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Mammalian Genome

, Volume 29, Issue 1–2, pp 63–79 | Cite as

Individual susceptibility to arsenic-induced diseases: the role of host genetics, nutritional status, and the gut microbiome

  • Liang Chi
  • Bei Gao
  • Pengcheng Tu
  • Chih-Wei Liu
  • Jingchuan Xue
  • Yunjia Lai
  • Hongyu Ru
  • Kun Lu
Review
First Online:
Received:
Accepted:

Abstract

Arsenic (As) contamination in water or food is a global issue affecting hundreds of millions of people. Although As is classified as a group 1 carcinogen and is associated with multiple diseases, the individual susceptibility to As-related diseases is highly variable, such that a proportion of people exposed to As have higher risks of developing related disorders. Many factors have been found to be associated with As susceptibility. One of the main sources of the variability found in As susceptibility is the variation in the host genome, namely, polymorphisms of many genes involved in As transportation, biotransformation, oxidative stress response, and DNA repair affect the susceptibility of an individual to As toxicity and then influence the disease outcomes. In addition, lifestyles and many nutritional factors, such as folate, vitamin C, and fruit, have been found to be associated with individual susceptibility to As-related diseases. Recently, the interactions between As exposure and the gut microbiome have been of particular concern. As exposure has been shown to perturb gut microbiome composition, and the gut microbiota has been shown to also influence As metabolism, which raises the question of whether the highly diverse gut microbiota contributes to As susceptibility. Here, we review the literature and summarize the factors, such as host genetics and nutritional status, that influence As susceptibility, and we also present potential mechanisms of how the gut microbiome may influence As metabolism and its toxic effects on the host to induce variations in As susceptibility. Challenges and future directions are also discussed to emphasize the importance of characterizing the specific role of these factors in interindividual susceptibility to As-related diseases.

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Notes

Acknowledgements

We are grateful to all investigators for their important contributions in the field. This review is by no means a complete list of all relevant studies due to the length and scope of the paper. The work is supported by the National Institute of Health/National Institute of Environmental Health Sciences (R01ES024950).

References

  1. Agusa T et al (2010) Genetic polymorphisms in glutathione S-transferase (GST) superfamily and arsenic metabolism in residents of the Red River Delta, Vietnam. Toxicol Appl Pharmacol 242(3):352–362PubMedCrossRefGoogle Scholar
  2. Ahsan H et al (2003) Susceptibility to arsenic-induced hyperkeratosis and oxidative stress genes myeloperoxidase and catalase. Cancer Lett 201(1):57–65PubMedCrossRefGoogle Scholar
  3. Ahsan H et al (2007) Arsenic metabolism, genetic susceptibility, and risk of premalignant skin lesions in Bangladesh. Cancer Epidemiol Prev Biomark 16(6):1270–1278CrossRefGoogle Scholar
  4. Antonelli R et al (2014) AS3MT, GSTO, and PNP polymorphisms: impact on arsenic methylation and implications for disease susceptibility. Environ Res 132:156–167PubMedCrossRefGoogle Scholar
  5. Bacher A et al (2000) Biosynthesis of vitamin B2 (riboflavin). Annu Rev Nutr 20(1):153–167PubMedCrossRefGoogle Scholar
  6. Bäckhed F et al (2005) Host-bacterial mutualism in the human intestine. Science 307(5717):1915–1920PubMedCrossRefGoogle Scholar
  7. Banerjee M et al (2007) Polymorphism in the ERCC2 codon 751 is associated with arsenic-induced premalignant hyperkeratosis and significant chromosome aberrations. Carcinogenesis 28(3):672–676PubMedCrossRefGoogle Scholar
  8. Banerjee N et al (2011) Polymorphisms in the TNF-α and IL10 gene promoters and risk of arsenic-induced skin lesions and other nondermatological health effects. Toxicol Sci 121(1):132–139PubMedPubMedCentralCrossRefGoogle Scholar
