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Carcinogenic effect of nickel compounds

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Abstract

Nickel is a widely distributed metal that is industrially applied in many forms. Accumulated epidemiological evidence confirms that exposures to nickel compounds are associated with increased nasal and lung cancer incidence, both in mostly occupational exposures. Although the molecular mechanisms by which nickel compounds cause cancer are still under intense investigation, the carcinogenic actions of nickel compounds are thought to involve oxidative stress, genomic DNA damage, epigenetic effects, and the regulation of gene expression by activation of certain transcription factors related to corresponding signal transduction pathways. The present review summarizes our current knowledge on the molecular mechanisms of nickel carcinogenesis, with special emphasis on the role of nickel induced reactive oxygen species (ROS) and signal transduction pathways.

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References

  1. International Agency for Research on Cancer: IARC monographs on the Evaluation of Carcinogenic Risks to Human, Vol 49, Chromium, Nickel and Welding, IARC Scientific Publications, Lyon, 1990, pp 1–648, 677–691

  2. Costa M: Mechanisms of nickel genotoxicity and carcinogenicity. In: L.W. Chang, L. Magos, T. Suzuki (eds). Toxicology of Metals, Lewis Publishers, New York, 1996, pp 245–251

  3. Denkhaus E, Salnikow K: Nickel essentiality, toxicity and carcinogenicity of nickel compounds. Crit Rev Oncol Hematol 42: 35–56, 2002

    PubMed  Google Scholar 

  4. Doll R: Reports of the International Committee on Nickel Carcinogenesis in Man. Scand J Work Environ Health 16: 9–82, 1990

    Google Scholar 

  5. Grimsrud TK, Berge SR, Martinsen JI, Andersen A: Lung cancer incidence among Norwegian nickel-refinery workers. J Environ Monit 5: 190–197, 2003

    Article  PubMed  Google Scholar 

  6. Kasprzak KS, Sunderman FW Jr, Salnikow K: Nickel carcinogenesis. Mutat Res 533: 67–97, 2003

    PubMed  Google Scholar 

  7. Salnikow K, An WG, Melillo G, Blagosklonny MV, Costa M: Nickel-induced transformation shifts the balance between HIF-1 and p53 transcription factors. Carcinogenesis 20: 1819–1823, 1999

    PubMed  Google Scholar 

  8. Lee SH, Shiao YH, Plisov SY, Kasprzak KS: Nickel(II) acetate-treated Chinese hamster ovary cells differentially express Vimentin, hsNF2H homologue, and H ferritin. Biochem Biophys Res Commun 258(3): 592–595, 1999

    Article  PubMed  Google Scholar 

  9. Zhong ZJ, Troll W, Koenig KL, Frenkel K: Carcinogenic sulfide salts of nickel and cadmium induce H2O2 formation by human polymorphonuclear leukocytes. Cancer Res 50(23): 7564–7570, 1990

    PubMed  Google Scholar 

  10. Knight JA, Plowman MR, Hopfer SM, Sunderman FW Jr: Pathological reactions in lung, liver, thymus, and spleen of rats after subacute parenteral administration of nickel sulfate. Annu Clin Lab Sci 21(4): 275–283, 1991

    Google Scholar 

  11. Salnikow K, Costa M: Epigenetic mechanisms of nickel carcinogenesis. J Environ Pathol Toxicol Oncol 19(3): 307–318, 2000

    PubMed  Google Scholar 

  12. Fletcher GG, Rosetto FE, Turnbull JD, Nieboer E: Toxicity, uptake, and mutagenicity of particulate and soluble nickel compounds. Environ Health Perspect 102(suppl 3): 69–79, 1994

    Google Scholar 

  13. Biggart NW, Costa M: Assessment of the uptake and mutagenicity of nickel chloride in Salmonella tester strains. Mutat Res 175: 209–215, 1986

    Article  PubMed  Google Scholar 

  14. Kargacin B, Klein CB, Costa M: Mutagenic responses of nickel oxides and nickel sulfides in Chinese hamster V79 cell lines as the xanthine-guanine phosphoribosyl transferase locus. Mutat Res 300: 63–72, 1993

    Article  PubMed  Google Scholar 

  15. Lee YW, Klein CB, Kargacin B, Salnikow K, Kitahara J, Dowjat K, Zhitkovich A, Christie NT, Costa M: Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: A new model for epigenetic carcinogens. Mol Cell Biol 15(5): 2547–2557, 1995

    PubMed  Google Scholar 

  16. Mayer C, Klein RG, Wesch H, Schmezer P: Nickel sulfide is genotoxic in vitro but shows no mutagenic potential in respiratory tract tissues of BigBlue rats and Muta Mouse mice in vivo after inhalation. Mutat Res 420: 85–98, 1998

    Google Scholar 

  17. Sutherland JE, Costa M: Epigenetics and the environment. Ann N Y Acad Sci 983: 151–160, 2003

    PubMed  Google Scholar 

  18. Huang Y, Davidson G, Li J, Yan Y, Chen F, Costa M, Chen LC, Huang C: Activation of nuclear factor-kappaB and not activator protein-1 in cellular response to nickel compounds. Environ Health Perspect 110(suppl 5): 835–839, 2002

    Google Scholar 

  19. Sunderman FW Jr., Oskarsson A: Nickel. In: E. Merian (ed). Metals and Their Compounds in the Environment: Occurrence, Analysis and Biological Relevance. VCH, Weinheim, 1991, pp 1101–1126

  20. Merian E: Introduction on environmental chemistry and global cycles of chromium, nickel, cobalt, beryllium, arsenic, cadmium, and selenium, and their derivatives. Toxicol Environ Chem 8: 9–38, 1984

    Google Scholar 

  21. Garrett RG: Natural sources of metals to the environment. In: J.A. Centeno, P. Collery, G. Fernet, R.B. Finkelman, H. Gibb, J.-C. Etienne (eds). Metal Ions in Biology and Medicine, Vol 6, John Libbey Eurotext, Paris, 2000, pp 508–510

  22. Oller R, Costa M, Oberdorster G: Caricinogenicity assessment of selected nickel compounds. Toxicol Appl Pharmacol 143(1): 152–166, 1997

    Article  PubMed  Google Scholar 

  23. Salnikow K, Wang S, Costa M: Induction of activating transcription factor 1 by nickel and its role as a negative regulator of thrombospondin I gene expression. Cancer Res 57: 5060–5066, 1997

    PubMed  Google Scholar 

  24. Kollmeier H, Seemann JW, Muller KM, Rothe G, Witting P, Schejbal VB: Increased chromium and nickel content in lung tissue and bronchial carcinoma. Am J Ind Med 11(6): 659–669, 1987

    PubMed  Google Scholar 

  25. Edelman DA, Roggli VL: The accumulation of nickel in human lungs. Environ Health Perspect 81: 221–224, 1989

    PubMed  Google Scholar 

  26. Nielson FH: Nickel. In: W. Mertz (ed). Trace Elements in Human and Animal Nutrition, Vol 1, 5th edn., Academic Press, San Diego, 1987, pp 245–273

  27. Tjalve H, Jasim S, Oskarsson A: Nickel mobilization by sodium diethyldithiocarbamate in nickel-carbonyl treated mice. In: F.W. Sunderman Jr (ed). Nickel in the Human Environment, IARC Scientific Press, Oxford, 1984, pp 311–320

  28. Boscolo P, Sabbioni E, Andreassi P, di Giacomo F, Giaccio M, di Giocchino M: Immune parameters and blood and urine trace elements in nonallergic and nickel-sensitised humans. In: P. Collery, P. Brätter, V. Negretti de Brätter, L. Khassanova, J.-C. Etienne (eds). Metal Ions in Biology and Medicine, Vol 5, John Libbey Eurotext, Paris, 1998, pp~545–555

  29. Sunderman FW Jr, Selin CE: The metabolism of nickel carbonyl. Toxicol Appl Pharmacol 36: 326–335, 1968

    Google Scholar 

  30. Oskarsson A, Tjalve H: Binding of 63Ni by cellular constituents in some tissues of mice after the administration of 63NiCl2 and 63Ni(CO)4. Acta Pharmacol Toxicol (Copenhagen) 45(4): 306–314, 1979

    Google Scholar 

  31. Osakarsson A, Tjalve H: An autoradiographic study on the distribution of 63Ni in mice. Ann Clin Lab Sci 9(1): 47–59, 1979

    PubMed  Google Scholar 

  32. Herlant-Peers MC, Hildebrand HF, Kerckaert J-P: In vitro and in vivo incorporation of 63Ni(II) into lung and liver subcallular fractions of Balb/C mice. Carcinogenesis 4: 387–392, 1983

    PubMed  Google Scholar 

  33. Calnan CD: Nickel dermatitis. Br J Dermatol Clin 68: 229–236, 1956

    Google Scholar 

  34. Marcussen PV: Spread of nickel dermatitis. Dermatologica 115: 596–607, 1957

    PubMed  Google Scholar 

  35. Peltonen L: Nickel sensitivity in the general population. Contact Dermatitis 5: 27–32, 1979

    PubMed  Google Scholar 

  36. Costa M, Abbracchio MP, Simmons-Hansen J: Factors influencing the phagocytosis, neoplastic transformation, and cytotoxicity of particulate nickel compounds in tissue culture systems. Toxicol Appl Pharmacol 60: 313–323, 1981

    Article  PubMed  Google Scholar 

  37. Costa M, Mollenhauer HH: Carcinogenic activity of particulate nickel compounds is proportional to their cellular uptake. Science 209: 515–517, 1980

    PubMed  Google Scholar 

  38. Conway K, Costa M: Nonrandom chromosomal alterations in nickel-transformed Chinese hamster embryo cells. Cancer Res 49: 6032–6038, 1989

    PubMed  Google Scholar 

  39. Costa M: Molecular mechanisms of nickel carcinogenesis. Ann Rev Pharmacol Toxicol 31: 321–337, 1991

    Article  Google Scholar 

  40. Tallkvist J, Wing AM, Tjalve H: Enhanced intestinal nickel absorption in iron-deficient rats. Pharmacol Toxicol 75: 244–249, 1994

    PubMed  Google Scholar 

  41. Schafer SG, Forth W: The influence of tin, nickel, and cadmium on the intestinal absorption of iron. Ecotoxicol Environ Safety 7: 87–95, 1983

    Article  PubMed  Google Scholar 

  42. Muller-Fassbender M, Elsenhans B, McKie AT, Schumann K: Different behaviour of 63Ni and 59Fe during absorption in iron-deficient and iron-adequate jejunal rat segments ex vivo. Toxicology 185: 141–153, 2003

    Article  PubMed  Google Scholar 

  43. Oskarsson A, Andersson Y, Tjalve H: Fate of nickel subsulfide during carcinogenesis studied by autoradiography and X-ray powder diffraction. Cancer Res 39: 4175–4182, 1979

    PubMed  Google Scholar 

  44. Kasprzak KS, Sunderman FW Jr: Mechanisms of dissolution of nickel subsulfide in rats serum. Res Commun Chem Pathol Pharmacol 16: 95–108, 1977

    PubMed  Google Scholar 

  45. Kuehn K, Sunderman FW Jr: Dissolution half-times of nickel compounds in water, rat serum and renal cytosol. J Inorg Biochem 17: 29–39, 1982

    Article  PubMed  Google Scholar 

  46. Leach CN Jr, Linden JV, Hopfer SM, Crisostomo MC, Sunderman FW Jr: Nickel concentrations in serum of patients with acute mycardinal infarction or unstable angina pectoris. Clin Chem 31: 556–560, 1985

    PubMed  Google Scholar 

  47. National Research Council: Medical and biological effects of environmental pollutants. Nickel. Committee on Medical and Biological Effects of Environmental Pollutants, National Academy of Sciences, Washington, DC, 1975

  48. Szathmary SC, Daldrup T: Determination of nickel by GC, GC-MS, and AAS in biological materials in a case of lethal poisoning. Fresenius J Anal Chem 313: 48–52, 1982

    Article  Google Scholar 

  49. Sunderman FW, Kincaid JF: Nickel poisoning: II. Studies on patients suffering from acute exposure to vapors of nickel carbonyl. JAMA 155: 889–894, 1954

    Google Scholar 

  50. Zhicheng S: Nickel carbonyl: Toxicity and human health. Sci Total Environ 148: 293–298, 1994

    Article  PubMed  Google Scholar 

  51. Shi Z: Acute nickel carbonyl poisoning: A report of 179 cases. Br J Ind Med 43: 422–424, 1986

    PubMed  Google Scholar 

  52. Massone L, Anonide A, Borghi S, Isola V: Positive patch test reactions to nickel, cobalt and potassium dichromate in a series of 576 patients. Cutis 47: 119–122, 1991

    PubMed  Google Scholar 

  53. Gawkrodger DJ, Lewis FW, Shah M: Contact sensitivity to nickel and other metals in jewelry reactors. J Am Acad Dermatol 43: 31–36, 2000

    Article  PubMed  Google Scholar 

  54. Meyer JD, Chen Y, Holt DL, Beck MH, Cherry NM: Occupational contact dermatitis in the UK: a surveillance report from EPIDERM and OPRA. Occup Med (Lond) 50: 265–273, 2000

    Google Scholar 

  55. Antico A, Soana R: Chronic allergic-like dermatopathies in nickel-sensitive patients: Results of dietary restrictions and challenge with nickel salts. Allergy Asthma Proc 20: 235–242, 1999

    PubMed  Google Scholar 

  56. Vyskocil A, Senft V, Viau C, Cizkova M, Kohout J: Biochemical renal changes in workers exposed to soluble nickel compounds. Hum Exp Toxicol 13: 257–261, 1994

    PubMed  Google Scholar 

  57. Vyskocil A, Viau C, Cizkova M: Chronic nephrotoxicity of soluble nickel in rats. Hum Exp Toxicol 13: 689–693, 1994

    PubMed  Google Scholar 

  58. Wing AJ, Brunner FP, Geerlings W, Broyer M: Contribution of toxic nephropathies to end-stage renal failure in Europe: a report from the EDTA-ERA registry. Toxicol Lett 46: 281–292, 1989

    Article  PubMed  Google Scholar 

  59. Boysen M, Solberg LA, Andersen I, Hogetveit AC, Torjussen W: Nasal histology and nickel concentrations in plasma and urine after improvements in working environment at a nickel refinery in Norway. Scand J Work Environ Health 8: 283–289, 1982

    PubMed  Google Scholar 

  60. Malo J-L, Cartier A, Doepner M: Occupational asthma caused by nickel sulfate. J Allergy Clin Immunol 69: 55–59, 1982

    Article  PubMed  Google Scholar 

  61. Dolovich J, Evans SL, Nieboer E: Occuaptional asthma from nickel sensitivity: I. Human serum albumin in the antigenic determinant. Br J Ind Med 41: 51–55, 1984

    PubMed  Google Scholar 

  62. Magnus K, Andersen A, Hogetveit AC: Cancer of respiratory organs among workers at a nickel refinery in Norway. Int J Cancer 30(6): 681–685, 1982

    PubMed  Google Scholar 

  63. Roberts RS, Julian JA, Muir DC, Shannon HS: Cancer mortality associated with the high-temperature oxidation of nickel subsulfide. IARC Sci Publ 53: 23–35, 1984

    PubMed  Google Scholar 

  64. Seilkop SK, Oller AR: Reparatory cancer risks associated with low-level nickel exposure: an integrated assessment based on animal, epidermiological, and mechanistic data. Regulat Toxicol Pharmacol 37: 173–190, 2003

    Article  Google Scholar 

  65. Shirali P, Decaestecker AM, Marez T, Hildebrand HF, Bailly C, Martinez R: Ni3S2 uptake by lung cells and its interaction with plasma membranes. J Appl Toxicol 11(4): 279–288, 1991

    PubMed  Google Scholar 

  66. Tveito G, Hansteen IL, Dalen H, Haugen A: Immortalization of normal human kidney epithelial cells by nickel(II). Cancer Res 49(7): 1829–1835, 1989

    PubMed  Google Scholar 

  67. Costa M, Simmons-Hansen J, Bedrossian CW, Bonura J, Caprioli RM: Phagocytosis, cellular distribution, and carcinogenic activity of particulate nickel compounds in tissue culture. Cancer Res 41: 2868–2876, 1981

    PubMed  Google Scholar 

  68. Costa M, Heck JD, Robison SH: Selective phagocytosis of crystalline metal sulfide particles and DNA strand breaks as a mechanism for the induction of cellular transformation. Cancer Res 42: 2757–2763, 1982

    PubMed  Google Scholar 

  69. Evans RM, Davies PJ, Costa M: Video time-lapse microscopy of phagocytosis and intracellular fate of crystalline nickel particles in cultured mammalian cells. Cancer Res 42: 2729–2735, 1982

    PubMed  Google Scholar 

  70. Rivedal E, Sanner T: Metal salts as promoters of in vitro morphological transformation of hamster embryo cells initiated by benzo[a]pyrene. Cancer Res 41: 2950–2953, 1981

    PubMed  Google Scholar 

  71. Miki H, Kasprzak KS, Kenney S, Heine UI: Inhibition of intercellular communication by nickel(II): antagonistic effect of magnesium. Carcinogenesis 8: 1757–1760, 1987

    PubMed  Google Scholar 

  72. Shimkin MB, Stoner GD, Theiss JC: Lung tumor response in mice to metals and metal salts. Adv Exp Med Biol 91: 85–91, 1977

    PubMed  Google Scholar 

  73. Stoner GD, Shimkin MB, Troxell MC, Thompson TL, Terry LS: Test for carcinogenicity of metallic compounds by the pulmonary tumor response in strain A mice. Cancer Res 36(5): 1744–1747, 1976

    PubMed  Google Scholar 

  74. Lau TJ, Hackett RL, Sunderman FW Jr: The carcinogenicity of intravenous nickel carbonyl in rats. Cancer Res 32(10): 2253–2258, 1972

    PubMed  Google Scholar 

  75. Pott F, Ziem U, Reiffer FJ, Huth F, Ernst H, Mohr U: Carcinogenicity studies on fibres, metal compounds, and some other dusts in rats. Exp Pathol 32(3): 129–152, 1987

    PubMed  Google Scholar 

  76. Hueper WC: Expewrimental studies in metal carcinogenesis: IX. Cancer produced by parenterally introduced metallic nickel. J Natl Cancer Inst 16: 55–67, 1955

    PubMed  Google Scholar 

  77. Horie A, Haratake J, Kodama Y, Tsuchiya K: Electron microscopical findings with special reference to cancer in rats caused by inhalation of nickel oxide. Biol Trace Elem Res 7: 223–239, 1985

    Google Scholar 

  78. Snow ET: Metal carcinogenesis: mechanistic implications. Pharmacol Ther 53(1): 31–65, 1992

    Article  PubMed  Google Scholar 

  79. Sen P, Costa M: Incidence and localization of sister chromatid exchanges induced by nickel and chromium compounds. Cancer Res 7: 1527–1533, 1985

    Google Scholar 

  80. Sahu RK, Katsifis SP, Kinney PL, Christie NT: Effects of nickel sulfate, lead sulfate, and sodium arsenite alone and with UV light on sister chromatid exchanges in cultured human lymphocytes. J Mol Toxicol 2: 129–136, 1989

    Google Scholar 

  81. Rosetto FE, Turnbull JD, Nieboer E: Characterization of nickel-induced mutations. Sci Total Environ 148: 201–206, 1994

    Article  PubMed  Google Scholar 

  82. Zienolddiny S, Ryberg D, Haugen A: Induction of microsatellite mutations by oxidative agents in human lung cancer cell lines. Carcinogenesis 21(8): 1521–1526, 2000

    Article  PubMed  Google Scholar 

  83. Chiocca SM, Sterner DA, Biggart NW, Murphy EC Jr: Nickel carcinogenesis: alteration of the MusVts110 thermosensitive splicing phenotype by a nickel-induced duplication of the 3′ splice site. Mol Carcinog 4: 61–71, 1991

    PubMed  Google Scholar 

  84. Higinbotham KG, Rice JM, Diwan BA, Kasprzak KS, Reed CD, Perantoni AO: GGT to GTT transversions in codon 12 of the K-ras oncogene in rat renal sarcomas induced with nickel subsulfide or nickel subsulfide/iron are consistent with oxidative damage to DNA. Cancer Res (52): 4747–4751

  85. Harty LC, Guinee DG Jr, Travis WD, Bennett WP, Jett J, Coby TV, Tazelaar H, Trastek V, Pairolero P, Liotta LA, Harris CC, Caporaso NE: p53 mutations and occupational exposures in a surgical series of lung cancers. Cancer Epidemiol Biomark Prev 5: 996–1003, 1996

    Google Scholar 

  86. Dubins JS, LaVelle JM: Nickel(II) genotoxicity: potentiation of mutagenesis of simple alkylating agents. Mutat Res 162: 187–199, 1986

    PubMed  Google Scholar 

  87. Christie NT, Tummolo DM, Klein CB, Rossman TG: Role of Ni(II) in mutation. In: E. Nieboer, J.O. Nriagu (eds). Nickel and Human Health: Current Perspectives, Wiley, New York, 1992, pp 305–317

  88. Trott DA, Cuthbert AP, Overell RW, Russo I, Newbold RF: Mechanisms involved in the immortalization of mammalian cells by ionizing radiation and chemical carcinogens. Carcinogenesis 16(2): 193–204, 1995

    PubMed  Google Scholar 

  89. Pennisi E: Behind the scenes of gene expression. Science 293: 1064–1067, 2001

    Article  PubMed  Google Scholar 

  90. Klein CB, Conway K, Wang XW, Bhamra RK, Lin XH, Cohen MD, Annab L, Barrett JC, Costa M: Senescence of nickel-transformed cells by an X chromosome possible epigenetic control. Science 251: 796–799, 1991

    PubMed  Google Scholar 

  91. Klein CB, Rossman TG: Transgenic Chinese hamster V79 cell lines which exhibit variable levels of gpt mutagenesis. Environ Mol Mutagen 16: 1–12, 1990

    Google Scholar 

  92. Klein CB, Snow ET: Localization of the gpt sequence in transgenic G12 cells by fluorescent in~situ hybridization. Environ Mol Mutagen 21: 35, 1993

    Google Scholar 

  93. Klein CB, Kargacin B, Su L, Cosentino S, Snow ET, Costa M: Metal mutagenesis in transgenic Chinese hamster cell lines. Environ Health Perspect 102(suppl 3): 63–67, 1994

    Google Scholar 

  94. Lee YW, Pons C, Tummolo DM, Klein CB, Rossman TG, Christie NT: Mutagenicity of soluble and insoluble nickel compounds at the gpt locus in G12 Chinese hamster cells. Environ Mol Mutagen 21: 365–371, 1993

    PubMed  Google Scholar 

  95. Ottolenghi AD, Haseman JK, Payne WW, Falk HL, MacFarland HN: Inhalation studies of nickel sulfide in pulmonary carcinogenesis of rats. J Natl Cancer Inst 54: 1165–1172, 1975

    PubMed  Google Scholar 

  96. Dunnick JK, Elwell MR, Radovsky AE, Benson JM, Hahn FF, Nikula KJ, Barr EB, Hobbs CH: Comparative carcinogenic effects of nickel subsulfide, nickel oxide, or nickel sulfate hexahydrate chronic exposures in the lung. Cancer Res 55: 5251–5256, 1955

    Google Scholar 

  97. Sunderman FW Jr, Hopfer SM, Reid MC, Shen SK, Kevorkian CB: Erythropoietin-mediated erythrocytosis in rodents after intrarenal injection of nickel subsulfide. Yale J Biol Med 55: 123–136, 1982

    PubMed  Google Scholar 

  98. Okamoto M: Induction of ocular tumor by nickel subsulfide in the Japanese common newt, Cynops pyrrhogaster. Cancer Res 47: 5213–5217, 1987

    PubMed  Google Scholar 

  99. Maenza RM, Pradham AM, Sunderman FW Jr: Rapid induction of sarcomas in rats by combination of nickel sulfide and 3,4-benzpyrene. Cancer Res 31: 2067–2071, 1971

    PubMed  Google Scholar 

  100. Sunderman FW Jr: Organ and species specificity in nickel subsulfide carcinogenesis. Basic Life Sci 24: 107–127, 1984

    Google Scholar 

  101. Govindarajan B, Klafter R, Miller MS, Mansur C, Mizesko M, Bai X, LaMontagne K Jr, Arbiser JL: Reactive oxygen-induced carcinogenesis causes hypermethylation of p16(Ink4a) and activation of MAP kinase. Mol Med 8: 1–8, 2002

    Article  PubMed  Google Scholar 

  102. Broday L, Peng W, Kuo MH, Salnikow K, Zoroddu M, Costa M: Nickel compounds are novel inhibitors of histone H4 acetylation. Cancer Res 60(2): 238–241, 2000

    PubMed  Google Scholar 

  103. Zoroddu M, Kowalik-Jankowaka T, Kozlowski H, Molinari H, Salnikow K, Broday L: Interaction of Ni(II) and Cu(II) with a metal binding sequence of histone: AKRHRK, a model of H4 tail. Biochem Biophys Acta 1475: 163–168, 2001

