Role of oxidative damage in the genotoxicity of arsenic

Free Radical Biology and Medicine

Volumn 37, Issue 5, 2004, Pages 574-581

  Hei, Tom K ^a,b   Filipic, Metka ^c  

^a Columbia University 10032 ^*  (United States)

^b Dept Genetic Toxicol Cancer Biol ^*  (United States)

^c NATIONAL INSTITUTE OF BIOLOGY   (Slovenia)

Author keywords

Arsenite; Free radicals; Multilocus mutation; Reactive nitrogen species; Reactive oxygen species

Indexed keywords

ANTIOXIDANT; ARSENIC; CARCINOGEN; CATALASE; MUTAGENIC AGENT; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ARSENIC POISONING; BACTERIAL CELL; BACTERIAL MUTATION; BLADDER CANCER; CANCER; CANCER INCIDENCE; CELL ASSAY; CHEMICAL MODEL; CHROMOSOME ABERRATION; ENVIRONMENT; GENE DELETION; GENE LOCUS; GENE MUTATION; GENOTOXICITY; HUMAN; KERATOSIS; KIDNEY CANCER; LIVER CANCER; LIVER INJURY; LUNG CANCER; MAMMAL CELL; NONHUMAN; OXIDATION; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; REVIEW; SKIN CANCER; TUMOR; WATER CONTAMINATION; X CHROMOSOME;

APOPTOSIS; HUMANS; METALS; NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 3342896731     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2004.02.003     Document Type: Review

References (85)

