Normal responses to restraint stress in mice lacking the gene for neuronal nitric oxide synthase

Journal of Andrology

Volumn 30, Issue 5, 2009, Pages 614-620

  Weissman, Ben Avi ^a   Sottas, Chantal M ^b   Holmes, Michael ^b   Zhou, Ping ^c   Iadecola, Costantino ^c   Hardy, Dianne O ^b   Ge, Ren Shan ^b,d   Hardy, Matthew P ^b  

^a IIBR   (Israel)

^b ROCKEFELLER UNIVERSITY   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Androgen; Glucocorticoid; nNOS null mice; Testosterone

Indexed keywords

CORTICOSTERONE; LUTEINIZING HORMONE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; GENOTYPE; IMMOBILIZATION STRESS; LEYDIG CELL; LUTEINIZING HORMONE BLOOD LEVEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEROIDOGENESIS; TESTIS WEIGHT; TESTOSTERONE BLOOD LEVEL;

ANIMALS; CORTICOSTERONE; LUTEINIZING HORMONE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; NITRITES; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; TESTIS; TESTOSTERONE;

EID: 70349485725     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.2164/jandrol.108.007443     Document Type: Article

References (57)

1. Adams ML, Nock B, Truong R, Cicero TJ. Nitric oxide control of steroidogenesis: endocrine effects of NG-nitro-L-arginine and comparisons to alcohol. Life Sci. 1992;50:PL35-PL40.
2. Afework M, Tomlinson A, Belai A, Burnstock G. Colocalization of nitric oxide synthase and NADPH-diaphorase in rat adrenal gland. Neuroreport. 1992;3:893-896.
3. Armario A, Castellanos JM. A comparison of corticoadrenal and gonadal responses to acute immobilization stress in rats and mice. Physiol Behav. 1984;32:517-519. (Pubitemid 14120924)
4. Bernstein HG, Keilhoff G, Seidel B, Stanarius A, Huang PL, Fishman MC, Reiser M, Bogerts B, Wolf G. Expression of hypothalamic peptides in mice lacking neuronal nitric oxide synthase: reduced beta-END immunoreactivity in the arcuate nucleus. Neuroendocrinal. 1998;68:403-411. (Pubitemid 29000849)
5. Burnett AL, Ricker DD, Chamness SL, Maguire MP, Crone JK, Bredt DS, Snyder SH, Chang TS. Localization of nitric oxide synthase in the reproductive organs of the male rat. Biol Reprod. 1995;52:1-7.
6. Calza L, Giardino L, Ceccatelli S. NOS mRNA in the paraventricular nucleus of young and old rats after immobilization stress. Neuroreport. 1993;4:627-630. (Pubitemid 23190877)
7. Chandrashekar V, Bartke A. Influence of endogenous prolactin on the luteinizing hormone stimulation of testicular steroidogenesis and the role of prolactin in adult male rats. Steroids. 1988;51:559-576. (Pubitemid 19037849)
8. Chrousos GP, Gold PW. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA. 1992;267:1244-1252.
9. Cochran RC, Ewing LL, Niswender GD. Serum levels of follicle-stimulating hormone, prolactin, testosterone, 5a-dihydrotestosterone, 5a-androstane-3a,17b- diol, 5a-androstane-3b,17b-diol and 17b-estradiol from male beagles with spontaneous or induced benign prostatic hyperplasia. Invest Urol. 1981;19:142-147.
10. Cymeryng CB, Dada LA, Podesta EJ. Effect of nitric oxide on rat adrenal zona fasciculata steroidogenesis. J Endocrinol. 1998;158:197-203. (Pubitemid 28342063)
11. Cymeryng CB, Lotito SP, Colonna C, Finkielstein C, Pomeraniec Y, Grion N, Gadda L, Maloberti P, Podesta EJ. Expression of nitric oxide synthases in rat adrenal zona fasciculata cells. Endocrinology. 2002;143:1235-1242. (Pubitemid 34274352)
