Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes

Journal of Pineal Research

Volumn 52, Issue 1, 2012, Pages 71-79

  Ji, Yan Li ^a   Wang, Hua ^a   Meng, Can ^b   Zhao, Xian Feng ^a   Zhang, Cheng ^a   Zhang, Ying ^a   Zhao, Mei ^a   Chen, Yuan Hua ^a   Meng, Xiu Hong ^a   Xu, De Xiang ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

^b Anhui Provincial Center for Disease Control and Prevention   (China)

Author keywords

cadmium; endoplasmic reticulum stress; germ cell apoptosis; heat stress; melatonin; testis

Indexed keywords

CADMIUM CHLORIDE; CHAPERONE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEME OXYGENASE 1; INITIATION FACTOR 2ALPHA; INOSITOL; INOSITOL REQUIRING ENDOPLASMIC RETICULUM TO NUCLEUS SIGNAL KINASE 1; MELATONIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL STRESS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GERM CELL; MALE; MOUSE; NICK END LABELING; NITRATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TESTIS; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CADMIUM; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GERM CELLS; HEME OXYGENASE-1; HISTOCYTOCHEMISTRY; IN SITU NICK-END LABELING; MALE; MELATONIN; MICE; MICE, INBRED ICR; TESTIS; TRANSCRIPTION FACTORS;

EID: 83555173352     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00921.x     Document Type: Article

References (62)

