Arsenic alters cytosine methylation patterns of the promoter of the tumor suppressor gene p53 in human lung cells: A model for a mechanism of carcinogenesis

Mutation Research - Reviews in Mutation Research

Volumn 386, Issue 3, 1997, Pages 263-277

  Mass, Marc J ^a   Wang, Liangjun ^b  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Arsenic; Carcinogenesis; DNA methylation

Indexed keywords

5 METHYLCYTOSINE; ARSENATE SODIUM; ARSENITE SODIUM; BISULFITE; CACODYLIC ACID; DNA; METHYLTRANSFERASE; ORGANOARSENIC DERIVATIVE; PROTEIN P53; S ADENOSYLMETHIONINE;

ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CONTROLLED STUDY; DNA METHYLATION; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; PRIORITY JOURNAL; PROMOTER REGION; TUMOR SUPPRESSOR GENE;

EID: 0030742792     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1383-5742(97)00008-2     Document Type: Review

References (67)

1. A. Albores, J. Koropatnick, M.G. Cherian, A.J. Zelazowski, Arsenic induces and enhances rat hepatic metallothionein production in vivo, Chem. Biol. Interact. 85 (1992) 127-140.
2. S.A. Belinsky, K.J. Nikula, S.B. Baylin, J.-P.J. Issa, Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer, Proc. Natl. Acad. Sci. USA 93 (1996) 4045-4050.
3. T.H. Bestor, V.M. Ingram, Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of action with DNA, Proc. Natl. Acad. Sci. USA 80 (1983) 5559-5563.
4. C.C. Brown, K.C. Chu, Implications of the multistage theory of carcinogenesis applied to occupational arsenic exposure, J. Natl. Cancer Inst. 70 (1983) 455-463.
5. J.P. Buchet, R. Lauwerys, Study of inorganic arsenic meth-ylation by rat liver in vitro: relevance for the interpretation of observations in man, Arch. Toxicol. 57 (1985) 125-129.
6. C.J. Chen, C.W. Chen, M.M. Wu, T.L. Kuo, Cancer potential in liver, lung, bladder, and kidney due to ingested inorganic arsenic in drinking water, Br. J. Cancer 66 (1992) 888-892.
7. C.J. Chen, M.M. Wu, S.S. Lee, T.M. Lin, Atherogenicity and carcinogenicity of high-arsenic artesian well water: multiple risk factors and related malignant neoplasms of blackfoot disease, Arteriosclerosis 8 (1988) 452-460.
8. S.-L. Chen, S.R. Dzeng, M.-O. Yang, K.-H. Chiu, G.-M. Shieh, C.-M. Wai, Arsenic species in groundwaters of the blackfoot disease area, Taiwan. Environ. Sci. Technol. 28 (1994) 877-881.
9. K.V. Chin, S. Tanaka, G. Darlington, I. Pastan, M.M. Gottesman, Heat shock and arsenite increase expression of the multidrug resistance (MDR1) gene in human renal carcinoma cells, J. Biol. Chem. 265 (1990) 221-226.
10. S.J. Clark, J. Harrison, M. Frommer, CpNpG methylation in mammalian cells, Nature Genet. 10 (1995) 20-27.
11. J.L. Counts, J.I. Goodman, Hypomethylation of DNA: an epigenetic mechanism involved in tumor promotion, Mol. Carcinog. 11 (1994) 185-188.
12. S. Darasch, D.D. Mosser, N.C. Bols, J.J. Heikakila, Heat shock gene expression in Xenopus Laevis A6 cells in response to heat shock and sodium arsenite treatments, Biochem. Cell Biol. 66 (1988) 862-870.
13. M. Delnomdedieu, M.M. Basti, J.D. Otvos, D.J. Thomas, Transfer of arsenite from glutathione to dithiols: a model of interaction, Chem. Res. Toxicol. 6 (1993) 598-602.
14. P.E. Enterline, R. Day, G.M. Marsh, Cancers related to exposure to arsenic at a copper smelter, Occup. Environ. Med. 52 (1995) 28-32.
