Role of Oxidative Damage in Metal-Induced Carcinogenesis

Chapter

Abstract

This chapter presents and discusses evidence of possible mechanistic involvement of oxidative DNA and protein damage in metal-induced carcinogenesis . Carcinogenic metals , e.g., Be, Cd, Cr, Co, Ni, and the metalloid As, are capable of generating various kinds of active oxygen and other reactive species in direct redox reactions with O2, O2 −●, H2O2, organic peroxides, and other cellular or tissue substrates, and/or indirectly—by inducing inflammation or unleashing physiological redox-active metals , Fe and Cu. The reactive species may damage all cell components, including DNA , RNA, free triphospho-nucleosides, proteins , and lipids, and exhaust cellular antioxidant defenses, e.g., deplete ascorbate. The damage may be aggravated by metal-assisted inhibition of DNA repair and histone demethylation systems. The association of oxidative damage with carcinogenesis is strongly supported by mutagenicity of DNA base products, strand breaks, apurinic sites, cross-links, and adducts typical for the attacking reactive species (oxygen-, carbon-, or sulfur-centered radicals), originating from oxidized amino acids and proteins , and 4-hydroxynonenal, a lipid oxidation product. Oxidative damage to nuclear proteins affects chromatin structure and gene expression, whereas such damage to regulatory proteins disturbs cell cycle and apoptosis. Thus, oxidative DNA damage may assist in the initiation while RNA and protein damage may facilitate the promotion and progression of cancer.

Keywords

Metal Metal Redox Activity Protein Protein FHIT Protein Promote Lipid Peroxidation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Author would like to thank Dr. Yih-Horng Shiao for critical reading of the manuscript. This project was supported by the Intramural Research Program of the NIH, National Cancer Institute, Center for Cancer Research. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.

References

  1. Asare GA, Kew MC, Mossanda KS, Paterson AC, Siziba K, Kahler-Venter CP (2009) Effects of exogenous antioxidants on dietary iron overload. J Clin Biochem Nutr 44:85–94PubMedCrossRefGoogle Scholar
  2. Aust AE, Eveleigh JF (1999) Mechanisms of DNA oxidation. Proc Soc Exp Biol Med 222:246–252PubMedCrossRefGoogle Scholar
  3. Bal W, Lukszo J, Jezowska-Bojczuk M, Kasprzak KS (1997a) Binding of nickel(II) and copper(II) to the N-terminal sequence of human protamine HP2. Chem Res Toxicol 10:906–914CrossRefGoogle Scholar
  4. Bal W, Lukszo J, Kasprzak KS (1997b) Mediation of oxidative DNA damage by nickel(II) and copper(II) complexes with the N-terminal sequence of human protamine HP2. Chem Res Toxicol 10:915–921CrossRefGoogle Scholar
  5. Bal W, Lukszo J, Bialkowski K, Kasprzak KS (1998) Interactions of nickel(II) with histones: interactions of Ni(II) with CH3COThr-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 11:1014–1023PubMedCrossRefGoogle Scholar
  6. Bal W, Liang R, Lukszo J, Lee SH, Dizdaroglu M, Kasprzak KS (2000a) Nickel(II) specifically cleaves the C-terminal tail of the major variant of histone H2A and forms oxidative damage-mediating complex with the cleaved-off octapeptide. Chem Res Toxicol 13:616–624CrossRefGoogle Scholar
  7. Bal W, Wojcik J, Maciejczyk M, Grochowski P, Kasprzak KS (2000b) Induction of a secondary structure in the N-terminal pentadecapeptide of human protamine HP2 through Ni(II) coordination. An NMR study. Chem Res Toxicol 13:823–830CrossRefGoogle Scholar
  8. Bal W, Protas AM, Kasprzak KS (2010) Genotoxicity of metal ions: chemical insights. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences, vol 8: metal ions in toxicology: effects, interactions, interdependencies. Royal Society of Chemistry Press, CambridgeGoogle Scholar
