Stress induces glucocorticoid-mediated apoptosis of rat Leydig cells in vivo

Stress

Volumn 15, Issue 1, 2012, Pages 74-84

  Chen, Yong ^a,b   Wang, Qian ^a   Wang, Fei Fei ^a   Gao, Hui Bao ^a   Zhang, Ping ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Adenovirus microRNA; Adrenalectomy; Apoptosis; Glucocorticoid receptor; Leydig cell; Testosterone

Indexed keywords

CARRIER PROTEIN; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; TESTOSTERONE;

ADENOVIRUS; ADRENALECTOMY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; CYTOPLASM; DOWN REGULATION; IN VITRO STUDY; IN VIVO STUDY; LEYDIG CELL; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE SYNTHESIS;

ADRENALECTOMY; ANIMALS; APOPTOSIS; COLD TEMPERATURE; CORTICOSTERONE; LEYDIG CELLS; MALE; MICRORNAS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCOCORTICOID; RESTRAINT, PHYSICAL; RNA INTERFERENCE; STRESS, PSYCHOLOGICAL; SWIMMING; TESTOSTERONE;

EID: 83455195502     PISSN: 10253890     EISSN: 16078888     Source Type: Journal    
DOI: 10.3109/10253890.2011.585188     Document Type: Article

References (50)