15. E. Farber, D. Solt, R. Cameron, B. Laishes, K. Ogawa, A. Medline, Newer insights into the pathogenesis of liver cancer, Am. J. Pathol. 89 (1977) 477-482.
16. Fowler, B. (1991) Toxic effects of metals, in: M.O. Amdur, J. Doull and C.D. Klaassen (Eds.), Casarett and Doull's Toxicology, McGraw-Hill, New York, pp. 623-643.
17. M. Frommer, L.E. McDonald, D.S. Millar, C.M. Collis, F. Watt, G.W. Grigg, P.L. Molloy, C.L. Paul, A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands, Proc. Natl. Acad. Sci. USA 89 (1992) 1827-1831.
18. M. Gonzalez-Zulueta, C.M. Bender, A.S. Yang, T. Nguyen, R.W. Beart, J.M. Van Turnout, P.A. Jones, Methylation of the 5′ CpG Island of the p16/CDKN2 tumor suppressor gene in normal and transformed humanm tissues correlates with gene silencing, Cancer Res. 55 (1995) 4531-4535.
19. C. Goyon, T.I.V. Nogueira, G. Faugeron, Perpetuation of cytosine methylation in Ascobolus immersus implies a novel type of maintenance methylase, J. Mol. Biol. 240 (1994) 42-51.
20. M.S. Greenblatt, W.P. Bennett, C.C. Harris, Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis, Cancer Res. 15 (1994) 4855-4878.
21. J.G. Herman, A. Merlo, L. Mao, R.G. Lapidus, J.J. Issa, N.E. Davidson, D. Sidransky, S.B. Baylin, Inactivation of the CDKN2/p16/MST1 gene is frequently associated with aberrant DNA methylation in all common human cancers, Cancer Res. 55 (1995) 4525-4530.
22. K.L. Hoover, P.H. Lynch, L.A. Poirier, Profound postinitiation enhancement by short-term severe methionine, choline, vitamin B12, and folate deficiency of hepatocarcinogenesis in F344 rats given a single low-dose diethylnitrosamine injection, J. Natl. Cancer Inst. 73 (1984) 1327-1333.
23. C. Hopenhayn-Rich, M.L. Biggs, A. Fuchs, R. Bergoglio, E.E. Tello, H. Nicolli, A.M. Smith, Bladder cancer mortality associated with arsenic in drinking water in Argentina, Epidemioogy 7 (1996) 117-124.
24. Y.-M. Hsueh, G.-S. Cheng, M.-M. Wu, T.-L. Kuo, C.-J. Chen, Multiple risk factors associted with arsenic-induced skin cancer: effects of chronic liver disease and malnutritional status, Br. J. Cancer 71 (1995) 109-114.
25. J.P. Issa, P.M. Vertino, J. Wu, S. Sazawal, P. Celano, B.D. Nelkin, S.R. Hamilton, S.B. Baylin, Increased cytosine DNA-methyltransferase activity during colon cancer progression, J. Natl. Cancer Inst. 85 (1993) 1235-1240.
26. M. Karon, W.F. Benedict, Chromatid breakage: differential effect of inhibitors of DNA synthesis during G 2 phase. Science 178 (1972) 62.
27. S.J. Kuerbitz, B.S. Plunkett, W.V. Walsh, M.B. Kastan, Wild-type p53 is a cell cycle checkpoint determinant following irradiation, Proc. Natl. Acad. Sci. USA 89 (1992) 7491-7495.
28. G. Kutty, B. Hayden, Y. Osawa, B. Wiggert, G.J. Chader, R.G. Kutty, Heme oxygenase: expression in human retina and modulation by stress agents in a retinoblastoma cell model system, Curr. Eye Res. 11 (1992) 153-160.
29. F. Larsen, G. Gundersen, R. Lopez, H. Prydz, CpG islands as gene markers in the human genome (Database on internet: http://benvub.ac.be/srs/srsc?-info+CpGisle), Genomics 13 (1992) 1095-1107.
30. T.-C. Lee, M. Oshimura, J.C. Barren, Comparison of arsenic-induced cell transformation, mutation and cytogenetic effects in Syrian hamster embryo cells in culture, Carcinogenesis 6 (1985) 1421-1426.