  9. Banerjee M et al (2014) A novel pathway for arsenic elimination: human multidrug resistance protein 4 (MRP4/ABCC4) mediates cellular export of dimethylarsinic acid (DMAV) and the diglutathione conjugate of monomethylarsonous acid (MMAIII). Mol Pharmacol 86(2):168–179PubMedCrossRefGoogle Scholar
  10. Banerjee M et al (2016) Polymorphic variants of MRP4/ABCC4 differentially modulate the transport of methylated arsenic metabolites and physiological organic anions. Biochem Pharmacol 120:72–82PubMedCrossRefGoogle Scholar
  11. Beebe-Dimmer JL et al (2012) Genetic variation in glutathione S-transferase omega-1, arsenic methyltransferase and methylene-tetrahydrofolate reductase, arsenic exposure and bladder cancer: a case–control study. Environ Health 11(1):43PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bhattacharjee P et al (2013) Association of NALP2 polymorphism with arsenic induced skin lesions and other health effects. Mutat Res Genet Toxicol Environ Mutagen 755(1):1–5CrossRefGoogle Scholar
  13. Breton CV et al (2007) Susceptibility to arsenic-induced skin lesions from polymorphisms in base excision repair genes. Carcinogenesis 28(7):1520–1525PubMedCrossRefGoogle Scholar
  14. Challenger F (1945) Biological methylation. Chem Rev 36(3):315–361CrossRefGoogle Scholar
  15. Chattopadhyay S et al (2002) Apoptosis and necrosis in developing brain cells due to arsenic toxicity and protection with antioxidants. Toxicol Lett 136(1):65–76PubMedCrossRefGoogle Scholar
  16. Chen H et al (1996) Methylation and demethylation of dimethylarsinic acid in rats following chronic oral exposure. Appl Organomet Chem 10(9):741–745CrossRefGoogle Scholar
  17. Chen C-L et al (2004) Ingested arsenic, cigarette smoking, and lung cancer risk: a follow-up study in arseniasis-endemic areas in Taiwan. JAMA 292(24):2984–2990PubMedCrossRefGoogle Scholar
  18. Chen C-J et al (2005) Biomarkers of exposure, effect, and susceptibility of arsenic-induced health hazards in Taiwan. Toxicol Appl Pharmacol 206(2):198–206PubMedCrossRefGoogle Scholar
  19. Chen Y et al (2006) Modification of risk of arsenic-induced skin lesions by sunlight exposure, smoking, and occupational exposures in Bangladesh. Epidemiology 17(4):459–467PubMedCrossRefGoogle Scholar
  20. Chen J-W et al (2012a) Arsenic methylation, GSTO1 polymorphisms, and metabolic syndrome in an arseniasis endemic area of southwestern Taiwan. Chemosphere 88(4):432–438PubMedCrossRefGoogle Scholar
  21. Chen S-C et al (2012b) Elevated risk of hypertension induced by arsenic exposure in Taiwanese rural residents: possible effects of manganese superoxide dismutase (MnSOD) and 8-oxoguanine DNA glycosylase (OGG1) genes. Arch Toxicol 86(6):869–878PubMedCrossRefGoogle Scholar
  22. Chi L et al (2016) Sex-specific effects of arsenic exposure on the trajectory and function of the gut microbiome. Chem Res Toxicol 29(6):949–951PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chi L et al (2017) The effects of an environmentally relevant level of arsenic on the gut microbiome and its functional metagenome. Toxicol Sci 160:193–204PubMedCrossRefGoogle Scholar
  24. Chiang C-I et al (2014) XRCC1 Arg194Trp and Arg399Gln polymorphisms and arsenic methylation capacity are associated with urothelial carcinoma. Toxicol Appl Pharmacol 279(3):373–379PubMedCrossRefGoogle Scholar
  25. Chiou H-Y et al (1997) Arsenic methylation capacity, body retention, and null genotypes of glutathione S-transferase M1 and T1 among current arsenic-exposed residents in Taiwan. Mutat Res Rev Mutat Res 386(3):197–207CrossRefGoogle Scholar
  26. Choi A, Alam J (1996) Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am J Respir Cell Mol Biol 15(1):9–19PubMedCrossRefGoogle Scholar
  27. Chowdhury UK et al (2006) Glutathione-S-transferase-omega [MMA (V) reductase] knockout mice: enzyme and arsenic species concentrations in tissues after arsenate administration. Toxicol Appl Pharmacol 216(3):446–457PubMedCrossRefGoogle Scholar
  28. Chung C-J et al (2011) Gene polymorphisms of glutathione S-transferase omega 1 and 2, urinary arsenic methylation profile and urothelial carcinoma. Sci Total Environ 409(3):465–470PubMedCrossRefGoogle Scholar
  29. Clemente MJ, Devesa V, Vélez D (2016) Dietary strategies to reduce the bioaccessibility of arsenic from food matrices. J Agric Food Chem 64(4):923–931PubMedCrossRefGoogle Scholar
  30. Consortium HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214CrossRefGoogle Scholar
  31. Cullen WR (2014) Chemical mechanism of arsenic biomethylation. Chem Res Toxicol 27(4):457–461PubMedCrossRefGoogle Scholar
  32. Cullen W, McBride B, Reglinski J (1984) The reduction of trimethylarsine oxide to trimethylarsine by thiols: a mechanistic model for the biological reduction of arsenicals. J Inorg Biochem 21(1):45–60CrossRefGoogle Scholar
  33. Dangleben NL, Skibola CF, Smith MT (2013) Arsenic immunotoxicity: a review. Environ Health 12(1):73PubMedPubMedCentralCrossRefGoogle Scholar
  34. Das N et al (2016) Association of single nucleotide polymorphism with arsenic-induced skin lesions and genetic damage in exposed population of West Bengal, India. Mutat Res Genet Toxicol Environ Mutagen 809:50–56CrossRefGoogle Scholar
  35. Dash JR et al (2013) Chronic arsenicosis in cattle: possible mitigation with Zn and Se. Ecotoxicol Environ Saf 92:119–122PubMedCrossRefGoogle Scholar
  36. De Chaudhuri S et al (2006) Association of specific p53 polymorphisms with keratosis in individuals exposed to arsenic through drinking water in West Bengal, India. Mutat Res Genet Toxicol Environ Mutagen 601(1):102–112CrossRefGoogle Scholar
  37. De Chaudhuri S et al (2008) Genetic variants associated with arsenic susceptibility: study of purine nucleoside phosphorylase, arsenic (+ 3) methyltransferase, and glutathione S-transferase omega genes. Environ Health Perspect 116(4):501PubMedPubMedCentralGoogle Scholar
  38. Dheeman DS et al (2014) Pathway of human AS3MT arsenic methylation. Chem Res Toxicol 27(11):1979–1989PubMedPubMedCentralCrossRefGoogle Scholar
  39. Ding W, Hudson LG, Liu KJ (2005) Inorganic arsenic compounds cause oxidative damage to DNA and protein by inducing ROS and RNS generation in human keratinocytes. Mol Cell Biochem 279(1):105–112PubMedCrossRefGoogle Scholar
  40. Ding L et al (2012) Methylation of arsenic by recombinant human wild-type arsenic (+ 3 oxidation state) methyltransferase and its methionine 287 threonine (M287T) polymorph: role of glutathione. Toxicol Appl Pharmacol 264(1):121–130PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dutta M et al (2014) High fat diet aggravates arsenic induced oxidative stress in rat heart and liver. Food Chem Toxicol 66:262–277PubMedCrossRefGoogle Scholar
  42. Eckburg PB et al (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638PubMedPubMedCentralCrossRefGoogle Scholar
  43. Engström KS et al (2007) Genetic polymorphisms influencing arsenic metabolism: evidence from Argentina. Environ Health Perspect 115(4):599PubMedCentralCrossRefGoogle Scholar
  44. Faita F et al (2013) Arsenic-induced genotoxicity and genetic susceptibility to arsenic-related pathologies. Int J Environ Res Public Health 10(4):1527–1546PubMedPubMedCentralCrossRefGoogle Scholar
  45. Falony G et al (2016) Population-level analysis of gut microbiome variation. Science 352(6285):560–564PubMedCrossRefGoogle Scholar
  46. Fox JT, Stover PJ (2008) Folate-mediated one-carbon metabolism. Vitam Horm 79:1–44PubMedCrossRefGoogle Scholar
  47. Frosina G (2004) Commentary DNA base excision repair defects in human pathologies. Free Radical Res 38(10):1037–1054CrossRefGoogle Scholar
  48. Fujihara J et al (2011) Polymorphic trial in oxidative damage of arsenic exposed Vietnamese. Toxicol Appl Pharmacol 256(2):174–178PubMedCrossRefGoogle Scholar
  49. Gamble MV et al (2005) Folate, homocysteine, and arsenic metabolism in arsenic-exposed individuals in Bangladesh. Environ Health Perspect 113(12):1683PubMedPubMedCentralCrossRefGoogle Scholar
  50. Gamble MV et al (2007) Folic acid supplementation lowers blood arsenic. Am J Clin Nutr 86(4):1202–1209PubMedPubMedCentralCrossRefGoogle Scholar