1. Atkinson HC, Wood SA, Kershaw YM, BateE, Lightman SL. 2006. Diurnal variation in the responsiveness of the hypothalamic-pituitary-adrenal axis of the male rat to noise stress. J Neuroendocrinol 18:526-533. (Pubitemid 43821724)
2. Bidzinska B, Petraglia F, Angioni S, Genazzani AD, Criscuolo M, Ficarra G, Gallinelli A, Trentini GP, Genazzani AR. 1993. Effect of different chronic intermittent stressors and acetyl-I-carnitine on hypothalamic beta-endorphin and GnRH and on plasma testosterone levels in male rats. Neuroendocrinology 57: 985-990. (Pubitemid 23260774)
3. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen B, Sakai RR. 1995. Visible burrow system as a model of chronic social stress: Behavioral and neuroendocrine correlates. Psycho-neuroendocrinology 20:117-134.
4. Blanchard RJ, Dulloog L, Markham C, Nishimura O, Compton JN, Jun A, Han C, Blanchard DC. 2001. Sexual and aggressive interactions in a visible burrow system with provisioned burrows. Physiol Behav 72:245-254. (Pubitemid 32184815)
5. Chai WR, Chen Y, Wang Q, Gao HB. 2008. Mechanism of nuclear factor of activated T-cells mediated FasL expression in corticosterone-treated mouse Leydig tumor cells. BMC Cell Biol 9:31.
6. Chen J, Young S, Subburaju S, Sheppard J, Kiss A, Atkinson H, Wood S, Lightman S, Serradeil-Le Gal C, Aguilera G. 2008. Vasopressin does not mediate hypersensitivity of the hypothala-mic pituitary adrenal axis during chronic stress. Ann N Y Acad Sci 1148:349-359.
7. Chrousos GP, Gold PW. 1992. The concepts of stress and stress system disorders. Overview of physical and behavioral homeo-stasis. J Am Med Assoc 267:1244-1252.
8. Contreras LN, Masini AM, Danna MM, Kral M, Bruno OD, Rossi MA, Andrada JA. 1996. Glucocorticoids: Their role on gonadal function and LH secretion. Minerva Endocrinol 21: 43-46.
9. De Boer SF, Koopmans SJ, Slangen JL, Van der Gugten J. 1989. Effects of fasting on plasma catecholamine, corticosterone and glucose concentrations under basal and stress conditions in individual rats. Physiol Behav 45:989-994. (Pubitemid 19158289)
10. Deviche PJ, Hurley LL, Fokidis HB, Lerbour B, Silverin B, Silverin B, Sabo J, Sharp PJ. 2010. Acute stress rapidly decreases plasma testosterone in a free-ranging male songbird: Potential site of action and mechanism. Gen Comp Endocrinol 169: 82-90.
11. Dong Q, Salva A, Sottas CM, Niu E, Holmes M, Hardy MP. 2004. Rapid glucocorticoid mediation of suppressed testosterone biosynthesis in male mice subjected to immobilization stress. J Androl 25:973-981. (Pubitemid 39425604)
12. Fenster L, Katz DF, Wyrobek AJ, Pieper C, Rempel DM, Oman D, Swan SH. 1997. Effects of psychological stress on human semen quality. J Androl 18:194-202. (Pubitemid 27204229)
13. Finlay JM, Zigmond MJ, Abercrombie ED. 1995.Increased dopamine and norepinephrine relase in medial prefrontal cortex induced by acute and chronic stress: Effects of diazepam. Neuroscience. 64:619-628.
14. Gao HB, Shan LX, Monder C, Hardy MP. 1996. Suppression of endogenous corticosterone levels in vivo increases the steroido-genic capacity of purified rat Leydig cells in vitro. Endocrinology 137:1714-1718. (Pubitemid 26133946)
15. Gao HB, Tong MH, Hu YQ, Guo QS, Ge RS, Hardy MP. 2002. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 143:130-138. (Pubitemid 34056411)
16. Gao HB, Tong MH, Hu YQ, You HY, Guo QS, Ge RS, Hardy MP. 2003. Mechanisms of glucocorticoid-induced Leydig cell apoptosis. Mol Cell Endocrinol 199:153-163. (Pubitemid 36170299)
17. Ge RS, Hardy DO, Catterall JF, Hardy MP. 1997. Developmental changes in glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase oxidative and reductive activities in rat Leydig cells. Endocrinology 138:5089-5095. (Pubitemid 27509664)
18. Gouirand AM, Matuszewich L. 2005. The effects of chronic unpredictable stress (CUS) on male rats in the water maze. Physiol Behav 86:21-31. (Pubitemid 41316605)
19. Gray GD, Smith ER, Damassa DA, Ehrenkranz JR, Davidson JM. 1978. Neuroendocrine mechanisms mediating the supression of circulating testosterone levels associated with chronic stress in male rats. Neuroendocrinology 25:247-256. (Pubitemid 8311281)
20. Hales DB, Payne AH. 1989. Glucocorticoid-mediated repression of P450scc mRNA and de novo synthesis in cultured Leydig cells. Endocrinology 124:2099-2104. (Pubitemid 19132003)
21. Hansson AC, Fuxe K. 2008. Time-course of immediate early gene expression in hippocampal subregions of adrenalectomized rats after acute corticosterone challenge. Brain Res 1215:1-10.
22. Hansson AC, Cintra A, Belluardo N, Sommer W, Bhatnagar M, Bader M, Ganten D, Fuxe K. 2000. Gluco-and mineralocorti-coid receptor-mediated regulation of neurotrophic factor gene expression in the dorsal hippocampus and the neocortex of the rat. Eur J Neurosci 12:2918-2934.
23. Hardy MP, Ganjam VK. 1997. Stress, 11beta-HSD, and Leydig cell function. J Androl 18:475-479. (Pubitemid 27454303)
24. Hardy MP, Sottas CM, Ge R, McKittrick CR, Tamashiro KL, McEwen BS, Haider SG, Markham CM, Blanchard RJ, Blanchard DC, Sakai RR. 2002. Trends of reproductive hormones in male rats during psychosocial stress: Role of glucocorticoid metabolism in behavioral dominance. Biol Reprod 67:1750-1755. (Pubitemid 35388004)
25. Hatanaka K, Ikegaya H, Takase I, Kobayashi M, Iwase H, Yoshida K. 2001. Immobilization stress-induced thymocyte apoptosis in rats. Life Sci 69:155-165. (Pubitemid 32523071)
