Nickel(II) induced JNK activation-regulated mitochondria-dependent apoptotic pathway leading to cultured rat pancreatic β-cell death

Toxicology

Volumn 289, Issue 2-3, 2011, Pages 103-111

  Wu, Hsi Chin ^a   Yang, Ching Yao ^b,c   Hung, Dong Zong ^a   Su, Chin Chuan ^d   Chen, Kuo Liang ^a   Yen, Cheng Chieh ^e,f   Ho, Tsung Jung ^g   Su, Yi Chang ^g   Huang, Chun Fa ^g   Chen, Chun Hung ^a   Tsai, Ling Mei ^h   Chen, Ya Wen ^h  

^a CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^f CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^g CHINA MEDICAL UNIVERSITY   (Taiwan)

^h CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; C jun n terminal kinase (JNK); Mitochondrial dysfunction; Nickel (Ni); Pancreatic cells

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BETA ACTIN; CASPASE 3; CASPASE 7; CASPASE 9; CYTOCHROME C; DNA; LIPOCORTIN 5; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 11; NICKEL CHLORIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAK; PROTEIN BID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; LD 50; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; APOPTOSIS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; ENZYME ACTIVATION; ENZYME INDUCTION; INSULIN-SECRETING CELLS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NICKEL; RATS;

RATTUS;

EID: 80052753111     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2011.07.013     Document Type: Article

References (66)