  51. Ghosh P et al (2006) Cytogenetic damage and genetic variants in the individuals susceptible to arsenic-induced cancer through drinking water. Int J Cancer 118(10):2470–2478PubMedCrossRefGoogle Scholar
  52. Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359PubMedPubMedCentralCrossRefGoogle Scholar
  53. Gomez A et al (2012) Loss of sex and age driven differences in the gut microbiome characterize arthritis-susceptible* 0401 mice but not arthritis-resistant* 0402 mice. PLoS ONE 7(4):e36095PubMedPubMedCentralCrossRefGoogle Scholar
  54. Gregus Z, Németi B (2002) Purine nucleoside phosphorylase as a cytosolic arsenate reductase. Toxicol Sci 70(1):13–19PubMedCrossRefGoogle Scholar
  55. Gregus Z et al (2009) Mechanism of thiol-supported arsenate reduction mediated by phosphorolytic-arsenolytic enzymes: II. Enzymatic formation of arsenylated products susceptible for reduction to arsenite by thiols. Toxicol Sci 110(2):282–292PubMedCrossRefGoogle Scholar
  56. Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170PubMedPubMedCentralCrossRefGoogle Scholar
  57. Guarner F, Malagelada J-R (2003) Gut flora in health and disease. Lancet 361(9356):512–519PubMedCrossRefGoogle Scholar
  58. Hall MN et al (2009) Folate, cobalamin, cysteine, homocysteine, and arsenic metabolism among children in Bangladesh. Environ Health Perspect 117(5):825PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hernández A, Marcos R (2008) Genetic variations associated with interindividual sensitivity in the response to arsenic exposure. Pharmacogenomics 9(8):1113–1132PubMedCrossRefGoogle Scholar
  60. Hernández A et al (2008) Role of the Met 287 Thr polymorphism in the AS3MT gene on the metabolic arsenic profile. Mutat Res Fundam Mol Mech Mutagen 637(1):80–92CrossRefGoogle Scholar
  61. Hernández A et al (2014) Micronucleus frequency in copper-mine workers exposed to arsenic is modulated by the AS3MT Met287Thr polymorphism. Mutat Res Genet Toxicol Environ Mutagen 759:51–55PubMedCrossRefGoogle Scholar
  62. Hill M (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6(2):S43–S45PubMedCrossRefGoogle Scholar
  63. Hirano S et al (2004) The accumulation and toxicity of methylated arsenicals in endothelial cells: important roles of thiol compounds. Toxicol Appl Pharmacol 198(3):458–467PubMedCrossRefGoogle Scholar
  64. Hou H et al (2017) Hepatic transcriptomic responses in mice exposed to arsenic and different fat diet. Environ Sci Pollut Res 24(11):10621–10629CrossRefGoogle Scholar
  65. Hsieh Y-C et al (2011) Significantly increased risk of carotid atherosclerosis with arsenic exposure and polymorphisms in arsenic metabolism genes. Environ Res 111(6):804–810PubMedCrossRefGoogle Scholar
  66. Hsu L-I et al (2015) Association of environmental arsenic exposure, genetic polymorphisms of susceptible genes, and skin cancers in Taiwan. BioMed Res Int 2015:892579.  https://doi.org/10.1155/2015/892579
  67. Hsueh Y-M et al (1997) Serum beta-carotene level, arsenic methylation capability, and incidence of skin cancer. Cancer Epidemiol Prev Biomark 6(8):589–596Google Scholar
  68. Hsueh Y-M et al (1998) Low serum carotene level and increased risk of ischemic heart disease related to long-term arsenic exposure. Atherosclerosis 141(2):249–257PubMedCrossRefGoogle Scholar
  69. Hsueh Y-M et al (2005) Genetic polymorphisms of oxidative and antioxidant enzymes and arsenic-related hypertension. J Toxicol Environ Health Part A 68(17–18):1471–1484PubMedCrossRefGoogle Scholar
  70. Huang C-Y et al (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(3):349–355PubMedCrossRefGoogle Scholar
  71. Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133(1):1–16PubMedCrossRefGoogle Scholar
  72. Ilett KF et al (1990) Metabolism of drugs and other xenobiotics in the gut lumen and wall. Pharmacol Ther 46(1):67–93PubMedCrossRefGoogle Scholar
  73. Isokpehi RD et al (2014) Evaluative profiling of arsenic sensing and regulatory systems in the human microbiome project genomes. Microbiol Insights 7:25PubMedPubMedCentralCrossRefGoogle Scholar
  74. Järup L, Pershagen G (1991) Arsenic exposure, smoking, and lung cancer in smelter workers—a case-control study. Am J Epidemiol 134(6):545–551PubMedCrossRefGoogle Scholar
