Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
권호 표지
DOI QR코드

DOI QR Code

Association between urinary arsenic concentration and genetic polymorphisms in Korean adults

  • Seul‑Gi Lee (Department of Preventive Medicine, College of Medicine, Chung-Ang University) ;
  • Sang‑Yong Eom (Department of Preventive Medicine, College of Medicine, Chungbuk National University) ;
  • Ji‑Ae Lim (Department of Preventive Medicine, College of Medicine, Dankook University) ;
  • Byung‑Sun Choi (Department of Preventive Medicine, College of Medicine, Chung-Ang University) ;
  • Ho‑Jang Kwon (Department of Preventive Medicine, College of Medicine, Dankook University) ;
  • Young‑Seoub Hong (Department of Preventive Medicine, College of Medicine, Dong-A University) ;
  • Yong‑Dae Kim (Department of Preventive Medicine, College of Medicine, Chungbuk National University) ;
  • Heon Kim (Department of Preventive Medicine, College of Medicine, Chungbuk National University) ;
  • Jung‑Duck Park (Department of Preventive Medicine, College of Medicine, Chung-Ang University)
  • Received : 2023.06.28
  • Accepted : 2023.10.25
  • Published : 2024.01.15
⟨ Previous Next ⟩

Abstract

Arsenic (As) is a human carcinogen widely distributed in the environment. This study evaluated the association between the urinary As concentration and single nucleotide polymorphisms (SNPs) in Korean adults to determine the genetic factors related to As concentration. The study included 496 participants for the genome-wide association study (GWAS) and 1483 participants for the candidate gene approach study. Participants were 19 years and older. The concentrations of total As (Tot As) and total As metabolites (Tmet As, the sum of inorganic As and their metabolites; arsenite, arsenate, monomethylarsonic, and dimethylarsinic acid) in the urine were analyzed. The GWAS identified four SNPs (rs1432523, rs3776006, rs11171747, and rs807573) associated with urinary Tot As and four SNPs (rs117605537, rs3776006, rs11171747, and rs148103384) significantly associated with urinary Tmet As concentration (P<1×10-4). The candidate gene study identified two SNPs (PRDX2 rs10427027 and GLRX rs3822751) in genes related to the reduction reaction associated with urinary Tot As and Tmet As. This study suggests that genetic factors may play a role in regulating As metabolism in the human body, affecting both exposure levels and its potential health risks in the general Korean population, even at low exposure levels.

Keywords

Acknowledgement

Funding was provided by a Grant (13162MFDS778 and 14162MFDS654) from the Ministry of Food and Drug Safety in 2013 and 2014.