12. de Oliveira RM, Aparecida Del Bel E, Mamede-Rosa ML, Padovan CM, Deakin JF, Guimaraes FS. Expression of neuronal nitric oxide synthase mRNA in stress-related brain areas after restraint in rats. Neurosci Lett. 2000;289:123-126. (Pubitemid 30440641)
13. Del Punta K, Charreau EH, Pignataro OP. Nitric oxide inhibits Leydig cell steroidogenesis. Endocrinology. 1996;137:5337-5343. (Pubitemid 26423094)
14. Dong Q, Salva A, Sottas CM, Niu E, Holmes M, Hardy MP. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl. 2004;25:972-981. (Pubitemid 39425604)
15. Echeverry MB, Guimaraes FS, Del Bel EA. Acute and delayed restraint stress-induced changes in nitric oxide producing neurons in limbic regions. Neuroscience. 2004;125:981-993.
16. Eskiocak S, Gozen AS, Yapar SB, Tavas F, Kilic AS, Eskiocak M. Glutathione and free sulphydryl content of seminal plasma in healthy medical students during and after exam stress. Hum Reprod. 2005;20:2595-2600. (Pubitemid 41222515)
17. Fenster L, Katz DF, Wyrobek AJ, Pieper C, Rempel DM, Oman D, Swan SH. Effects of psychological stress on human semen quality. J Androl. 1997;18:194-202. (Pubitemid 27204229)
18. Giordano M, Vermeulen M, Trevani AS, Dran G, Andonegui G, Geffner JR. Nitric oxide synthase inhibitors enhance plasma levels of corticosterone and ACTH. Acta Physiol Scand. 1996;157:259-264. (Pubitemid 26178823)
19. Greenberg SS, Ouyang J, Zhao X, Parrish C, Nelson S, Giles TD. Effects of ethanol on neutrophil recruitment and lung host defense in nitric oxide synthase I and nitric oxide synthase II knockout mice. Alcohol Clin Exp Res. 1999;23:1435-1445. (Pubitemid 29468438)
20. Gulati K, Chakraborti A, Ray A. Modulation of stress-induced neurobehavioral changes and brain oxidative injury by nitric oxide (NO) mimetics in rats. Behav Brain Res. 2007;183:226-230. (Pubitemid 47351242)
21. Gulati K, Ray A, Masood A, Vijayan VK. Involvement of nitric oxide (NO) in the regulation of stress susceptibility and adaptation in rats. Indian J Exp Biol. 2006;44:809-815. (Pubitemid 44569241)
22. Gyurko R, Leupen S, Huang PL. Deletion of exon 6 of the neuronal nitric oxide synthase gene in mice results in hypogonadism and infertility. Endocrinology. 2002;143:2767-2774. (Pubitemid 34701341)
23. Hauser W, Sassmann A, Qadri F, Johren O, Dominiak P. Expression of nitric oxide synthase isoforms in hypothalamo-pituitary-adrenal axis during the development of spontaneous hypertension in rats. Brain Res Mol Brain Res. 2005;138:198-204. (Pubitemid 41138039)
24. Hikim AP, Vera Y, Vernet D, Castanares M, Diaz-Romero M, Ferrini M, Swerdloff RS, Gonzalez-Cadavid NF, Wang C. Involvement of nitric oxide-mediated intrinsic pathway signaling in age-related increase in germ cell apoptosis in male Brown-Norway rats. J Gerontol A Biol Sci Med Sci. 2005;60:702-708. (Pubitemid 40881175)
25. Hjollund NH, Bonde JP, Henriksen TB, Giwercman A, Olsen J. Job strain and male fertility. Epidemiology. 2004a;15:114-117.
26. Hjollund NH, Bonde JP, Henriksen TB, Giwercman A, Olsen J. Reproductive effects of male psychologic stress. Epidemiology. 2004b;15:21-27. (Pubitemid 40416993)
27. Hori N, Lee MC, Sasaguri K, Ishii H, Kamei M, Kimoto K, Toyoda M, Sato S. Suppression of stress-induced nNOS expression in the rat hypothalamus by biting. J Dent Res. 2005;84:624-628. (Pubitemid 43827843)