  75. Jhee K-H, Kruger WD (2005) The role of cystathionine β-synthase in homocysteine metabolism. Antioxid Redox Signal 7(5–6):813–822PubMedCrossRefGoogle Scholar
  76. Kaya-Akyüzlü D, Kayaaltı Z, Söylemezoğlu T (2016) Influence of MRP1 G1666A and GSTP1 Ile105Val genetic variants on the urinary and blood arsenic levels of Turkish smelter workers. Environ Toxicol Pharmacol 43:68–73PubMedCrossRefGoogle Scholar
  77. Koppel N, Rekdal VM, Balskus EP (2017) Chemical transformation of xenobiotics by the human gut microbiota. Science 356(6344):eaag2770PubMedPubMedCentralCrossRefGoogle Scholar
  78. Kubachka KM et al (2009) In vitro biotransformation of dimethylarsinic acid and trimethylarsine oxide by anaerobic microflora of mouse cecum analyzed by HPLC-ICP-MS and HPLC-ESI-MS. J Anal At Spectrom 24(8):1062–1068CrossRefGoogle Scholar
  79. Kumar A et al (2010) Protective role of zinc in ameliorating arsenic-induced oxidative stress and histological changes in rat liver. J Environ Pathol Toxicol Oncol 29(2)Google Scholar
  80. Kundu M et al (2011) Precancerous and non-cancer disease endpoints of chronic arsenic exposure: the level of chromosomal damage and XRCC3 T241M polymorphism. Mutat Res Fundam Mol Mech Mutagen 706(1):7–12CrossRefGoogle Scholar
  81. Kuroda K et al (2004) Microbial metabolite of dimethylarsinic acid is highly toxic and genotoxic. Toxicol Appl Pharmacol 198(3):345–353PubMedCrossRefGoogle Scholar
  82. Laird BD et al (2007) Gastrointestinal microbes increase arsenic bioaccessibility of ingested mine tailings using the simulator of the human intestinal microbial ecosystem. Environ Sci Technol 41(15):5542–5547PubMedCrossRefGoogle Scholar
  83. LeBlanc JG et al (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opin Biotechnol 24(2):160–168CrossRefGoogle Scholar
  84. Li L et al (2008) Nutritional status has marginal influence on the metabolism of inorganic arsenic in pregnant Bangladeshi women. Environ Health Perspect 116(3):315PubMedCrossRefGoogle Scholar
  85. Lin G-F et al (2006) Arsenic-related skin lesions and glutathione S-transferase P1 A1578G (Ile105Val) polymorphism in two ethnic clans exposed to indoor combustion of high arsenic coal in one village. Pharmacogenet Genomics 16(12):863–871PubMedCrossRefGoogle Scholar
  86. Lin G-f et al (2007) Glutathione S-transferases M1 and T1 polymorphisms and arsenic content in hair and urine in two ethnic clans exposed to indoor combustion of high arsenic coal in Southwest Guizhou. China Arch Toxicol 81(8):545–551PubMedCrossRefGoogle Scholar
  87. Lin G-f et al (2010) Association of XPD/ERCC2 G23591A and A35931C polymorphisms with skin lesion prevalence in a multiethnic, arseniasis-hyperendemic village exposed to indoor combustion of high arsenic coal. Arch Toxicol 84(1):17PubMedCrossRefGoogle Scholar
  88. Lindberg A-L et al (2007) Metabolism of low-dose inorganic arsenic in a central European population: influence of sex and genetic polymorphisms. Environ Health Perspect 115(7):1081PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lindenbaum J et al (1981) Inactivation of digoxin by the gut flora: reversal by antibiotic therapy. N Engl J Med 305(14):789–794PubMedCrossRefGoogle Scholar
  90. Liu Z et al (2004) Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem Biophys Res Commun 316(4):1178–1185PubMedCrossRefGoogle Scholar
  91. Liu Z et al (2006) Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem Biophys Res Commun 351(2):424–430PubMedPubMedCentralCrossRefGoogle Scholar
  92. Lu K et al (2013) Gut microbiome perturbations induced by bacterial infection affect arsenic biotransformation. Chem Res Toxicol 26(12):1893–1903PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lu K et al (2014a) Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ Health Perspect 122(3):284–291PubMedPubMedCentralGoogle Scholar
  94. Lu K et al (2014b) Gut microbiome phenotypes driven by host genetics affect arsenic metabolism. Chem Res Toxicol 27(2):172–174PubMedPubMedCentralCrossRefGoogle Scholar
