Arsenic and the Epigenome: Interindividual Differences in Arsenic Metabolism Related to Distinct Patterns of DNA Methylation

Journal of Biochemical and Molecular Toxicology

Volumn 27, Issue 2, 2013, Pages 106-115

  Bailey, Kathryn A ^a   Wu, Michael C ^b   Ward, William O ^c   Smeester, Lisa ^a   Rager, Julia E ^a   García Vargas, Gonzalo ^d   Del Razo, Luz Maria ^e   Drobná, Zuzana ^f   Stýblo, Miroslav ^a,f   Fry, Rebecca C ^a  

^a University of North Carolina at Chapel Hill   (United States)

^b IL   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^d UNIVERSIDAD JUÁREZ DEL ESTADO DE DURANGO   (Mexico)

^e DEPARTAMENTO DE FÍSICA   (Mexico)

^f University of North Carolina   (United States)

Author keywords

Arsenic; Arsenic biotransformation; DNA Methylation; Epigenome

Indexed keywords

ARSENIC; DNA; DRINKING WATER;

ARTICLE; BIOTRANSFORMATION; DIABETES MELLITUS; DNA METHYLATION; EPIGENETICS; HUMAN; IMPAIRED GLUCOSE TOLERANCE; MEXICO; PROMOTER REGION; URINE LEVEL;

ARSENIC; ARSENIC POISONING; BIOLOGICAL MARKERS; DIABETES MELLITUS; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LEUKOCYTES; MALE;

EID: 84874022257     PISSN: 10956670     EISSN: 10990461     Source Type: Journal    
DOI: 10.1002/jbt.21462     Document Type: Article

References (75)