28. Huang PL, Dawson TM, Bredt DS, Snyder SH, Fishman MC. Targeted disruption of the neuronal nitric oxide synthase gene. Cell. 1993;75:1273-1286. (Pubitemid 24021903)
29. Kishimoto J, Tsuchiya T, Emson PC, Nakayama Y. Immobilization-induced stress activates neuronal nitric oxide synthase (nNOS) mRNA and protein in hypothalamic-pituitary-adrenal axis in rats. Brain Res. 1996;720:159-171. (Pubitemid 26179823)
30. Knorr DW, Vanha-Perittula T, Lipsett MB. Structure and function of rat testis through pubescence. Endocrinology. 1970;86:1298-1304.
31. Kostic TS, Andric SA, Maric D, Stojilkovic SS, Kovacevic R. Involvement of inducible nitric oxide synthase in stress-impaired testicular steroidogenesis. J Endocrinol. 1999;163:409-416. (Pubitemid 30033736)
32. Kriegsfeld LJ, Dawson TM, Dawson VL, Nelson RJ, Snyder SH. Aggressive behavior in male mice lacking the gene for neuronal nitric oxide synthase requires testosterone. Brain Res. 1997;769:66-70. (Pubitemid 27455888)
33. Lai F-J, Hsin Y-C, Huang S-C, Cheng C-L, Hsin S-C, Hsieh M-C, Shin S-J. Down-regulation of adrenal neuronal nitric oxide synthase mRNAs and proteins after deoxycorticosterone acetate-salt treatment in rats. J Steroid Biochem Mol Biol. 2006;101:197-203.
34. Madrigal JL, Moro MA, Lizasoain I, Lorenzo P, Castrillo A, Bosca L, Leza JC. Inducible nitric oxide synthase expression in brain cortex after acute restraint stress is regulated by nuclear factor kappaB-mediated mechanisms. J Neurochem. 2001;76:532-538. (Pubitemid 32097029)
35. McEwen BS, Albeck D, Cameron H, Chao HM, Gould E, Hastings N, Kuroda Y, Luine V, Magarinos AM, McKittrick CR. Stress and the brain: a paradoxical role for adrenal steroids. Vitam Horm. 1995;51:371-402.
36. Miyake S, Takahashi SS, Yoshino F, Todoki K, Sasaguri K, Sato S, Lee MC. Nitric oxide levels in rat hypothalamus are increased by restraint stress and decreased by biting. Redox Rep. 2008;13:31-39.
37. Mohn CE, Fernandez-Solari J, De Laurentiis A, Prestifilippo JP, de la Cal C, Funk R, Bornstein SR, McCann SM, Rettori V. The rapid release of corticosterone from the adrenal induced by ACTH is mediated by nitric oxide acting by prostaglandin E2. Proc Natl Acad Sci U S A. 2005;102:6213-6218. (Pubitemid 40594280)
38. Nelson RJ, Demas GE, Huang PL, Fishman MC, Dawson VL, Dawson TM, Snyder SH. Behavioural abnormalities in male mice lacking neuronal nitric oxide synthase. Nature. 1995;378:383-386.
39. Okere CO, Waterhouse BD. Acute restraint increases NADPH-diaphorase staining in distinct subregions of the rat dorsal raphe nucleus: implications for raphe serotonergic and nitrergic transmission. Brain Res. 2006;1119:174-181.
40. Orlando GF, Langnaese K, Landgraf R, Spina MG, Wolf G, Engelmann M. Neural nitric oxide gene inactivation affects the release profile of oxytocin into the blood in response to forced swimming. Nitric Oxide. 2007;16:64-70. (Pubitemid 44820879)
41. Orr TE, Mann DR. Role of glucocorticoid in the stress-induced suppression of testicular steroidogenesis in adult male rats. Horm Behav. 1992;26:350-363.
42. Orr TE, Taylor MF, Bhattacharyya AK, Collins DC, Mann DR. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17a-hydroxylase and 17,20-lyase without affecting the binding of LH/hCG receptors. J Androl. 1994;15:302-308.