1. Afridi H.I., Kazi T.G., Kazi N., Jamali M.K., Arain M.B., Jalbani N., Baig J.A., Sarfraz R.A. Evaluation of status of toxic metals in biological samples of diabetes mellitus patients. Diabetes Res. Clin. Pract. 2008, 80:280-288.
2. Agency for Toxic Substances and Disease Registry (ATSDR) Toxicological Profile for Nickel 2005, US Department of Health and Human Services, Atlanta, USA.
3. Ahamed M., Akhtar M.J., Siddiqui M.A., Ahmad J., Musarrat J., Al-Khedhairy A.A., AlSalhi M.S., Alrokayan S.A. Oxidative stress mediated apoptosis induced by nickel ferrite nanoparticles in cultured A549 cells. Toxicology 2011, 283:101-108.
4. Alloway B.J. Heavy Metal in Soils 1995, 25-34. Blackie Academic and Professional, London, UK. B.J. Alloway (Ed.).
5. Bhathena S.J., Awoke S., Voyles N.R., Wilkins S.D., Recant L., Oie H.K., Gazdar A.F. Insulin, glucagon, and somatostatin secretion by cultured rat islet cell tumor and its clones. Proc. Soc. Exp. Biol. Med. 1984, 175:35-38.
6. Bozec A., Chuzel F., Chater S., Paulin C., Bars R., Benahmed M., Mauduit C. The mitochondrial-dependent pathway is chronically affected in testicular germ cell death in adult rats exposed in utero to anti-androgens. J. Endocrinol. 2004, 183:79-90.
7. Bwititi P.T., Ashorobi R.B. Effects of chronic oral nickel chloride administration on glycaemia and renal function in normal and diabetic rats. Afr. J. Health Sci. 1998, 5:198-201.
8. Cai H.R., Cao M., Meng F.Q., Wei J.Y., Hou J. Giant cell interstitial pneumonia in a nickel metal hydride battery worker: a case report and literature review. Chin. Med. J. (Engl.) 2005, 118:1668-1672.
9. Cartana J., Arola L. Nickel-induced hyperglycaemia: the role of insulin and glucagon. Toxicology 1992, 71:181-192.
10. Chen C.Y., Lin T.K., Chang Y.C., Wang Y.F., Shyu H.W., Lin K.H., Chou M.C. Nickel(II)-induced oxidative stress, apoptosis, G2/M arrest, and genotoxicity in normal rat kidney cells. J. Toxicol. Environ. Health A 2010, 73:529-539.
11. Chen Y.W., Huang C.F., Yang C.Y., Yen C.C., Tsai K.S., Liu S.H. Inorganic mercury causes pancreatic beta-cell death via the oxidative stress-induced apoptotic and necrotic pathways. Toxicol. Appl. Pharmacol. 2010, 243:323-331.
12. Chen Y.W., Chen K.L., Chen C.H., Wu H.C., Su C.C., Wu C.C., Way T.D., Hung D.Z., Yen C.C., Yang Y.T., Lu T.H. Pyrrolidine dithiocarbamate (PDTC)/Cu complex induces lung epithelial cell apoptosis through mitochondria and ER-stress pathways. Toxicol. Lett. 2010, 199:333-340.
13. Chen Y.W., Yang C.Y., Huang C.F., Hung D.Z., Leung Y.M., Liu S.H. Heavy metals and islet function and diabetes development. Islets 2009, 1:1-8.
14. Chen Y.W., Huang C.F., Tsai K.S., Yang R.S., Yen C.C., Yang C.Y., Lin-Shiau S.Y., Liu S.H. Methylmercury induces pancreatic beta-cell apoptosis and dysfunction. Chem. Res. Toxicol. 2006, 19:1080-1085.
15. Cheon H., Cho J.M., Kim S., Baek S.H., Lee M.K., Kim K.W., Yu S.W., Solinas G., Kim S.S., Lee M.S. Role of JNK activation in pancreatic beta-cell death by streptozotocin. Mol. Cell. Endocrinol. 2010, 321:131-137.
16. Cortijo J., Milara J., Mata M., Donet E., Gavara N., Peel S.E., Hall I.P., Morcillo E.J. Nickel induces intracellular calcium mobilization and pathophysiological responses in human cultured airway epithelial cells. Chem. Biol. Interact. 2010, 183:25-33.
17. Cowan K.J., Storey K.B. Mitogen-activated protein kinases: new signaling pathways functioning in cellular responses to environmental stress. J. Exp. Biol. 2003, 206:1107-1115.
18. Chashschin V.P., Artunina G.P., Norseth T. Congenital defects, abortion and other health effects in nickel refinery workers. Sci, Total Environ. 1994, 148:287-291.
19. Daniel P.T., Schulze-Osthoff K., Belka C., Guner D. Guardians of cell death: the Bcl-2 family proteins. Essays Biochem. 2003, 39:73-88.
20. Das K.K., Das S.N., Dhundasi S.A. Nickel, its adverse health effects & oxidative stress. Indian J. Med. Res. 2008, 128:412-425.
21. Doreswamy K., Shrilatha B., Rajeshkumar T., Muralidhara Nickel-induced oxidative stress in testis of mice: evidence of DNA damage and genotoxic effects. J. Androl. 2004, 25:996-1003.
22. Druwe I.L., Vaillancourt R.R. Influence of arsenate and arsenite on signal transduction pathways: an update. Arch. Toxicol. 2010, 84:585-596.
23. Easton D.F. Nickel and Human Health: Current Perspectives 1992, 603-619. Wiley, New York. E. Nieboer, J.O. Nriagu (Eds.).
24. Ghiotto F., Fais F., Bruno S. BH3-only proteins: the death-puppeteer's wires. Cytometry A 2010, 77:11-12.
25. Godeny S., Borbely-Kiss I., Koltay E., Laszlo S., Szabo G. Determination of trace and bulk elements in plasma and erythrocytes of diabetic pregnant women by PIXE method. Int. J. Gynaecol. Obstet. 1986, 24:201-207.
26. Grandjean P. Human Exposure to Nickel 1984, IARC Sci. Publ., pp. 469-485.
27. Gupta S., Ahmad N., Husain M.M., Srivastava R.C. Involvement of nitric oxide in nickel-induced hyperglycemia in rats. Nitric Oxide 2000, 4:129-138.
28. Hayashi T., Faustman D.L. Role of defective apoptosis in type 1 diabetes and other autoimmune diseases. Recent. Prog. Horm. Res. 2003, 58:131-153.
29. Health Protection Agency (HPA) Nickel, Toxicological Overview 2009, HPA, UK.
30. Horak E., Sunderman F.W. Effects of Ni(II) upon plasma glucagon and glucose in rats. Toxicol. Appl. Pharmacol. 1975, 33:388-391.
31. Huang D.C., Strasser A. BH3-only proteins-essential initiators of apoptotic cell death. Cell 2000, 103:839-842.
32. Iglesias A.V., Burgos D.S., Marchetti P.N., Silva Z.C., Pino Z.P. Urinary nickel in children exposed to petcoke pollution. Rev, Med, Chil 2008, 136:1039-1046.
33. Igwilo I.O., Afonne O.J., Maduabuchi U.J., Orisakwe O.E. Toxicological study of the Anam River in Otuocha, Anambra State, Nigeria. Arch. Environ. Occup. Health 2006, 61:205-208.
34. Israili A.W. Occurrence of heavy metals in Ganga river and sediments. Indian J. Environ. Health 1992, 34:63-66.
35. Kang D., Hamasaki N. Alterations of mitochondrial DNA in common diseases and disease states: aging, neurodegeneration, heart failure, diabetes, and cancer. Curr. Med. Chem. 2005, 12:429-441.
36. Kasprzak K.S., Sunderman F.W., Salnikow K. Nickel carcinogenesis. Mutat. Res. 2003, 533:67-97.
37. Kim H., Rafiuddin-Shah M., Tu H.C., Jeffers J.R., Zambetti G.P., Hsieh J.J., Cheng E.H. Hierarchical regulation of mitochondrion-dependent apoptosis by BCL-2 subfamilies. Nat. Cell. Biol. 2006, 8:1348-1358.
38. Kim K., Lee S.H., Seo Y.R., Perkins S.N., Kasprzak K.S. Nickel(II)-induced apoptosis in murine T cell hybridoma cells is associated with increased fas ligand expression. Toxicol. Appl. Pharmacol. 2002, 185:41-47.
39. Kim J.Y., Huh K.H., Park Y.J., Fang Y., Kang C.M., Kim Y.S. Molecular mechanisms of cell death of mycophenolic acid-treated primary isolated rat islets: implication of mitogen-activated protein kinase activation. Transplant. Proc. 2008, 40:2575-2577.
40. Knopfel M., Schulthess G., Funk F., Hauser H. Characterization of an integral protein of the brush border membrane mediating the transport of divalent metal ions. Biophys. J. 2000, 79:874-884.
41. Kok K. Investigation into the distribution of chlorpromazine and 10-(3'-dimethylaminopropyl)-phenothiazine (RP 3276). Acta. Physiol. Pharmacol. Neerl. 1955, 4:388-394.
42. Kolachi, N.F., Kazi, T.G., Afridi, H.I., Kazi, N., Khan, S., Kandhro, G.A., Shah, A.Q., Baig, J.A., Wadhwa, S.K., Shah, F., Jamali, M.K., Arain, M.B. Status of toxic metals in biological samples of diabetic mothers and their neonates. Biol. Trace. Elem. Res., in press.
43. Kroemer G., Zamzami N., Susin S.A. Mitochondrial control of apoptosis. Immunol. Today 1997, 18:44-51.
44. Lee J.W., Kim W.H., Lim J.H., Song E.H., Song J., Choi K.Y., Jung M.H. Mitochondrial dysfunction: glucokinase downregulation lowers interaction of glucokinase with mitochondria, resulting in apoptosis of pancreatic beta-cells. Cell Signal. 2009, 21:69-78.