31. Y.-W. Lee, C.B. Klein, B. Kagacin, K. Salnikow, J. Kitahara, K. Dowjat, N.T. Zhitkovitch, M. Costa, Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: a new model for epigenetic carcinogens, Mol. Cell Biol. 15 (1995) 2547-2557.
32. T.A. Lehman, W.P. Bennett, R.A. Metcalf, J.A. Welsh, J. Ecker, R.V. Modali, S. Ullrich, J.W. Romano, E. Appella, J.R. Testa et al., p53 mutations, ras mutations, and p53-heat shock 70 protein complexes in human lung carcinoma cell lines, Cancer Res. 51 (1991) 4090-4096.
33. M. Lubbert, C.W. Miller, L. Crawford, H.P. Koeffler, p53 in chronic myelogenous leukemia, J. Exp. Med. 167 (1988) 873-886.
34. M. Makos, B.D. Nelkin, M.I. Lerman, F. Latif, B. Zbar, S.B. Baylin, Distinct hypermethylation patterns occur at altered chromosome loci in human lung and colon cancer, Proc. Natl. Acad. Sci. USA 89 (1992) 1929-1933.
35. M.J. Mass, Human carcinogenesis by arsenic, Environ. Geochem. Health 14 (1992) 49-54.
36. P. Meyer, I. Niedenhof, M.T. Lohuis, Evidence for cytosine methylation of non-symmetrical sequences in transgenic Petunia hybrida, EMBO J. 13 (1994) 2084-2088.
37. P. Mushak, A.F. Crocetti, Risk and revisionism in arsenic cancer risk assessment, Environ. Health Perspect. 103 (1995) 684-689.
38. N. Ohtani Fujita, T. Fujita, A. Aoike, N.E. Osifchin, P.D. Robbins, T. Sakai, CpG methylation inactivates the promoter activity of the human retinoblastoma tumor-suppressor gene, Oncogene 8 (1993) 1063-1067.
39. P. Perticone, R. Cozzi, B. Gustavino, Sister chromatid exchanges induced by DNA demethylating agents persist through several cell cycles in mammalian cells, Carcinogenesis 8 (1987) 1059-1063.
40. I.P. Pogribny, A.C. Basnakian, B.J. Miller, N.G. Lopatina, L.A. Poirier, S.J. James, Breaks in genomic DNA and within p53 are associated with hypomethylation in livers of folate/methyl-deficient rats, Cancer Res. 55 (1995) 1894-1901.
41. W.M. Rideout, G.A. Coetzee, A.F. Olumi, C.H. Spruck, P.A. Jones, 5-Methylcytosine as an endogenous mutagen in the p53 tumor suppressor gene, Princess. Takamatsu. Symp. 22 (1991) 207-219.
42. A.D. Riggs, P.A. Jones, 5-methylcytosine, gene regulation, and cancer, Adv. Cancer Res. 40 (1983) 1-30.
43. K.I. Rother, J. Silker, O. Georgiev, W. Schaffner, K. Matsuo, Influence of DNA sequence and methylation status on bisulfite conversion of cytosine residues, Anal. Biochem. 231 (1995) 263-265.
44. 1 checkpoint-competent cells, Cancer Res. 55 (1995) 1639-1642.
45. C. Schmutte, A.S. Yang, T.T. Nguyen, R.W. Beart, P.A. Jones, Mechanisms for the involvement of DNA methylation in colon carcinogenesis, Cancer Res. 56 (1996) 2375-2381.
46. E.U. Selker, D.Y. Fritz, M.J. Singer, Dense nonsymmetrical DNA methylation resulting from repeat-induced point mutation in Neurospora, Science 262 (1993) 1724-1728.
47. V. Senft, F. Losan, M. Tucek, Cytogenetic analysis of chromosomal aberrations of peripheral lymphocytes in workers occupationally exposed to nickel, Mutation Res. 279 (1992) 171-179.
48. A.H. Smith, C. Hopenhayn-Rich, M.N. Bates, H.M. Goeden, I. Hertz-Picciotto, H.M. Duggan, R. Wood, M.J. Kosnett, M.T. Smith, Cancer risks for arsenic in drinking water, Environ. Health Perspect. 97 (1992) 259-267.
49. M.J. Steenman, S. Rainier, C.J. Dobry, P. Grundy, I.L. Horon, A.P. Feinberg, Loss of imprinting of IGF2 is linked to reduced expression and abnormal methylation of H19 in Wilms' tumour, Nature Genet. 7 (1994) 433-439.
