Requirement of arsenic biomethylation for oxidative DNA damage

Journal of the National Cancer Institute

Volumn 101, Issue 24, 2009, Pages 1670-1681

  Kojima, Chikara ^a   Ramirez, Dario C ^a   Tokar, Erik J ^a   Himeno, Seiichiro ^b   Drobná, Zuzana ^c   Stýblo, Miroslav ^c   Mason, Ronald P ^a   Waalkes, Michael P ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^c IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; ARSENITE SODIUM; DNA; GELATINASE A; GELATINASE B; SODIUM SELENITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INVASION; COLONY FORMATION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; ENZYME RELEASE; EPITHELIUM CELL; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; METHYLATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL;

ANIMALS; ARSENIC; ARSENITES; CARCINOGENS; CELLS, CULTURED; DNA DAMAGE; DNA METHYLATION; ENZYME INHIBITORS; EPITHELIAL CELLS; HUMANS; LIVER; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; METHYLTRANSFERASES; NEOPLASMS, EXPERIMENTAL; OXIDATIVE STRESS; PHENOTYPE; POLYMORPHISM, GENETIC; PROSTATE; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SODIUM COMPOUNDS; SODIUM SELENITE; SPIN TRAPPING; TIME FACTORS; URINARY BLADDER;

EID: 72649102951     PISSN: 00278874     EISSN: 14602105     Source Type: Journal    
DOI: 10.1093/jnci/djp414     Document Type: Article

References (51)