  9. Bartosz G (1995) Druga twarz tlenu. PWN, WarszawaGoogle Scholar
  10. Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82:493–512PubMedCrossRefGoogle Scholar
  11. Bialkowski K, Kasprzak KS (1998) A novel assay of 8-oxo-2′-deoxyguanosine 5′-triphosphate pyrophosphohydrolase (8-oxo-dGTPase) activity in cultured cells and its use for evaluation of cadmium(II) inhibition of this activity. Nucl Acids Res 26:3194–3201PubMedCrossRefGoogle Scholar
  12. Bialkowski K, Bialkowska A, Kasprzak KS (1999) Cadmium(II), but not nickel(II), inhibits 8-oxo-dGTPase activity and increases 8-oxo-dG levels in DNA of the rat testis, a target organ for cadmium(II) carcinogenesis. Carcinogenesis 20:1621–1624PubMedCrossRefGoogle Scholar
  13. Borges KM, Wetterhahn KE (1989) Chromium cross-links glutathione and cysteine to DNA. Carcinogenesis 10:2165–2168PubMedCrossRefGoogle Scholar
  14. Bregadze VG, Gelagutashvili ES, Tsakadze KJ, Melikishvili SZ (2008) Metal-induced point defects in DNA: model and mechanisms. Chem Biodivers 5:1980–1989PubMedCrossRefGoogle Scholar
  15. Brink A, Richter I, Lutz U, Wanek P, Stopper H, Lutz WK (2009) Biological significance of DNA adducts: comparison of increments over background for various biomarkers of genotoxicity in L5178Y tk(+/−) mouse lymphoma cells treated with hydrogen peroxide and cumene hydroperoxide. Mutat Res 678:123–128PubMedCrossRefGoogle Scholar
  16. Bryan SE (1981) Heavy metals in the cell’s nucleus. In: Eichhorn GL, Marzilli LG (eds) Metal ions in genetic information transfer. Elsevier, New YorkGoogle Scholar
  17. Buzard GS, Kasprzak KS (2000) Possible roles of nitric oxide and redox cell signaling in metal-induced toxicity and carcinogenesis: a review. J Environ Pathol Toxicol Oncol 19:179–199PubMedGoogle Scholar
  18. Cai Y, Zhuang Z (1999) DNA damage in human peripheral blood lymphocyte caused by nickel and cadmium. Zhonghua Yu Fang Yi Xue Za Zhi 33:75–77PubMedGoogle Scholar
  19. Chang J, Watson WP, Randerath E, Randerath K (1993) Bulky DNA-adduct formation induced by Ni(II) in vitro and in vivo as assayed by 32P-postlabeling. Mutat Res 291:147–159Google Scholar
  20. Chiaverini N, De Ley M (2010) Protective effect of metallothionein on oxidative stress-induced DNA damage. Free Radic Res 44:605–613PubMedCrossRefGoogle Scholar
  21. Chiocca SM, Sterner DA, Biggart NW, Murphy EC Jr (1991) Nickel mutagenesis: alteration of the MuSVts110 thermosensitive splicing phenotype by a nickel-induced duplication of the 3′ splice site. Mol Carcinog 4:61–71PubMedCrossRefGoogle Scholar
  22. Chválová K, Brabec V, Kaspárková J (2007) Mechanism of the formation of DNA–protein cross-links by antitumor cisplatin. Nucleic Acids Res 35:1812–1821PubMedCrossRefGoogle Scholar
  23. De Boeck M, Hoet P, Lombaert N, Nemery B, Kirsch-Volders M, Lison D (2003) In vivo genotoxicity of hard metal dust: induction of micronuclei in rat type II epithelial lung cells. Carcinogenesis 24:1793–1800 PubMedCrossRefGoogle Scholar
  24. Dizdaroglu M (1992) Oxidative damage to DNA in mammalian chromatin. Mutat Res 275:331–342PubMedCrossRefGoogle Scholar
  25. Dizdaroglu M (1994) Chemical determination of oxidative base damage in DNA by gas chromatography–mass spectrometry. Methods Enzymol 234:3–16PubMedCrossRefGoogle Scholar
  26. Dizdaroglu M, Rao G, Halliwell B, Gajewski E (1991) Damage to the DNA bases in mammalian chromatin by hydrogen peroxide in the presence of ferric and cupric ions. Arch Biochem Biophys 285:317–324PubMedCrossRefGoogle Scholar
  27. Dizdaroglu M, Jaruga P, Birincioglu M, Rodriguez H (2002) Free radical-induced damage to DNA: mechanisms and measurement. Free Radic Biol Med 32:1102–1115PubMedCrossRefGoogle Scholar