50. H. Stopper, C. Korber, P. Gibbis, D.L. Spencer, W.J. Cas pary, Micronuclei induced by modulators of methylation: analogs of 5-azacytidine, Carcinogenesis 16 (1995) 1647-1650.
51. M. Styblo, D.J. Thomas, In vitro inhibition of glutathione reductase by arsenotriglutathione, Biochem. Pharmacol. 49 (1995) 971-977.
52. E.S. Tasheva, D.J. Roufa, Densely methylated DNA islands in mammalian chromosomal replication origins, Mol. Cell Biol. 14 (1994) 5636-5644.
53. E.S. Tasheva, D.J. Roufa, A densely methylated DNA island is associated with a chromosomal replication origin in the human RPS14 locus, Somatic Cell Mol. Genetics 21 (1995) 369-383.
54. P.H. Tate, A.P. Bird, Effects of DNA methylation on DNA-binding proteins and gene expression, Curr. Opin. Genet. Dev. 3 (1993) 226-231.
55. D.H. Tsao, A.H. Maki, Optically detected magnetic resonance study of the interaction of an arsenic(III) derivative of cacodylic acid with EcoRI methyl transferase, Biochemistry 30 (1991) 4565-4572.
56. W.P. Tseng, H.M. Chu, S.W. How, J.M. Fong, C.S. Lin, S. Yeh, Prevalence of skin cancer in an endemic area of chronic arsenicism in Taiwan, J. Natl. Cancer Inst. 40 (1968) 453-463.
57. U.S. Environmental Protection Agency (1988) Special report on ingested arsenic. EPA/625/3-87/013. Risk Assessment Forum, USEPA, Washington, DC.
58. M. Vahter, J. Envall, In vivo reduction of arsenate in mice and rabbits, Environ. Res. 32 (1983) 14-24.
59. M. Vahter, E. Marafante, Intracellular interaction and metabolic fate of arsenite and arsenate in mice and rabbits, Chem. Biol. Interact. 47 (1983) 29-44.
60. P.M. Vertino, J.P. Issa, O.M. Pereira Smith, S.B. Baylin, Stabilization of DNA methyltransferase levels and CpG island hypermethylation precede SV40-induced immortalization of human fibroblasts, Cell Growth Differ. 5 (1994) 1395-1402.
61. M.M. Wales, M.A. Biel, W. el Deiry, B.D. Nelkin, J.P. Issa, W.K. Cavenee, S.J. Kuerbitz, S.B. Baylin, p53 activates expression of Hic-1, a new candidate tumour suppressor gene on 17p13.3, Nat. Med 1 (1995) 570-577.
62. D.M. Woodcock, P.J. Crowther, W.P. Diver, The majority of methylated deoxycytidines in human DNA are not in the CpG dinucleotide, Biochem. Biophys. Res. Commun. 145 (1987) 888-894.
63. S. Yamamoto, Y. Konishi, T. Matsuda, T. Murai, M.A. Shibata, I. Matsui-Yuasa, S. Otani, K. Kuroda, G. Endo, S. Fukushima, Cancer induction by an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in F344/DuCrj rats after pretreatment with five carcinogens, Cancer Res. 15 (1995) 1271-1276.
64. Yamauchi, H. and B. Fowler (1994) Toxicity and metabolism of inorganic and methylated arsenicals, in: J.O. Nriagu (Ed.), Arsenic in the environment. Part II: Human health and ecosystem effects, Wiley, New York, pp. 35-43.
65. H.S. Yu, K.S. Chiou, R.C. Yang, S.F. Chang, Progressive alterations of cytokeratin expressions in the process of chronic arsenism, J. Dermatol. 20 (1993) 741-745.
66. S.H. Yuspa, The pathogenesis of squamous cell cancer: lessons learned from studies of skin carcinogenesis - thirty-third G. H.A. Clowes Memorial Award Lecture, Cancer Res. 54 (1994) 1178-1189.
67. R. Zakharyan, Y. Wu, G.M. Bogdan, H.V. Aposian, Enzymatic methylation of arsenic compounds: assay, partial purification, and properties of arsenite methyltransferase and monomethylarsonic acid methyltransferase of rabbit liver, Chem. Res. Toxicol. 8 (1995) 1029-1038.