References

  1. Caldwell KL, Jones RL, Verdon CP, Jarrett JM, Caudill SP, Osterloh JD (2009) Levels of urinary total and speciated arsenic in the US population: National Health and Nutrition Examination Survey 2003-2004. J Expo Sci Environ Epidemiol 19:59-68. https://doi.org/10.1038/jes.2008.32
  2. ATSDR (2007) Toxicological profle for arsenic. Agency for Toxic Substances and Disease Registry, Division of Toxicology, Atlanta
  3. WHO (2001) Arsenic and arsenic compounds. Environmental health criteria 224. World Health Organization, Geneva
  4. IARC (2004) Some drinking-water disinfectants and contaminants, including arsenic. In IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, IARC Press, Lyon, France
  5. Schuhmacher-Wolz U, Dieter HH, Klein D, Schneider K (2009) Oral exposure to inorganic arsenic: evaluation of its carcinogenic and non-carcinogenic effects. Crit Rev Toxicol 39:271-298. https://doi.org/10.1080/10408440802291505
  6. Moon KA, Guallar E, Umans JG, Devereux RB, Best LG, Francesconi KA, Goessler W, Pollak J, Silbergeld EK, Howard BV, Navas-Acien A (2013) Association between exposure to low to moderate arsenic levels and incident cardiovascular disease. A prospective cohort study. Ann Intern Med 159:649-659. https://doi.org/10.7326/0003-4819-159-10-201311190-00719
  7. National Research Council (NRC) (1999) Arsenic in drinking water. National Academy Press, Washington
  8. Yoshida T, Yamauchi H, Sun GF (2004) Chronic health effects in people exposed to arsenic via the drinking water: dose-response relationships in review. Toxicol Appl Pharmacol 198:243-252. https://doi.org/10.1016/j.taap.2003.10.022
  9. EFSA Panel on Contaminants in the Food Chain (CONTAM) (2009) Scientific opinion on arsenic in food. EFSA J 7:1351. https://doi.org/10.2903/j.efsa.2009.1351
  10. Heinrich-Ramm R, Mindt-Prufert S, Szadkowski D (2002) Arsenic species excretion after controlled seafood consumption. J Chromatogr B Analyt Technol Biomed Life Sci 778:263-273. https://doi.org/10.1016/S0378-4347(01)00443-1
  11. Das HK, Mitra AK, Sengupta PK, Hossain A, Islam F, Rabbani GH (2004) Arsenic concentrations in rice, vegetables, and fish in Bangladesh: a preliminary study. Environ Int 30:383-387. https://doi.org/10.1016/j.envint.2003.09.005
  12. Ahmed MK, Shaheen N, Islam MS, Habibullah-Al-Mamun M, Islam S, Islam MM, Kundu GK, Bhattacharjee L (2015) A comprehensive assessment of arsenic in commonly consumed foodstuffs to evaluate the potential health risk in Bangladesh. Sci Total Environ 544:125-133. https://doi.org/10.1016/j.scitotenv.2015.11.133
  13. Lee SG, Kang I, Seo MN, Lee JE, Eom SY, Hwang MS, Park KS, Choi BS, Kwon HJ, Hong YS, Kim H, Park JD (2022) Exposure levels and contributing factors of various arsenic species and their health effects on Korean adults. Arch Environ Contam Toxicol 82:391-402. https://doi.org/10.1007/s00244-022-00913-y
  14. Petrick JS, Jagadish B, MashEA AHV (2001) Monomethylarsonous acid (MMA(III)) and arsenite: LD(50) in hamsters and in vitro inhibition of pyruvate dehydrogenase. Chem Res Toxicol 14:651-656. https://doi.org/10.1021/tx000264z
  15. Styblo M, Drobna Z, Jaspers I, Lin S, Thomas DJ (2002) The role of biomethylation in toxicity and carcinogenicity of arsenic: a research update. Environ Health Perspect 110:767-771. https://doi.org/10.1289/ehp.110-1241242
  16. Burchiel SW, Lauer FT, Beswick EJ, Gandolf AJ, Parvez F, Liu KJ, Hudson LG (2014) Differential susceptibility of human peripheral blood T cells to suppression by environmental levels of sodium arsenite and monomethylarsonous acid. PLoS One 9:e109192. https://doi.org/10.1371/journal.pone.0109192
  17. Vahter M, Concha G, Nermell B (2000) Factors influencing arsenic methylation in humans. J Trace Elem Exp Med 13:173-184. https://doi.org/10.1002/(SICI)1520-670X(2000)13:1%3c173::AID-JTRA18%3e3.0.CO;2-T
  18. Tseng CH (2009) A review on environmental factors regulating arsenic methylation in humans. Toxicol Appl Pharmacol 235:338-350. https://doi.org/10.1016/j.taap.2008.12.016
  19. Jansen RJ, Argos M, Tong L, Li J, Rakibuz-Zaman M, Islam MT, Slavkovich V, Ahmed A, Navas-Acien A, Parvez F, Chen Y, Gamble MV, Graziano JH, Pierce BL, Ahsan H (2016) Determinants and consequences of arsenic metabolism effciency among 4,794 individuals: demographics, lifestyle, genetics, and toxicity. Cancer Epidemiol Biomarkers Prev 25:381-390. https://doi.org/10.1158/1055-9965.EPI-15-0718
  20. Chung JS, Kalman DA, Moore LE, Kosnett MJ, Arroyo AP, Beeris M, Mazumder DN, