Catalase has a key role in protecting cells from the genotoxic effects of monomethylarsonous acid: A highly active metabolite of arsenic

Environmental and Molecular Mutagenesis

Volumn 54, Issue 5, 2013, Pages 317-326

  Muñiz Ortiz, Jorge G ^a   Wallace, Kathleen A ^a   Leinisch, Fabian ^b   Kadiiska, Maria B ^b   Mason, Ronald P ^b   Kligerman, Andrew D ^a  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

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

Author keywords

Arsenicals; Comet assay; DNA damage; Mode of action; Reactive oxygen species

Indexed keywords

5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; ARSENIC; ARSONIC ACID DERIVATIVE; CATALASE; DNA; MONOMETHYLARSONOUS ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL PROTECTION; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; EXPOSURE; GENOTOXICITY; LIVER CELL; LYMPHOCYTE; MOUSE; NONHUMAN;

ANIMALS; CATALASE; CELLS, CULTURED; CYTOPROTECTION; DNA DAMAGE; ELECTRON SPIN RESONANCE SPECTROSCOPY; MICE; MICE, KNOCKOUT; MUTAGENS; ORGANOMETALLIC COMPOUNDS;

EID: 84878912279     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.21780     Document Type: Article

References (58)

1. Ahsan H, Chen Y, Kibriya MG, Islam MN, Slavkovich VN, Graziano JH, Santella RM. 2003. Susceptibility to arsenic-induced hyperkeratosis and oxidative stress genes myeloperoxidase and catalase. Cancer Lett 201:57-65.
2. Argos M, Kalra T, Pierce BL, Chen Y, Parvez F, Islam T, Ahmed A, Hasan R, Hasan K, Sarwar G, Levy D, Slavkovich V, Graziano JH, Rathouz PJ, Ahsan H. 2011. A prospective study of arsenic exposure from drinking water and incidence of skin lesions in Bangladesh. Am J Epidemiol 174:185-194..
3. Banerjee M, Banerjee N, Ghosh P, Das JK, Basu S, Sarkar AK, States JC, Giri AK. 2010. Evaluation of the serum catalase and myeloperoxidase activities in chronic arsenic-exposed individuals and concomitant cytogenetic damage. Toxicol Appl Pharmacol 249:47-54.
4. Beers RF Jr, Sizer IW. 1952. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133-140.
5. Bredfeldt TG, Jagadish B, Eblin KE, Mash EA, Gandolfi AJ. 2006. Monomethylarsonous acid induces transformation of human bladder cells. Toxicol Appl Pharmacol 216:69-79.
6. Chen Y, Graziano JH, Parvez F, Liu M, Slavkovich V, Kalra T, Argos M, Islam T, Ahmed A, Rakibuz-Zaman M, Hasan R, Sarwar G, Levy D, van Geen A, Ahsan H. 2011. Arsenic exposure from drinking water and mortality from cardiovascular disease in Bangladesh: Prospective cohort study. BMJ 342:d2431.
7. Cohen SM, Arnold LL, Uzvolgyi E, Cano M, St. John M, Yamamoto S, Lu X, Le XC. 2002. Possible role of dimethylarsinous acid in dimethylarsinic acid-induced urothelial toxicity and regeneration in the rat. Chem Res Toxicol 15:1150-1157.
8. Cohen SM, Ohnishi T, Arnold LL, Le XC. 2007. Arsenic-induced bladder cancer in an animal model. Toxicol Appl Pharmacol 222:258-263.
9. Dopp E, Hartmann LM, Florea AM, von Recklinghausen U, Pieper R, Shokouhi B, Rettenmeier AW, Hirner AV, Obe G. 2004. Uptake of inorganic and organic derivatives of arsenic associated with induced cytotoxic and genotoxic effects in Chinese hamster ovary (CHO) cells. Toxicol Appl Pharmacol 201:156-165.
10. Duling DR. 1994. Simulation of multiple isotropic spin-trap EPR spectra. J Magn Reson B 104:105-110.
11. Dunnett CW. 1955. A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc 50:1096-1121.
12. Eblin KE, Bowen ME, Cromey DW, Bredfeldt TG, Mash EA, Lau SS, Gandolfi AJ. 2006. Arsenite and monomethylarsonous acid generate oxidative stress response in human bladder cell culture. Toxicol Appl Pharmacol 217:7-14.
13. Forsberg L, Lyrenas L, de Faire U, Morgenstern R. 2001. A common functional C-T substitution polymorphism in the promoter region of the human catalase gene influences transcription factor binding, reporter gene transcription and is correlated to blood catalase levels. Free Radic Biol Med 30:500-505.
14. García-Chávez E, Santamaria A, Diaz-Barriga F, Mandeville P, Juarez BI, Jimenez-Capdeville ME. 2003. Arsenite-induced formation of hydroxyl radical in the striatum of awake rats. Brain Res 976:82-89.
