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

References

1. Chrousos G. Organization and integration of the endocrine system. Sleep Med Clin 2007;2:125–45.10.1016/j.jsmc.2007.04.004Search in Google Scholar PubMed PubMed Central

2. Potemina T. Impairment of spermatogenesis in male rats during stress. Bull Exp Biol Med 2008;145:700–2.10.1007/s10517-008-0173-8Search in Google Scholar PubMed

3. Retana-Márquez S, Bonilla-Jaime H, Vázquez-Palacios G, Martínez-García R, Velázquez-Moctezuma J. Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm Behav 2003;44:327–37.10.1016/j.yhbeh.2003.04.001Search in Google Scholar PubMed

4. Yilmaz F. Effect of immobilization stress on gonadotropic hormones and gonadal steroid hormones. Zh Evol Biokhim Fiziol 2003;39:226–8.Search in Google Scholar

5. Hjollund N, Bonde J, Henriksen T, Giwercman A, Olsen J. Reproductive effects of male psychologic stress. Epidemiology 2004;159:21–7.10.1097/01.ede.0000100289.82156.8bSearch in Google Scholar PubMed

6. Wingfield J, Sapolsky R. Reproduction and resistance to stress: when and how. J Neuroendocrinol 2003;15:711–24.10.1046/j.1365-2826.2003.01033.xSearch in Google Scholar PubMed

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;109:457–67.10.1172/JCI0213190Search in Google Scholar

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: 416–25.10.1016/j.taap.2006.06.016Search in Google Scholar PubMed

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;121:241–7.10.1097/00029330-200802010-00012Search in Google Scholar

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;237:184–93.10.1016/j.tox.2007.05.014Search in Google Scholar PubMed

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: 3893–900.10.1182/blood-2002-08-2608Search in Google Scholar PubMed

12. Kvetnansky R, Mikulaj L. Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology 1970;87:738–43.10.1210/endo-87-4-738Search in Google Scholar

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;65:532–43.10.1007/s11418-011-0535-9Search in Google Scholar

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.Search in Google Scholar

15. Silber R, Busch R, Oslapas R. Practical procedure for estimation of corticosterone or hydrocortisone. Clin Chem 1958;4:278–85.10.1093/clinchem/4.4.278Search in Google Scholar

16. Ciarlone A. Further modification of fluorometric method for analyzing brain amines. Microchem J 1978;23:9–12.10.1016/0026-265X(78)90034-6Search in Google Scholar

17. Mayes R. Measurement of carbon monoxide and cyanide in blood. J Clin Pathol 1993;46:982–8.10.1136/jcp.46.11.982Search in Google Scholar PubMed PubMed Central

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;5:105–13.10.1530/ror.0.0050105Search in Google Scholar PubMed

19. Pacak K, Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 2001;22:502–48.10.1210/edrv.22.4.0436Search in Google Scholar PubMed

20. Bulger E, Garcia I, Maier R. Induction of heme-oxygenase 1 inhibits endothelial cell activation by endotoxin and oxidant stress. Surgery 2003;134:146–52.10.1067/msy.2003.215Search in Google Scholar PubMed

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;86:267–79.10.1007/s00109-007-0276-0Search in Google Scholar PubMed

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;9:2139–55.10.1089/ars.2007.1803Search in Google Scholar PubMed

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;348:615–9.10.1042/bj3480615Search in Google Scholar

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.Search in Google Scholar

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.Search in Google Scholar

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;25:973–81.10.1002/j.1939-4640.2004.tb03170.xSearch in Google Scholar

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;73:1018–24.10.1016/j.steroids.2007.12.020Search in Google Scholar

28. Martin L, Tremblay J. Glucocorticoids antagonize cAMP-induced star transcription in Leydig cells through the orphan nuclear receptor NR4A1. J Mol Endocrinol 2008;41:165–75.10.1677/JME-07-0145Search in Google Scholar