1. International Agency for Research on Cancer (IARC). Arsenic in Drinking Water. International Agency for Research on Cancer Monographs on the Evaluation of Carcinogenic Risk to Humans. Vol.84. Lyon, France:IARC Press; 2004:269-477.
2. National Research Council. Arsenic in Drinking Water. Washington, DC:National Academy Press; 1999.
3. Achanzar WE. Brambila EM. Diwan BA. Webber MM. Waalkes MP. Inorganic arsenite-induced malignant transformation of human prostate epithelial cells. J Natl Cancer Inst. 2002; 94(34):1888-1891.
4. Sens DA. Park S. Gurel V. Sens MA. Garrett SH. Somji S. Inorganic cadmium-and arsenic-induced malignant transformation of human bladder epithelial cells. Toxicol Sci. 2004; 79(3):56-63.
5. Bredfeldt TG. Jagadish B. Eblin KE. Mash EA. Gandolfi AJ. Monomethylarsonous acid induces transformation of human bladder cells. Toxicol Appl Pharmacol. 2006; 216(3):69-79.
6. Pi J. He Y. Bortner C. et al. Low level, long-term inorganic arsenite exposure causes generalized resistance to apoptosis in cultured human kerati-nocytes:potential role in skin co-carcinogenesis. Int J Cancer. 2005; 116(3):20-26.
7. Zhao CQ. Young MR. Diwan BA. Coogan TP. Waalkes MP. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci U S A. 1997; 94(30):10907-10912.
8. Hayakawa T. Kobayashi Y. Cui X. Hirano S. A new metabolic pathway of arsenite:arsenite-glutathione complexes are substrates for human arsenic methyltransferase Cyt19. Arch Toxicol. 2005; 79(3):183-191.
9. Thomas DJ. Li J. Waters SB. et al. Arsenic (+3 oxidation state) methyl-transferase and the methylation of arsenicals. Exp Biol Med. 2007; 232(3):3-13.
10. Waters SB. Devesa V. Del Razo LM. Styblo M. Thomas DJ. Endogenous reductants support catalytic function of recombinant rat cyt19, an arsenic methyltransferase. Chem Res Toxicol. 2004; 17(3):404-409.
11. Sakurai T. Kaise T. Matsubara C. Inorganic and methylated arsenic compounds induce cell death in murine macrophages via different mechanisms. Chem Res Toxicol. 1998; 11(3):273-283.
12. Sakurai T. Qu W. Sakurai MH. Waalkes MP. A major human arsenic metabolite, dimethylarsinic acid, requires reduced glutathione to induce apoptosis. Chem Res Toxicol. 2002; 15(3):629-637
13. Gomez SE. del Razo LM. Munoz Sanchez JL. Induction of DNA damage by free radicals generated either by organic or inorganic arsenic (AsIII, MMAIII, and DMAIII) in cultures of B and T lymphocytes. Biol Trace Elem Res. 2006; 108(3-3):115-126.
14. Kojima C. Qu W. Waalkes MP. Himeno S. Sakurai T. Chronic exposure to methylated arsenicals stimulates arsenic excretion pathways and induces arsenic tolerance in rat liver cells. Toxicol Sci. 2006; 91(3):70-81.
15. Kojima C. Sakurai T. Waalkes MP. Himeno S. Cytolethality of gluta-thione conjugates with monomethylarsenic or dimethylarsenic compounds. Biol Pharm Bull. 2005; 28(30):1827-1832.
16. Mass MJ. Tennant A. Roop BC. et al. Methylated trivalent arsenic species are genotoxic. Chem Res Toxicol. 2001; 14(3):355-361.
17. Sakurai T. Kojima C. Kobayashi Y. et al. Toxicity of a trivalent organic arsenic compound, dimethylarsinous glutathione in a rat liver cell line (TRL 1215). Br J Pharmacol. 2006; 149(3):888-897.
18. Styblo M. del Razo LM. Vega L. et al. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol. 2000; 74(3):289-299.
19. Petrick JS. Ayala-Fierro F. Cullen WR. Carter DE. Vasken Aposhian H. Monomethylarsonous acid (MMA(III)) is more toxic than arsenite in Chang human hepatocytes. Toxicol Appl Pharmacol. 2000; 163(3):203-207.
20. Nakamuro K. Sayato Y. Comparative studies of chromosomal aberration induced by trivalent and pentavalent arsenic. Mutat Res. 1981; 88(3):73-80.
21. Rossman TG. Mechanism of arsenic carcinogenesis:an integrated approach. Mutat Res. 2003; 533(3-2):37-65.
22. Hei TK. Filipic M. Role of oxidative damage in the genotoxicity of arsenic. Free Radic Biol Med. 2004; 37(3):574-581.
23. Eblin KE. Bowen ME. Cromey DW. et al. Arsenite and monomethylar-sonous acid generate oxidative stress response in human bladder cell culture. Toxicol Appl Pharmacol. 2006; 217(3):7-14.
24. Yamauchi H. Aminaka Y. Yoshida K. Sun G. Pi J. Waalkes MP. Evaluation of DNA damage in patients with arsenic poisoning:urinary 8-hydroxydeoxyguanine. Toxicol Appl Pharmacol. 2004; 198(3):291-296.
25. Collins AR. Cadet J. Möller L. Poulsen HE. Viña J. Are we sure we know how to measure 8-oxo-7,8-dihydroguanine in DNA from human cells? Arch Biochem Biophys. 2004; 423(3):57-65.
26. Halliwell B. Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture:how should you do it and what do the results mean? Br J Pharmacol. 2004; 142(3):231-255.
