Chronic stress induces ageing-associated degeneration in rat Leydig cells

Asian Journal of Andrology

Volumn 14, Issue 4, 2012, Pages 643-648

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

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

Author keywords

Ageing; chronic stress; DNA damage; Leydig cells; reactive oxygen species

Indexed keywords

DNA; GLUCOCORTICOID; LIPOFUSCIN; REACTIVE OXYGEN METABOLITE; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN NORWAY RAT; CELL AGING; CELL DEGENERATION; CELL STRUCTURE; CHRONIC STRESS; CONTROLLED STUDY; DNA DAMAGE; HYPOTHESIS; LEYDIG CELL; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; TESTOSTERONE RELEASE;

AGING; ANIMALS; CELL COUNT; CORTICOSTERONE; DNA DAMAGE; LEYDIG CELLS; LIPOFUSCIN; MALE; ORGAN SIZE; RATS; RATS, INBRED BN; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL; TESTIS; TESTOSTERONE;

EID: 84863644516     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.1038/aja.2011.183     Document Type: Article

References (49)

1. Pare WP. The effect of chronic environmental stress on premature aging in the rat. J Gerontol 1965; 20: 78-84
2. Landfield PW, Eldridge JC. Evolving aspects of the glucocorticoid hypothesis of brain aging: hormonal modulation of neuronal calcium homeostasis. Neurobiol Aging 1994; 15: 579-88.
3. Sapolsky RM. The physiological relevance of glucocorticoid endangerment of the hippocampus. Ann NY Acad Sci 1994;13: 294-304; discussion 304-7.
4. Reagan LP, McEwen BS. Controversies surrounding glucocorticoid-mediated cell death in the hippocampus. J Chem Neuroanat 1997; 13: 149-67.
5. Maric D, Kostic T, Kovacevic R. Effects of acute and chronic immobilization stress on rat Leydig cell steroidogenesis. J Steroid Biochem Mol Biol 1996; 58: 351-5.
6. Harman SM, Metter EJ, Tobin JD, Pearson J, Blackman MR. Longitudinal effects of aging on serum total and free testosterone levels in healthy men. Baltimore Longitudinal Study of Aging. J Clin Endocrinol Metab 2001; 86: 724-31.
7. Matsumoto AM. Andropause: clinical implications of the decline in serum testosterone levels with aging in men. J Gerontol A Biol Sci Med Sci 2002; 57: M76-99.
8. Vermeulen A. Clinical review 24: androgens in the aging male. J Clin Endocrinol Metab 1991; 73: 221-4.
9. Hardy MP, Gao HB, Dong Q, Ge R, WangQet al. Stress hormone and male reproductive function. Cell Tissue Res 2005; 322: 147-53.
10. Brunk UT, Terman A. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur J Biochem 2002; 269: 1996-2002.
11. Ruffoli R, Carpi A, Giambelluca MA, Grasso L, Scavuzzo MC et al. Diazepam administration prevents testosterone decrease and lipofuscin accumulation in testis of mouse exposed to chronic noise stress. Andrologia 2006; 38: 159-65.
12. Beckman KB, Ames BN. The free radical theory of aging matures. Physiol Rev 1998; 78: 547-81.
13. Chen H, Cangello D, Benson S, Folmer J, Zhu H et al. Age-related increase in mitochondrial superoxide generation in the testosterone-producing cells of Brown Norway rat testes: relationship to reduced steroidogenic function? Exp Gerontol 2001; 36: 1361-73.
14. Cao L, Leers-Sucheta S, Azhar S. Aging alters the functional expression of enzymatic and non-enzymatic anti-oxidant defense systems in testicular rat Leydig cells. J Steroid Biochem Mol Biol 2004; 88: 61-7.
15. Garinis GA, van der Horst GT, Vijg J, Hoeijmakers JH. DNA damage and ageing: newage ideas for an age-old problem. Nat Cell Biol 2008; 10: 1241-7.
16. Chen JH, Hales CN, Ozanne SE. DNA damage, cellular senescence and organismal ageing: causal or correlative? Nucleic Acids Res 2007; 35: 7417-28.
17. Bertram C, Hass R. Cellular responses to reactive oxygen species-induced DNA damage and aging. Biol Chem 2008; 389: 211-20.
18. Seviour EG, Lin SY.The DNA damage response: balancing the scale between cancer and ageing. Aging (Albany NY) 2010; 2: 900-7.
19. Chen Y, Wang Q, Wang FF, Gao HB, Zhang P. Stress induces glucocorticoid-mediated apoptosis of rat Leydig cells in vivo. Stress 2012; 15: 74-84.
20. Gundersen HJ. Stereology of arbitrary particles. A review of unbiased number and size estimators and the presentation of some new ones, in memory of William R. Thompson. J Microsc 1986; 143: 3-45.
21. Wang C, Leung A, Sinha-Hikim AP. Reproductive aging in the male brown-Norway rat: a model for the human. Endocrinology 1993; 133: 2773-81.
22. Papanicolaou KN, Ngoh GA, Dabkowski ER, O'Connell KA, Ribeiro RF et al. Cardiomyocyte deletion of mitofusin-1 leads to mitochondrial fragmentation and improves tolerance to ROS-induced mitochondrial dysfunction and cell death. Am J Physiol Heart Circ Physiol 2012; 302: H167-79.