15. Hafeman DM, Ahsan H, Louis ED, Siddique AB, Slavkovich V, Cheng Z, van Geen A, Graziano JH. 2005. Association between arsenic exposure and a measure of subclinical sensory neuropathy in Bangladesh. J Occup Environ Med 47:778-784.
16. Hartwig A, Schwerdtle T. 2002. Interactions by carcinogenic metal compounds with DNA repair processes: toxicological implications. Toxicol Lett 127:47-54.
17. Hei TK, Liu SX, Waldren C. 1998. Mutagenicity of arsenic in mammalian cells: Role of reactive oxygen species. Proc Natl Acad Sci USA 95:8103-8107.
18. Ho YS, Xiong Y, Ma W, Spector A, Ho DS. 2004. Mice lacking catalase develop normally but show differential sensitivity to oxidant tissue injury. J Biol Chem 279:32804-32812.
19. Hsu LI, Chiu AW, Huan SK, Chen CL, Wang YH, Hsieh FI, Chou WL, Wang LH, Chen CJ. 2008. SNPs of GSTM1, T1, P1, epoxide hydrolase and DNA repair enzyme XRCC1 and risk of urinary transitional cell carcinoma in southwestern Taiwan. Toxicol Appl Pharmacol 228:144-155.
20. Huang CY, Su CT, Chu JS, Huang SP, Pu YS, Yang HY, Chung CJ, Wu CC, Hsueh YM. 2011. The polymorphisms of P53 codon 72 and MDM2 SNP309 and renal cell carcinoma risk in a low arsenic exposure area. Toxicol Appl Pharmacol 257:349-355.
21. IARC. 2012. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. A Review of Human Carcinogens: Metals, Arsenic, Fibres and Dusts, Vol. 100C. Available at: http://www.iarc.fr/en/publications/list/monographs/index.php. Accessed on March 19, 2013.
22. Jensen TJ, Wozniak RJ, Eblin KE, Wnek SM, Gandolfi AJ, Futscher BW. 2009. Epigenetic mediated transcriptional activation of WNT5A participates in arsenical-associated malignant transformation. Toxicol Appl Pharmacol 235:39-46.
23. Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M. 2011. Arsenic: Toxicity, oxidative stress and human disease. J Appl Toxicol 31:95-107.
24. Kitchin KT, Wallace K. 2008. The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J Inorg Biochem 102:532-539.
25. Klaunig JE, Wang Z, Pu X, Zhou S. 2011. Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol Appl Pharmacol 254:86-99.
26. Kligerman AD, Tennant AH. 2007. Insights into the carcinogenic mode of action of arsenic. Toxicol Appl Pharmacol 222:281-288.
27. Kligerman AD, Doerr CL, Tennant AH, Harrington-Brock K, Allen JW, Winkfield E, Poorman-Allen P, Kundu B, Funasaka K, Roop BC, Mass MJ, DeMarini DM. 2003. Methylated trivalent arsenicals as candidate ultimate genotoxic forms of arsenic: Induction of chromosomal mutations but not gene mutations. Environ Mol Mutagen 42:192-205.
28. Kligerman AD, Doerr CL, Tennant AH. 2005. Oxidation and methylation status determine the effects of arsenic on the mitotic apparatus. Mol Cell Biochem 279:113-121.
29. Kligerman AD, Malik SI, Campbell JA. 2010. Cytogenetic insights into DNA damage and repair of lesions induced by a monomethylated trivalent arsenical. Mutat Res 695:2-8.
30. Kobayashi Y, Hirano S. 2008. Effects of endogenous hydrogen peroxide and glutathione on the stability of arsenic metabolites in rat bile. Toxicol Appl Pharmacol 232:33-40.
31. Kuppusamy P, Zweier JL. 1989. Characterization of free radical generation by xanthine oxidase. Evidence for hydroxyl radical generation. J Biol Chem 264:9880-9884.
32. Li JH, Rossman TG. 1989. Inhibition of DNA ligase activity by arsenite: a possible mechanism of its comutagenesis. Mol Toxicol 2:1-9.
33. Li WC, Ralphs KL, Tosh D. 2010. Isolation and culture of adult mouse hepatocytes. Methods Mol Biol 633:185-196.
34. Liu SX, Athar M, Lippai I, Waldren C, Hei TK. 2001. Induction of oxyradicals by arsenic: Implication for mechanism of genotoxicity. Proc Natl Acad Sci USA 98:1643-1648.
35. Mahata J, Basu A, Ghoshal S, Sarkar JN, Roy AK, Poddar G, Nandy AK, Banerjee A, Ray K, Natarajan AT, Nilsson R, Giri AK. 2003. Chromosomal aberrations and sister chromatid exchanges in individuals exposed to arsenic through drinking water in West Bengal, India. Mutat Res 534:133-143.
36. Mass MJ, Tennant A, Roop BC, Cullen WR, Styblo M, Thomas DJ, Kligerman AD. 2001. Methylated trivalent arsenic species are genotoxic. Chem Res Toxicol 14:355-361.
37. Miller DM, Buettner GR, Aust SD. 1990. Transition metals as catalysts of "autoxidation" reactions. Free Radic Biol Med 8:95-108.