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;322:147–53.10.1007/s00441-005-0006-2Search in Google Scholar

30. Gao H, Tong M, Hu Y, Guo Q, Ge R, Hardy M. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 2002;143:130–8.10.1210/endo.143.1.8604Search in Google Scholar

31. Jara M, Carballada R, Esponda P. Age-induced apoptosis in the male genital tract of the mouse. Reproduction 2004;127: 359–66.10.1530/rep.1.00092Search in Google Scholar

32. Rai J, Pandey S, Srivastava R. Effect of immobilization stress on spermatogenesis of albino rats. J Anat Soc 2003;52:55–7.Search in Google Scholar

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;48:607–13.10.1016/S1043-6618(03)00241-XSearch in Google Scholar

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;1158:1–10.10.1016/j.brainres.2007.04.080Search in Google Scholar PubMed PubMed Central

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;67:1750–5.10.1095/biolreprod.102.006312Search in Google Scholar PubMed

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;14:4505–16.10.3390/molecules14114505Search in Google Scholar PubMed PubMed Central

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;30:567–78.10.1177/0960327110376548Search in Google Scholar PubMed

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;10:18.10.1186/1472-6882-10-18Search in Google Scholar PubMed PubMed Central

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;86:878–85.10.1016/j.fertnstert.2006.02.111Search in Google Scholar PubMed

40. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008;59:2–11.10.1111/j.1600-0897.2007.00559.xSearch in Google Scholar PubMed

41. Otterbein L, Choi A. Heme oxygenase: colors of defense against cellular stress. Am J Physiol Lung Cell Mol Physiol 2000;279:L1029–37.10.1152/ajplung.2000.279.6.L1029Search in Google Scholar PubMed

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;98:4611–6.10.1073/pnas.081082098Search in Google Scholar PubMed PubMed Central

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;44:847–55.10.1016/j.freeradbiomed.2007.11.012Search in Google Scholar PubMed PubMed Central

44. Wang R, Wang Z, Wu L. Carbon-monoxide-induced vasorelaxation and the underlying mechanisms. Br J Pharmacol 1997;121:927–34.10.1038/sj.bjp.0701222Search in Google Scholar PubMed PubMed Central

45. Roman R. P450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002;82:131–85.10.1152/physrev.00021.2001Search in Google Scholar PubMed

46. Wu L, Wang R. Carbon monoxide: endogenous production, physiological functions, and pharmacological applications. Pharmacol Rev 2005;57:585–630.10.1124/pr.57.4.3Search in Google Scholar PubMed

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;22:1182–90.10.1097/00004872-200406000-00020Search in Google Scholar PubMed

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;318:8–16.10.1124/jpet.105.099051Search in Google Scholar PubMed

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:E1351–9.10.1152/ajpendo.00653.2005Search in Google Scholar PubMed

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;194:11–20.10.1677/JOE-06-0199Search in Google Scholar PubMed

51. Hodel A. Effects of glucocorticoids on adrenal chromaffin cells. J Neuroendocrinol 2001;13:216–20.Search in Google Scholar

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;47:771–8.10.1136/gut.47.6.771Search in Google Scholar PubMed PubMed Central

53. Kim D, Choi H, Kim S, Hwang O. Upregulation of catecholamine biosynthetic enzymes by nitric oxide. J Neurosci Res 2003;72:98–104.10.1002/jnr.10557Search in Google Scholar PubMed

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;2228:64–9.10.1177/153537020322800109Search in Google Scholar PubMed

55. Shiraishi K, Naito K. Increased expression of Leydig cell haem oxygenase-1 preserves spermatogenesis in varicocele. Hum Reprod 2005;20:2608–26.10.1093/humrep/dei063Search in Google Scholar PubMed

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;177:1928–33.10.1016/j.juro.2007.01.015Search in Google Scholar PubMed

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: 6122–32.10.3748/wjg.14.6122Search in Google Scholar PubMed PubMed Central