    Google Scholar 

  104. Bal W, Liang R, Lukszo J, Lee SH, Dizdaroglu M, Kasprzak KS: Ni(II) specificially cleaves the C-terminal tail of the major variant of histone H2A and forms an oxidative damage-mediating complex with the cleaved-off octapeptide. Chem Res Toxicol 13: 616–624, 2000

    Article  PubMed  Google Scholar 

  105. Bal W, Lukszo J, Bialkowski K, Kasprzak KS: Interactions of Nickel(II) with histones: interactions of Nickel(II) with CH3CO-Thr-Glu-Ser-His-His-Lys-NH2, a peptide modeling the potential metal binding site in the “C-tail” region of histone H2A. Chem Res Toxicol 11(9): 1014–1023, 1998

    Article  PubMed  Google Scholar 

  106. Zhang Q, Salnikow K, Kluz T, Chen LC, Su WC, Costa M: Inhibition and reversal of nickel-induced transformation by the histone deacetylase inhibitor trichostatin A. Toxicol Appl Pharmacol 192: 201–211, 2003

    Article  PubMed  Google Scholar 

  107. Yan Y, Kluz T, Chen HB, Costa M: Analysis of specific lysine histone H3 and H4 acetylation and methylation status in clones of cells with a gene silenced by nickel exposure. Toxicol Appl Pharmacol 190: 272–277, 2003

    Article  PubMed  Google Scholar 

  108. Nakao M: Epigenetics: interaction of DNA methylation and chromatin. Gene 278: 25–31, 2001

    Article  PubMed  Google Scholar 

  109. Shi XL, Dalal NS: Evidence for a Fenton-type mechanism for the generation of OH radicals in the reduction of Cr(VI) in cellular media. Arch Biochem Biophys 281(1): 90–95, 1990

    Article  PubMed  Google Scholar 

  110. Shi XL, Dalal NS: Chromium(V) and hydroxyl radical formation during the glutathione reductase-catalyzed reduction of chromium(VI). Biochem Biophys Res Commun 163(1): 627–634, 1989

    Article  PubMed  Google Scholar 

  111. Wiseman H, Halliwell B: Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem J 313 (Pt 1): 17–29, 1996

    Google Scholar 

  112. Huang C, Ding M, Li J, Leonard SS, Rojanasakul Y, Castranova V, Vallyathan V, Shi X: Vanadate induces NFAT transactivation through hydrogen peroxide. J Biol Chem 276(25): 22397–22403, 2001

    Article  PubMed  Google Scholar 

  113. Hoyal CR, Thomas AP, Forman HJ: Hydroperoxide-induced increases in intracellular calcium due to annexin VI translocation and inactivation of plasma membrane Ca2+-ATPase. J Biol Chem 271(46): 29205–29210, 1996

    Article  PubMed  Google Scholar 

  114. Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI: Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406(6797): 731–734, 2000

    Article  PubMed  Google Scholar 

  115. Shackelford RE, Kaufmann WK, Paules RS: Oxidative stress and cell cycle checkpoint function. Free Radical Biol Med 28(9): 1387–1404, 2000

    Article  Google Scholar 

  116. Wattanapitayakul SK, Bauer JA: Oxidative pathways in cardiovascular disease: roles, mechanisms, and therapeutic implications. Pharmacol Ther 89(2): 187–206, 2001

    Article  PubMed  Google Scholar 

  117. Xu A, Wu LJ, Santella RM, Hei TK: Role of oxyradicals in mutagenicity and DNA damage induced by crocidolite asbestos in mammalian cells. Cancer Res 59(23): 5922–5926, 1999

    PubMed  Google Scholar 

  118. Davis MA, Flaws JA, Young M, Collins K, Colburn NH: Effect of ceramide on intracellular glutathione determines apoptotic or necrotic cell death of JB6 tumor cells. Toxicol Sci 53(1): 48–55, 2000

    Article  PubMed  Google Scholar 

  119. Yen HC, Oberley TD, Vichitbandha S, Ho YS, St Clair DK: The protective role of manganese superoxide dismutase against adriamycin-induced acute cardiac toxicity in transgenic mice. J Clin Invest 98(5): 1253–1260, 1996

    PubMed  Google Scholar 

  120. Majima HJ, Oberley TD, Furukawa K, Mattson MP, Yen HC, Szweda LI, St Clair DK: Prevention of mitochondrial injury by manganese superoxide dismutase reveals a primary mechanism for alkaline-induced cell death. J Biol Chem 273(14): 8217–8224, 1998

    Article  PubMed  Google Scholar 

  121. Kiningham KK, Oberley TD, Lin S, Mattingly CA, St Clair DK: Overexpression of manganese superoxide dismutase protects against mitochondrial-initiated poly(ADP-ribose) polymerase-mediated cell death. FASEB J 13(12): 1601–1610, 1999

    PubMed  Google Scholar 

  122. Huang C, Zhang Z, Ding M, Li J, Ye J, Leonard SS, Shen HM, Butterworth L, Lu Y, Costa M, Rojanasakul Y, Castranova V, Vallyathan V, Shi X: vanadate induces p53 transactivation through hydrogen peroxide and causes apoptosis. J Biol Chem 275(42): 32516–32522, 2000

    Article  PubMed  Google Scholar 

  123. Dalton TP, Shertzer HG, Puga A: Regulation of gene expression by reactive oxygen. Annu Rev Pharmacol Toxicol 39: 67–101, 1999

    Article  PubMed  Google Scholar 

  124. Yao Y, Hoffer A, Chang CY, Puga A: Dioxin activates HIV-1 gene expression by an oxidative stress pathway requiring a functional cytochrome P450 CYP1A1 enzyme. Environ Health Perspect 103(4): 366–371, 1995

    PubMed  Google Scholar 

  125. Huang C, Ma WY, Bowden GT, Dong Z: Ultraviolet B-induced activated protein-1 activation does not require epidermal growth factor receptor but is blocked by a dominant negative PKClambda/iota. J Biol Chem 271(49): 31262–31268, 1996

    Article  PubMed  Google Scholar 

  126. Zhong W, Oberley LW, Oberley TD, St Clair DK: Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene 14(4): 481–490, 1997

    Article  PubMed  Google Scholar 

  127. Long DJ II, Waikel RL, Wang XJ, Perlaky L, Roop DR, Jaiswal AK: NAD(P)H: Quinone oxidoreductase 1 deficiency increases susceptibility to benzo(a)pyrene-induced mouse skin carcinogenesis. Cancer Res 60(21): 5913–5915, 2000

    PubMed  Google Scholar 

  128. Long DJ II, Waikel RL, Wang XJ, Roop, Jaiswal AK: NAD(P)H: Quinone oxidoreductase 1 deficiency and increased susceptibility to 7,12-dimethylbenz[a]-anthracene-induced carcinogenesis in mouse skin. J Natl Cancer Inst 93(15): 1166–1170, 2001

  129. Chen Y, Liu X, Pisha E, Constantinou AI, Hua Y, Shen L, van Breemen RB, Elguindi EC, Blond SY, Zhang F, Bolton JL: A metabolite of equine estrogens, 4-hydroxyequilenin, induces DNA damage and apoptosis in breast cancer cell lines. Chem Res Toxicol 13(5): 342–350, 2000

    Article  PubMed  Google Scholar 

  130. Khan AU, Kovacic D, Kolbanovskiy A, Desai M, Frenkel K, Geacintov NE: The decomposition of peroxynitrite to nitroxyl anion (NO) and singlet oxygen in aqueous solution. Proc Natl Acad Sci USA 97(7): 2984–2989, 2000

    Article  PubMed  Google Scholar 

  131. Xu Y, Krishnan A, Wan XS, Majima H, Yeh CC, Ludewig G, Kasarskis EJ, St Clair DK: Uutations in the promoter reveal a cause for the reduced expression of the human manganese superoxide dismutase gene in cancer cells. Oncogene 18(1): 93–102, 1999

    Article  PubMed  Google Scholar 

  132. Li JJ, Oberley LW, Fan M, Colburn NH: Inhibition of AP-1 and NF-kappaB by manganese-containing superoxide dismutase in human breast cancer cells. FASEB J 12(15): 1713–1723, 1998

    PubMed  Google Scholar 

  133. Reinke LA, Moore DR, McCay PB: Free radical formation in livers of rats treated acutely and chronically with alcohol. Alcohol Clin Exp Res 21(4): 642–646, 1997