38. Nadif R, Mintz M, Jedlicka A, Bertrand JP, Kleeberger SR, Kauffmann F. 2005. Association of CAT polymorphisms with catalase activity and exposure to environmental oxidative stimuli. Free Radic Res 39:1345-1350.
39. Negrini S, Gorgoulis VG, Halazonetis TD. 2010. Genomic instability-An evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220-228.
40. Nesnow S, Roop BC, Lambert G, Kadiiska M, Mason RP, Cullen WR, Mass MJ. 2002. DNA damage induced by methylated trivalent arsenicals is mediated by reactive oxygen species. Chem Res Toxicol 15:1627-1634.
41. Pou SA, Osella AR, Diaz Mdel P. 2011. Bladder cancer mortality trends and patterns in Cordoba, Argentina (1986-2006). Cancer Causes Control 22:407-415.
42. Schriner SE, Ogburn CE, Smith AC, Newcomb TG, Ladiges WC, Dolle ME, Vijg J, Fukuchi K, Martin GM. 2000. Levels of DNA damage are unaltered in mice overexpressing human catalase in nuclei. Free Radic Biol Med 29:664-673.
43. Sertel S, Tome M, Briehl MM, Bauer J, Hock K, Plinkert PK, Efferth T. 2012. Factors determining sensitivity and resistance of tumor cells to arsenic trioxide. PLoS One 7:e35584.
44. Singh NP, Tice RR, Stephens RE, Schneider EL. 1991. A microgel electrophoresis technique for the direct quantitation of DNA damage and repair in individual fibroblasts cultured on microscope slides. Mutat Res 252:289-296.
45. Tennant AH, Kligerman AD. 2011. Superoxide dismutase protects cells from DNA damage induced by trivalent methylated arsenicals. Environ Mol Mutagen 52:238-243.
46. Tokar EJ, Diwan BA, Waalkes MP. 2010a. Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ Health Perspect 118:108-115.
47. Tokar EJ, Qu W, Liu J, Liu W, Webber MM, Phang JM, Waalkes MP. 2010b. Arsenic-specific stem cell selection during malignant transformation. J Natl Cancer Inst 102:638-649.
48. Tokar EJ, Diwan BA, Thomas DJ, Waalkes MP. 2012. Tumors and proliferative lesions in adult offspring after maternal exposure to methylarsonous acid during gestation in CD1 mice. Arch Toxicol 86:975-982.
49. Waalkes MP, Liu J, Diwan BA. 2007. Transplacental arsenic carcinogenesis in mice. Toxicol Appl Pharmacol 222:271-280.
50. Wadhwa SK, Kazi TG, Chandio AA, Afridi HI, Kolachi NF, Khan S, Kandhro GA, Nasreen S, Shah AQ, Baig JA. 2011. Comparative study of liver cancer patients in arsenic exposed and non-exposed areas of Pakistan. Biol Trace Elem Res 144:86-96.
51. Wang TS, Hsu TY, Chung CH, Wang AS, Bau DT, Jan KY. 2001. Arsenite induces oxidative DNA adducts and DNA-protein cross-links in mammalian cells. Free Radic Biol Med 31:321-330.
52. Wnek SM, Medeiros MK, Eblin KE, Gandolfi AJ. 2009. Persistence of DNA damage following exposure of human bladder cells to chronic monomethylarsonous acid. Toxicol Appl Pharmacol 241:202-209.
53. Wnek SM, Jensen TJ, Severson PL, Futscher BW, Gandolfi AJ. 2010. Monomethylarsonous acid produces irreversible events resulting in malignant transformation of a human bladder cell line following 12 weeks of low-level exposure. Toxicol Sci 116:44-57.
54. Wnek SM, Kuhlman CL, Camarillo JM, Medeiros MK, Liu KJ, Lau SS, Gandolfi AJ. 2011. Interdependent genotoxic mechanisms of monomethylarsonous acid: Role of ROS-induced DNA damage and poly(ADP-ribose) polymerase-1 inhibition in the malignant transformation of urothelial cells. Toxicol Appl Pharmacol 257:1-13.
55. Yager JW, Wiencke JK. 1997. Inhibition of poly(ADP-ribose) polymerase by arsenite. Mutat Res 386:345-351.
56. Yokohira M, Arnold LL, Pennington KL, Suzuki S, Kakiuchi-Kiyota S, Herbin-Davis K, Thomas DJ, Cohen SM. 2010. Severe systemic toxicity and urinary bladder cytotoxicity and regenerative hyperplasia induced by arsenite in arsenic (+3 oxidation state) methyltransferase knockout mice. A preliminary report. Toxicol Appl Pharmacol 246:1-7.
57. Yue Qian S, Kadiiska MB, Guo Q, Mason RP. 2005. A novel protocol to identify and quantify all spin trapped free radicals from in vitro/in vivo interaction of HO(·-) and DMSO: LC/ESR, LC/MS, and dual spin trapping combinations. Free Radic Biol Med 38:125-135.
58. Zhou X, Sun H, Ellen TP, Chen H, Costa M. 2008. Arsenite alters global histone H3 methylation. Carcinogenesis 29:1831-1836.