1. Leonard A., Lauwerys R.R. Carcinogenicity, teratogenicity, and mutagenicity of arsenic. Mutat. Res. 75:1980;49-62
2. Chapell W.R., Beck B.D., Brown K.G., Chaney R., Cothern R., Irgolic K.L., North D.W., Thornton I., Tsongas T.A. Inorganic arsenic: a need and an opportunity to improve risk assessment. Environ. Health Perspect. 105:1997;1060-1067
3. U.S. EPA, Soil Screening Guidance Technical Background Document. Office of Solid Waste and Emergency Response. EPA/540/R-95/128. Washington, DC: U.S. Environmental Protection Agency; 1996.
4. Barrett J.C., Lamb P.W., Wang T.C., Lee T.C. Mechanisms of arsenic induced cell transformation. Biol. Trace Element Res. 21:1989;421-429
5. Chowdhury U.K., Biswas B.K., Chowdhury T.R., Samanta G., Mandal B.K., Basu G.C., Chanda C.R., Lodh D., Saha K.C., Mukherjee S.K., Roy S., Kabir S., Quamruzzaman Q., Chakraborti D. Ground water arsenic contamination in Bangladesh and West Bengal, India. Environ. Health Perspect. 108:2000;393-397
6. Nickson R., McArthur J., Burgess W., Ahmed K.M., Ravenscroft P., Rahman M. Arsenic poisoning of Bangladesh groundwater. Nature. 395:1998;338
7. Dhar R.K., Biswas B.K., Samanta G., Mandal B.K., Chakraborti D., Roy S., Jafar A., Islam A., Ara G., Kabir S., Khan A.W., Ahmed S.A., Hadi S.A. Groundwater arsenic calamity in Bangladesh. Cur. Sci. 73:1997;48-59
8. Chan P.C., Huff J. Arsenic carcinogenesis in animals and in humans: mechanistic, experimental and epidemiological evidence. Environ. Carcinogen. Ecotoxicol. Rev. 15:1997;83-122
9. Warner M.L., Moore L.E., Smith M.T., Kalman D.A., Fanning E., Smith A.H. Increased micronuclei in exofoliated bladder cells of individuals who chronically ingested arsenic-contaminated water in Nevada. Cancer Epidemiol. Biomarkers Prevent. 3:1994;583-590
10. Xuan X.Z., Lubin J.H., Li J.Y., Yang L.F., Lou A.S., Lan Y., Wang J.Z., Blot W. A cohort study in Southern China of tin miners exposed to radon and radon decay products. Health Phys. 64:1993;120-131
11. Monograph on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Suppl. 4. 1982;50-51 IARC, Lyon
12. Huff J., Chan P., Nyska A. Is the human carcinogen arsenic carcinogenic to laboratory animals. Toxicol. Sci. 55:2000;17-23
13. Wei M., Wanibuchi H., Morimura K., Iwai S., Yoshida K., Endo G., Nakae D., Fukushima S. Carcinogenicity of dimethylarsinic acid in male F344 rats and genetic alterations in induced urinary bladder tumors. Carcinogenesis. 23:2001;1387-1397
14. Yamanaka K., Takabayashi F., Mizoi M., An Y., Hasegawa A., Okada S. Oral exposure of dimethylarsinic acid, a main metabolite of inorganic arsenic, in mice leads to an increase in 8-oxo-2′-deoxyguanosine level, specially in the target organs for arsenic carcinogenesis. Biochem. Biophys. Res. Commun. 287:2001;66-70
15. Petrick J.S., Ayala-Fierro F., Cullen W.R., Carter D.E., Aposhian H.V. Monomethylarsonous acid is more toxic than arsenite in Chang human hepatocytes. Toxicol. Appl. Pharmacol. 163:2000;203-207
16. Wang Z., Rossman T.G. The carcinogenicity of arsenic. Chang T. Toxicology of Metals. 1996;221-229 CRC Press, Boca Raton, FL
17. Lee T.C., Ko J.L., Jan K.Y. Differential cytotoxicity of sodium arsenite in human fibroblasts and CHO cells. Toxicology. 56:1989;289-299
18. Simeonova P.P., Luster M.I. Mechanisms of arsenic carcinogenicity: genetic or epigenetic mechanisms? J. Environ. Pathol. Toxicol. Oncol. 19:2000;281-286
19. Lee T.C., Oshimura M., Barrett J.C. Comparison of arsenic induced cell transformation, cytotoxicity, mutation and cytogenetic effects in Syrian hamster embryo cells in culture. Carcinogenesis. 6:1985;1421-1426
20. 3H 1OT1/2 and diploid human fibroblasts by unique carcinogenic, non-mutagenic metal compounds. Biol. Trace Element Res. 21:1989;459-467
21. Rossman T.G., Stone D., Molina M., Troll W. Absence of arsenite mutagenicity in E. coli and Chinese hamster cells. Environ. Mutagen. 2:1980;371-379
