L, Chen H, Zirkin B (2005) Temporal relationship among testosterone production, steroidogenic acute regulatory protein (StAR) and P450 side-chain cleavage enzyme (P450scc) during Leydig cell aging. J Androl 26:25-31.
63. Marti O, Garcia A, Vellès A, Harbuz M, Armario A (2001) Evidence that a single exposure to aversive stimuli triggers long-lasting effects in the hypothalamus-pituitary-adrenal axis that consolidate with time. Eur J Neurosci 13:129-136.
64. Nurmi M, Kiianmaa K, Sinclair J (1994) Brain ethanol in AA, ANA, and Wistar rats monitored with one-minute microdialysis. Alcohol 11:315-321.
65. O'Connor KA, Ginsberg AB, Maksimova E, Wieseler Frank JL, Johnson JD, Spencer RL, Campeau S, Watkins LR, Maier SF (2004) Stress-induced sensitization of the hypothalamic-pituitary adrenal axis is associated with alterations of hypothalamic and pituitary gene expression. Neuroendocrinology 80:252-263.
66. Ogilvie K, Rivier C (1997a) Effect of alcohol on the proestrous surge of luteinizing hormone (LH) and the activation of LH-releasing hormone (LHRH) neurons in the female rat. J Neurosci 17:2595-2604.
67. Ogilvie K, Rivier C (1997b) Effect of three different modes of alcohol administration on the activity of the rat hypothalamic-pituitary-adrenal axis. Alcohol Clin Exp Res 21:467-476.
68. Ogilvie K, Rivier C (1998) The intracerebroventricular injection of interleukin-1β blunts the testosterone response to human chorionic gonadotropin: role of prostaglandin- and adrenergic-dependent pathways. Endocrinology 139:3088-3095.
69. Orpana AK, Harkonen M, Eriksson CJP (1990a) Ethanol-induced inhibition of testosterone biosynthesis in rat Leydig cells - role of mitochondrial substrate shuttles and citrate. Alcohol Alcohol 25:499-507.
70. Orpana AK, Orava MM, Vihko RK, Harkonen M, Eriksson CJ (1990b) Role of ethanol metabolism in the inhibition of testosterone biosynthesis in rats in vivo: importance of gonadotropin stimulation. J Steroid Biochem Mol Biol 37:273-278.
71. Papadopoulos V (2004) In search of the function of the peripheral-type benzodiazepine receptor. Endocrine Res 30:677-684.
72. Papadopoulos V, Amri H, Boujrad N, Cascio C, Culty M, Garnier M, Hardwick M, Li H, Vidic B, Brown AS, Reversa JL, Bernassau JM, Drieu K (1997a) Peripheral benzodiazepine receptor in cholesterol transport and steroidogenesis. Steroids 62:21-28.
73. Papadopoulos V, Amri H, Li H, Boujrad N, Vidic B, Garnier M (1997b) Targeted disruption of the peripheral-type benzodiazepine receptor gene inhibits steroidogenesis in the R2C Leydig tumor cell line. J Biol Chem 272:32129-32135.
74. Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrine Rev 25:947-970.
75. Plagemann A, Staudt A, Götz F, Malz U, Rhode W, Rake A, Dörner G (1998) Long-term effects of early postnatally administered interleukin-1β on the hypothalamic-pituitary-adrenal (HPA) axis in rats. Endocrine Regul 32:77-85.
76. Pomerantz DK, Pitelka V (1998) Nitric oxide is a mediator of the inhibitory effect of activated macrophages on production of androgen by the Leydig cell of the mouse. Endocrinology 139:922-931.
77. Pon L, Hartigan J, Orme-Johnson N (1986) Acute ACTH regulation of adrenal corticosteroid biosynthesis: rapid accumulation of a phosphoprotein. J Biol Chem 261:13309-13316.