  95. Maiti S et al (2017) Green tea (Camellia sinensis) protects against arsenic neurotoxicity via antioxidative mechanism and activation of superoxide dismutase activity. Cent Nerv Syst Agents Med Chem 17(3):187–195PubMedCrossRefGoogle Scholar
  96. Markle JG et al (2013) Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339(6123):1084–1088PubMedCrossRefGoogle Scholar
  97. Martin F-PJ et al (2010) Dietary modulation of gut functional ecology studied by fecal metabonomics. J Proteome Res 9(10):5284–5295PubMedCrossRefGoogle Scholar
  98. McCarty KM et al (2006) The impact of diet and betel nut use on skin lesions associated with drinking-water arsenic in Pabna, Bangladesh. Environ Health Perspect 114(3):334PubMedCrossRefGoogle Scholar
  99. McCarty KM et al (2007a) Polymorphisms in XPD (Asp312Asn and Lys751Gln) genes, sunburn and arsenic-related skin lesions. Carcinogenesis 28(8):1697–1702PubMedCrossRefGoogle Scholar
  100. McCarty KM et al (2007b) A case-control study of GST polymorphisms and arsenic related skin lesions. Environmental Health 6(1):5PubMedPubMedCentralCrossRefGoogle Scholar
  101. Meza MM et al (2005) Developmentally restricted genetic determinants of human arsenic metabolism: association between urinary methylated arsenic and CYT19 polymorphisms in children. Environ Health Perspect 113(6):775PubMedPubMedCentralCrossRefGoogle Scholar
  102. Mitra SR et al (2004) Nutritional factors and susceptibility to arsenic-caused skin lesions in West Bengal, India. Environ Health Perspect 112(10):1104PubMedPubMedCentralCrossRefGoogle Scholar
  103. Mukherjee S et al (2006) Synergistic effect of folic acid and vitamin B 12 in ameliorating arsenic-induced oxidative damage in pancreatic tissue of rat. J Nutr Biochem 17(5):319–327PubMedCrossRefGoogle Scholar
  104. Naranmandura H, Suzuki N, Suzuki KT (2006) Trivalent arsenicals are bound to proteins during reductive methylation. Chem Res Toxicol 19(8):1010–1018PubMedCrossRefGoogle Scholar
  105. Naranmandura H, Ibata K, Suzuki KT (2007) Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 20(8):1120–1125PubMedCrossRefGoogle Scholar
  106. Naujokas MF et al (2013) The broad scope of health effects from chronic arsenic exposure: update on a worldwide public health problem. Environ Health Perspect 121(3):295PubMedPubMedCentralCrossRefGoogle Scholar
  107. Nicholson JK et al (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267PubMedCrossRefGoogle Scholar
  108. Petrick JS et al (2001) Monomethylarsonous acid (MMAIII) and arsenite: LD50 in hamsters and in vitro inhibition of pyruvate dehydrogenase. Chem Res Toxicol 14(6):651–656PubMedCrossRefGoogle Scholar
  109. Pinyayev TS et al (2011) Preabsorptive metabolism of sodium arsenate by anaerobic microbiota of mouse cecum forms a variety of methylated and thiolated arsenicals. Chem Res Toxicol 24(4):475–477PubMedCrossRefGoogle Scholar
  110. Porter KE et al (2010) Association of genetic variation in cystathionine-β-synthase and arsenic metabolism. Environ Res 110(6):580–587PubMedPubMedCentralCrossRefGoogle Scholar
  111. Radabaugh TR et al (2002) Arsenate reductase II. Purine nucleoside phosphorylase in the presence of dihydrolipoic acid is a route for reduction of arsenate to arsenite in mammalian systems. Chem Res Toxicol 15(5):692–698PubMedCrossRefGoogle Scholar
  112. Ramanathan K, Balakumar B, Panneerselvam C (2002) Effects of ascorbic acid and a-tocopherol on arsenic-induced oxidative stress. Hum Exp Toxicol 21(12):675–680PubMedCrossRefGoogle Scholar
  113. Raposo JC, Olazábal MA, Madariaga JM (2006) Complexation and precipitation of arsenate and iron species in sodium perchlorate solutions at 25 °C. J Solution Chem 35(1):79–94CrossRefGoogle Scholar
  114. Recio-Vega R et al (2015) MRP1 expression in bronchoalveolar lavage cells in subjects with lung cancer who were chronically exposed to arsenic. Environ Mol Mutagen 56(9):759–766PubMedCrossRefGoogle Scholar
  115. Reddy PS et al (2011) Protective effects of N-acetylcysteine against arsenic-induced oxidative stress and reprotoxicity in male mice. J Trace Elem Med Biol 25(4):247–253PubMedCrossRefGoogle Scholar
