Skip to main content

Advertisement

Log in

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

  • Review
  • Published:
Mammalian Genome Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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):352–362

    Article  CAS  PubMed  Google Scholar 

  • Ahsan H et al (2003) Susceptibility to arsenic-induced hyperkeratosis and oxidative stress genes myeloperoxidase and catalase. Cancer Lett 201(1):57–65

    Article  CAS  PubMed  Google Scholar 

  • Ahsan H et al (2007) Arsenic metabolism, genetic susceptibility, and risk of premalignant skin lesions in Bangladesh. Cancer Epidemiol Prev Biomark 16(6):1270–1278

    Article  CAS  Google Scholar 

  • Antonelli R et al (2014) AS3MT, GSTO, and PNP polymorphisms: impact on arsenic methylation and implications for disease susceptibility. Environ Res 132:156–167

    Article  CAS  PubMed  Google Scholar 

  • Bacher A et al (2000) Biosynthesis of vitamin B2 (riboflavin). Annu Rev Nutr 20(1):153–167

    Article  CAS  PubMed  Google Scholar 

  • Bäckhed F et al (2005) Host-bacterial mutualism in the human intestine. Science 307(5717):1915–1920

    Article  PubMed  CAS  Google Scholar 

  • 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):672–676

    Article  CAS  PubMed  Google Scholar 

  • 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):132–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):168–179

    Article  PubMed  CAS  Google Scholar 

  • Banerjee M et al (2016) Polymorphic variants of MRP4/ABCC4 differentially modulate the transport of methylated arsenic metabolites and physiological organic anions. Biochem Pharmacol 120:72–82

    Article  CAS  PubMed  Google Scholar 

  • 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):43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1–5

    Article  CAS  Google Scholar 

  • Breton CV et al (2007) Susceptibility to arsenic-induced skin lesions from polymorphisms in base excision repair genes. Carcinogenesis 28(7):1520–1525

    Article  CAS  PubMed  Google Scholar 

  • Challenger F (1945) Biological methylation. Chem Rev 36(3):315–361

    Article  CAS  Google Scholar 

  • Chattopadhyay S et al (2002) Apoptosis and necrosis in developing brain cells due to arsenic toxicity and protection with antioxidants. Toxicol Lett 136(1):65–76

    Article  CAS  PubMed  Google Scholar 

  • Chen H et al (1996) Methylation and demethylation of dimethylarsinic acid in rats following chronic oral exposure. Appl Organomet Chem 10(9):741–745

    Article  CAS  Google Scholar 

  • 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):2984–2990

    Article  CAS  PubMed  Google Scholar 

  • Chen C-J et al (2005) Biomarkers of exposure, effect, and susceptibility of arsenic-induced health hazards in Taiwan. Toxicol Appl Pharmacol 206(2):198–206

    Article  CAS  PubMed  Google Scholar 

  • 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):459–467

    Article  PubMed  Google Scholar 

  • Chen J-W et al (2012a) Arsenic methylation, GSTO1 polymorphisms, and metabolic syndrome in an arseniasis endemic area of southwestern Taiwan. Chemosphere 88(4):432–438

    Article  CAS  PubMed  Google Scholar 

  • 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):869–878

    Article  CAS  PubMed  Google Scholar 

  • 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):949–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi L et al (2017) The effects of an environmentally relevant level of arsenic on the gut microbiome and its functional metagenome. Toxicol Sci 160:193–204

    Article  PubMed  Google Scholar 

  • 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):373–379

    Article  CAS  PubMed  Google Scholar 

  • 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):197–207

    Article  Google Scholar 

  • 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):9–19

    Article  CAS  PubMed  Google Scholar 

  • 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):446–457

    Article  CAS  PubMed  Google Scholar 

  • 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):465–470

    Article  CAS  PubMed  Google Scholar 

  • Clemente MJ, Devesa V, Vélez D (2016) Dietary strategies to reduce the bioaccessibility of arsenic from food matrices. J Agric Food Chem 64(4):923–931

    Article  CAS  PubMed  Google Scholar 

  • Consortium HMP (2012) Structure, function and diversity of the healthy human microbiome. Nature 486(7402):207–214