78. Raff H, Hong JJ, Oaks MK, Widmaier EP (2003) Adrenocortical responses to ACTH in neonatal rats: effect of hypoxia from birth on corticosterone, StAR, and PBR. Am J Physiol Regul Integr Comp Physiol 284:R78-R85.
79. Rivest S, Rivier C (1995) The role of corticotropin-releasing factor and interleukin-1 in the regulation of neurons controlling reproductive functions. Endocrine Rev 16:177-199.
80. Rivier C (1996) Alcohol stimulates ACTH secretion in the rat: mechanisms of action and interactions with other stimuli. Alcohol Clin Exp Res 20:240-254.
81. Rivier C (1999) Alcohol rapidly lowers plasma testosterone levels in the rat: evidence that a neural brain-gonadal pathway may be important for decreased testicular responsiveness to gonadotropin. Alcohol Clin Exp Res 23:38-45.
82. Rivier C (2002) Inhibitory effect of neurogenic and immune stressors on testosterone secretion in rats. Neuroimmunomodulation 10:17-29.
83. Rivier C, Rivest S, Vale W (1992) Alcohol-induced inhibition of LH secretion in intact and gonadectomized male and female rats: possible mechanisms. Alcohol Clin Exp Res 16:928-934.
84. Rivier C, Vale W (1989) In the rat, interleukin-1α acts at the level of the brain and the gonads to interfere with gonadotropin and sex steroid secretion. Endocrinology 124:2105-2109.
85. Saez J (1994) Leydig cells: endocrine, paracrine and autocrine regulation. Endocrine Rev 15:574-626.
86. Salonen I, Eriksson CJP (1989) Penetration of ethanol into the male reproductive tract. Alcohol Clin Exp Res 13:746-751.
87. Salonen I, Huhtaniemi I (1990) Effects of chronic ethanol diet on pituitary-testicular function of the rat. Biol Reprod 42:55-62.
88. Salzmann C, Otis M, Long H, Roberge C, Gallo-Payet N, Walker CD (2004) Inhibition of steroidogenic response to adrenocorticotropin by leptin: implications for the adrenal response to maternal separation in neonatal rats. Endocrinology 145:1810-1822.
89. Saxena S, Meehan D, Coney P, Wimalasena J (1990) Ethanol has direct inhibitory effects on steroidogenesis in human granulosa cells: specific inhibition of LH action. Alcohol Clin Exp Res 14:522-527.
90. Schmidt ED, Aguilera G, Binnekade R, Tilders FJ (2003) Single administration of interleukin-1 increased corticotropin releasing hormone and corticotropin releasing hormone-receptor mRNA in the hypothalamic paraventricular nucleus which paralleled long-lasting (weeks) sensitization to emotional stressors. Neuroscience 116:275-283.
91. Schmidt ED, Schoffelmeer AN, De Vries TJ, Wardeh G, Dogterom G, Bol JG, Binnekade R, Tilders FJ (2001) A single administration of interleukin-1 or amphetamine induces long- lasting increases in evoked noradrenaline release in the hypothalamus and sensitization of ACTH and corticosterone responses in rats. Eur J Neurosci 13:1923-1930.
92. Selvage D, Hales D, Rivier C (2004a) Comparison between the influence of the systemic and central injection of alcohol on Leydig cell activity. Alcohol Clin Exp Res 28:480-488.
93. Selvage D, Lee S, Parsons L, Seo D, Rivier C (2004b) A hypothalamic-testicular neural pathway is influenced by brain catecholamines, but not testicular blood flow. Endocrinology 145:1750-1759.
94. Selvage D, Rivier C (2003) Importance of the paraventricular nucleus of the hypothalamus as a component of a neural pathway between the brain and the testes that modulates testosterone secretion independently of the pituitary. Endocrinology 144:594-598.
95. Selvage DJ, Rivier C (2004) Leydig cell activity is regulated by a neural pathway between the hypothalamus and the testes that does not include the pituitary, in Recent Research Developments in Endocrinology, Vol. 4, pp 97-114. Transworld Research Network, Kerala, India.