22. Zhao C.Q., Young M.R., Diwan B.A., Coogan T.P., Waalkes M.P. Association of arsenic induced malignant transformation with DNA methylation and aberrant gene expression. Proc. Natl. Acad. Sci. USA. 94:1997;10907-10912
23. Lynn S., Lai H.T., Gurr G.R., Jan K.Y. Arsenite retards DNA break rejoining by inhibiting DNA ligation. Mutagenesis. 12:1997;353-358
24. Nakamuro K., Sayato Y. Comparative studies of chromosomal aberrations induced by trivalent and pentavalent arsenic. Mutat. Res. 88:1981;73-80
25. Kochhar T.S., Howard W., Hoffman S., Brammer-Carleton L. Effect of trivalent and pentavalent arsenic in causing chromosomal alterations in cultured Chinese hamster ovary cells. Toxicol. Lett. 84:1996;37-42
26. Hei T.K., Liu S.X., Waldren C.A. Mutagenicity of arsenic in mammalian cells: role of reactive oxygen species. Proc. Natl. Acad. Sci. USA. 95:1998;8103-8107
27. Liu S.X., Athar M., Lippai I., Waldren C.A., Hei T.K. Induction of oxyradicals by arsenic: implications for mechanisms of genotoxicity. Proc. Natl. Acad. Sci. USA. 98:2001;1643-1648
28. - mutant lymphocytes in a population of copper roasters in Antofagasta, Chile: a pilot study. Mutat. Res. 431:1999;247-257
29. Thilly W.G. Dead cells don't form mutant colonies: a serious source of bias in mutation assays. Environ. Mutagen. 7:1985;255-258
30. Yamada Y., Park M.S., Okinaka R.T., Chen D.J. Molecular analysis and comparison of radiation-induced large deletions of the HPRT locus in primary human skin fibroblasts. Radiat. Res. 145:1996;481-490
31. + and ATP binding sites of the ouabain complexed-ATPase: implications for the mechanism of ouabain action. Prog. Clin. Biol. Res. 268:1988;211-218
32. Wiencke J.K., Yager J.W., Varkonyi A., Hultner M., Lutze L.H. Study of arsenic mutagenesis using the plasmid shuttle vector pZ189 propagated in DNA repair proficient human cells. Mutat. Res. 386:1997;335-344
33. Helleday T., Nilsson R., Jenssen D. Arsenic(III) and heavy metal ions induce intrachromosomal homologous recombination in the hprt gene of V79 Chinese hamster ovary cells. Environ. Mol. Mutagen. 35:2000;114-122
34. LeBel C.P., Ischiropoulos H., Bondy S.C. Evaluation of the probe 2′,7′-dichlorofluorescein as an indicator of reactive oxygen species formation and oxidative stress. Chem. Res. Toxicol. 5:1992;227-231
35. Szejda P., Parce J'W., Seeds M.S., Bass D.A. Flow cytometric quantification of oxidative product formation by polymorphonuclear leukocytes during phagocytosis. J. Immunol. 133:1984;3303-3307
36. Hahn S.M., Krishna M.C., DeLuca A.M., Coffin D., Mitchell J.B. Evaluation of the hydroxylamine Tempol-H as an in vivo radioprotector. Free Radic. Biol. Med. 28:2000;953-958
37. Meister A., Anderson M.E. Glutathione. Annu. Rev. Biochem. 52:1983;711-760
38. Xu A., Wu L.J., Santella R., Hei T.K. Role of reactive oxygen species in the mutagenicity and DNA damage induced by crocidolite fibers in mammalian cells. Cancer Res. 59:1999;5615-5624
39. Hei T.K., Geard C.R., Hall E.J. Effects of cellular non-protein sulfhydryl depletion in radiation induced oncogenic transformation and genotoxicity in mouse 10T1/2 cells. Int. J. Radiat. Oncol. Biol. Phys. 10:1984;1255-1259
40. Liu L., Trimarchi J.R., Navarro P., Blasco M.A., Keefe D.L. Oxidative stress contributes to arsenic induced telomere attrition, chromosomal instability and apoptosis. J. Biol. Chem. 278:2003;31998-32004
41. Deneke S.M. Induction of cysteine transport in bovine pulmonary artery endothelial cells by sodium arsenite. Biochim. Biophys. Acta. 1109:1992;127-131
42. Engel R.R., Hopenhayn-Rich C., Receveur O., Smith A.H. Vascular effects of chronic arsenic exposure. Epidemiol. Res. 16:1994;184-208
43. Barchowsky A., Dudek E.J., Treadwell M.D., Wetterhahn K.E. Arsenic induces oxidant stress and NF-kappa B activation in cultured aortic endothelial cells. Free Radic. Biol. Med. 21:1996;783-790