    PubMed  Google Scholar 

  134. Sen CK, Packer L: Antioxidant and redox regulation of gene transcription. FASEB J 10(7): 709–720, 1996

    PubMed  Google Scholar 

  135. Lander HM: An essential role for free radicals and derived species in signal transduction. FASEB J 11(2): 118–124, 1997

    PubMed  Google Scholar 

  136. Wiseman H, Halliwell B: Damage to DNA by reactive oxygen and nitrogen species: Role in inflammatory disease and progression to cancer. Biochem J 313(Pt 1): 17–29, 1996

    PubMed  Google Scholar 

  137. Huang X, Zhuang Z, Frenkel K, Klein CB, Costa M: The role of nickel and nickel-mediated reactive oxygen species in the mechanism of nickel carcinogenesis. Environ Health Perspect 102(suppl 3): 281–284, 1994

    PubMed  Google Scholar 

  138. Zhuang Z, Huang X, Costa M: Protein oxidation and amino acid–DNA crosslinking by nickel compounds in intact cultured cells. Toxicol Appl Pharmacol 126(2): 319–325, 1994

    Article  PubMed  Google Scholar 

  139. Shirali P, Decaestecker AM, Marez T, Hildebrand HF, Bailly C, Martinez R: Ni3S2 uptake by lung cells and its interaction with plasma membranes. J Appl Toxicol 11(4): 279–288, 1991

    PubMed  Google Scholar 

  140. Huang C, Li J, Costa M, Zhang Z, Leonard SS, Castranova V, Vallyathan V, Ju G, Shi X: Hydrogen peroxide mediates activation of nuclear factor of activated T cells(NFAT) by nickel subsulfide. Cancer Res 61: 8051–8057, 2001

    PubMed  Google Scholar 

  141. Bal W, Kozlowski H, Kasprzak KS: Molecular models in nickel carcinogenesis. J Inorg Biochem 79(1–4): 213–218, 2000

    Article  PubMed  Google Scholar 

  142. Huang X, Klein CB, Costa M: Crystalline Ni3S2 specifically enhances the formation of oxidants in the nuclei of CHO cells as detected by dichlorofluorescein. Carcinogenesis 15(3): 545–548, 1994

    PubMed  Google Scholar 

  143. Lin X, Costa M: Transformation of human osteoblasts to anchorage-independent growth by insoluble nickel particles. Environ Health Perspect 102(suppl 3): 289–292, 1994

    PubMed  Google Scholar 

  144. Chen CY, Wang YF, Lin YH, Yen SF: Nickel-induced oxidative stress and effect of antioxidants in human lymphocytes. Arch Toxicol 77: 123–130, 2003

    Article  PubMed  Google Scholar 

  145. Sunderman FW Jr, Hopfer SM, Lin SM, Plowman MC, Stojanovic T, Wong SH, Zaharia O, Ziebka L: Toxicity to alveolar macrophages in rats following parenteral injection of nickel chloride. Toxicol Appl Pharmacol 100(1): 107–118, 1989

    Article  PubMed  Google Scholar 

  146. Rodriguez RE, Misra M, North SL, Kasprzak KS: Nickel-induced lipid peroxidation in the liver of different strains of mice and its relation to nickel effects on antioxidant systems. Toxicol Lett 57(3): 269–281, 1991

    Article  PubMed  Google Scholar 

  147. Herrero MC, Alvarez C, Cartana J, Blade C, Arola L: Nickel effects on hepatic amino acids. Res Commun Chem Pathol Pharmacol 79(2): 243–248, 1993

    PubMed  Google Scholar 

  148. Kawanishi S, Inoue S, Yamamoto K: Site-specific DNA damage induced by nickel(II) ion in the presence of hydrogen peroxide. Carcinogenesis 10: 2231–2235, 1989

    PubMed  Google Scholar 

  149. Tkeshelashvili LK, Reid TM, McBride TJ, Loeb LA: Nickel induces a signature mutation for oxygen free radical damage. Cancer Res 53: 4172–4174, 1993

    PubMed  Google Scholar 

  150. Huang X, Kitahara J, Zhitkovich A, Dowjat K, Costa M: Heterochromatic proteins specifically enhance nickel-induced 8-oxo-dG formation. Carcinogenesis 16: 1753–1759, 1995

    PubMed  Google Scholar 

  151. Salnikow K, Gao M, Voitkun V, Huang X, Costa M: Altered oxidative stress responses in nickel resistant mammalian cells. Cancer Res 54: 6407–6412, 1994

    PubMed  Google Scholar 

  152. Kang J, Zhang Y, Chen J, Chen H, Lin C, Wang Q, Ou Y: Nickel-induced histone hypoacetylation: the role of reactive oxygen species. Toxicol Sci 74: 279–286, 2003

    Article  PubMed  Google Scholar 

  153. Cavallo D, Ursini CL, Setini A, Chianese C, Piegari P, Perniconi B, Iavicoli S: Evaluation of oxidative damage and inhibition of DNA repair in an in vitro study of nickel exposure. Toxicol In Vitro 17: 603–607, 2003

    Article  PubMed  Google Scholar 

  154. Yin Z, Ivanov VN, Habelhah H, Tew K, Ronai Z: Glutathione S-transferase p elicits protection against H2O2-induced cell death via coordinated regulation of stress kinases. Cancer Res 60(15): 4053–4057, 2000

    PubMed  Google Scholar 

  155. Petit PX, Susin SA, Zamzami N, Mignotte B, Kroemer G: Mitochondria and programmed cell death: back to the future. FEBS Lett 396(1): 7–13, 1996

    Article  PubMed  Google Scholar 

  156. Shiao YH, Lee SH, Seo YR, Kasprzak KS: Cell cycle arrest, apoptosis and p53 expression in nickel(II) acetate-treated Chinese hamster ovary cells. Carcinogenesis 19: 1203–1207, 1998

    Article  PubMed  Google Scholar 

  157. Kim K, Lee SH, Seo YR, Perkins SN, Kasprzak KS: Nickel(II)-induced apoptosis in murine T cell hybridoma cells is associated with increased fas ligand expression. Toxicol Appl Pharmacol 185: 41–47, 2002

    Article  PubMed  Google Scholar 

  158. Goebeler M, Roth J, Brocker EB, Sorg C, Schulze-Osthoff K, Activation of nuclear factor-kappa B and gene expression in human endothelial cells by the common haptens nickel and cobalt. J Immunol 155: 2459–2467, 1995

    Google Scholar 

  159. Pulido MD, Parrish AR: Metal-induced apoptosis: mechanisms. Mutat Res 533: 227–241, 2003

    PubMed  Google Scholar 

  160. Lynn S, Yew FH, Chen KS, Jan KY: Reactive oxygen species are involved in nickel inhibition of DNA repair. Environ Mol Mutagen 29: 208–216, 1997

    Article  PubMed  Google Scholar 

  161. Harris GK, Shi X: Signaling by carcinogenic metals and metal-induced reactive oxygen species. Mutat Res 533: 183–200, 2003

    PubMed  Google Scholar 

  162. Shi X, Dalal NS: Hydroxyl radical generation in the NADH/ microsomal reduction of vanadate. Free Radical Res Commun 17(6): 369–376, 1992

    Google Scholar 

  163. Ye J, Wang S, Leonard SS, Sun Y, Butterworth L, Antonini J, Ding M, Rojanasakul Y, Vallyathan V, Castranova V, Shi X: Role of reactive oxygen species and p53 in chromium(VI)-induced apoptosis. J Biol Chem 274(49): 34974–34980, 1999

    Article  PubMed  Google Scholar 

  164. Ding M, Li JJ, Leonard SS, Ye JP, Shi X, Colburn NH, Castranova V, Vallyathan V: Vanadate-induced activation of activator protein-1: role of reactive oxygen species. Carcinogenesis 20(4): 663–668, 1999

    Article  PubMed  Google Scholar 

  165. Sundaresan M, Yu ZX, Ferrans VJ, Irani K, Finkel T: Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270(5234): 296–299, 1995

    PubMed  Google Scholar 

  166. Shibanuma M, Kuroki T, Nose K: Stimulation by hydrogen peroxide of DNA synthesis, competence family gene expression and phosphorylation of a specific protein in quiescent Balb/3T3 cells. Oncogene 5(7): 1025–1032, 1990

    PubMed  Google Scholar 

  167. Devary Y, Gottlieb RA, Lau LF, Karin M: Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol 11(5): 2804–2811, 1991