  28. Engström KS, Vahter M, Johansson G, Lindh CH, Teichert F, Singh R, Kippler M, Nermell B, Raqib R, Strömberg U, Broberg K (2010) Chronic exposure to cadmium and arsenic strongly influences concentrations of 8-oxo-7,8-dihydro-2′-deoxyguanosine in urine. Free Radic Biol Med 48:1211–1217PubMedCrossRefGoogle Scholar
  29. Evans MD, Dizdaroglu M, Cooke MS (2004) Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 567:1–61PubMedCrossRefGoogle Scholar
  30. Feng Z, Hu W, Amin S, Tang MS (2003) Mutational spectrum and genotoxicity of the major lipid peroxidation product, trans-4-hydroxy-2-nonenal, induced DNA adducts in nucleotide excision repair-proficient and -deficient human cells. Biochemistry 42:7848–7854PubMedCrossRefGoogle Scholar
  31. Fernandes PH, Wang H, Rizzo CJ, Lloyd RS (2003) Site-specific mutagenicity of stereochemically defined 1,N2-deoxyguanosine adducts of trans-4-hydroxynonenal in mammalian cells. Environ Mol Mutagen 42:68–74PubMedCrossRefGoogle Scholar
  32. Francia C, Bodoardo F, Penazzi N, Corazzari I, Fenoglio I (2007) Characterization of the electrochemical process responsible for the free radical release in hard metals. Electrochim Acta 52:7438–7443CrossRefGoogle Scholar
  33. Fujikawa K, Kamiya H, Yakushiji H, Nakabeppu Y, Kasai H (2001) Human MTH1 protein hydrolyzes the oxidized ribonucleotide, 2-hydroxy-ATP. Nucl Acids Res 29:449–454PubMedCrossRefGoogle Scholar
  34. Guz J, Foksinski M, Siomek A, Gackowski D, Rozalski R, Dziaman T, Szpila A, Olinski R (2008) The relationship between 8-oxo-7,8-dihydro-2′-deoxyguanosine level and extent of cytosine methylation in leukocytes DNA of healthy subjects and in patients with colon adenomas and carcinomas. Mutat Res 640:170–173PubMedCrossRefGoogle Scholar
  35. Hailer-Morrison MK, Kotler JM, Martin BD, Sugden KD (2003) Oxidized guanine lesions as modulators of gene transcription. Altered p50 binding affinity and repair shielding by 7,8-dihydro-8-oxo-2′-deoxyguanosine lesions in the NF-kappaB promoter element. Biochemistry 42:9761–9770PubMedCrossRefGoogle Scholar
  36. Hamazaki S, Okada S, Li JL, Toyokuni S, Midorikawa O (1989) Oxygen reduction and lipid peroxidation by iron chelates with special reference to ferric nitrilotriacetate. Arch Biochem Biophys 272:10–17Google Scholar
  37. Hartwig A (1994) Role of DNA repair inhibition in lead- and cadmium-induced genotoxicity: a review. Environ Health Perspect 102(Suppl 3):45–50PubMedCrossRefGoogle Scholar
  38. Hartwig A (1995) Current aspects in metal genotoxicity. BioMetals 8:3–11PubMedCrossRefGoogle Scholar
  39. Hartwig A, Klyszcz-Nasko H, Schleppegrell L, Beyersmann D (1993) Cellular damage by ferric nitrilotriacetate and ferric citrate in V79 cells: interrelationship between lipid peroxidation, DNA strand breaks and sister chromatid exchanges. Carcinogenesis 14:107–112PubMedCrossRefGoogle Scholar
  40. Hawkins CL, Davies MJ (1997) Oxidative damage to collagen and related substrates by metal ion/hydrogen peroxide systems: random attack or site-specific damage? Biochim Biophys Acta 1360:84–96Google Scholar
  41. Higinbotham KG, Rice JM, Diwan BA, Kasprzak KS, Reed CD, Perantoni AO (1992) 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 52:4747–4751PubMedGoogle Scholar
  42. Huang X, Kitahara J, Zhitkovich A, Dowjat K, Costa M (1995) Heterochromatic proteins specifically enhance nickel-induced 8-oxo-dG formation. Carcinogenesis 16:1753–1759PubMedCrossRefGoogle Scholar
  43. Ingrosso D, Cimmino A, D’Angelo S, Alfinito F, Zappia V, Galletti P (2002) Protein methylation as a marker of aspartate damage in glucose-6-phosphate dehydrogenase-deficient erythrocytes: role of oxidative stress. Eur J Biochem 269:2032–2039PubMedCrossRefGoogle Scholar
  44. Inoue S, Kawanishi S (1987) Hydroxyl radical production and human DNA damage induced by ferric nitrilotriacetate and hydrogen peroxide. Cancer Res 47:6522–6527PubMedGoogle Scholar