1. Beveridge R, Pintos J, Parent ME, et al., Lung cancer risk associated with occupational exposure to nickel, chromium VI, and cadmium in two population-based case-control studies in Montreal. Am J Ind Med 2010; 53: 476-485.
2. Honda R, Swaddiwudhipong W, Nishijo M, et al., Cadmium induced renal dysfunction among residents of rice farming area downstream from a zinc-mineralized belt in Thailand. Toxicol Lett 2010; 198: 26-32.
3. Lafuente A, Cano P, Esquifino A,. Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent? Biometals 2003; 16: 243-250. (Pubitemid 36135456)
4. Lafuente A, Gonzalez-Carracedo A, Romero A, et al., Cadmium exposure differentially modifies the circadian patterns of norepinephrine at the median eminence and plasma LH, FSH and testosterone levels. Toxicol Lett 2004; 146: 175-182. (Pubitemid 37487831)
5. Laskey JW, Phelps PV,. Effect of cadmium and other metal cations on in vitro Leydig cell testosterone production. Toxicol Appl Pharmacol 1991; 108: 296-306.
6. Ji YL, Wang H, Liu P, et al., Pubertal cadmium exposure impairs testicular development and spermatogenesis via disrupting testicular testosterone synthesis in adult mice. Reprod Toxicol 2010; 29: 176-183.
7. Pant N, Upadhyay G, Pandey S, et al., Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reprod Toxicol 2003; 17: 447-450. (Pubitemid 36875185)
8. Xu DX, Shen HM, Zhu QX, et al., The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutat Res 2003; 534: 155-163.
9. Telisman S, Cvitkovic P, Jurasovic J, et al., Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ Health Perspect 2000; 108: 45-53. (Pubitemid 30064094)
10. Wu HM, Lin-Tan DT, Wang ML, et al., Cadmium level in seminal plasma may affect the pregnancy rate for patients undergoing infertility evaluation and treatment. Reprod Toxicol 2008; 25: 481-484.
11. Siu ER, Mruk DD, Porto CS, et al., Cadmium-induced testicular injury. Toxicol Appl Pharmacol 2009; 238: 240-249.
12. Ozawa N, Goda N, Makino N, et al., Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J Clin Invest 2002; 109: 457-467. (Pubitemid 34171776)
13. Kim J, Soh J,. Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicol Lett 2009; 188: 45-51.
14. Oteiza PI, Adonaylo VN, Keen CL,. Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake. Toxicology 1999; 137: 13-22. (Pubitemid 29421689)
15. Ates I, Suzen HS, Aydin A, et al., The oxidative DNA base damage in testes of rats after intraperitoneal cadmium injection. Biometals 2004; 17: 371-377. (Pubitemid 38870171)
16. Sen Gupta R, Sen Gupta E, Dhakal BK, et al., Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Mol Cells 2004; 17: 132-139. (Pubitemid 39137056)
17. Acharya UR, Mishra M, Patro J, et al., Effect of vitamins C and E on spermatogenesis in mice exposed to cadmium. Reprod Toxicol 2008; 25: 84-88. (Pubitemid 50009013)
18. Ognjanovic BI, Markovic SD, Ethordevic NZ, et al., Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q(10) and vitamin E. Reprod Toxicol 2010; 29: 191-197.
19. Tan DX, Chen LD, Poeggeler B, et al., Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
20. Tan DX, Manchester LC, Terron MP, et al., One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007; 42: 28-42. (Pubitemid 44924323)
21. Hardeland R, Tan DX, Reiter RJ,. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009; 47: 109-126.
22. Ressmeyer AR, Mayo JC, Zelosko V, et al., Antioxidant properties of the melatonin metabolite N1-acetyl-5-methoxykynuramine (AMK): scavenging of free radicals and prevention of protein destruction. Redox Rep 2003; 8: 205-213. (Pubitemid 37236233)
23. Schaefer M, Hardeland R,. The melatonin metabolite N-acetyl-5- methoxykynuramine is a potent singlet oxygen scavenger. J Pineal Res 2009; 46: 49-52.
24. Barlow-Walden LR, Reiter RJ, Abe M, et al., Melatonin stimulates brain glutathione peroxidase activity. Neurochem Int 1995; 26: 497-502.
25. Pablos MI, Agapito MT, Gutierrez R, et al., Melatonin stimulates the activity of the detoxifying enzyme glutathione peroxidase in several tissues of chicks. J Pineal Res 1995; 19: 111-115.
26. Rodriguez C, Mayo JC, Sainz RM, et al., Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9. (Pubitemid 38130283)
27. Tomas-Zapico C, Coto-Montes A,. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 2005; 39: 99-104. (Pubitemid 41140746)
28. Poliandri AH, Esquifino AI, Cano P, et al., In vivo protective effect of melatonin on cadmium-induced changes in redox balance and gene expression in rat hypothalamus and anterior pituitary. J Pineal Res 2006; 41: 238-246. (Pubitemid 44337719)
29. El-Sokkary GH, Nafady AA, Shabash EH,. Melatonin administration ameliorates cadmium-induced oxidative stress and morphological changes in the liver of rat. Ecotoxicol Environ Saf 2010; 73: 456-463.
30. Alonso-Gonzalez C, Gonzalez A, Mazarrasa O, et al., Melatonin prevents the estrogenic effects of sub-chronic administration of cadmium on mice mammary glands and uterus. J Pineal Res 2007; 42: 403-410. (Pubitemid 46581665)
31. Jang SS, Kim WD, Park WY,. Melatonin exerts differential actions on X-ray radiation-induced apoptosis in normal mice splenocytes and Jurkat leukemia cells. J Pineal Res 2009; 47: 147-155.
32. Tunon MJ, San Miguel B, Crespo I, et al., Melatonin attenuates apoptotic liver damage in fulminant hepatic failure induced by the rabbit hemorrhagic disease virus. J Pineal Res 2011; 50: 38-45.