    PubMed  Google Scholar 

  168. Nose K, Shibanuma M, Kikuchi K, Kageyama H, Sakiyama S, Kuroki T: Transcriptional activation of early-response genes by hydrogen peroxide in a mouse osteoblastic cell line. Eur J Biochem 201(1): 99–106, 1991

    Article  PubMed  Google Scholar 

  169. Schreck R, Rieber P, Baeuerle PA: Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1. EMBO J 10(8): 2247–2258, 1991

    PubMed  Google Scholar 

  170. Los M, Schenk H, Hexel K, Baeuerle PA, Droge W, Schulze-Osthoff K: IL-2 gene expression and NF-kappa B activation through CD28 requires reactive oxygen production by 5-lipoxygenase. EMBO J 14(15): 3731–3740, 1995

    PubMed  Google Scholar 

  171. MacLeod MC, Powell KL, Kuzmin VA, Kolbanovskiy A, Geacintov NE: Interference of benzo[a]pyrene diol epoxide-deoxyguanosine adducts in a GC box with binding of the transcription factor Sp1. Mol Carcinog 16(1): 44–52, 1996

    Article  PubMed  Google Scholar 

  172. Zhao YL, Piao CQ, Wu LJ, Suzuki M, Hei TK: Differentially expressed genes in asbestos-induced tumorigenic human bronchial epithelial cells: Implication for mechanism. Carcinogenesis 21(11): 2005–2010, 2000

    Article  PubMed  Google Scholar 

  173. Piao CQ, Willey JC, Hei TK: Alterations of p53 in tumorigenic human bronchial epithelial cells correlate with metastatic potential. Carcinogenesis 20(8): 1529–1533, 1999

    Article  PubMed  Google Scholar 

  174. Runge D, Runge DM, Drenning SD, Bowen WC Jr, Grandis JR, Michalopoulos GK: Growth and differentiation of rat hepatocytes: changes in transcription factors HNF-3, HNF-4, STAT-3, and STAT-5. Biochem Biophys Res Commun 250(3): 762–768, 1998

    Article  PubMed  Google Scholar 

  175. Huang C, Ke Q, Costa M, Shi X: Molecular mechanisms of arsenic caricinogenesis. Mol Cell Biochem 255: 57–66, 2004

    Article  PubMed  Google Scholar 

  176. Ghosh S, May MJ, Kopp EB: NF-kappa B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225–260, 1998

    Article  PubMed  Google Scholar 

  177. Garcia-Pineres AJ, Henkel T: Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 12: 141–179, 1994

    PubMed  Google Scholar 

  178. Baldwin A: The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 14: 649–683, 1996

    Article  PubMed  Google Scholar 

  179. Sweeney C, Li L, Shanmugam R, Bhat-Nakshatri P, Jayaprakasan V, Baldridge LA, Gardner T, Smith M, Nakshatri H, Cheng L: Nuclear factor-kappa B is constitutively activated in prostate cancer in vitro and is overexpressed in prostatic intraepithelial neoplasia and adenocarcinoma of the prostate. Clin Cancer Res 10: 5501–5507, 2004

    Article  PubMed  Google Scholar 

  180. Li JJ, Westergaard C, Ghosh P, Colburn NH: Inhibitors of both nuclear factor-kappaB and activator protein-1 activation block the neoplastic transformation response. Cancer Res 57: 3569–3576, 1997

    PubMed  Google Scholar 

  181. Gilmore TD, Koedood M, Piffat KA, White DW: Rel/NF-kappaB/IkappaB proteins and cancer. Oncogene 13: 1367–1378, 1996

    PubMed  Google Scholar 

  182. Huang C, Chen N, Ma W-Y, Dong Z: Vanadium induces AP-1 and NFκB-dependent transcription activity. Int J Oncol 13: 711–715, 1998

    PubMed  Google Scholar 

  183. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S: Rel/NF-kappa B/I kappa B family: intimate tales of association and dissociation. Genes Dev 9: 2723–2735, 1995

    PubMed  Google Scholar 

  184. Galang CK, Garcia-Ramirez J, Solski PA, Westwick JK, Der CJ, Neznanov NN, Oshima RG, Hauser CA: Oncogenic Neu/ErbB-2 increases Ets, AP-1, and NF-kappaB-dependent gene expression, and inhibiting ets activation blocks Neu-mediated cellular transformation. J Biol Chem 271: 7992–7998, 1996

    Article  PubMed  Google Scholar 

  185. Finco TS, Baldwin AS Jr: Kappa B site-dependent induction of gene expression by diverse inducers of nuclear factor kappa B requires Raf-1. J Biol Chem 268: 17676–17679, 1993

    PubMed  Google Scholar 

  186. Bruder JT, Heidecker G, Rapp UR: Serum-, TPA-, and Ras-induced expression from Ap-1/Ets-driven promoters requires Raf-1 kinase. Genes Dev 6: 545–556, 1992

    PubMed  Google Scholar 

  187. Finco TS, Westwick JK, Norris JL, Beg AA, Der CJ, Baldwin AS Jr: Oncogenic Ha-Ras-induced signaling activates NF-kappaB transcriptional activity, which is required for cellular transformation. J Biol Chem 272: 24113–24116, 1997

    Article  PubMed  Google Scholar 

  188. Cruz MT, Conçalo M, Figueiredo A, Carvalho AP, Duarte CB, Lopes MC: Contact sensitizer nickel sulfate activates the transcription factors NF-κB and AP-1 and increases the expression of nitric oxide synthase in a skin dendritic cell line. Exp Dermatol 13: 18–26, 2004

    Article  PubMed  Google Scholar 

  189. Rincon M, Flavell RA: Transcription mediated by NFAT is highly inducible in effector CD4+ T helper 2 (Th2) cells but not in Th1 cells. Mol Cell Biol 17(3): 1522–1534, 1997

    PubMed  Google Scholar 

  190. Durand DB, Shaw JP, Bush MR, Replogle RE, Belagaje R, Crabtree GR: Characterization of antigen receptor response elements within the interleukin-2 enhancer. Mol Cell Biol 8(4): 1715–1724, 1988

    PubMed  Google Scholar 

  191. Serfling E, Barthelmas R, Pfeuffer I, Schenk B, Zarius S, Swoboda R, Mercurio F, Karin M: Ubiquitous and lymphocyte-specific factors are involved in the induction of the mouse interleukin 2 gene in T lymphocytes. EMBO J 8(2): 465–473, 1989

    PubMed  Google Scholar 

  192. Shaw JP, Utz PJ, Durand DB, Toole JJ, Emmel EA, Crabtree GR: Identification of a putative regulator of early T cell activation genes. Science 241(4862): 202–205, 1988

    PubMed  Google Scholar 

  193. Rao A, Luo C, Hogan PG: Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15: 707–747, 1997

    Article  PubMed  Google Scholar 

  194. Clipstone NA, Crabtree GR: Identification of calcineurin as a key signaling enzyme in T-lymphocyte activation. Nature 357(6380): 695–697, 1992

    Article  PubMed  Google Scholar 

  195. Jain J, McCaffrey PG, Valge-Archer VE, Rao A: Nuclear factor of activated T cells contains Fos and Jun. Nature 356(6372): 801–804, 1992

    Article  PubMed  Google Scholar 

  196. Emmel EA, Verweij CL, Durand DB, Higgins KM, Lacy E, Crabtree GR: Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science 246(4937): 1617–1620, 1989

    PubMed  Google Scholar 

  197. Flanagan WM, Corthesy B, Bram RJ, Crabtree GR: Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352(6338): 803–807, 1991

    Article  PubMed  Google Scholar 

  198. Jain J, McCaffrey PG, Miner Z, Kerppola TK, Lambert JN, Verdine GL, Curran T, Rao A: The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365(6444): 352–355, 1993

    Article  PubMed  Google Scholar 

  199. Crabtree GR, Clipstone NA: Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu Rev Biochem 63: 1045–1083, 1994

    Article  PubMed  Google Scholar 

  200. McCaffrey PG, Luo C, Kerppola TK, Jain J, Badalian TM, Ho AM, Burgeon E, Lane WS, Lambert JN, Curran T, Verdine, GL, Rao, A, Hogan, PG: Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262(5134): 750–754, 1993

    PubMed  Google Scholar 

  201. Luo C, Burgeon E, Carew JA, McCaffrey PG, Badalian TM, Lane WS, Hogan PG, Rao A: Recombinant NFAT1 (NFATp) is regulated by calcineurin in T cells and mediates transcription of several cytokine genes. Mol Cell Biol 16(7): 3955–3966, 1996

