Effect of acute immobilization stress with or without a heme oxygenase inducer on testicular structure and function in male albino rats

Journal of Basic and Clinical Physiology and Pharmacology

Volumn 24, Issue 4, 2013, Pages 255-262

  Aziz, Neven Makram ^a   Ragy, Merhan Mamdouh ^a   Gayyed, Mariana Fathy ^a  

^a Minia University   (Egypt)

Author keywords

Heme oxygenase 1; Hemin; Immobilization stress; Testosterone

Indexed keywords

ADRENALIN; CARBOXYHEMOGLOBIN; CATALASE; CORTICOSTERONE; HEME OXYGENASE 1; HEMIN; LUTEINIZING HORMONE; MALONALDEHYDE; NORADRENALIN; TESTOSTERONE;

ADRENALIN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CATECHOLAMINE BLOOD LEVEL; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; ENZYME ACTIVITY; GERM CELL; HISTOPATHOLOGY; IMMOBILIZATION STRESS; LUTEINIZING HORMONE BLOOD LEVEL; MALE; NONHUMAN; NORADRENALIN BLOOD LEVEL; RAT; SEMINIFEROUS TUBULE; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS; TESTIS FUNCTION; TESTIS INJURY; TESTOSTERONE BLOOD LEVEL; UPREGULATION;

ACUTE DISEASE; ANIMALS; CARBOXYHEMOGLOBIN; CATECHOLAMINES; CORTICOSTERONE; ENZYME INDUCTION; HEME OXYGENASE (DECYCLIZING); HEMIN; LUTEINIZING HORMONE; MALE; PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; STRESS, PSYCHOLOGICAL; TESTIS; TESTOSTERONE;

EID: 84898637735     PISSN: 07926855     EISSN: 21910286     Source Type: Journal    
DOI: 10.1515/jbcpp-2012-0066     Document Type: Article

References (57)