27. Ramirez DC. Mejiba SE. Mason RP. Immuno-spin trapping of DNA radicals. Nat Methods. 2006; 3(3):123-127.
28. Ramirez DC. Gomez-Mejiba SE. Mason RP. Immuno-spin trapping analyses of DNA radicals. Nat Protoc. 2007; 2(3):512-522.
29. Benbrahim-Tallaa L. Waterland RA. Styblo M. Achanzar WE. Webber MM. Waalkes MP. Molecular events associated with arsenic-induced malignant transformation of human prostatic epithelial cells:aberrant genomic DNA methylation and K-ras oncogene activation. Toxicol Appl Pharmacol. 2005; 206(3):288-298.
30. Drobná Z. Waters SB. Devesa V. Harmon AW. Thomas DJ. Stýblo M. Metabolism and toxicity of arsenic in human urothelial cells expressing rat arsenic (+3 oxidation state)-methyltransferase. Toxicol Appl Pharmacol. 2005; 207(3):147-159.
31. Petzoldt JL. Leigh IM. Duffy PG. Sexton C. Masters JR. Immortalisation of human urothelial cells. Urol Res. 1995; 23(3):377-380.
32. Hester SD. Drobna Z. Andrews DMK. et al. Expression of AS3MT alters transcriptional profi les in human urothelial cells exposed to arsenite. Hum Exp Toxicol. 2009; 28(3):49-61.
33. Durkan GC. Nutt JE. Marsh C. et al. Alteration in urinary matrix metalloproteinase-9 to tissue inhibitor of metalloproteinase-1 ratio predicts recurrence in nonmuscle-invasive bladder cancer. Clin Cancer Res. 2003; 9(3):2576-2582.
34. Papathoma AS. Petraki C. Grigorakis A. et al. Prognostic signifi cance of matrix metalloproteinases 2 and 9 in bladder cancer. Anticancer Res. 2000; 20(3B):2009-2013.
35. Wallard MJ. Pennington CJ. Veerakumarasivam A. et al. Comprehensive profi ling and localisation of the matrix metalloproteinases in urothelial carcinoma. Br J Cancer. 2006; 94(3):569-577.
36. Cooper KL. Myers TA. Rosenberg M. Chavez M. Hudson LG. Roles of mitogen activated protein kinases and EGF receptor in arsenite-stimulated matrix metalloproteinase-9 production. Toxicol Appl Pharmacol. 2004; 200(3):177-185.
37. Albini A. Benelli R. The chemoinvasion assay:a method to assess tumor and endothelial cell invasion and its modulation. Nat Protoc. 2007; 2(3):504-511.
38. Hamburger AW. Salmon SE. Primary bioassay of human tumor stem cells. Science. 1977; 197(3302):461-463.
39. Liu J. Benbrahim-Tallaa L. Qian X. et al. Further studies on aberrant gene expression associated with arsenic-induced malignant transformation in rat liver TRL1215 cells. Toxicol Appl Pharmacol. 2006; 216(3):407-415.
40. Leslie EM. Haimeur A. Waalkes MP. Arsenic transport by the human mul-tidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J Biol Chem. 2004; 279(31):32700-32708.
41. Walton FS. Waters SB. Jolley SL. LeCluyse EL. Thomas DJ. Styblo M. Selenium compounds modulate the activity of recombinant rat AsIII- methyltransferase and the methylation of arsenite by rat and human hepatocytes. Chem Res Toxicol. 2003; 16(3):261-265.
42. Drake EN. Cancer chemoprevention:selenium as a prooxidant, not an antioxidant. Med Hypotheses. 2006; 67(3):318-322.
43. Pi J. Yamauchi H. Kumagai Y. et al. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environ Health Perspect. 2002; 110(3):331-336.
44. Nesnow S. Roop BC. Lambert G. et al. DNA damage induced by methylated trivalent arsenicals is mediated by reactive oxygen species. Chem Res Toxicol. 2002; 15(32):1627-1634.
45. Thomas DJ. Styblo M. Lin S. The cellular metabolism and systemic tox-icity of arsenic. Toxicol Appl Pharmacol. 2001; 176(3):127-144.
46. Liu J. Chen H. Miller DS. et al. Overexpression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol Pharmacol. 2001; 60(3):302-309.
47. Romach EH. Zhao CQ. del Razo LM. Cebrián ME. Waalkes MP. Studies on the mechanisms of arsenic-induced self tolerance developed in liver epithelial cells through continuous low-level arsenite exposure. Toxicol Sci. 2000; 54(3):500-508.
48. Pi J. Qu W. Reece JM. Kumagai Y. Waalkes MP. Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes:involvement of hydrogen peroxide. Exp Cell Res. 2003; 290(3):234-245.
49. Scandalios JG. Oxidative stress:molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res. 2005; 38(3):995-1014.
50. Schläwicke Engström K. Nermell B. Concha G. Strömberg U. Vahter M. Broberg K. Arsenic metabolism is infl uenced by polymorphisms in genes involved in one-carbon metabolism and reduction reactions. Mutat Res. 2009; 667(3-2):4-14.
51. Drobna Z. Naranmandura H. Kubachka KM. et al. Disruption of arsenic (+3 oxidation state) methyltransferase gene in the mouse alters the phenotype for methylation of arsenic and affects distribution and rentention of orally administered arsenate. Chem Res Toxicol. 2009; 22(30):1713-1720