  45. Jacobs AT, Marnett LJ (2010) Systems analysis of protein modification and cellular responses induced by electrophile stress. Acc Chem Res 43:673–683PubMedCrossRefGoogle Scholar
  46. Ji C, Kozak KR, Marnett LJ (2001) IkappaB kinase, a molecular target for inhibition by 4-hydroxy-2-nonenal. J Biol Chem 276:18223–18228PubMedCrossRefGoogle Scholar
  47. Kaczmarek M, Timofeeva O, Karaczyn A, Malyguine A, Kasprzak KS, Salnikow K (2007) The role of ascorbate in the modulation of HIF-1a protein and HIF-dependent transcription by chromium(VI) and nickel(II). Free Radic Biol Med 42:1246–1257PubMedCrossRefGoogle Scholar
  48. Kalinich JF, Emond CA, Dalton TK, Mog SR, Coleman GD, Kordell JE, Miller AC, McClain DE (2005) Embedded weapons-grade tungsten alloy shrapnel rapidly induces metastatic high-grade rhabdomyosarcomas in F344 rats. Environ Health Perspect 113:729–734PubMedCrossRefGoogle Scholar
  49. Kanazawa A, Sawa T, Akaik T, Maeda H (2000) Formation of abasic sites in DNA by t-butyl peroxyl radicals: implication for potent genotoxicity of lipid peroxyl radicals. Cancer Lett 156:51–55PubMedCrossRefGoogle Scholar
  50. Karaczyn AA, Golebiowski F, Kasprzak KS (2005) Truncation, deamidation, and oxidation of histone H2B in cells cultured with nickel(II). Chem Res Toxicol 18:1934–1942PubMedCrossRefGoogle Scholar
  51. Kasprzak KS (1996) Oxidative DNA damage in metal-induced carcinogenesis. In: Chang LW (ed) Toxicology of metals. CRC Lewis Publishers, Boca RatonGoogle Scholar
  52. Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radic Biol Med 32:958–967PubMedCrossRefGoogle Scholar
  53. Kasprzak KS, Bare RM (1989) In vitro polymerization of histones by carcinogenic nickel compounds. Carcinogenesis 10:621–624PubMedCrossRefGoogle Scholar
  54. Kasprzak KS, Buzard GS (2000) The role of metals in oxidative damage and redox cell signaling derangement. In: Koropatnick J, Zalups R (eds) Molecular biology and toxicology of metals. Taylor and Francis, LondonGoogle Scholar
  55. Kasprzak KS, Salnikow K (2007) Nickel toxicity and carcinogenesis. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences: nickel and its surprising impact in nature, vol. 2. Wiley, ChichesterGoogle Scholar
  56. Kasprzak KS, Sunderman FW Jr (1977) Mechanisms of dissolution of nickel subsulfide in rat serum. Res Commun Chem Pathol Pharmacol 16:95–108PubMedGoogle Scholar
  57. Kasprzak KS, Misra M, Rodriguez RE, North SL (1991) Nickel-induced oxidation of renal DNA guanine residues in vivo and in vitro. Toxicologist 11:233Google Scholar
  58. Kasprzak KS, Diwan BA, Rice JM, Misra M, Riggs CW, Olinski R, Dizdaroglu M (1992) Nickel(II)-mediated oxidative DNA base damage in renal and hepatic chromatin of pregnant rats and their fetuses. Possible relevance to carcinogenesis. Chem Res Toxicol 5:809–815PubMedCrossRefGoogle Scholar
  59. Kasprzak KS, Diwan BA, Rice JM (1994a) Iron accelerates while magnesium inhibits nickel-induced carcinogenesis in the rat kidney. Toxicology 90:129–140CrossRefGoogle Scholar
  60. Kasprzak KS, Zastawny TH, North SL, Riggs CW, Diwan BA, Rice JM, Dizdaroglu M (1994b) Oxidative DNA base damage in renal, hepatic, and pulmonary chromatin of rats after intraperitoneal injection of cobalt(II) acetate. Chem Res Toxicol 7:329–335CrossRefGoogle Scholar
  61. Kasprzak KS, Nakabeppu Y, Kakuma T, Sakai Y, Sekiguchi M, Ward JM, Diwan BA, Nagashima K, Kasprzak BH (2001) Intracellular distribution of the antimutagenic enzyme MTH1 in the liver, kidney and testis of F344 rats and its modulation by cadmium(II). Exp Toxicol Pathol 53:325–336PubMedCrossRefGoogle Scholar
  62. Kawanishi S, Inoue S, Sano S (1986) Mechanism of DNA cleavage induced by sodium chromate(VI) in the presence of hydrogen peroxide. J Biol Chem 261:5952–5958PubMedGoogle Scholar