1. Chrousos G. Organization and integration of the endocrine system. Sleep Med Clin 2007;2:125-45.
2. Potemina T. Impairment of spermatogenesis in male rats during stress. Bull Exp Biol Med 2008;145:700-2.
3. Retana-Marquez S, Bonilla-Jaime H, Vazquez-Palacios G, Martinez-Garcia R, Velazquez-Moctezuma J. Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm Behav 2003;44:327-37.
4. Yilmaz F. Effect of immobilization stress on gonadotropic hormones and gonadal steroid hormones. Zh Evol Biokhim Fiziol 2003;39:226-8.
5. Hjollund N, Bonde J, Henriksen T, Giwercman A, Olsen J. Reproductive effects of male psychologic stress. Epidemiology 2004;159:21-7.
6. Wingfield J, Sapolsky R. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003;15:711-24.
7. Ozawa N, Goda N, Makino N, Yamaguchi T, Yoshimura Y, Suematsu M. Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J Clin Invest 2002;109:457-67.
8. Morio L, Leone A, Sawant S, Nie A, Parker J, Taggart P, et al. Hepatic expression of heme oxygenase-1 and antioxidant response element-mediated genes following administration of ethinyl estradiol to rats. Toxicol Appl Pharmacol 2006;216: 416-25.
9. Chen Y, Zhu X, Zhao X, Xing H, Li Y. Hemin, a heme oxygenase-1 inducer, improves aortic dysfunction in insulin resistant rats. Chin Med J 2008;121:241-7.
10. Wen T, Wu Z, Liu Y, Tan Y, Ren F, Wu H. Upregulation of heme oxygenase-1 with hemin prevents D-galactosamine and lipopolysaccharide-induced acute hepatic injury in rats. Toxicology 2007;237:184-93.
11. Ndisang J, Wu L, Zhao W, Wang R. Induction of heme oxygenase-1 and stimulation of cGMP production by hemin in aortic tissues from hypertensive rats. Blood 2003;101: 3893-900.
12. Kvetnansky R, Mikulaj L. Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology 1970;87:738-43.
13. Bhatia N, Jaggi A, Singh N, Anand P, Dhawan R. Adaptogenic potential of curcumin in experimental chronic stress and chronic unpredictable stress-induced memory deficits and alterations in functional homeostasis. J Nat Med 2011;65:532-43.
14. Bhattacharya D, Sur T. The effect of Panax ginseng and diazepam on brain and hypothalamic 5-hydroxytryptamine during stress. Indian J Physiol Pharmacol 1999;43:505-9.
15. Silber R, Busch R, Oslapas R. Practical procedure for estimation of corticosterone or hydrocortisone. Clin Chem 1958;4:278-85.
16. Ciarlone A. Further modification of fluorometric method for analyzing brain amines. Microchem J 1978;23:9-12.
17. Mayes R. Measurement of carbon monoxide and cyanide in blood. J Clin Pathol 1993;46:982-8.
18. Tilbrook A, Turner A, Clarke I. Effects of stress on reproduction in non-rodent mammals: The role of glucocorticoids and sex differences. Rev Reprod 2000;5:105-13.
19. Pacak K, Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001;22:502-48.
20. Bulger E, Garcia I, Maier R. Induction of heme-oxygenase 1 inhibits endothelial cell activation by endotoxin and oxidant stress. Surgery 2003;134:146-52.
21. Bilban M, Haschemi A, Wegiel B, Chin B, Wagner O, Otterbein L. Heme oxygenase and carbon monoxide initiate homeostatic signaling. J Mol Med (Berl) 2008;86:267-79.
22. Desmard M, Boczkowski J, Poderoso J, Motterlini R. Mitochondrial and cellular heme-dependent proteins as targets for the bioactive function of the heme oxygenase/carbon monoxide system. Antioxid Redox Signal 2007;9:2139-55.
23. Clark J, Foresti R, Green C, Motterlini R. Dynamics of haemoxygenase-1 expression and bilirubin production in cellular protection against oxidative stress. Biochem J 2000;348:615-9.
24. Erario M, Gonzales S, Noriega G, Tomaro M. Bilirubin and ferritin as protectors against hemin-induced oxidative stress in rat liver. Cell Mol Biol 2002;48:877-84.
25. Orr T, Taylor M, Bhattacharyya A, Collins D, Mann D. Acute immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17α-hydroxylase and 17, 20-lyase without affecting the binding of LH/hCG receptors. J Androl 1994;15:302-8.
26. Dong Q, Salva A, Sottas C, Niu E, Holmes M, Hardy M. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl 2004;25:973-81.
27. Hu G, Lian Q, Lin H, Latif S, Morris D, Hardy M, et al. Rapid mechanisms of glucocorticoid signaling in the Leydig cell. Steroids 2008;73:1018-24.
28. Martin L, Tremblay J. Glucocorticoids antagonize cAMP-induced star transcription in Leydig cells through the orphan nuclear receptor NR4A1. J Mol Endocrinol 2008;41:165-75.
29. Hardy M, Gao H, Dong Q, Ge R, Wang Q, Chai W, et al. Stress hormone and male reproductive function. Cell Tissue Res 2005;322:147-53.
30. Gao H, Tong M, Hu Y, Guo Q, Ge R, Hardy M. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 2002;143:130-8.