  116. Roggenbeck BA, Banerjee M, Leslie EM (2016) Cellular arsenic transport pathways in mammals. J Environ Sci 49:38–58CrossRefGoogle Scholar
  117. Rossi M, Amaretti A, Raimondi S (2011) Folate production by probiotic bacteria. Nutrients 3(1):118–134PubMedPubMedCentralCrossRefGoogle Scholar
  118. Rowland I, Davies M (1981) In vitro metabolism of inorganic arsenic by the gastro-intestinal microflora of the rat. J Appl Toxicol 1(5):278–283PubMedCrossRefGoogle Scholar
  119. Rubin SSD et al (2014) Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. Environ Health Perspect 122(8):817Google Scholar
  120. Ruby MV et al (1996) Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ Sci Technol 30(2):422–430CrossRefGoogle Scholar
  121. Schloissnig S et al (2013) Genomic variation landscape of the human gut microbiome. Nature 493(7430):45–50PubMedCrossRefGoogle Scholar
  122. Schromm AB et al (2000) Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem 267(7):2008–2013PubMedCrossRefGoogle Scholar
  123. Sinha D et al (2003) Modulation of arsenic induced cytotoxicity by tea. Asian Pac J Cancer Prev 4(3):233–238PubMedGoogle Scholar
  124. Sinha D, Roy S, Roy M (2010) Antioxidant potential of tea reduces arsenite induced oxidative stress in Swiss albino mice. Food Chem Toxicol 48(4):1032–1039PubMedCrossRefGoogle Scholar
  125. Spanogiannopoulos P et al (2016) The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat Rev Microbiol 14(5):273–287PubMedPubMedCentralCrossRefGoogle Scholar
  126. Steinmaus C et al (2007) Genetic polymorphisms in MTHFR 677 and 1298, GSTM1 and T1, and metabolism of arsenic. J Toxicol Environ Health Part A 70(2):159–170PubMedCrossRefGoogle Scholar
  127. Steinmaus C et al (2010) Individual differences in arsenic metabolism and lung cancer in a case-control study in Cordoba, Argentina. Toxicol Appl Pharmacol 247(2):138–145PubMedCrossRefGoogle Scholar
  128. Styblo M et al (2000) Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 74(6):289–299PubMedCrossRefGoogle Scholar
  129. Suez J et al (2014) Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514(7521):181–186PubMedCrossRefGoogle Scholar
  130. Sun H-J et al (2014) Arsenic and selenium toxicity and their interactive effects in humans. Environ Int 69:148–158PubMedCrossRefGoogle Scholar
  131. Sun B-F et al (2015) Exercise prevents memory impairment induced by arsenic exposure in mice: implication of hippocampal BDNF and CREB. PLoS ONE 10(9):e0137810PubMedPubMedCentralCrossRefGoogle Scholar
  132. Suzuki T et al (1992) NAD (P) H-dependent chromium (VI) reductase of Pseudomonas ambigua G-1: a Cr (V) intermediate is formed during the reduction of Cr (VI) to Cr (III). J Bacteriol 174(16):5340–5345PubMedPubMedCentralCrossRefGoogle Scholar
  133. Takeno S, Sakai T (1991) Involvement of the intestinal microflora in nitrazepam-induced teratogenicity in rats and its relationship to nitroreduction. Teratology 44(2):209–214PubMedCrossRefGoogle Scholar
  134. Tanaka-Kagawa T et al (2003) Functional characterization of two variant human GSTO 1-1s (Ala140Asp and Thr217Asn). Biochem Biophys Res Commun 301(2):516–520PubMedCrossRefGoogle Scholar
  135. Taneja V (2014) Arthritis susceptibility and the gut microbiome. FEBS Lett 588(22):4244–4249PubMedPubMedCentralCrossRefGoogle Scholar
  136. Theriot CM et al (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114PubMedPubMedCentralCrossRefGoogle Scholar
  137. Thomas DJ (2010) Arsenolysis and thiol-dependent arsenate reduction. Toxicol Sci 117(2):249–252PubMedCrossRefGoogle Scholar
  138. Thompson LH et al (1990) Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol Cell Biol 10(12):6160–6171PubMedPubMedCentralCrossRefGoogle Scholar
  139. Tsang BL et al (2015) Assessing the association between the methylenetetrahydrofolate reductase (MTHFR) 677C > T polymorphism and blood folate concentrations: a systematic review and meta-analysis of trials and observational studies. Am J Clin Nutr 101(6):1286–1294PubMedCrossRefGoogle Scholar
  140. Tseng C-H (2009) A review on environmental factors regulating arsenic methylation in humans. Toxicol Appl Pharmacol 235(3):338–350PubMedCrossRefGoogle Scholar