    PubMed  Google Scholar 

  202. Hoey T, Sun YL, Williamson K, Xu X: Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2(5): 461–472, 1995

    Article  PubMed  Google Scholar 

  203. Ho SN, Thomas DJ, Timmerman LA, Li X, Francke U, Crabtree GR: NFATc3, a lymphoid-specific NFATc family member that is calcium-regulated and exhibits distinct DNA binding specificity. J Biol Chem 270(34): 19898–19907, 1995

    Article  PubMed  Google Scholar 

  204. Park J, Takeuchi A, Sharma S: Characterization of a new isoform of the NFAT (nuclear factor of activated T cells) gene family member NFATc. J Biol Chem 271(34): 20914–20921, 1996

    Article  PubMed  Google Scholar 

  205. Huang C, Mattjus P, Ma WY, Rincon M, Chen NY, Brown RE, Dong Z: Involvement of nuclear factor of activated T cells activation in UV response. Evidence from cell culture and transgenic mice. J Biol Chem 275(13): 9143–9149, 2000

    Article  PubMed  Google Scholar 

  206. Northrop JP, Ho SN, Chen L, Thomas DJ, Timmerman LA, Nolan GP, Admon A, Crabtree GR: NFAT components define a family of transcription factors targeted in T-cell activation. Nature 369(6480): 497–502, 1994

    Article  PubMed  Google Scholar 

  207. Chow CW, Rincon M, Davis RJ: Requirement for transcription factor NFAT in interleukin-2 expression. Mol Cell Biol 19(3): 2300–2307, 1999

    PubMed  Google Scholar 

  208. Shibasaki F, Price ER, Milan D, McKeon F: Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NF-AT4. Nature 382(6589): 370–373, 1996

    Article  PubMed  Google Scholar 

  209. Chow CW, Rincon M, Cavanagh J, Dickens M, Davis RJ: Nuclear accumulation of NFAT4 opposed by the JNK signal transduction pathway. Science 278(5343): 1638–1641, 1997

    Article  PubMed  Google Scholar 

  210. Tsatsanis C, Patriotis C, Tsichlis PN: Tpl-2 induces IL-2 expression in T-cell lines by triggering multiple signaling pathways that activate NFAT and NF-kappaB. Oncogene 17(20): 2609–2618, 1998

    Article  PubMed  Google Scholar 

  211. Iniguez MA, Martinez-Martinez S, Punzon C, Redondo JM, Fresno M: An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J Biol Chem 275(31): 23627–23635, 2000

    Article  PubMed  Google Scholar 

  212. Jauliac S, Lopez-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A: The role of NFAT transcription factors in integrin-mediated carcinoma invasion. J Cell Biol 4(7): 540–544, 2002

    Google Scholar 

  213. Jiang H, Yamamoto S, Nishikawa K, Kato R: Anti-tumor-promoting action of FK506, a potent immunosuppressive agent. Carcinogenesis 14(1): 67–71, 1993

    PubMed  Google Scholar 

  214. Singh RK, Gutman M, Reich R, Bar-Eli M: Ultraviolet B irradiation promotes tumorigenic and metastatic properties in primary cutaneous melanoma via induction of interleukin 8. Cancer Res 55(16): 3669–3674, 1995

    PubMed  Google Scholar 

  215. Costa M, Yan Y, Zhao DJ, Salnikow K: Molecular mechanisms of nickel carcinogenesis: gene silencing by nickel delivery to the nucleus and gene activation/inactivation by nickel-induced cell signaling. J Environ Monit 5: 222–223, 2003

    Article  PubMed  Google Scholar 

  216. Semenza GL: Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15: 551–578, 1999

    Article  PubMed  Google Scholar 

  217. Huang LE, Gu J, Schau M, Bunn HF: Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteosome pathway. Proc Natl Acad Sci USA 97: 4748–4753, 1998

    Google Scholar 

  218. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WGJ: HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464–468, 2001

    PubMed  Google Scholar 

  219. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ: Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468–472, 2001

    PubMed  Google Scholar 

  220. Yu F, White SB, Zhao Q, Lee FS: HIF-1α binding to VHL is regulated by stimulus-sensitive proline hydroxylation. Proc Natl Acad Sci USA 98: 9630–9635, 2001

    Article  PubMed  Google Scholar 

  221. McNeill LA, Hewitson KS, Claridge TD, Seibel JF, Horsfall LE, Schofield CJ: Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the beta-carbon of asparagine-803. Biochem J 367: 571–575, 2002

    Article  PubMed  Google Scholar 

  222. Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML: Asparagine hydroxylation of the HIF transcription domain a hypoxic switch. Science 295: 858–861, 2002

    Article  PubMed  Google Scholar 

  223. Folkman J: Tumor angiogenesis: therapeutic implications. N Engl J Med 285: 1182–1186, 1971

    PubMed  Google Scholar 

  224. Semenza GL, Roth PH, Fang HM, Wang GL: Transcriptional regulation of genes encoding glycolitic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757–23763, 1994

    PubMed  Google Scholar 

  225. Rolfs A, Kvietikova I, Gassmann K, Wenger RH: Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor 1. J Biol Chem 272: 20055–20062, 1997

    Article  PubMed  Google Scholar 

  226. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L: A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182: 1683–1693, 1995

    Article  PubMed  Google Scholar 

  227. Garayoa M, Martinez A, Lee S, Pio R, An WG, Neckers L, Trepel J, Montuenga LM, Ryan H, Johnson R, Gassmann M, Cuttitta F: Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: A possible promotion mechanism of carcinogenesis. Mol Endocrinol 14: 848–862, 2000

    Article  PubMed  Google Scholar 

  228. Salnikow K, Davidson T, Zhang QW, Chen LC, Su W, Costa M: The involvement of hypoxia-inducible transcription factor-1-dependent pathway in nickel carcinogenesis. Cancer Res 63: 3524–3530, 2003

    PubMed  Google Scholar 

  229. Hopfer SM, Sunderman FW Jr, Fredrickson TN, Morse EE: Increased serum erythropoietin activity in rats following intrarenal injection of nickel subsulfide. Res Commun Chem Pathol Pharmacol 23(1): 155–170, 1979

    PubMed  Google Scholar 

  230. Salnikow K, Davidson T, Kluz T, Chen H, Zhou D, Costa M: GeneChip analysis of signaling pathways effected by nickel. J Environ Monit 5: 206–209, 2003

    Article  PubMed  Google Scholar 

  231. Bruick RK: Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc Natl Acad Sci USA 97(16): 9082–9087, 2000

    Article  PubMed  Google Scholar 

  232. Taylor MS: Characterization and comparative analysis of the EGLN gene family. Gene (Amst) 275: 125–132, 2001

    Article  Google Scholar 

  233. Epstein AC, Gleadle JM, McNeil LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ: C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43–54, 2001

    Article  PubMed  Google Scholar 

  234. Takahashi Y, Takahashi S, Shiga Y, Yoshimi T, Miura T: Hypoxic induction of prolyl-4-hydroxylase α(I) in cultured cells. J Biol Chem 275: 14139–14146, 2000

    Article  PubMed  Google Scholar 

  235. Cangul H, Salnikow K, Yee H, Zagzag D, Commes T, Costa M: Enhanced overexpression of an HIF-1/hypoxia-related protein in cancer cells. Environ Health Perspect 110(suppl 5): 783–788, 2002

    Google Scholar 

  236. Salnikow K, Zhou D, Kluz T, Wang C, Costa M: Cap43: A new gene induced by a rise in free intracellular Ca2+ following Ni2+ exposure. In: B Sarkar (ed). Metals and Genetics, Plenum Publishing, New York, 1999, pp 131–144

  237. Salnikow K, Blagosklonny MV, Ryan H, Johnson R, Costa M: Carcinogenic nickel induced genes involved with hypoxic stress. Cancer Res 60: 38–41, 2000

    PubMed  Google Scholar 

  238. Masuda K, Ono M, Okamoto M, Morikawa W, Otsubo M, Migita T, Tsuneyoshi M, Okuda H, Shun T, Naito S, Kuwano M: Down regulation of Cap43 gene by von Hippel-Lindau tumor suppressor protein in human renal cancer cells. Int J Cancer 105: 803–810, 2003

    Article  PubMed  Google Scholar 

  239. Zhao J, Chen H, Davidson T, Kluz T, Zhang Q, Costa M: Nickel-induced 1,4-α-glucan branching enzyme 1 up-regulation via the hypoxic signaling pathway. Toxicol Appl Pharmacol 196: 404–409, 2004