31. Jara M, Carballada R, Esponda P. Age-induced apoptosis in the male genital tract of the mouse. Reproduction 2004;127: 359-66.
32. Rai J, Pandey S, Srivastava R. Effect of immobilization stress on spermatogenesis of albino rats. J Anat Soc 2003;52:55-7.
33. Sanchez A, Toledo-Pinto E, Menezes M, Pereira O. Changes in norepinephrine and epinephrine concentrations in adrenal gland of the rats submitted to acute immobilization stress. Pharmacol Res 2003;48:607-13.
34. Xu L, Chen X, Sun B, Sterling C, Tank A. Evidence for regulation of tyrosine hydroxylase mRNA translation by stress in rat adrenal medulla. Brain Res 2007;1158:1-10.
35. Hardy M, Sottas C, Ge R, McKittrick C, Tamashiro K, McEwen B, et al. Trends of reproductive hormones in male rats during psychosocial stress: role of glucocorticoid metabolism in behavioral dominance. Biol Reprod 2002;67:1750-5.
36. Popovic M, Janicijevic-Hudomal S, Kaurinovic B, Rasic J, Trivic S, Vojnović M. Antioxidant effects of some drugs on immobilization stress combined with cold restraint stress. Molecules 2009;14:4505-16.
37. Dhanabalan S, Jubendradass R, Latha P, Mathur P. Effect of restraint stress on 2, 3, 7, 8 tetrachlorodibenzo-p-dioxin induced testicular and epididymal toxicity in rats. Hum Exp Toxicol 2011;30:567-78.
38. Kumar A, Garg R, Prakash A. Effect of St. John's Wort (Hypericum perforatum) treatment on restraint stress-induced behavioral and biochemical alteration in mice. BMC Complement Altern Med 2010;10:18.
39. Agarwal A, Sharma R, Nallella K, Thomas A, Alvarez J, Sikka S. Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril 2006;86:878-85.
40. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: An update. Am J Reprod Immunol 2008;59:2-11.
41. Otterbein L, Choi A. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000;279:L1029-37.
42. Chan K, Han X, Kan Y. An important function of NRF2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 2001;98:4611-6.
43. Lin Q, Weis S, Yang G, Zhuang T, Abate A, Dennery P. Catalytic inactive heme oxygenase-1 protein regulates its own expression in oxidative stress. Free Radic Biol Med 2008;44:847-55.
44. Wang R, Wang Z, Wu L. Carbon-monoxide-induced vasorelaxation and the underlying mechanisms. Br J Pharmacol 1997;121:927-34.
45. Roman R. P450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002;82:131-85.
46. Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 2005;57:585-630.
47. Lo W, Hsiao M, Tung C, Tseng C. The cardiovascular effects of nitric oxide and carbon monoxide in the nucleus tractus solitarii of rats. J Hypertens 2004;22:1182-90.
48. Lo W, Lu P, Ho W, Hsiao M, Tseng C. Induction of heme oxygenase-1 is involved in carbon monoxide-mediated central cardiovascular regulation. J Pharmacol Exp Ther 2006;318:8-16.
49. Asif A, Ljubojevic M, Sabolic I, Shnitsar V, Metten M, Anzai N, et al. Regulation of steroid hormones biosynthesis and organic anion transporters by forskolin and DHEA-S treatment in adrenocortical cells. Am J Physiol Endocrinol Metab 2006;291:E1351-9.
50. Grion N, Repetto E, Pomeraniec Y, Calejman CM, Astort F, Sanchez R, et al. Induction of nitric oxide synthase and heme oxygenase activities by endotoxin in the rat adrenal cortex: involvement of both signaling systems in the modulation of ACTH-dependent steroid production. J Endocrinol 2007;194:11-20.
51. Hodel A. Effects of glucocorticoids on adrenal chromaffin cells. J Neuroendocrinol 2001;13:216-20.
52. Cavicchi M, Gibbs L, Whittle B. Inhibition of inducible nitric oxide synthase in the human intestinal epithelial cell line, DLD-1, by the inducers of heme oxygenase 1, bismuth salts, heme, and nitric oxide donors. Gut 2000;47:771-8.
53. Kim D, Choi H, Kim S, Hwang O. Upregulation of catecholamine biosynthetic enzymes by nitric oxide. J Neurosci Res 2003;72:98-104.
54. Alexandreanu L, Lawson D. Heme oxygenase in the rat anterior pituitary: immunohistochemical localization and possible role in gonadotropin and prolactin secretion. Exp Biol Med 2003;2228:64-9.
55. Shiraishi K, Naito K. Increased expression of Leydig cell haem oxygenase-1 preserves spermatogenesis in varicocele. Hum Reprod 2005;20:2608-26.
56. Yang S, Shih H, Chow Y, Tsai P, Wang T, Wang P, et al. The protective role of heme oxygenase-1 induction on testicular tissues after testicular torsion and detorsion. J Urol 2007;177:1928-33.
57. Li Volti G, Sacerdoti D, Di Giacomo C, Barcellona M, Scacco A, Murabito P, et al. Natural heme oxygenase-1 inducers in hepatobiliary function. World J Gastroenterol 2008;14: 6122-32.