  63. Kawanishi S, Inoue S, Yamamoto K (1989) Site-specific DNA damage by nickel(II) ion in the presence of hydrogen peroxide. Carcinogenesis 12:2231–2235CrossRefGoogle Scholar
  64. Kinoshita A, Wanibuchi H, Morimura K, Wei M, Nakae D, Arai T, Minowa O, Noda T, Nishimura S, Fukushima S (2007) Carcinogenicity of dimethylarsinic acid in Ogg1-deficient mice. Cancer Sci 98:803–814PubMedCrossRefGoogle Scholar
  65. Kitchin KT, Conolly R (2010) Arsenic-induced carcinogenesis–oxidative stress as a possible mode of action and future research needs for more biologically based risk assessment. Chem Res Toxicol 23:327–335PubMedCrossRefGoogle Scholar
  66. Klein CB, Frenkel K, Costa M (1991) The role of oxidative processes in metal carcinogenesis. Chem Res Toxicol 4:592–604PubMedCrossRefGoogle Scholar
  67. Klug A (2010) The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu Rev Biochem 79:213–231PubMedCrossRefGoogle Scholar
  68. Knöbel Y, Weise A, Glei M, Sendt W, Claussen U, Pool-Zobel BL (2007) Ferric iron is genotoxic in non-transformed and preneoplastic human colon cells. Food Chem Toxicol 45:804–811PubMedCrossRefGoogle Scholar
  69. Kon SH (1978) Biological autoxidation. I. Decontrolled iron: an ultimate carcinogen and toxicant: an hypothesis. Med Hypotheses 4:445–471PubMedCrossRefGoogle Scholar
  70. Kong Q, Lin CL (2010) Oxidative damage to RNA: mechanisms, consequences, and diseases. Cell Mol Life Sci 67:1817–1829PubMedCrossRefGoogle Scholar
  71. Kong L, Saavedra JE, Buzard GS, Xu X, Hood BL, Conrads TP, Veenstra TD, Keefer LK (2006) Deamidation of peptides in aerobic nitric oxide solution by a nitrosative pathway. Nitric Oxide 14:144–151PubMedCrossRefGoogle Scholar
  72. Kowara R, Karaczyn A, Fivash MJ Jr, Kasprzak KS (2002) In vitro inhibition of the enzymatic activity of tumor suppressor FHIT gene product by carcinogenic transition metals. Chem Res Toxicol 15:319–325PubMedCrossRefGoogle Scholar
  73. Kowara R, Salnikow K, Diwan BA, Bare RM, Waalkes MP, Kasprzak KS (2004) Reduced Fhit protein expression in nickel-transformed mouse cells and in nickel-induced murine sarcomas. Mol Cell Biochem 255:195–202PubMedCrossRefGoogle Scholar
  74. Kroncke KD, Klotz LO (2009) Zinc fingers as biologic redox switches? Antioxid Redox Signa 11:1015–1027CrossRefGoogle Scholar
  75. Kukiełka E, Cederbaum AI (1990) NADPH- and NADH-dependent oxygen radical generation by rat liver nuclei in the presence of redox cycling agents and iron. Arch Biochem Biophys 283:326–333PubMedCrossRefGoogle Scholar
  76. Lancaster JR Jr (1988) The bioinorganic chemistry of nickel. VCH, New York.Google Scholar
  77. Landolph JR (1999) Role of free radicals in metal-induced carcinogenesis. In: Sigel H, Sigel A (eds) Metal ions in biological systems, vol 36. M. Dekker, New YorkGoogle Scholar
  78. Lee JE, Ciccarelli RB, Jennette KW (1982) Solubilization of the carcinogen nickel subsulfide and its interaction with deoxyribonucleic acid and protein. Biochemistry 21:771–778PubMedCrossRefGoogle Scholar
  79. Liang R, Senturker S, Shi X, Bal W, Dizdaroglu M, Kasprzak KS (1999) Effect of Ni(II) and Cu(II) on DNA interaction with the N-terminal sequence of human protamine P2: enhancement of binding and mediation of oxidative DNA strand scission and base damage. Carcinogenesis 20:893–898PubMedCrossRefGoogle Scholar
  80. Lison D, Carbonnelle P, Mollo L, Lauwerys R, Fubini B (1995) Physicochemical mechanism of the interaction between cobalt metal and carbide particles to generate toxic activated oxygen species. Chem Res Toxicol 8:600–606PubMedCrossRefGoogle Scholar
  81. Loeb LA, James EA, Waltersdorph AM, Klebanoff SJ (1988) Mutagenesis by the autoxidation of iron with isolated DNA. Proc Natl Acad Sci U S A 85:3918–3922PubMedCrossRefGoogle Scholar