1. World Health Organization. Guidelines for drinking water quality. Geneva, Switzerland: WHO Press; 2006.
2. Centeno JA, Tseng CH, Van der Voet GB, Finkelman RB. Global impacts of geogenic arsenic: a medical geology research case. Ambio 2007;36(1):78-81.
3. Rahman MM, Ng JC, Naidu R. Chronic exposure of arsenic via drinking water and its adverse health impacts on humans. Environ Geochem Health 2009;31 Suppl 1:189-200.
4. Jomova K, Jenisova Z, Feszterova M, Baros S, Liska J, Hudecova D, Rhodes CJ, Valko M. Arsenic: toxicity, oxidative stress and human disease. J Appl Toxicol 2011;31(2):95-107.
5. Kitchin KT, Wallace K. The role of protein binding of trivalent arsenicals in arsenic carcinogenesis and toxicity. J Inorgan Biochem 2008;102(3):532-539.
6. Druwe IL, Vaillancourt RR. Influence of arsenate and arsenite on signal transduction pathways: an update. Arch Toxicol 2010;84(8):585-596.
7. Rossman TG, Klein CB. Genetic and epigenetic effects of environmental arsenicals. Metallomics 2011;3(11):1135-1141.
8. Bailey KA, Fry RC. Arsenic-induced changes to the epigenome, In: SC Sahu, editor. Toxicology and Epigenetics. West Sussex, United Kingdom: Wiley; 2012. pp 149-190.
9. Haluskova J. Epigenetic studies in human diseases. Folia Biol 2010;56(3):83-96.
10. Chen H, Liu J, Zhao CQ, Diwan BA, Merrick BA, Waalkes MP. Association of c-myc overexpression and hyperproliferation with arsenite-induced malignant transformation. Toxicol Appl Pharmacol 2001;175(3):260-268.
11. Takahashi M, Barrett JC, Tsutsui T. Transformation by inorganic arsenic compounds of normal Syrian hamster embryo cells into a neoplastic state in which they become anchorage-independent and cause tumors in newborn hamsters. Int J Cancer 2002;99(5):629-634.
12. Chai CY, Huang YC, Hung WC, Kang WY, Chen WT. Arsenic salts induced autophagic cell death and hypermethylation of DAPK promoter in SV-40 immortalized human uroepithelial cells. Toxicol Lett 2007;173(1):48-56.
13. Cui X, Wakai T, Shirai Y, Yokoyama N, Hatakeyama K, Hirano S. Arsenic trioxide inhibits DNA methyltransferase and restores methylation-silenced genes in human liver cancer cells. Hum Pathol 2006;37(3):298-311.
14. Thomas DJ, Styblo M, Lin S. The cellular metabolism and systemic toxicity of arsenic. Toxicol Appl Pharmacol 2001;176(2):127-144.
15. Vahter M. Mechanisms of arsenic biotransformation. Toxicol 2002;181-182:211-217.
16. Kitchin KT, Ahmad S. Oxidative stress as a possible mode of action for arsenic carcinogenesis. Toxicol Lett 2003;137(1-2):3-13.
17. Styblo M, Del Razo LM, Vega L, Germolec DR, LeCluyse EL, Hamilton GA, Reed W, Wang C, Cullen WR, Thomas DJ. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 2000;74(6):289-299.
18. Tseng CH. Metabolism of inorganic arsenic and non-cancerous health hazards associated with chronic exposure in humans. J Environ Biol 2007;28(2 Suppl):349-357.
19. Tseng CH. Arsenic methylation, urinary arsenic metabolites and human diseases: current perspective. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 2007;25(1):1-22.
20. Mass MJ, Wang L. 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. Mutat Res 1997;386(3):263-277.
21. 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 USA 1997;94(20):10907-10912.
22. Mosharov E, Cranford MR, Banerjee R. The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes. Biochem 2000;39(42):13005-13011.
23. Thomas DJ, Li J, Waters SB, Xing W, Adair BM, Drobna Z, Devesa V, Styblo M. Arsenic (+3 oxidation state) methyltransferase and the methylation of arsenicals. Exp Biol Med 2007;232(1):3-13.
24. Leslie EM. Arsenic-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). J Inorg Biochem 2012;108:141-149.
25. Shimizu M, Hochadel JF, Fulmer BA, Waalkes MP. Effect of glutathione depletion and metallothionein gene expression on arsenic-induced cytotoxicity and c-myc expression in vitro. Toxicol Sci 1998;45(2):204-211.
26. Valenzuela OL, Drobna Z, Hernandez-Castellanos E, Sanchez-Pena LC, Garcia-Vargas GG, Borja-Aburto VH, Styblo M, Del Razo LM. Association of AS3MT polymorphisms and the risk of premalignant arsenic skin lesions. Toxicol Appl Pharmacol 2009;239(2):200-207.
27. Del Razo LM, Garcia-Vargas GG, Valenzuela OL, Castellanos EH, Sanchez-Pena LC, Currier JM, Drobna Z, Loomis D, Styblo M. Exposure to arsenic in drinking water is associated with increased prevalence of diabetes: a cross-sectional study in the Zimapan and Lagunera regions in Mexico. Environ Health 2011;10:73.
28. Smeester L, Rager JE, Bailey KA, Guan X, Smith N, Garcia-Vargas G, Del Razo LM, Drobna Z, Kelkar H, Styblo M, Fry RC. Epigenetic changes in individuals with arsenicosis. Chem Res Toxicol 2011;24(2):165-167.
29. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003;4(2):249-264.
30. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 1995;57:289-300.
31. Efron B. Size, power and false discovery rates. Ann Stat 2007;35:1351.
32. Storey JD. A direct approach to false discovery rates. J R Stat Soc Ser B (Methodol) 2002;64:479-498.
33. Diagnosis and classification of diabetes mellitus. Diabetes Care 2012;35 Suppl 1:S64-S71.
34. Li X, Li B, Xu Y, Wang Y, Jin Y, Itoh T, Yoshida T, Sun G. Arsenic methylation capacity and its correlation with skin lesions induced by contaminated drinking water consumption in residents of chronic arsenicosis area. Environ Toxicol 2011;26(2):118-123.
35. Huang YK, Huang YL, Hsueh YM, Yang MH, Wu MM, Chen SY, Hsu LI, Chen CJ. Arsenic exposure, urinary arsenic speciation, and the incidence of urothelial carcinoma: a twelve-year follow-up study. Cancer Causes Control 2008;19(8):829-839.
36. Yoshida T, Yamauchi H, Fan Sun G. Chronic health effects in people exposed to arsenic via the drinking water: dose-response relationships in review. Toxicol Appl Pharmacol 2004;198(3):243-252.
37. Hsieh YC, Lien LM, Chung WT, Hsieh FI, Hsieh PF, Wu MM, Tseng HP, Chiou HY, Chen CJ. Significantly increased risk of carotid atherosclerosis with arsenic exposure and polymorphisms in arsenic metabolism genes. Environ Res 2011;111(6):804-810.
38. Chiou HY, Huang WI, Su CL, Chang SF, Hsu YH, Chen CJ. Dose-response relationship between prevalence of cerebrovascular disease and ingested inorganic arsenic. Stroke 1997;28(9):1717-1723.
39. Tseng WP. Effects and dose-response relationships of skin cancer and blackfoot disease with arsenic. Environ Health Perspect 1977;19:109-119.
40. Online supporting information. Available at: http://www.bios.unc.edu/research/epigenetics.
41. Suk K, Kim S, Kim YH, Kim KA, Chang I, Yagita H, Shong M, Lee MS. IFN-gamma/TNF-alpha synergism as the final effector in autoimmune diabetes: a key role for STAT1/IFN regulatory factor-1 pathway in pancreatic beta cell death. J Immunol 2001;166(7):4481-4489.
42. Mandrup-Poulsen T. Apoptotic signal transduction pathways in diabetes. Biochem Pharmacol 2003;66(8):1433-1440.
43. Yoon JW, Jun HS. Cellular and molecular pathogenic mechanisms of insulin-dependent diabetes mellitus. Ann N Y Acad Sci 2001;928:200-211.
44. Hirai H, Miura J, Hu Y, Larsson H, Larsson K, Lernmark A, Ivarsson SA, Wu T, Kingman A, Tzioufas AG, Notkins AL. Selective screening of secretory vesicle-associated proteins for autoantigens in type 1 diabetes: VAMP2 and NPY are new minor autoantigens. Clin Immunol 2008;127(3):366-374.
45. Fernandez-Real JM, Broch M, Ricart W, Casamitjana R, Gutierrez C, Vendrell J, Richart C. Plasma levels of the soluble fraction of tumor necrosis factor receptor 2 and insulin resistance. Diabetes 1998;47(11):1757-1762.
46. Clement S, Krause U, Desmedt F, Tanti JF, Behrends J, Pesesse X, Sasaki T, Penninger J, Doherty M, Malaisse W, Dumont JE, Le Marchand-Brustel Y, Erneux C, Hue L, Schurmans S. The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 2001;409(6816):92-97.
47. Howard JK, Flier JS. Attenuation of leptin and insulin signaling by SOCS proteins. Trends Endocrinol Metab 2006;17(9):365-371.
48. Lebrun P, Van Obberghen E. SOCS proteins causing trouble in insulin action. Acta Physiol (Oxf) 2008;192(1):29-36.
49. Maier VH, Melvin DR, Lister CA, Chapman H, Gould GW, Murphy GJ. v- and t-SNARE protein expression in models of insulin resistance: normalization of glycemia by rosiglitazone treatment corrects overexpression of cellubrevin, vesicle-associated membrane protein-2, and syntaxin 4 in skeletal muscle of Zucker diabetic fatty rats. Diabetes 2000;49(4):618-625.
50. Babu DA, Deering TG, Mirmira RG. A feat of metabolic proportions: Pdx1 orchestrates islet development and function in the maintenance of glucose homeostasis. Mol Genet Metab 2007;92(1-2):43-55.
51. Fujimoto K, Polonsky KS. Pdx1 and other factors that regulate pancreatic beta-cell survival. Diabetes Obes Metab 2009;11 Suppl 4:30-37.
52. Mokhtari D, Myers JW, Welsh N. The MAPK kinase kinase-1 is essential for stress-induced pancreatic islet cell death. Endocrinology 2008;149(6):3046-3053.
53. Cantley J, Boslem E, Laybutt DR, Cordery DV, Pearson G, Carpenter L, Leitges M, Biden TJ. Deletion of protein kinase Cdelta in mice modulates stability of inflammatory genes and protects against cytokine-stimulated beta cell death in vitro and in vivo. Diabetologia 2011;54(2):380-389.
54. Brand C, Cipok M, Attali V, Bak A, Sampson SR. Protein kinase Cdelta participates in insulin-induced activation of PKB via PDK1. Biochem Biophys Res Commun 2006;349(3):954-962.