    Article  PubMed  Google Scholar 

  240. Salnikow K, Kluz T, Costa M, Piquemal D, Demidenko ZN, Xie K, Blagosklonny MV: The regulation of hypoxic genes by calcium involves c-Jun/AP-1, which cooperates with hypoxia-inducible factor 1 in response to hypoxia. Mol Cell Biol 22(6): 1734–1741, 2002

    Article  PubMed  Google Scholar 

  241. Millhorn DE, Raymond R, Conforti I, Zhu W, Beitner-Johnson D, Filisko T, Genter MB, Kobayashi S, Peng M: Regulation of gene expression for tyrosine hydroxylase in oxygen sensitive cells by hypoxia. Kidney Int 51: 527–535, 1997

    PubMed  Google Scholar 

  242. Huang SM, Schonthal AH, Stallcup MR: Enhancement of p53-dependent gene activation by the transcriptional co-activator Zac1. Oncogene 20: 2134–2143, 2001

    Article  PubMed  Google Scholar 

  243. Zhao J, Yan Y, Salnikow K, Kluz T, Costa M: Nickel-induced down-regulation of serpin by hypoxic signaling. Toxicol Appl Pharmacol 194: 60–68, 2004

    Article  PubMed  Google Scholar 

  244. Li J, Davidson G, Huang Y, Jiang BH, Shi X, Costa M, Huang C: Nickel compounds act through phosphatidylinositol-3-kinase/Akt-dependent, p70S6k-independent pathway to induce hypoxia inducible factor transactivation and Cap43 expression in mouse epidermal C141 cells. Cancer Res 64: 94–101, 2004

    Article  PubMed  Google Scholar 

  245. Hernandez-Boussard T, Rodriguez-Tome P, Montesano R, Hainaut P: IARC p53 mutation database: A relational database to compile and analyze p53 mutations in human tumors and cell lines. Hum Mutat 14: 1–8, 1999

    Article  PubMed  Google Scholar 

  246. Weghorst CM, Dragnev KH, Buzard GS, Thorne KL, Vandeborne GF, Vincent KA, Rice JM: Low incidence of point mutations detected in the p53 tumor suppressor gene from chemically induced rat renal mesenchymal tumors. Cancer Res 154: 215–219, 1994

    Google Scholar 

  247. Romano JW, Ehrhart JC, Duthu A, Kim CM, Appella E, May P: Identification and characterization of a p53 gene mutation in a human osteosarcoma cell line. Oncogene 4: 1483–1488, 1989

    PubMed  Google Scholar 

  248. Rani AS, Qu DQ, Sidhu MK, Panagakos F, Shah V, Klein KM, Brown N, Pathak S, Kumar S: Transformation of immortal, non-tumorigenic osteoblast-like human osteosarcoma cells to the tumorigenic phenotype by nickel sulfate. Carcinogenesis 14: 947–953, 1993

    PubMed  Google Scholar 

  249. Lin X, Dowjat WK, Costa M: Nickel-induced transformation of human cells causes loss of the phosphorylation of the retinoblastoma protein. Cancer Res 54: 2751–2754, 1994

    PubMed  Google Scholar 

  250. Miller AC, Blakely WF, Livengood D, Whittaker T, Xu J, Ejnik JW, Hamilton MM, Parlette E, John TS, Gerstenberg HM, Hsu H: Transformation of human osteoblast cells to the tumorigenic phenotype by depleted uranium-uranyl chloride. Environ Health Perspect 106: 465–471, 1998

    PubMed  Google Scholar 

  251. An WG, Kanekal M, Simon MC, Maltepe E, Blagosklonny MV, Neckers LM: Stabilization of wild-type p53 by hypoxia-inducible factor 1alpha. Nature 392: 405–408, 1998

    Article  PubMed  Google Scholar 

  252. Salnikow K, Davidson T, Costa M: The role of hypoxia-inducible signaling pathway in nickel carcinogenesis. Environ Health Perspect 110(suppl 5): 831–834, 2002

    PubMed  Google Scholar 

  253. Boislève F, Kerdine-Römer S, Rougier-Larzat N, Pallardy M: Nickel and DNCB induce CCR7 expression on human dendritic cells through different signaling pathways: role of TNF-α and MAPK. J Invest Dermatol 123: 494–502, 2004

    Article  PubMed  Google Scholar 

  254. Salnikow K, Cosentino S, Klein C, Costa M: Loss of thrombospondin transcriptional activity in nickel-transformed cells. Mol Cell Biol 14: 851–858, 1994

    PubMed  Google Scholar 

  255. Shaywitz AJ, Greenberg ME: CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68: 821–861, 1999

    Article  PubMed  Google Scholar 

  256. Kouzarides T: Transcriptional control by the retinoblastoma protein. Semin Cancer Biol 6: 91–98, 1995

    Article  PubMed  Google Scholar 

  257. Hankinson O: The aryl hydrocarbon receptor complex. Annu Rev Pharmacol 35: 307–340, 1995

    Article  Google Scholar 

  258. Davidson T, Salnikow K, Costa M: Hypoxia inducible factor-1α-independent suppression of aryl hydrocarbon receptor-regulated genes by nickel. Mol Pharmacol 64: 1485–1493, 2003

    Article  PubMed  Google Scholar 

  259. Pollenz RS, Davarinos NA, Shearer TP: Analysis of aryl hydrocarbon receptor-mediated signaling during physiological hypoxia reveals lack of competition for the aryl hydrocarbon nuclear translocator transcription factor. Mol Pharmacol 56: 1127–1137, 1999

    PubMed  Google Scholar 

  260. Gradin K, McGuire J, Wenger RH, Kvietikova I, Fhitelaw ML, Toftgard R, Tora L, Gassman M, Poelinger L: Functional interference hypoxia and dioxin signal transduction pathways: competition for recruitment of the ARNT transcription factor. Mol Cell Biol 16: 5221–5231, 1996

    PubMed  Google Scholar 

  261. Kim JE, Sheen YY: Inhibition of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-stimulated Cyp1a1 promoter activity by hypoxic agents. Biochem Pharmacol 59: 1549–1556, 2000

    Article  PubMed  Google Scholar 

  262. Reisdorph R, Lindahl R: Hypoxia exerts cell-type-specific effects on expression of the class 3 aldehyde dehydrogenase gene. Biochem Biophys Res Commun 249: 709–712, 1998

    Article  PubMed  Google Scholar 

  263. Nie M, Blankenship AL, Giesy JP: Interactions between aryl hydrocarbon(AhR) and hypoxia signaling pathways. Environ Toxicol Pharmacol 10: 17–27, 2001

    Article  PubMed  Google Scholar 

  264. Trapasso F, Krakowiak A, Cesari R, Arkles J, Yendamuri S, Ishii H, Vecchione A, Kuroki T, Bieganowski P, Pace HC, Huebner K, Croce CM, Brenner C: Designed FHIT alleles establish that Fhit-induced apoptosis in cancer cells is limited by substrate binding. Proc Natl Acad Sci USA 100: 1592–1597, 2003

    Article  PubMed  Google Scholar 

  265. Kowara R, Karaczyn A, Fivash MJ, Kasprzak KS: In vitro inhibition of the enzymatic activity of tumor suppressor FHIT gene product by carcinogenic transition metals. Chem Res Toxicol 15: 319–325, 2002

    Article  PubMed  Google Scholar 

  266. Kowara R, Salnikow K, Diwan AB, Bare RM, Waalkes MP, Kasprzak KS: Reduced Fhit protein expression in nickel-transformed mouse cells and in nickel-induced murine sarcomas. Mol Cell Biochem 255: 195–202, 2004

    Article  PubMed  Google Scholar 

  267. Verma R, Ramnath J, Clemens F, Kaspin LC, Landolph JR: Molecular biology of nickel carcinogenesis: identification of differentially expressed genes in morphologically transformed C3H10T1/2 C1 8 mouse embryo fibroblast cell lines induced by specific insoluble nickel compounds. Mol Cell Biochem 255: 203–216, 2004

    Article  PubMed  Google Scholar 

  268. Sunderman FW Jr: Mechanisms of nickel carcinogenesis. Scand J Work Environ Health 15: 1–12, 1989

    Google Scholar 

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Correspondence to Chuanshu Huang.

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Lu, H., Shi, X., Costa, M. et al. Carcinogenic effect of nickel compounds. Mol Cell Biochem 279, 45–67 (2005). https://doi.org/10.1007/s11010-005-8215-2

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