  82. Ma Y, Zhang D, Kawabata T, Kiriu T, Toyokuni S, Uchida K, Okada S (1997) Copper and iron-induced oxidative damage in non-tumor bearing LEC rats. Pathol Int 47:203–208PubMedCrossRefGoogle Scholar
  83. Marquez A, Villa-Treviño S, Guéraud F (2007) The LEC rat: a useful model for studying liver carcinogenesis related to oxidative stress and inflammation. Redox Rep 12:35–39PubMedCrossRefGoogle Scholar
  84. Marquez-Quiñones A, Cipak A, Zarkovic K, Fattel-Fazenda S, Villa-Treviño S, Waeg G, Zarkovic N, Guéraud F (2010) HNE-protein adducts formation in different pre-carcinogenic stages of hepatitis in LEC rats. Free Radic Res 44:119–127PubMedCrossRefGoogle Scholar
  85. Miller AC, McClain D (2007) A review of depleted uranium biological effects: in vitro and in vivo studies. Rev Environ Health 22:75–89PubMedCrossRefGoogle Scholar
  86. Misra M, Olinski R, Dizdaroglu M, Kasprzak KS (1993) Enhancement by l-histidine of nickel(II)-induced DNA–protein cross-linking and oxidative DNA base damage in the rat kidney. Chem Res Toxicol 6:33–37PubMedCrossRefGoogle Scholar
  87. Mosammaparast N, Shi Y (2010) Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79:155–179PubMedCrossRefGoogle Scholar
  88. Myers JM, Antholine WE, Myers CR (2008) Hexavalent chromium causes the oxidation of thioredoxin in human bronchial epithelial cells. Toxicology 246:222–233PubMedCrossRefGoogle Scholar
  89. Mylonas M, Malandrinos G, Plakatouras J, Hadjiliadis N, Kasprzak KS, Krezel A, Bal W (2001) Stray Cu(II) may cause oxidative damage when coordinated to the C-terminal tail of histone H2A. Chem Res Toxicol 14:1177–1183PubMedCrossRefGoogle Scholar
  90. Nackerdien Z, Kasprzak KS, Rao G, Halliwell B, Dizdaroglu M (1991) Nickel(II)- and cobalt(II)-dependent damage by hydrogen peroxide to the DNA bases in isolated human chromatin. Cancer Res 51:5837–5842PubMedGoogle Scholar
  91. Nair J, Barbin A, Velic I, Bartsch H (1999) Etheno DNA-base adducts from endogenous reactive species. Mutat Res 424:59–69PubMedCrossRefGoogle Scholar
  92. Nakabeppu Y (2001) Molecular genetics and structural biology of human MutT homolog, MTH1. Mutat Res 477:59–70PubMedCrossRefGoogle Scholar
  93. Nakamura T, Meshitsuka S, Kitagawa S, Abe N, Yamada J, Ishino T, Nakano H, Tsuzuki T, Doi T, Kobayashi Y, Fujii S, Sekiguchi M, Yamagata Y (2010) Structural and dynamic features of the MutT protein in the recognition of nucleotides with the mutagenic 8-oxoguanine base. J Biol Chem 285:444–452PubMedCrossRefGoogle Scholar
  94. Nassi-Calò L, Mello-Filho C, Meneghini R (1989) o-phenanthroline protects mammalian cells from hydrogen peroxide-induced gene mutation and morphological transformation. Carcinogenesis 10:1055–1057PubMedCrossRefGoogle Scholar
  95. Ngu TT, Stillman MJ (2009) Metalation of metallothioneins. IUBMB Life 61:438–446PubMedCrossRefGoogle Scholar
  96. Nordberg M (1998) Metallothioneins: historical review and state of knowledge. Talanta 46:243–254PubMedCrossRefGoogle Scholar
  97. Oskarsson A, Anderssonm Y, Tjälve H (1979) Fate of nickel subsulfide during carcinogenesis studied by autoradiography and X-ray powder diffraction. Cancer Res 39:4175–4182PubMedGoogle Scholar
  98. Petit A, Mwale F, Tkaczyk C, Antoniou J, Zukor DJ, Huk OL (2006) Cobalt and chromium ions induce nitration of proteins in human U937 macrophages in vitro. J Biomed Mater Res A 79:599–605PubMedGoogle Scholar
  99. Porter DW, Yakushiji H, Nakabeppu Y, Sekiguchi M, Fivash MJ Jr, Kasprzak KS (1997) Sensitivity of Escherichia coli (MutT) and human (MTH1) 8-oxo-dGTPases to in vitro inhibition by the carcinogenic metals, nickel(II), copper(II), cobalt(II) and cadmium(II). Carcinogenesis 18:1785–1791PubMedCrossRefGoogle Scholar