45. Li B.F., Liu Y.F., Cheng Y., Zhang J.L., Wang B.G. The effect of iNOS gene expression inhibited by RNA inference on the pancreas islet apoptosis and function in rats. Zhonghua Wai Ke Za Zhi 2009, 47:1406-1409.
46. Li Q., Suen T.C., Sun H., Arita A., Costa M. Nickel compounds induce apoptosis in human bronchial epithelial Beas-2B cells by activation of c-Myc through ERK pathway. Toxicol. Appl. Pharmacol. 2009, 235:191-198.
47. Little M.C., Gawkrodger D.J., MacNeil S. Chromium- and nickel-induced cytotoxicity in normal and transformed human keratinocytes: an investigation of pharmacological approaches to the prevention of Cr(VI)-induced cytotoxicity. Br. J. Dermatol. 1996, 134:199-207.
48. Lu T.H., Chen C.H., Lee M.J., Ho T.J., Leung Y.M., Hung D.Z., Yen C.C., He T.Y., Chen Y.W. Methylmercury chloride induces alveolar type II epithelial cell damage through an oxidative stress-related mitochondrial cell death pathway. Toxicol. Lett. 2010, 194:70-78.
49. Mas A., Alemany M., Arola L. Effects of a nickel load upon the concentration of plasma metabolites in pregnant rats. Gynecol. Obstet. Invest. 1986, 21:193-197.
50. M'Bemba-Meka P., Lemieux N., Chakrabarti S.K. Role of oxidative stress, mitochondrial membrane potential, and calcium homeostasis in human lymphocyte death induced by nickel carbonate hydroxide in vitro. Arch. Toxicol. 2006, 80:405-420.
51. Min H.Y., Kim M.S., Jang D.S., Park E.J., Seo E.K., Lee S.K. Suppression of lipopolysaccharide-stimulated inducible nitric oxide synthase (iNOS) expression by a novel humulene derivative in macrophage cells. Int. Immunopharmacol. 2009, 9:844-849.
52. Pearson G., Robinson F., Beers, Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 2001, 22:153-183.
53. Phillips J.I., Green F.Y., Davies J.C., Murray J. Pulmonary and systemic toxicity following exposure to nickel nanoparticles. Am. J. Ind. Med. 2010, 53:763-767.
54. Placzkiewicz-Jankowska E., Szybinski Z., Huszno B. Environmental factors in the development of type 1 diabetes-a new insight. Przegl. Lek. 2007, 64:175-179.
55. Raff M. Cell suicide for beginners. Nature 1998, 396:119-122.
56. Rendall R.E., Phillips J.I., Renton K.A. Death following exposure to fine particulate nickel from a metal arc process. Ann. Occup. Hyg. 1994, 38:921-930.
57. Serdar M.A., Bakir F., Hasimi A., Celik T., Akin O., Kenar L., Aykut O., Yildirimkaya M. Trace and toxic element patterns in nonsmoker patients with noninsulin-dependent diabetes mellitus, impaired glucose tolerance, and fasting glucose. Int. J. Diabetes Dev. Ctries. 2009, 29:35-40.
58. Shimizu S., Narita M., Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 1999, 399:483-487.
59. Sunderman F.W., Dingle B., Hopfer S.M., Swift T. Acute nickel toxicity in electroplating workers who accidently ingested a solution of nickel sulfate and nickel chloride. Am. J. Ind. Med. 1988, 14:257-266.
60. Thompson S.A. An overview of nickel-titanium alloys used in dentistry. Int. Endod. J. 2000, 33:297-310.
61. Trombetta D., Mondello M.R., Cimino F., Cristani M., Pergolizzi S., Saija A. Toxic effect of nickel in an in vitro model of human oral epithelium. Toxicol. Lett. 2005, 159:219-225.
62. Tsujimoto Y., Shimizu S. Bcl-2 family: life-or-death switch. FEBS Lett. 2000, 466:6-10.
63. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
64. Yen C.C., Lu F.J., Huang C.F., Chen W.K., Liu S.H., Lin-Shiau S.Y. The diabetogenic effects of the combination of humic acid and arsenic: in vitro and in vivo studies. Toxicol. Lett. 2007, 172:91-105.
65. Yuan H., Zhang X., Huang X., Lu Y., Tang W., Man Y., Wang S., Xi J., Li J. NADPH oxidase 2-derived reactive oxygen species mediate FFAs-induced dysfunction and apoptosis of beta-cells via JNK, p38 MAPK and p53 pathways. PLoS One 2010, 5:e15726-e15734.
66. Yusuf M., Fariduddin Q., Hayat S., Ahmad A. Nickel: an overview of uptake, essentiality and toxicity in plants. Bull. Environ. Contam. Toxicol. 2011, 86:1-17.