    Article  CAS  Google Scholar 

  • Cullen WR (2014) Chemical mechanism of arsenic biomethylation. Chem Res Toxicol 27(4):457–461

    Article  CAS  PubMed  Google Scholar 

  • 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):45–60

    Article  CAS  Google Scholar 

  • Dangleben NL, Skibola CF, Smith MT (2013) Arsenic immunotoxicity: a review. Environ Health 12(1):73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 809:50–56

    Article  CAS  Google Scholar 

  • Dash JR et al (2013) Chronic arsenicosis in cattle: possible mitigation with Zn and Se. Ecotoxicol Environ Saf 92:119–122

    Article  CAS  PubMed  Google Scholar 

  • 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):102–112

    Article  CAS  Google Scholar 

  • 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):501

    PubMed  PubMed Central  Google Scholar 

  • Dheeman DS et al (2014) Pathway of human AS3MT arsenic methylation. Chem Res Toxicol 27(11):1979–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):105–112

    Article  CAS  PubMed  Google Scholar 

  • 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):121–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dutta M et al (2014) High fat diet aggravates arsenic induced oxidative stress in rat heart and liver. Food Chem Toxicol 66:262–277

    Article  CAS  PubMed  Google Scholar 

  • Eckburg PB et al (2005) Diversity of the human intestinal microbial flora. Science 308(5728):1635–1638

    Article  PubMed  PubMed Central  Google Scholar 

  • Engström KS et al (2007) Genetic polymorphisms influencing arsenic metabolism: evidence from Argentina. Environ Health Perspect 115(4):599

    Article  PubMed Central  CAS  Google Scholar 

  • Faita F et al (2013) Arsenic-induced genotoxicity and genetic susceptibility to arsenic-related pathologies. Int J Environ Res Public Health 10(4):1527–1546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falony G et al (2016) Population-level analysis of gut microbiome variation. Science 352(6285):560–564

    Article  CAS  PubMed  Google Scholar 

  • Fox JT, Stover PJ (2008) Folate-mediated one-carbon metabolism. Vitam Horm 79:1–44

    Article  CAS  PubMed  Google Scholar 

  • Frosina G (2004) Commentary DNA base excision repair defects in human pathologies. Free Radical Res 38(10):1037–1054

    Article  CAS  Google Scholar 

  • Fujihara J et al (2011) Polymorphic trial in oxidative damage of arsenic exposed Vietnamese. Toxicol Appl Pharmacol 256(2):174–178

    Article  CAS  PubMed  Google Scholar 

  • Gamble MV et al (2005) Folate, homocysteine, and arsenic metabolism in arsenic-exposed individuals in Bangladesh. Environ Health Perspect 113(12):1683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamble MV et al (2007) Folic acid supplementation lowers blood arsenic. Am J Clin Nutr 86(4):1202–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):2470–2478

    Article  CAS  PubMed  Google Scholar 

  • Gill SR et al (2006) Metagenomic analysis of the human distal gut microbiome. Science 312(5778):1355–1359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):e36095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregus Z, Németi B (2002) Purine nucleoside phosphorylase as a cytosolic arsenate reductase. Toxicol Sci 70(1):13–19

    Article  CAS  PubMed  Google Scholar 

  • 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):282–292

    Article  CAS  PubMed  Google Scholar 

  • Grice EA, Segre JA (2012) The human microbiome: our second genome. Annu Rev Genomics Hum Genet 13:151–170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guarner F, Malagelada J-R (2003) Gut flora in health and disease. Lancet 361(9356):512–519

    Article  PubMed  Google Scholar 

  • Hall MN et al (2009) Folate, cobalamin, cysteine, homocysteine, and arsenic metabolism among children in Bangladesh. Environ Health Perspect 117(5):825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernández A, Marcos R (2008) Genetic variations associated with interindividual sensitivity in the response to arsenic exposure. Pharmacogenomics 9(8):1113–1132