  100. Rana SV (2008) Metals and apoptosis: recent developments. J Trace Elem Med Biol 22:262–284PubMedCrossRefGoogle Scholar
  101. Randerath K, Randerath E, Smith CV, Jian C (1996) Structural origins of bulky oxidative DNA adducts (type II I-compounds) as deduced by oxidation of oligonucleotides of known sequence. Chem Res Toxicol 9:247–254PubMedCrossRefGoogle Scholar
  102. Requena JR, Chao C-C, Levine LR, Stadtman ER (2001a) Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci U S A 98:69–74CrossRefGoogle Scholar
  103. Requena JR, Groth D, Legname G, Stadtman ER, Prusiner SB, Levine RL (2001b) Copper-catalyzed oxidation of the recombinant Sha(29-231) prion protein. Proc Natl Acad Sci U S A 98:7170–7175CrossRefGoogle Scholar
  104. Robbiano L, Baroni D, Novello L, Brambilla G (2006) Correlation between induction of DNA fragmentation in lung cells from rats and humans and carcinogenic activity. Mutat Res 605:94–102PubMedCrossRefGoogle Scholar
  105. Rodriguez H, Holmquist GP, D’Agostino R Jr, Keller J, Akman SA (1997) Metal ion-dependent hydrogen peroxide-induced DNA damage is more sequence specific than metal specific. Cancer Res 57:2394–2403PubMedGoogle Scholar
  106. Salnikow K, Costa M (2000) Epigenetic mechanisms of nickel carcinogenesis. J Environ Pathol Toxicol Oncol 19:307–318PubMedGoogle Scholar
  107. Salnikow K, Kasprzak KS (2005) Ascorbate depletion: a critical step in nickel carcinogenesis? Environ Health Perspect 113:577–584PubMedCrossRefGoogle Scholar
  108. Salnikow K, Kasprzak KS (2007) Nickel-dependent gene expression. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in life sciences: nickel and its surprising impact in nature, vol 2. Wiley, ChichesterGoogle Scholar
  109. Salnikow K, Zhitkovich A (2008) Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic and chromium. Chem Res Toxicol 21:28–44PubMedCrossRefGoogle Scholar
  110. Salnikow K, Donald S, Bruick R, Zhitkovich A, Phang J, Kasprzak KS (2004) Depletion of intracellular ascorbate by carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 279:40337–40344PubMedCrossRefGoogle Scholar
  111. Saplakoğlu U, Işcan M, Işcan M (1997) DNA single-strand breakage in rat lung, liver and kidney after single and combined treatments of nickel and cadmium. Mutat Res 394:133–140PubMedCrossRefGoogle Scholar
  112. Sedgwick B (2004) Repairing DNA methylation damage. Nat Rev Mol Cell Biol 5:148–157PubMedCrossRefGoogle Scholar
  113. Shi XG, Sun XL, Gannett PM, Dalal NS (1992) Deferoxamine inhibition of Cr(V)-mediated radical generation and deoxyguanine hydroxylation: ESR and HPLC evidence. Arch Biochem Biophys 293:281–286PubMedCrossRefGoogle Scholar
  114. Shi X, Dalal NS, Kasprzak KS (1993) Generation of free radicals of hydrogen peroxide and lipid hydroperoxides in the presence of Cr(III). Arch Biochem Biophys 302:294–299PubMedCrossRefGoogle Scholar
  115. Shi X, Dalal NS, Kasprzak KS (1994) Enhanced generation of hydroxyl and sulfur trioxide anion radicals from oxidation of sodium sulfite, nickel(II) sulfite, and nickel subsulfide in the presence of nickel(II) complexes. Environ Health Perspect 102(Suppl 3):91–96PubMedCrossRefGoogle Scholar
  116. Sigel H (1974) Metal ions and hydrogen peroxide. XXIX. On the kinetics and mechanism of the catalase-like activity of nickel(II) and nickel(II) amine complexes. J Coord Chem 3:235–247CrossRefGoogle Scholar
  117. Singh J, Bridgewater LC, Patierno SR (1998) Differential sensitivity of chromium-mediated DNA interstrand crosslinks and DNA–protein crosslinks to disruption by alkali and EDTA. Toxicol Sci 45:72–76PubMedGoogle Scholar
  118. Stadtman ER (1993) Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem 62:797–821PubMedCrossRefGoogle Scholar