96. Serra M, Pisu MG, Floris I, Floris S, Cannas E, Mossa A, Trapani G, Latrofa A, Purdy RH, Biggio G (2004) Social isolation increases the response of peripheral benzodiazepine receptors in the rat. Neurochem Int 45:141-148.
97. Shi Q, Emanuele NV, Emanuele MA (1998a) Effect of nitric oxide synthase inhibitors on preventing ethanol-induced suppression of the hypothalamic- pituitary-gonadal axis in the male rat. Alcohol Clin Exp Res 22:1763-1770.
98. Shi Q, Hales DB, Emanuele NV, Emanuele MA (1998b) Interaction of ethanol and nitric oxide in the hypothalamic-pituitary-gonadal axis in the male rat. Alcohol Clin Exp Res 22:1754-1762.
99. Sridaran R, Philip GH, Li H, Culty M, Liu Z, Stocco DM, Papadopoulos V (1999) GnRH agonist treatment decreases progesterone synthesis, luteal peripheral benzodiazepine receptor mRNA, ligand binding and steroidogenic acute regulatory protein expression during pregnancy. J Mol Endocrinol 22:45-54.
100. Srivastava VK, Hiney JK, Dearth RK, Dees WL (2001) Acute effects of ethanol on steroidogenic acute regulatory protein (StAR) in the prepubertal rat ovary. Alcoholi Clin Exp Res 25:1500-1505.
101. Srivastava VK, Hiney JK, Dearth RK, Dees WL (2002) Chronic effects of prepubertal ethanol administration on steroidogenic acute regulatory protein in the rat ovary. Alcohol Clin Exp Res 26:107-113.
102. Steiner J, Holloran M, Jabamoni K, Emaluele N, Emanuele M (1996) Sustained effects of a single injection of ethanol on the hypothalamic- pituitary-gonadal axis in the male rat. Alcohol Clin Exp Res 20:1368-1374.
103. Stocco DM, Clark BJ (1996) Regulation of the acute production of steroids in steroidogenic cells. Endocrine Rev 17:221-244.
104. Tatsumi N, Fujisawa M, Kanzaki M, Okuda Y, Okada H, Arakawa S, Kamidono S (1997) Nitric oxide production by cultured rat Leydig cells. Endocrinology 138:994-998.
105. Tilders FJH, Schmidt ED, Hoogedijk WJG, Swaab DF (1999) Delayed effects of stress and immune activation. Best Pract Res Clin Endocrinol Metab 13:523-540.
106. Turnbull AV, Rivier C (1997) Inhibition of gonadotropin-induced testosterone secretion by the intracerebroventricular injection of interleukin-1β in the male rat. Endocrinology 138:1008-1013.
107. Valles A, Marti O, Armario A (2003) Long-term effects of a single exposure to immobilization stress on the hypothalamic-pituitary-adrenal axis: transcriptional evidence for a progressive desensitization process. Eur J Neurosci 18:1353-1361.
108. 2-terminal truncated nitric-oxide synthase. J Biol Chem 272:11392-11401.
109. Wang Y, Newton DC, Miller TL, Teichert AM, Phillips MJ, Davidoff MS, Marsden PA (2002) An alternative promoter of the human neuronal nitric oxide synthase gene is expressed specifically in Leydig cells. Am J Pathol 160:369-380.
110. Welch C, Watson ME, Poth M, Hong T, Francis GL (1995) Evidence to suggest nitric oxide is an interstitial regulator of Leydig cell steroidogenesis. Metabolism 44:234-238.
111. West LA, Horvat RD, Roess DA, Barisas BG, Juengel JL, Niswender GD (2001) Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology 142:502-505.
112. Zilz A, Li H, Castello R, Papadopoulos V, Widmaier EP (1999) Developmental expression of the peripheral-type benzodiazepine receptor and the advent of steroidogenesis in rat adrenal glands. Endocrinology 140:859-864.