    Article  PubMed  CAS  Google Scholar 

  • 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):80–92

    Article  CAS  Google Scholar 

  • 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 759:51–55

    Article  PubMed  CAS  Google Scholar 

  • Hill M (1997) Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6(2):S43–S45

    Article  PubMed  Google Scholar 

  • 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):458–467

    Article  CAS  PubMed  Google Scholar 

  • Hou H et al (2017) Hepatic transcriptomic responses in mice exposed to arsenic and different fat diet. Environ Sci Pollut Res 24(11):10621–10629

    Article  CAS  Google Scholar 

  • 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):804–810

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Hsueh Y-M et al (1997) Serum beta-carotene level, arsenic methylation capability, and incidence of skin cancer. Cancer Epidemiol Prev Biomark 6(8):589–596

    CAS  Google Scholar 

  • 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):249–257

    Article  CAS  PubMed  Google Scholar 

  • 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):1471–1484

    Article  CAS  PubMed  Google Scholar 

  • 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):349–355

    Article  CAS  PubMed  Google Scholar 

  • Hughes MF (2002) Arsenic toxicity and potential mechanisms of action. Toxicol Lett 133(1):1–16

    Article  CAS  PubMed  Google Scholar 

  • Ilett KF et al (1990) Metabolism of drugs and other xenobiotics in the gut lumen and wall. Pharmacol Ther 46(1):67–93

    Article  CAS  PubMed  Google Scholar 

  • Isokpehi RD et al (2014) Evaluative profiling of arsenic sensing and regulatory systems in the human microbiome project genomes. Microbiol Insights 7:25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Järup L, Pershagen G (1991) Arsenic exposure, smoking, and lung cancer in smelter workers—a case-control study. Am J Epidemiol 134(6):545–551

    Article  PubMed  Google Scholar 

  • Jhee K-H, Kruger WD (2005) The role of cystathionine β-synthase in homocysteine metabolism. Antioxid Redox Signal 7(5–6):813–822

    Article  CAS  PubMed  Google Scholar 

  • 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 43:68–73

    Article  PubMed  CAS  Google Scholar 

  • Koppel N, Rekdal VM, Balskus EP (2017) Chemical transformation of xenobiotics by the human gut microbiota. Science 356(6344):eaag2770

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):1062–1068

    Article  CAS  Google Scholar 

  • 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)

  • 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):7–12

    Article  CAS  Google Scholar 

  • Kuroda K et al (2004) Microbial metabolite of dimethylarsinic acid is highly toxic and genotoxic. Toxicol Appl Pharmacol 198(3):345–353

    Article  CAS  PubMed  Google Scholar 

  • 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):5542–5547

    Article  CAS  PubMed  Google Scholar 

  • LeBlanc JG et al (2013) Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Current Opin Biotechnol 24(2):160–168

    Article  CAS  Google Scholar 

  • 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):315

    Article  CAS  PubMed  Google Scholar 

  • 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):863–871

    Article  CAS  PubMed  Google Scholar 

  • 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):545–551

    Article  CAS  PubMed  Google Scholar 

  • 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):17

    Article  CAS  PubMed  Google Scholar 

  • 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):1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindenbaum J et al (1981) Inactivation of digoxin by the gut flora: reversal by antibiotic therapy. N Engl J Med 305(14):789–794

    Article  CAS  PubMed  Google Scholar 

  • Liu Z et al (2004) Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem Biophys Res Commun 316(4):1178–1185

    Article  CAS  PubMed  Google Scholar 

  • Liu Z et al (2006) Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem Biophys Res Commun 351(2):424–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu K et al (2013) Gut microbiome perturbations induced by bacterial infection affect arsenic biotransformation. Chem Res Toxicol 26(12):1893–1903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):284–291

    PubMed  PubMed Central  Google Scholar 

  • Lu K et al (2014b) Gut microbiome phenotypes driven by host genetics affect arsenic metabolism. Chem Res Toxicol 27(2):172–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):187–195

    Article  CAS  PubMed  Google Scholar 

  • Markle JG et al (2013) Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339(6123):1084–1088