  141. Turnbaugh PJ et al (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1131PubMedCrossRefGoogle Scholar
  142. Ueland PM, Holm PI, Hustad S (2005) Betaine: a key modulator of one-carbon metabolism and homocysteine status. Clin Chem Lab Med 43(10):1069–1075PubMedCrossRefGoogle Scholar
  143. Vahter M, Marafante E (1987) Effects of low dietary intake of methionine, choline or proteins on the biotransformation of arsenite in the rabbit. Toxicol Lett 37(1):41–46PubMedCrossRefGoogle Scholar
  144. Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health Part C 27(2):120–139CrossRefGoogle Scholar
  145. Van de Wiele T et al (2010) Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ Health Perspect 118:1004–1009PubMedPubMedCentralCrossRefGoogle Scholar
  146. Villa-Bellosta R, Sorribas V (2010) Arsenate transport by sodium/phosphate cotransporter type IIb. Toxicol Appl Pharmacol 247(1):36–40PubMedCrossRefGoogle Scholar
  147. Wang Y, Zhao F (2009) Effects of exogenous glutathione on arsenic distribution and NO metabolism in brain of female mice exposed to sodium arsenite through drinking water. J Environ Health 26(12):1046–1048Google Scholar
  148. Wang Y-H et al (2007) Effects of arsenic exposure and genetic polymorphisms of p53, glutathione S-transferase M1, T1, and P1 on the risk of carotid atherosclerosis in Taiwan. Atherosclerosis 192(2):305–312PubMedCrossRefGoogle Scholar
  149. Wlodarczyk BJ, Zhu H, Finnell RH (2014) Mthfr gene ablation enhances susceptibility to arsenic prenatal toxicity. Toxicol Appl Pharmacol 275(1):22–27PubMedCrossRefGoogle Scholar
  150. Wood RD et al (2001) Human DNA repair genes. Science 291(5507):1284–1289PubMedCrossRefGoogle Scholar
  151. Wu J et al (2008) High dietary fat exacerbates arsenic-induced liver fibrosis in mice. Exp Biol Med 233(3):377–384CrossRefGoogle Scholar
  152. Wu M-M et al (2010) GT-repeat polymorphism in the heme oxygenase-1 gene promoter and the risk of carotid atherosclerosis related to arsenic exposure. J Biomed Sci 17(1):70PubMedPubMedCentralCrossRefGoogle Scholar
  153. Wu M-M et al (2011) Association of heme oxygenase-1 GT-repeat polymorphism with blood pressure phenotypes and its relevance to future cardiovascular mortality risk: an observation based on arsenic-exposed individuals. Atherosclerosis 219(2):704–708PubMedCrossRefGoogle Scholar
  154. Wu C-C et al (2013) Polymorphism of inflammatory genes and arsenic methylation capacity are associated with urothelial carcinoma. Toxicol Appl Pharmacol 272(1):30–36PubMedCrossRefGoogle Scholar
  155. Wu M et al (2014) Cell-type-dependent associations of heme oxygenase-1 GT-repeat polymorphisms with the cancer risk in arsenic-exposed individuals: a preliminary report. In: 5th international congress on arsenic in the environment, As 2014. CRC Press/Balkema, Boca RatonGoogle Scholar
  156. Yatsunenko T et al (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222PubMedPubMedCentralGoogle Scholar
  157. Yin N et al (2015) In vitro method to assess soil arsenic metabolism by human gut microbiota: arsenic speciation and distribution. Environ Sci Technol 49(17):10675–10681PubMedCrossRefGoogle Scholar
  158. Yin N et al (2017) Interindividual variability of soil arsenic metabolism by human gut microbiota using SHIME model. ChemosphereGoogle Scholar
  159. Yu H et al (2016a) Arsenic metabolism and toxicity influenced by ferric iron in simulated gastrointestinal tract and the roles of gut microbiota. Environ Sci Technol 50(13):7189–7197PubMedCrossRefGoogle Scholar
  160. Yu H et al (2016b) Influence of diet, vitamin, tea, trace elements and exogenous antioxidants on arsenic metabolism and toxicity. Environ Geochem Health 38(2):339–351PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Environmental Sciences and EngineeringUniversity of North Carolina at Chapel HillChapel HillUSA
  2. 2.NIH West Coast Metabolomics CenterUniversity of CaliforniaDavisUSA
  3. 3.Department of Population Health and PathobiologyNorth Carolina State UniversityRaleighUSA

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