26. Joëls M, Karst H, Alfarez D, Heine VM, Qin Y, van Riel E, Verkuyl M, Lucassen PJ, Krugers HJ. 2004. Effects of chronic stress on structure and cell function in rat hippocampus and hypothala-mus. Stress 7:221-231. (Pubitemid 40591422)
27. Klinefelter GR, Hall PF, Ewing LL. 1987. Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol Reprod 6:769-783.
28. Korte SM. 2001. Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 25:117-142. (Pubitemid 32377167)
29. Manikandan S, Srikumar R, Jeya Parthasarathy N, Sheela Devi R. 2005. Protective effect of Acorus calamus LINN on free radical scavengers and lipid peroxidation in discrete regions of brain against noise stress exposed rat. Biol Pharm Bull 28:2327-2330. (Pubitemid 41757430)
30. Marić D, Kostić T, Kovacević R. 1996. Effects of acute and chronic immobilization stress on rat Leydig cell steroidogenesis. J Steroid Biochem Mol Biol 58:351-355. (Pubitemid 26301128)
31. Monder C, Miroff Y, Marandici A, Hardy MP. 1994a. 11 beta-Hydroxysteroid dehydrogenase alleviates glucocorticoid-mediated inhibition of steroidogenesis in rat Leydig cells. Endocrinology 134:1199-1204.
32. Monder C, Sakai RR, Miroff Y, Blanchard DC, Blanchard RJ. 1994b. Reciprocal changes in plasma corticosterone and testosterone in stressed male rats maintained in a visible burrow system: Evidence for a mediating role of testicular 11 beta-hydroxysteroid dehydrogenase. Endocrinology 134:1193-1198.
33. Mormède P, Lemaire V, Castanon N, Dulluc J, Laval M, Le Moal M. 1990. Multiple neuroencodrine responses to chronic social stress: Interaction between individual characteristics and situational factors. Physiol Behav 47:1099-1105. (Pubitemid 20224208)
34. Mravec B, Tillinger A, Bodnar I, Nagy GM, Palkovits M, Kvetnanský R. 2008. The response of plasma catecholamines in rats simultaneously exposed to immobilization and painful stimuli. Ann N Y Acad Sci 1148:196-200.
35. Munck A, Guyre PM, Holbrook NJ. 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 5:25-44.
36. Orr TE, Taylor MF, Bhattacharyya AK, Collins DC, Mann DR. 1994. Immobilization stress disrupts testicular steroidogenesis in adult male rats by inhibiting the activities of 17a-hydroxylase and 17, 20-lyase without affecting the binding LH/hCG receptors. J Androl 15:302-308. (Pubitemid 24256643)
37. Papp M, Nalepa I, Antkiewicz-Michaluk L, Sanchez C. 2002. Behavioural and biochemical studies of citalopram and WAY 100635 in rat chronic mild stress model. Pharmacol Biochem Behav 72:465-474. (Pubitemid 34251360)
38. Payne AH, Sha LL. 1991. Multiple mechanisms for regulation of 3 beta-hydroxysteroid dehydrogenase/delta 5-delta 4-isomerase, 17 alpha-hydroxylase/C17-20 lyase cytochrome P450, and cholesterol side-chain cleavage cytochrome P450 messenger ribonucleic acid levels in primary cultures of mouse Leydig cells. Endocrinology 129:1429-1435.
39. Payne AH, Downing JR, Wong KL. 1980. Luteinizing hormone receptor and testosterone synthesis in two distinct populations of Leydig cells. Endocrinology 106:1424-1429. (Pubitemid 10094440)
40. Retana-Márquez S, Bonilla-Jaime H, Vázquez-Palacios G, Mart́?nez-Garć?a R, Velázquez-Moctezuma J. 2003. Changes in masculine sexual behavior, corticosterone and testosterone in response to acute and chronic stress in male rats. Horm Behav 44:327-337. (Pubitemid 37378212)
41. Sahin E, Gümüşlü S. 2007. Stress-dependent induction of protein oxidation, lipid peroxidation and anti-oxidants in peripheral tissues of rats: Comparison of three stress models (immobilization, cold and immobilization-cold). Clin Exp Pharmacol Physiol 34:425-431. (Pubitemid 46494466)
42. Samson J, Sheeladevi R, Ravindran R, Senthilvelan M. 2007. Stress response in rat brain after different durations of noise exposure. Neurosci Res 57:143-147. (Pubitemid 46073255)
43. Sriraman V, Rao VS, Sairam MR, Rao AJ. 2000. Effect of deprival of LH on Leydig cell roliferation: Involvement of PCNA, cyclin D3 and IGF-I. Mol Cell Endocrinol 162:113-120. (Pubitemid 30347454)
44. Srivastava RK, Taylor MF, Mann DR. 1993. Effect of immobilization stress on plasma luteinizing hormone, testosterone, and corticosterone concentrations and on 3 beta-hydroxysteroid dehydrogenase activity in the testes of adult rats. Proc Soc Exp Biol Med 204:231-235. (Pubitemid 23312821)
45. Vierhapper H, Nowotny P, Waldhausl W. 2000. Production rates of testosterone in patients with Cushing's syndrome. Metabolism 49:229-231. (Pubitemid 30090889)
46. Welsh TH, Jr, Bambino TH, Hsueh AJ:. 1982. Mechanism of glucocorticoid-induced suppression of testicular androgen biosynthesis in vitro. Biol Reprod 27(5):1138-1146. (Pubitemid 13174872)
47. Whirledge S, Cidlowski JA. 2010. Glucocorticoids, stress, and fertility. Minerva Endocrinol 35:109-125.
48. Willner P, Towell A, Sampson D, Sophokleous S, Muscat R. 1987. Reduction of sucrose reference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 93:358-364. (Pubitemid 17160661)
49. Willner P, Moreau JL, Nielsen CK, Papp M, Sluzewska A. 1996. Decreased hedonic responsiveness following chronic mild stress is not secondary to loss of body weight. Physiol Behav 60: 129-134. (Pubitemid 126335862)
50. Wright RL, Lightner EN, Harman JS, Meijer OC, Conrad CD. 2006. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur J Neurosci 24:595-605. (Pubitemid 44100351)