    Article  CAS  PubMed  Google Scholar 

  • Martin F-PJ et al (2010) Dietary modulation of gut functional ecology studied by fecal metabonomics. J Proteome Res 9(10):5284–5295

    Article  CAS  PubMed  Google Scholar 

  • 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):334

    Article  CAS  PubMed  Google Scholar 

  • McCarty KM et al (2007a) Polymorphisms in XPD (Asp312Asn and Lys751Gln) genes, sunburn and arsenic-related skin lesions. Carcinogenesis 28(8):1697–1702

    Article  CAS  PubMed  Google Scholar 

  • McCarty KM et al (2007b) A case-control study of GST polymorphisms and arsenic related skin lesions. Environmental Health 6(1):5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitra SR et al (2004) Nutritional factors and susceptibility to arsenic-caused skin lesions in West Bengal, India. Environ Health Perspect 112(10):1104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):319–327

    Article  CAS  PubMed  Google Scholar 

  • Naranmandura H, Suzuki N, Suzuki KT (2006) Trivalent arsenicals are bound to proteins during reductive methylation. Chem Res Toxicol 19(8):1010–1018

    Article  CAS  PubMed  Google Scholar 

  • Naranmandura H, Ibata K, Suzuki KT (2007) Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 20(8):1120–1125

    Article  CAS  PubMed  Google Scholar 

  • 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):295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicholson JK et al (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267

    Article  CAS  PubMed  Google Scholar 

  • 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):651–656

    Article  CAS  PubMed  Google Scholar 

  • 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):475–477

    Article  CAS  PubMed  Google Scholar 

  • Porter KE et al (2010) Association of genetic variation in cystathionine-β-synthase and arsenic metabolism. Environ Res 110(6):580–587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):692–698

    Article  CAS  PubMed  Google Scholar 

  • Ramanathan K, Balakumar B, Panneerselvam C (2002) Effects of ascorbic acid and a-tocopherol on arsenic-induced oxidative stress. Hum Exp Toxicol 21(12):675–680

    Article  CAS  PubMed  Google Scholar 

  • 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):79–94

    Article  CAS  Google Scholar 

  • 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):759–766

    Article  CAS  PubMed  Google Scholar 

  • 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):247–253

    Article  CAS  PubMed  Google Scholar 

  • Roggenbeck BA, Banerjee M, Leslie EM (2016) Cellular arsenic transport pathways in mammals. J Environ Sci 49:38–58

    Article  Google Scholar 

  • Rossi M, Amaretti A, Raimondi S (2011) Folate production by probiotic bacteria. Nutrients 3(1):118–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowland I, Davies M (1981) In vitro metabolism of inorganic arsenic by the gastro-intestinal microflora of the rat. J Appl Toxicol 1(5):278–283

    Article  CAS  PubMed  Google Scholar 

  • Rubin SSD et al (2014) Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. Environ Health Perspect 122(8):817

    CAS  Google Scholar 

  • Ruby MV et al (1996) Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ Sci Technol 30(2):422–430

    Article  CAS  Google Scholar 

  • Schloissnig S et al (2013) Genomic variation landscape of the human gut microbiome. Nature 493(7430):45–50

    Article  PubMed  CAS  Google Scholar 

  • Schromm AB et al (2000) Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur J Biochem 267(7):2008–2013

    Article  CAS  PubMed  Google Scholar 

  • Sinha D et al (2003) Modulation of arsenic induced cytotoxicity by tea. Asian Pac J Cancer Prev 4(3):233–238

    PubMed  Google Scholar 

  • 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):1032–1039

    Article  CAS  PubMed  Google Scholar 

  • Spanogiannopoulos P et al (2016) The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat Rev Microbiol 14(5):273–287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):159–170

    Article  CAS  PubMed  Google Scholar 

  • 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):138–145

    Article  CAS  PubMed  Google Scholar 

  • Styblo M et al (2000) Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 74(6):289–299

    Article  CAS  PubMed  Google Scholar 

  • Suez J et al (2014) Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514(7521):181–186

    Article  CAS  PubMed  Google Scholar 

  • Sun H-J et al (2014) Arsenic and selenium toxicity and their interactive effects in humans. Environ Int 69:148–158