55. Valenzuela OL, Borja-Aburto VH, Garcia-Vargas GG, Cruz-Gonzalez MB, Garcia-Montalvo EA, Calderon-Aranda ES, Del Razo LM. Urinary trivalent methylated arsenic species in a population chronically exposed to inorganic arsenic. Environ Health Perspect 2005;113(3):250-254.
56. Foley DL, Craig JM, Morley R, Olsson CA, Dwyer T, Smith K, Saffery R. Prospects for epigenetic epidemiology. Am J Epidemiol 2009;169(4):389-400.
57. Huang CF, Chen YW, Yang CY, Tsai KS, Yang RS, Liu SH. Arsenic and diabetes: current perspectives. Kaohsiung J Med Sci 2011;27(9):402-410.
58. Tseng CH, Tseng CP, Chiou HY, Hsueh YM, Chong CK, Chen CJ. Epidemiologic evidence of diabetogenic effect of arsenic. Toxicol Lett 2002;133(1):69-76.
59. Navas-Acien A, Silbergeld EK, Streeter RA, Clark JM, Burke TA, Guallar E. Arsenic exposure and type 2 diabetes: a systematic review of the experimental and epidemiological evidence. Environ Health Perspect 2006;114(5):641-648.
60. Coronado-Gonzalez JA, Del Razo LM, Garcia-Vargas G, Sanmiguel-Salazar F, Escobedo-de la Pena J. Inorganic arsenic exposure and type 2 diabetes mellitus in Mexico. Environ Res 2007;104(3):383-389.
61. Islam MR, Khan I, Hassan SM, McEvoy M, D'Este C, Attia J, Peel R, Sultana M, Akter S, Milton AH. Association between type 2 diabetes and chronic arsenic exposure in drinking water: A cross sectional study in Bangladesh. Environ Health 2012;11:38.
62. Paul DS, Harmon AW, Devesa V, Thomas DJ, Styblo M. Molecular mechanisms of the diabetogenic effects of arsenic: inhibition of insulin signaling by arsenite and methylarsonous acid. Environ Health Perspect 2007;115(5):734-742.
63. Paul DS, Hernandez-Zavala A, Walton FS, Adair BM, Dedina J, Matousek T, Styblo M. Examination of the effects of arsenic on glucose homeostasis in cell culture and animal studies: development of a mouse model for arsenic-induced diabetes. Toxicol Appl Pharmacol 2007;222(3):305-314.
64. Fu J, Woods CG, Yehuda-Shnaidman E, Zhang Q, Wong V, Collins S, Sun G, Andersen ME, Pi J. Low-level arsenic impairs glucose-stimulated insulin secretion in pancreatic beta cells: involvement of cellular adaptive response to oxidative stress. Environ Health Perspect 2010;118(6):864-870.
65. Davila-Esqueda ME, Morales JM, Jimenez-Capdeville ME, De la Cruz E, Falcon-Escobedo R, Chi-Ahumada E, Martin-Perez S. Low-level subchronic arsenic exposure from prenatal developmental stages to adult life results in an impaired glucose homeostasis. Exp Clin Endocrinol Diabetes 2011;119(10):613-617.
66. Terry MB, Delgado-Cruzata L, Vin-Raviv N, Wu HC, Santella RM. DNA methylation in white blood cells: association with risk factors in epidemiologic studies. Epigenetics 2011;6(7):828-837.
67. Xu X, Gammon MD, Hernandez-Vargas H, Herceg Z, Wetmur JG, Teitelbaum SL, Bradshaw PT, Neugut AI, Santella RM, Chen J. DNA methylation in peripheral blood measured by LUMA is associated with breast cancer in a population-based study. FASEB J 2012;26(6):2657-2666.
68. Zhao J, Goldberg J, Bremner JD, Vaccarino V. Global DNA methylation is associated with insulin resistance: a monozygotic twin study. Diabetes 2012;61(2):542-546.
69. Toperoff G, Aran D, Kark JD, Rosenberg M, Dubnikov T, Nissan B, Wainstein J, Friedlander Y, Levy-Lahad E, Glaser B, Hellman A. Genome-wide survey reveals predisposing diabetes type 2-related DNA methylation variations in human peripheral blood. Hum Mol Genet 2012;21(2):371-383.
70. Baumgartener JW. SHIP2: an emerging target for the treatment of type 2 diabetes mellitus. Curr Drug Targets Immune Endocrin Metabol Disord 2003;3(4):291-298.
71. Aronoff S, Berkowitz K, Shreiner B, Want L. Glucose metabolism and regulation: beyond insulin and glucagon. Diabetes Spectr 2004;17(3):183-190.
72. Benjafield AV, Glenn CL, Wang XL, Colagiuri S, Morris BJ. TNFRSF1B in genetic predisposition to clinical neuropathy and effect on HDL cholesterol and glycosylated hemoglobin in type 2 diabetes. Diabetes Care 2001;24(4):753-757.
73. Kuo JZ, Guo X, Klein R, Klein BE, Cui J, Rotter JI, Ipp E, Chen YD. Systemic soluble tumor necrosis factor receptors 1 and 2 are associated with severity of diabetic retinopathy in hispanics. Ophthalmology 2012;119(5):1041-1046.
74. Niewczas MA, Gohda T, Skupien J, Smiles AM, Walker WH, Rosetti F, Cullere X, Eckfeldt JH, Doria A, Mayadas TN, Warram JH, Krolewski AS. Circulating TNF receptors 1 and 2 predict ESRD in type 2 diabetes. J Am Soc Nephrol 2012;23(3):507-515.
75. Gohda T, Niewczas MA, Ficociello LH, Walker WH, Skupien J, Rosetti F, Cullere X, Johnson AC, Crabtree G, Smiles AM, Mayadas TN, Warram JH, Krolewski AS. Circulating TNF receptors 1 and 2 predict stage 3 CKD in type 1 diabetes. J Am Soc Nephrol 2012;23(3):516-524.