44. Imlay J.A., Linn S. DNA damage and oxygen radical toxicity. Science. 240:1988;1302-1309
45. Kessel M., Liu S.X., Xu A., Santella R., Hei T.K. Arsenic induces oxidative DNA damage in mammalian cells. Mol. Cell. Biochem. 234:2002;301-308
46. Wang T.S., Huang H. Active oxygen species are involved in the induction of micronuclei by arsenite in XRS-5 cells. Mutagenesis. 9:1994;253-257
47. Applegate L.A., Luscher P., Tyrrell R.M. Induction of heme oxygenase: a general response of oxidant stress in cultured mammalian cells. Cancer Res. 51:1991;974-978
48. Nordenson I., Beckman L. Is the genotoxic effect of arsenic mediated by oxygen free radicals. Hum. Hered. 41:1991;71-73
49. Matsui M., Nishigori C., Toyokuni S., Takada J., Akaboshi M., Ishihawa M., Imamura S., Miyachi Y. The role of oxidative DNA damage in human arsenic carcinogenesis: detection of 8-OhdG in arsenic related Bowen's disease. J. Invest. Dermatol. 113:1999;26-31
50. Wanibuchi H., Hori T., Meenakshi V., Ichihara T., Yamamoto S., Yano Y., Otani S., Nakae D., Konishi Y., Fukushima S. Promotion of rat hepatocarcino-genesis by dimethylarsinic acid: association with elevated ornithine decarboxylase activity and formation of 8-hydroxydeoxyguanosine in the liver. Jpn. J. Cancer Res. 88:1997;1149-1154
51. Le X.C., Lu X., Ma M., Cullen W.R., Aposhian H.V., Zheng B. Speciation of key arsenic metabolic intermediates in human urine. Anal. Chem. 72:2000;5172-5177
52. Styblo M., Delnomdedieu M., Thomas D.J. Mono- and dimethylation of arsenic in rat liver cytosol in vitro. Chem. Biol. Interact. 99:1996;147-164
53. Wagner S.L., Weswig P. Arsenic in blood and urine of forest workers as indices of exposure to cacodylic acid. Arch. Environ. Health. 28:1974;77-79
54. Moore M.M., Harrington-Brock K., Doerr C.L. Relative genotoxic potency of arsenic and its methylated metabolites. Mutat. Res. 386:1997;279-290
55. Andrewes P., Kitchin K.T., Wallace K. Dimethyarsine and trimethylarsine are potent genotoxins in vitro. Chem. Res. Toxicol. 16:2003;994-1003
56. Le X.C., Ma M., Cullen W.R., Aposhian H.V., Lu X., Zheng B. Determination of monomethylarsonous acid, a key arsenic methylation intermediate in human urine. Environ. Health Perspect. 108:2000;1015-1018
57. Nesnow S., Roop B.C., Lambert G., Kadiiska M., Mason R., Cullen W.R., Mass M.J. DNA damage induced by methylated trivalent arsenicals is mediated by reactive oxygen species. Chem. Res. Toxicol. 15:2002;1627-1634
58. Maiti S., Chatterjee A.K. Differential response of cellular antioxidant mechanism of liver and kidney to arsenic exposure and its relation to dietary protein deficiency. Environ. Toxicol. Pharmacol. 8:2000;227-235
59. Ramanathan K., Shila S., Kumaran S., Panneerselvam C. Ascorbic acid and alpha-tocopherol as potent modulators on arsenic induced toxicity in mitochondria. J. Nutr. Biochem. 14:2003;416-420
60. Pi J., Yamauchi H., Kumagai Y., Sun G., Yoshida T., Aikawa H., Hopenhayn-Rich C., Shimojo N. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environ. Health Perspect. 110:2002;331-336
61. Lin T.H., Huang Y.L., Tseng W.C. Arsenic and lipid peroxidation in patients with blackfoot disease. Bull. Environ. Contam. Toxicol. 54:1995;488-493
62. Smith K.R., Klei L.R., Barchowsky A. Arsenite stimulates plasma membrane NADPH oxidase in vascular endothelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 280:2001;442-449
63. Oller A.R., Thilly W.G. Mutation spectra in human B-cells: spontaneous, oxygen and hydrogen peroxide induced mutations at the hprt gene. J. Mol. Biol. 228:1992;813-826
64. Moody C.S., Hassan H.M. Mutagenicity of oxygen free radicals. Proc. Natl. Acad. Sci. USA. 79:1982;2855-2859
65. Hsie A.W., Xu W., Yu Y., Sognier M.A., Hrelia P. Molecular analysis of reactive oxygen species induced mammalian gene mutation. Teratogen. Carcinogen. Mutagen. 10:1990;115-124