    Article  CAS  PubMed  Google Scholar 

  • 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):e0137810

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):5340–5345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeno S, Sakai T (1991) Involvement of the intestinal microflora in nitrazepam-induced teratogenicity in rats and its relationship to nitroreduction. Teratology 44(2):209–214

    Article  CAS  PubMed  Google Scholar 

  • Tanaka-Kagawa T et al (2003) Functional characterization of two variant human GSTO 1-1s (Ala140Asp and Thr217Asn). Biochem Biophys Res Commun 301(2):516–520

    Article  CAS  PubMed  Google Scholar 

  • Taneja V (2014) Arthritis susceptibility and the gut microbiome. FEBS Lett 588(22):4244–4249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theriot CM et al (2014) Antibiotic-induced shifts in the mouse gut microbiome and metabolome increase susceptibility to Clostridium difficile infection. Nat Commun 5:3114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thomas DJ (2010) Arsenolysis and thiol-dependent arsenate reduction. Toxicol Sci 117(2):249–252

    Article  CAS  PubMed  Google Scholar 

  • 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):6160–6171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1286–1294

    Article  CAS  PubMed  Google Scholar 

  • Tseng C-H (2009) A review on environmental factors regulating arsenic methylation in humans. Toxicol Appl Pharmacol 235(3):338–350

    Article  CAS  PubMed  Google Scholar 

  • Turnbaugh PJ et al (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444(7122):1027–1131

    Article  PubMed  Google Scholar 

  • Ueland PM, Holm PI, Hustad S (2005) Betaine: a key modulator of one-carbon metabolism and homocysteine status. Clin Chem Lab Med 43(10):1069–1075

    Article  CAS  PubMed  Google Scholar 

  • 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):41–46

    Article  CAS  PubMed  Google Scholar 

  • 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):120–139

    Article  CAS  Google Scholar 

  • Van de Wiele T et al (2010) Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ Health Perspect 118:1004–1009

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Villa-Bellosta R, Sorribas V (2010) Arsenate transport by sodium/phosphate cotransporter type IIb. Toxicol Appl Pharmacol 247(1):36–40

    Article  CAS  PubMed  Google Scholar 

  • 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):1046–1048

    CAS  Google Scholar 

  • 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):305–312

    Article  CAS  PubMed  Google Scholar 

  • Wlodarczyk BJ, Zhu H, Finnell RH (2014) Mthfr gene ablation enhances susceptibility to arsenic prenatal toxicity. Toxicol Appl Pharmacol 275(1):22–27

    Article  CAS  PubMed  Google Scholar 

  • Wood RD et al (2001) Human DNA repair genes. Science 291(5507):1284–1289

    Article  CAS  PubMed  Google Scholar 

  • Wu J et al (2008) High dietary fat exacerbates arsenic-induced liver fibrosis in mice. Exp Biol Med 233(3):377–384

    Article  CAS  Google Scholar 

  • 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):70

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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):704–708

    Article  CAS  PubMed  Google Scholar 

  • Wu C-C et al (2013) Polymorphism of inflammatory genes and arsenic methylation capacity are associated with urothelial carcinoma. Toxicol Appl Pharmacol 272(1):30–36

    Article  CAS  PubMed  Google Scholar 

  • 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 Raton

    Google Scholar 

  • Yatsunenko T et al (2012) Human gut microbiome viewed across age and geography. Nature 486(7402):222

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):10675–10681

    Article  CAS  PubMed  Google Scholar 

  • Yin N et al (2017) Interindividual variability of soil arsenic metabolism by human gut microbiota using SHIME model. Chemosphere

  • 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):7189–7197

    Article  CAS  PubMed  Google Scholar 

  • 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):339–351

    Article  CAS  PubMed  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kun Lu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chi, L., Gao, B., Tu, P. et al. Individual susceptibility to arsenic-induced diseases: the role of host genetics, nutritional status, and the gut microbiome. Mamm Genome 29, 63–79 (2018). https://doi.org/10.1007/s00335-018-9736-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-018-9736-9

Keywords

Navigation