23. Wang Q, Gao HB. Involvement of nuclear factor-kappaB on corticosterone-induced rat Leydig cell apoptosis. Asian J Androl 2006; 8: 693-702.
24. Payne AH, Downing JR, Wong KL. Luteinizing hormone receptors and testosterone synthesis in two distinct populations of Leydig cells. Endocrinology 1980; 106: 1424-9.
25. Mahfouz RZ, du Plessis SS, Aziz N, Sharma R, Sabanegh E et al. Sperm viability, apoptosis, and intracellular reactive oxygen species levels in human spermatozoa before and after induction of oxidative stress. Fertil Steril 2010; 93: 814-21.
26. Munck A, Guyre PM, Holbrook NJ. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 1984; 5: 25-44.
27. Yates KE, Korbel GA, Shtutman M, Roninson IB, DiMaio D. Repression of the SUMOspecific protease Senp1 induces p53-dependent premature senescence in normal human fibroblasts. Aging Cell 2008; 7: 609-21.
28. Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M et al. DNA repair, genome stability, and aging. Cell 2005; 120: 497-512.
29. Gruz P, Shimizu M. Origins of age-related DNA damage and dietary strategies for its reduction. Rejuvenation Res 2010; 13: 285-7.
30. Herbert KE, Mistry Y, Hastings R, Poolman T, Niklason L et al. Angiotensin IImediated oxidative DNA damage accelerates cellular senescence in cultured human vascular smooth muscle cells via telomere-dependent and independent pathways. Circ Res 2008; 102: 201-8.
31. Inturi S, Tewari-Singh N, Gu M, Shrotriya S, Gomez J et al. Mechanisms of sulfur mustard analog 2-chloroethyl ethyl sulfide-induced DNA damage in skin epidermal cells and fibroblasts. Free Radic Biol Med 2011; 51: 2272-80.
32. Chen J, Patschan S, Goligorsky MS. Stress-induced premature senescence of endothelial cells. J Nephrol 2008; 21: 337-44.
33. Landfield PW, Eldridge JC. Evolving aspects of the glucocorticoid hypothesis of brain aging: hormonal modulation of neuronal calcium homeostasis. Neurobiol Aging 1994; 15: 579-88.
34. Zirkin BR, Santulli R, Strandberg JD, Wright WW, Ewing LL. Testicular steroidogenesis in the aging Brown Norway rat. J Androl 1993; 14: 118-23.
35. Chen H, Hardy MP, Huhtaniemi I, Zirkin BR. Age-related decreased Leydig cell testosterone production in the Brown Norway rat. J Androl 1994; 15: 551-7.
36. Kostic TS, Stojkov NJ, Janjic MM, Maric D, Andric SA. The adaptive response of adult rat Leydig cells to repeated immobilization stress: the role of protein kinase A and steroidogenic acute regulatory protein. Stress 2008; 11: 370-80.
37. Dimri GP, Lee X, Basile G, Acosta M, Scott G et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995; 92: 9363-7.
38. Kang HT, Lee KB, Kim SY, Choi HR, Park SC. Autophagy impairment induces premature senescence in primary human fibroblasts. PLoS ONE 2011; 6: e23367.
39. McClearn GE. Biogerontologic theories. Exp Gerontol 1997; 32: 3-10.
40. Collado M, Blasco MA, Serrano M. Cellular senescence in cancer and aging. Cell 2007; 130:22333.
41. Russell LD, de Franca LR, Hess R, Cooke P. Characteristics of mitotic cells in developing and adult testes with observations on cell lineages. Tissue Cell 1995; 27: 105-28.
42. Quinn PG, Payne AH. Oxygen-mediated damage of microsomal cytochrome P-450 enzymes in cultured Leydig cells. Role in steroidogenic desensitization. J Biol Chem 1984; 259: 4130-5.
43. Hanukoglu I. Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metab Rev 2006; 38: 171-96.
44. Spiteller G. Lipid peroxidation in aging and age-dependent diseases. Exp Gerontol 2001; 36: 1425-57.
45. Wang XJ, Dyson MT, Jo Y, Eubank DW, Stocco DM. Involvement of 5-lipoxygenase metabolites of arachidonic acid in cyclic AMP-stimulated steroidogenesis and steroidogenic acute regulatory protein gene expression. J Steroid Biochem Mol Biol 2003; 85: 159-66.
46. Chen H, Zirkin BR. Long-term suppression of Leydig cell steroidogenesis prevents Leydig cell aging. Proc Natl Acad Sci USA 1999; 96: 14877-81.
47. Hwang TI, Liao TL, Lin JF, Lin YC, Lee SY et al. Low-dose testosterone treatment decreases oxidative damage in TM3 Leydig cells. Asian J Androl 2011; 13: 432-7.
48. Lee SY, Gong EY, Hong CY, Kim KH, Han JS et al. ROS inhibit the expression of testicular steroidogenic enzyme genes via the suppression of Nur77 transactivation. Free Radic Biol Med 2009; 47: 1591-600.
49. Yared E,McMillan TJ,Martin FL. Genotoxic effects of oestrogens in breast cells detected by the micronucleus assay and the Comet assay. Mutagenesis 2002; 17: 345-52.