66. Oya Y., Yamamoto K., Tonomura A. The biological activity of hydrogen peroxide: induction of chromosome type aberrations susceptible to inhibition by scavengers of hydroxyl radicals in human embryonic fibroblasts. Mutat. Res. 172:1986;245-253
67. Kruszewski M., Szumei I. DNA damage induced by hydrogen peroxide treatment at 4 degree and 37 degrees C in murine lymphoma L5178Y sublines. Acta Biochem. Pol. 41:1994;120-121
68. Evans H.H., Mencl J., Jorng M.F., Ricanati M., Sanches C., Hozier J. Locus specificity in the mutability of L5178 mouse lymphoma cells: the role of multilocus lesions. Proc. Natl. Acad. Sci USA. 83:1986;4379-4383
69. Evans H.H. Failla Memorial Lecture: the prevalence of multilocus lesions in radiation induced mutants. Radiat. Res. 137:1994;131-144
70. Meng Z., Hsie A.W. Polymerase chain reaction based deletion analysis of spontaneous and arsenite enhanced gpt mutants in CHO-AS52 cells. Mutat. Res. 356:1996;255-259
71. Chance N., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59:1979;527-605
72. Miller W.H. Jr., Hyman M.S., Lee J.S., Singer J., Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 62:2002;3893-3903
73. Shen Z.Y., Shen W.Y., Chen M.H., Shen J., Cai W.J., Zeng Y. The alteration of mitochondria is an early event of arsenic trioxide induced apoptosis in esophageal carcinoma cells. Int. J. Mol. Med. 9:2000;385-390
74. Shen Z.X., Chen G.Q., Ni J.H., Li X.S., Xiong S.M., Qiu Q.Y., Zhu J., Tang W., Sun G.L., Yang K.Q., Chen Y., Zhou L., Fang Z.W., Wang Y.T., Ma J., Zhang P., Zhang T.D., Chen S.J., Chen Z., Wang Z.Y. Use of arsenic trioxide in the treatment of acute promyelocytic leukemia: II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood. 89:1997;3354-3360
75. Larochette N., Decaudin D., Jacotot E., Brenner C., Marzo I., Susin S.A., Zamzami N., Xie Z., Reed J., Kroemer G. Arsenic induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Exp. Cell Res. 249:1999;413-421
76. Woo S.H., Park I.C., Park M.J., Lee H.C., Lee S.J., Chun U.L., Lee S.H., Hong S., Rhee C.H. Arsenic trioxide induces apoptosis through a reactive oxygen species dependent pathway and loss of mitochondrial membrane potential in HeLa cells. Int. J. Oncol. 21:2002;57-63
77. Kao Y.H., Yu C.L., Chang L.W., Yu H.S. Low concentrations of arsenic induce vascular endothelial growth factor and nitric oxide release and stimulate angiogenesis in vitro. Chem. Res. Toxicol. 16:2003;460-468
78. Yuan S.S., Hou M.F., Chang H.L., Chan T.F., Wu Y.H., Wu Y.C., Su J.H. Arsenic induced nitric oxide generation is cell cycle dependent and aberrant in NBS cells. Toxicol. In Vitro. 17:2003;139-143
79. Lymer S., Hurst J.K. Rapid reaction between peroxynitrite ion and carbon dioxide: implications for biological activity. J. Am. Chem. Soc. 117:1995;8867-8868
80. Klotz L., Schroeder P., Sies H. Peroxynitrite signaling: receptor tyrosine kinases and activation of stress responsive pathways. Free Radic. Biol. Med. 33:2002;737-743
81. Minetti M., Mallozzi C., Michela Di Stasi A.M. Peroxynitrite activates kinases of the src family and upregulates tyrosine phosphorylation signaling. Free Radic. Biol. Med. 33:2002;744-754
82. Radi R., Peluffo G., Alvarez M.N., Naviliat M., Cayota A. Unraveling peroxynitrite formation in biological systems. Free Radic. Biol. Med. 30:2001;463-488
83. Lee M.Y., Jung B.I., Seung M.C., Bae O.N., Lee J.Y., Park J.D., Yang J.S., Lee H., Chung J.H. Arsenic induced dysfunction in relaxation of blood vessels. Environ. Health Perspect. 111:2003;513-517
84. Ahmad S., Kitchin K.T., Cullen W.R. Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch. Biochem. Biophys. 382:2000;195-202
85. Li J.M., Shah A.M. ROS generation by non-phagocytic NADPH oxidase: potential relevance in diabetic nephropathy. J. Am. Soc. Nephrol. 14:2003;S221-S226