Ascorbic acid protects against cadmium-induced endoplasmic reticulum stress and germ cell apoptosis in testes

Reproductive Toxicology

Volumn 34, Issue 3, 2012, Pages 357-363

  Ji, Yan Li ^a   Wang, Zhen ^a   Wang, Hua ^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)

Author keywords

Apoptosis; Ascorbic acid; Cadmium; Endoplasmic reticulum stress; Testis

Indexed keywords

ASCORBIC ACID; CADMIUM CHLORIDE; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEME OXYGENASE 1; PROTEIN IRE1; PROTEIN IRE1 ALPHA; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 2 ALPHA; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GERM CELL; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TESTICULAR EDEMA; TESTIS; TESTIS INJURY; TESTIS WEIGHT; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; ASCORBIC ACID; CADMIUM; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; GERM CELLS; HEAT-SHOCK PROTEINS; HEME OXYGENASE-1; MALE; MAP KINASE KINASE 4; MEMBRANE PROTEINS; MICE; PROTEIN-SERINE-THREONINE KINASES; TESTIS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

MUS;

EID: 84865566570     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.04.011     Document Type: Article

References (53)

1. Honda R., Swaddiwudhipong W., Nishijo M., Mahasakpan P., Teeyakasem W., Ruangyuttikarn W., et al. Cadmium induced renal dysfunction among residents of rice farming area downstream from a zinc-mineralized belt in Thailand. Toxicology Letters 2010, 198:26-32.
2. Pant N., Upadhyay G., Pandey S., Mathur N., Saxena D.K., Srivastava S.P. Lead and cadmium concentration in the seminal plasma of men in the general population: correlation with sperm quality. Reproductive Toxicology 2003, 17:447-450.
3. Telisman S., Cvitkovic P., Jurasovic J., Pizent A., Gavella M., Rocic B. Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environmental Health Perspectives 2000, 108:45-53.
4. Xu B., Chia S.E., Tsakok M., Ong C.N. Trace elements in blood and seminal plasma and their relationship to sperm quality. Reproductive Toxicology 1993, 7:613-618.
5. Xu D.X., Shen H.M., Zhu Q.X., Chua L., Wang Q.N., Chia S.E., et al. The associations among semen quality, oxidative DNA damage in human spermatozoa and concentrations of cadmium, lead and selenium in seminal plasma. Mutation Research 2003, 534:155-163.
6. Wu H.M., Lin-Tan D.T., Wang M.L., Huang H.Y., Wang H.S., Soong Y.K., et al. Cadmium level in seminal plasma may affect the pregnancy rate for patients undergoing infertility evaluation and treatment. Reproductive Toxicology 2008, 25:481-484.
7. Siu E.R., Mruk D.D., Porto C.S., Cheng C.Y. Cadmium-induced testicular injury. Toxicology and Applied Pharmacology 2009, 238:240-249.
8. Niewenhuis R.J., Prozialeck W.C. Calmodulin inhibitors protect against cadmium-induced testicular damage in mice. Biology of Reproduction 1987, 37:127-133.
9. El-Ashmawy I.M., Youssef S.A. The antagonistic effect of chlorpromazine on cadmium toxicity. Toxicology and Applied Pharmacology 1999, 161:34-39.
10. Kim J., Soh J. Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicology Letters 2009, 188:45-51.
11. 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. Journal of Clinical Investigation 2002, 109:457-467.
12. Ferri K.F., Kroemer G. Organelle-specific initiation of cell death pathways. Nature Cell Biology 2001, 3:E255-E263.
13. Rao R.V., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death and Differentiation 2004, 11:372-380.
14. Rasheva V.I., Domingos P.M. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 2009, 14:996-1007.
15. Wek R.C., Cavener D.R. Translational control and the unfolded protein response. Antioxidants and Redox Signalling 2007, 9:2357-2371.
16. Kohno K. How transmembrane proteins sense endoplasmic reticulum stress. Antioxidants and Redox Signalling 2007, 9:2295-2303.
17. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology 2007, 8:519-529.
18. Kim R., Emi M., Tanabe K., Murakami S. Role of the unfolded protein response in cell death. Apoptosis 2006, 11:5-13.
19. Ji Y.L., Wang H., Meng C., Zhao X.F., Zhang C., Zhang Y., et al. Melatonin alleviates cadmium-induced cellular stress and germ cell apoptosis in testes. Journal of Pineal Research 2012, 52:71-79.
20. Ji Y.L., Wang H., Zhao X.F., Wang Q., Zhang C., Zhang Y., et al. Crosstalk between endoplasmic reticulum stress and mitochondrial pathway mediates cadmium-induced germ cell apoptosis in testes. Toxicological Sciences 2011, 124:446-459.
21. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword. Antioxidants and Redox Signalling 2007, 9:2277-2293.
22. Sen Gupta R., Sen Gupta E., Dhakal B.K., Thakur A.R., Ahnn J. Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Molecules and Cells 2004, 17:132-139.
23. Ardais A.P., Santos F.W., Nogueira C.W. Ebselen attenuates cadmium-induced testicular damage in mice. Journal of Applied Toxicology 2008, 28:322-328.
24. Acharya U.R., Mishra M., Patro J., Panda M.K. Effect of vitamins C and E on spermatogenesis in mice exposed to cadmium. Reproductive Toxicology 2008, 25:84-88.
25. Ola-Mudathir K.F., Suru S.M., Fafunso M.A., Obioha U.E., Faremi T.Y. Protective roles of onion and garlic extracts on cadmium-induced changes in sperm characteristics and testicular oxidative damage in rats. Food and Chemical Toxicology 2008, 46:3604-3611.