43. Repcekova D, Mikulaj L. Plasma testosterone of rats subjected to immobilization stress and/or HCG administration. Horm Res. 1977;8:51-57. (Pubitemid 8145089)
44. Rettori V, Mohn C, Scorticati C, Vissio P, Cella M, Farina M, Franchi A, McCann SM. Effect of neurogenic stress and ethanol on nitric oxide synthase and cyclooxygenase activities in rat adrenals. Ann N Y Acad Sci. 2003;992:86-98. (Pubitemid 36706639)
45. Rivier C, Shen GH. In the rat, endogenous nitric oxide modulates the response of the hypothalamic-pituitary-adrenal axis to interleukin-1 beta, vasopressin, and oxytocin. J Neurosci. 1994;14:1985-1993.
46. Salchner P, Lubec G, Engelmann M, Orlando GF, Wolf G, Sartori SB, Hoeger H, Singewald N. Genetic functional inactivation of neuronal nitric oxide synthase affects stress-related Fos expression in specific brain regions. Cell Mol Life Sci. 2004;61:1498-1506. (Pubitemid 38858355)
47. Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 2000;21:55-89.
48. Spencer RL, Miller AH, Moday H, McEwen BS, Blanchard RJ, Blanchard DC, Sakai RR. Chronic social stress produces reductions in available splenic type II corticosteroid receptor binding and plasma corticosteroid binding globulin levels. Psychoneuroendocrinology. 1996;21:95-109. (Pubitemid 26130399)
49. Sugama S, Fujita M, Hashimoto M, Conti B. Stress induced morphological microglial activation in the rodent brain: involvement of interleukin-18. Neuroscience. 2007;146:1388-1399. (Pubitemid 46694135)
50. Tanaka K, Chiba T. Ultrastructural localization of nerve terminals containing nitric oxide synthase in rat adrenal gland. Neurosci Lett. 1996;204:153-156. (Pubitemid 26054666)
51. Trainor BC, Workman JL, Jessen R, Nelson RJ. Impaired nitric oxide synthase signaling dissociates social investigation and aggression. Behav Neurosci. 2007;121:362-369. (Pubitemid 47445088)
52. Tsuchiya T, Kishimoto J, Nakayama Y. Marked increases in neuronal nitric oxide synthase (nNOS) mRNA and NADPH-diaphorase histostaining in adrenal cortex after immobilization stress in rats. Psychoneuroendocrinology. 1996;21:287-293. (Pubitemid 26246856)
53. Tunctan B, Weigl Y, Dotan A, Peleg L, Zengil H, Ashkenazi I, Abacioglu N. Circadian variation of nitric oxide synthase activity in mouse tissue. Chronobiol Int. 2002;19:393-404. (Pubitemid 34478035)
54. Wang Y, Goligorsky MS, Lin M, Wilcox JN, Marsden PA. A novel, testis-specific mRNA transcript encoding an NH2-terminal truncated nitric-oxide synthase. J Biol Chem. 1997;272:11392-11401. (Pubitemid 27184144)
55. Weissman BA, Niu E, Ge R, Sottas CM, Holmes M, Hutson JC, Hardy MP. Paracrine modulation of androgen synthesis in rat Leydig cells by nitric oxide. J Androl. 2005;26:369-378. (Pubitemid 40628974)
56. Weissman BA, Sottas CM, Zhou P, Iadecola C, Hardy MP. Testosterone production in mice lacking inducible nitric oxide synthase expression is sensitive to restraint stress. Am J Physiol Endocrinol Metab. 2007;292:E615-E620. (Pubitemid 46220587)
57. Yang G, Zhang Y, Ross ME, Iadecola C. Attenuation of activity-induced increases in cerebellar blood flow in mice lacking neuronal nitric oxide synthase. Am J Physiol Heart Circ Physiol. 2003;285:H298-H304. (Pubitemid 36736442)