33. Benoff S, Hauser R, Marmar JL, et al., Cadmium concentrations in blood and seminal plasma: correlations with sperm number and motility in three male populations (infertility patients, artificial insemination donors, and unselected volunteers). Mol Med 2009; 15: 248-262.
34. Benoff SH, Millan C, Hurley IR, et al., Bilateral increased apoptosis and bilateral accumulation of cadmium in infertile men with left varicocele. Hum Reprod 2004; 19: 616-627. (Pubitemid 38344526)
35. Angenard G, Muczynski V, Coffigny H, et al., Cadmium increases human fetal germ cell apoptosis. Environ Health Perspect 2010; 118: 331-337.
36. Feng Z, Zhang JT,. Melatonin reduces amyloid beta-induced apoptosis in pheochromocytoma (PC12) cells. J Pineal Res 2004; 37: 257-266. (Pubitemid 39457047)
37. Luchetti F, Canonico B, Curci R, et al., Melatonin prevents apoptosis induced by UV-B treatment in U937 cell line. J Pineal Res 2006; 40: 158-167.
38. Choi SI, Joo SS, Yoo YM,. Melatonin prevents nitric oxide-induced apoptosis by increasing the interaction between 14-3-3beta and p-Bad in SK-N-MC cells. J Pineal Res 2008; 44: 95-100.
39. Andrabi SA, Sayeed I, Siemen D, et al., Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 2004; 18: 869-871.
40. Jou MJ, Peng TI, Hsu LF, et al., Visualization of melatonin's multiple mitochondrial levels of protection against mitochondrial Ca(2+)-mediated permeability transition and beyond in rat brain astrocytes. J Pineal Res 2010; 48: 20-38.
41. Wang H, Xu DX, Lv JW, et al., Melatonin attenuates lipopolysaccharide (LPS)-induced apoptotic liver damage in d-galactosamine-sensitized mice. Toxicology 2007; 237: 49-57. (Pubitemid 47031404)
42. Li Z, Nickkholgh A, Yi X, et al., Melatonin protects kidney grafts from ischemia/reperfusion injury through inhibition of NF-kB and apoptosis after experimental kidney transplantation. J Pineal Res 2009; 46: 365-372.
43. Huang F, Ning H, Xin QQ, et al., Melatonin pretreatment attenuates 2-bromopropane-induced testicular toxicity in rats. Toxicology 2009; 256: 75-82.
44. Ron D, Walter P,. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529. (Pubitemid 46985379)
45. Shimizu Y, Hendershot LM,. Oxidative folding: cellular strategies for dealing with the resultant equimolar production of reactive oxygen species. Antioxid Redox Signal 2009; 11: 2317-2331.
46. Rutkowski DT, Hegde RS,. Regulation of basal cellular physiology by the homeostatic unfolded protein response. J Cell Biol 2010; 189: 783-794.
47. Di Sano F, Ferraro E, Tufi R, et al., Endoplasmic reticulum stress induces apoptosis by an apoptosome-dependent but caspase 12-independent mechanism. J Biol Chem 2006; 281: 2693-2700. (Pubitemid 43845732)
48. Lin JH, Li H, Yasumura D, et al., IRE1 signaling affects cell fate during the unfolded protein response. Science 2007; 318: 944-949. (Pubitemid 350098984)
49. Lisbona F, Rojas-Rivera D, Thielen P, et al., BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell 2009; 33: 679-691.
50. Gong Y, Wu J, Huang Y, et al., Nonylphenol induces apoptosis in rat testicular Sertoli cells via endoplasmic reticulum stress. Toxicol Lett 2009; 186: 84-95.
51. Wang H, Li L, Zhao M, et al., Melatonin alleviates lipopolysaccharide- induced placental cellular stress response in mice. J Pineal Res 2011; 50: 418-426.
52. Lin AM, Fang SF, Chao PL, et al., Melatonin attenuates arsenite-induced apoptosis in rat brain: involvement of mitochondrial and endoplasmic reticulum pathways and aggregation of alpha-synuclein. J Pineal Res 2007; 43: 163-171. (Pubitemid 47078924)
53. Lin AM, Feng SF, Chao PL, et al., Melatonin inhibits arsenite-induced peripheral neurotoxicity. J Pineal Res 2009; 46: 64-70.
54. Ewing JF, Maines MD,. Distribution of constitutive (HO-2) and heat-inducible (HO-1) heme oxygenase isozymes in rat testes: HO-2 displays stage-specific expression in germ cells. Endocrinology 1995; 136: 2294-2302.
55. Maines MD, Ewing JF,. Stress response of the rat testis: in situ hybridization and immunohistochemical analysis of heme oxygenase-1 (HSP32) induction by hyperthermia. Biol Reprod 1996; 54: 1070-1079. (Pubitemid 26127850)
56. Alam J, Cook JL,. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 2007; 36: 166-174. (Pubitemid 46233469)
57. Wang Z, Zhang J, Liu H, et al., Melatonin, a potent regulator of heme oxygenase-1, reduces cardiopulmonary bypass-induced renal damage in rats. J Pineal Res 2009; 46: 248-254.
58. Jung KH, Hong SW, Zheng HM, et al., Melatonin ameliorates cerulein-induced pancreatitis by the modulation of nuclear erythroid 2-related factor 2 and nuclear factor-kappaB in rats. J Pineal Res 2010; 48: 239-250.
59. Negi G, Kumar A, Sharma SS,. Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades. J Pineal Res 2011; 50: 124-131.
60. Kwon KJ, Kim JN, Kim MK, et al., Melatonin synergistically increases resveratrol-induced heme oxygenase-1 expression through the inhibition of ubiquitin-dependent proteasome pathway: a possible role in neuroprotection. J Pineal Res 2011; 50: 110-123.
61. Ryter SW, Choi AM,. Heme oxygenase-1: redox regulation of a stress protein in lung and cell culture models. Antioxid Redox Signal 2005; 7: 80-91. (Pubitemid 40187927)
62. Kireev RA, Tresguerres AC, Garcia C, et al., Melatonin is able to prevent the liver of old castrated female rats from oxidative and pro-inflammatory damage. J Pineal Res 2008; 45: 394-402.