26. Ognjanovic B.I., Markovic S.D., Ethordevic N.Z., Trbojevic I.S., Stajn A.S., Saicic Z.S. Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q(10) and vitamin E. Reproductive Toxicology 2010, 29:191-197.
27. Malhotra J.D., Miao H., Zhang K., Wolfson A., Pennathur S., Pipe S.W., et al. Antioxidants reduce endoplasmic reticulum stress and improve protein secretion. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:18525-18530.
28. Chen Y.H., Xu D.X., Zhao L., Wang H., Wang J.P., Wei W. Ascorbic acid protects against lipopolysaccharide-induced intra-uterine fetal death and intra-uterine growth retardation in mice. Toxicology 2006, 217:39-45.
29. Latendresse J.R., Warbrittion A.R., Jonassen H., Creasy D.M. Fixation of testes and eyes using a modified Davidson's fluid: comparison with Bouin's fluid and conventional Davidson's fluid. Toxicologic Pathology 2002, 30:524-533.
30. Iwakoshi N.N., Lee A.H., Vallabhajosyula P., Otipoby K.L., Rajewsky K., Glimcher L.H. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nature Immunology 2003, 4:321-329.
31. Yokouchi M., Hiramatsu N., Hayakawa K., Kasai A., Takano Y., Yao J., et al. Atypical, bidirectional regulation of cadmium-induced apoptosis via distinct signaling of unfolded protein response. Cell Death and Differentiation 2007, 14:1467-1474.
32. Yokouchi M., Hiramatsu N., Hayakawa K., Okamura M., Du S., Kasai A., et al. Involvement of selective reactive oxygen species upstream of proapoptotic branches of unfolded protein response. Journal of Biological Chemistry 2008, 283:4252-4260.
33. Komoike Y., Inamura H., Matsuoka M. Effects of salubrinal on cadmium-induced apoptosis in HK-2 human renal proximal tubular cells. Archives of Toxicology 2012, 86:37-44.
34. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death and Differentiation 2004, 11:381-389.
35. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes and Development 1998, 12:982-995.
36. Oyadomari S., Koizumi A., Takeda K., Gotoh T., Akira S., Araki E., et al. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. Journal of Clinical Investigation 2002, 109:525-532.
37. Tajiri S., Oyadomari S., Yano S., Morioka M., Gotoh T., Hamada J.I., et al. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death and Differentiation 2004, 11:403-415.
38. Tsutsumi S., Gotoh T., Tomisato W., Mima S., Hoshino T., Hwang H.J., et al. Endoplasmic reticulum stress response is involved in nonsteroidal anti-inflammatory drug-induced apoptosis. Cell Death and Differentiation 2004, 11:1009-1016.
39. Lin J.H., Li H., Yasumura D., Cohen H.R., Zhang C., Panning B., et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 2007, 318:944-949.
40. Gotoh T., Terada K., Oyadomari S., Mori M. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death and Differentiation 2004, 11:390-402.
41. Puthalakath H., O'Reilly L.A., Gunn P., Lee L., Kelly P.N., Huntington N.D., et al. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129:1337-1349.
42. Yang W., Tiffany-Castiglioni E., Koh H.C., Son I.H. Paraquat activates the IRE1/ASK1/JNK cascade associated with apoptosis in human neuroblastoma SH-SY5Y cells. Toxicology Letters 2009, 191:203-210.
43. Kato H., Nakajima S., Saito Y., Takahashi S., Katoh R., Kitamura M. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death and Differentiation 2012, 19:310-320.
44. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
45. Nishitoh H., Matsuzawa A., Tobiume K., Saegusa K., Takeda K., Inoue K., et al. ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes and Development 2002, 16:1345-1355.
46. Luo D., He Y., Zhang H., Yu L., Chen H., Xu Z., et al. AIP1 is critical in transducing IRE1-mediated endoplasmic reticulum stress response. Journal of Biological Chemistry 2008, 283:11905-11912.
47. Ewing J.F., Maines M.D. 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.
48. Ahmed E.A., Omar H.M., Elghaffar S., Ragb S.M., Nasser A.Y. The antioxidant activity of vitamin C, DPPD and l-cysteine against Cisplatin-induced testicular oxidative damage in rats. Food and Chemical Toxicology 2011, 49:1115-1121.
49. Wang C., Zhang Y., Liang J., Shan G., Wang Y., Shi Q. Impacts of ascorbic acid and thiamine supplementation at different concentrations on lead toxicity in testis. Clinica Chimica Acta 2006, 370:82-88.
50. Lin A.M., Fang S.F., Chao P.L., Yang C.H. Melatonin attenuates arsenite-induced apoptosis in rat brain: involvement of mitochondrial and endoplasmic reticulum pathways and aggregation of alpha-synuclein. Journal of Pineal Research 2007, 43:163-171.
51. Chao P.L., Fan S.F., Chou Y.H., Lin A.M. N-Acetylcysteine attenuates arsenite-induced oxidative injury in dorsal root ganglion explants. Annals of the New York Academy of Sciences 2007, 1122:276-288.
52. Lin A.M., Feng S.F., Chao P.L., Yang C.H. Melatonin inhibits arsenite-induced peripheral neurotoxicity. Journal of Pineal Research 2009, 46:64-70.
53. Yazama F., Furuta K., Fujimoto M., Sonoda T., Shigetomi H., Horiuchi T., et al. Abnormal spermatogenesis in mice unable to synthesize ascorbic acid. Anatomical Science International 2006, 81:115-125.