  119. Stadtman ER, Berlett BS (1991) Fenton chemistry: amino acid oxidation. J Biol Chem 266:17201–17211PubMedGoogle Scholar
  120. Stadtman ER, Berlett BS (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10:485–494PubMedCrossRefGoogle Scholar
  121. Standeven AM, Wetterhahn KE (1991) Is there a role for reactive oxygen species in the mechanism of chromium(VI) carcinogenesis? Chem Res Toxicol 4:616–625PubMedCrossRefGoogle Scholar
  122. Sugden KD, Stearns DM (2000) The role of chromium(V) in the mechanism of chromate-induced oxidative DNA damage and cancer. J Environ Pathol Toxicol Oncol 19:215–230PubMedGoogle Scholar
  123. Sunderman FW Jr (1986) Metals and lipid peroxidation. Acta Pharmacol Toxicol 59(Suppl 7):248–255Google Scholar
  124. Tkeshelashvili LK, Reid TM, McBride TJ, Loeb LA (1993) Oxidative damage in carcinogenesis. Nickel induces a signature mutation for oxygen free radical damage. Cancer Res 53:4172–4174PubMedGoogle Scholar
  125. Toyokuni S (2009) Role of iron in carcinogenesis: cancer as a ferrotoxic disease. Cancer Sci 100:9–16PubMedCrossRefGoogle Scholar
  126. Umemura T, Sai K, Takagi A, Hasegawa R, Kurokawa Y (1990) Formation of 8-hydroxydeoxyguanosine (8-OH-dG) in rat kidney DNA after intraperitoneal administration of ferric nitrilotriacetate (Fe-NTA). Carcinogenesis 11:345–347PubMedCrossRefGoogle Scholar
  127. Umemura T, Sai K, Takagi A, Hasegawa R, Kurokawa Y (1991) The effects of exogenous glutathione and cysteine on oxidative stress induced by ferric nitrilotriacetate. Cancer Lett 58:49–56PubMedCrossRefGoogle Scholar
  128. Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160:1–40PubMedCrossRefGoogle Scholar
  129. Valverde M, Fortoul TI, Díaz-Barriga F, Mejia J, del Castillo ER (2000) Induction of genotoxicity by cadmium chloride inhalation in several organs of CD-1 mice. Mutagenesis 15:109–114PubMedCrossRefGoogle Scholar
  130. Valverde M, Trejo C, Rojas E (2001) Is the capacity of lead acetate and cadmium chloride to induce genotoxic damage due to direct DNA–metal interaction? Mutagenesis 16:265–270PubMedCrossRefGoogle Scholar
  131. Wei H-J, Luo X-M, Yang SP (1985) Effects of molybdenum and tungsten on mammary carcinogenesis in SD rats. J Natl Cancer Inst 74:469–473PubMedGoogle Scholar
  132. West JD, Marnett LJ (2005) Alterations in gene expression induced by the lipid peroxidation product, 4-hydroxy-2-nonenal. Chem Res Toxicol 18:1642–1653PubMedCrossRefGoogle Scholar
  133. Wetterhahn KE, Hamilton JW, Aiyar J, Borges KM, Floyd R (1989) Mechanisms of chromium(VI) carcinogenesis. Reactive intermediates and effect on gene expression. Biol Trace Elem Res 21:405–411PubMedCrossRefGoogle Scholar
  134. Wild P, Bourgkard E, Paris C (2009) Lung cancer and exposure to metals: the epidemiological evidence. Methods Mol Biol 472:139–167PubMedCrossRefGoogle Scholar
  135. Witkiewicz-Kucharczyk A, Bal W (2006) Damage of zinc fingers in DNA repair proteins, a novel molecular mechanism in carcinogenesis. Toxicol Lett 162:29–42PubMedCrossRefGoogle Scholar
  136. Wu B, Davey CA (2010) Using soft X-rays for a detailed picture of divalent metal binding in the nucleosome. J Mol Biol 398:633–640PubMedCrossRefGoogle Scholar
  137. Xu A, Wu L-J, Santella RM, Hei TK (1999) Role of oxyradicals in mutagenicity and DNA damage induced by crocidolite asbestos in mammalian cells. Cancer Res 59:5922–5926PubMedGoogle Scholar
  138. Zoroddu MA, Kowalik-Jankowska T, Kozlowski H, Molinari H, Salnikow K, Broday L, Costa M (2000) Interaction of Ni(II) and Cu(II) with a metal binding sequence of histone H4: AKRHRK, a model of the H4 tail. Biochim Biophys Acta 1475:163–168PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Laboratory of Comparative CarcinogenesisNational Cancer Institute at FrederickFrederickUSA

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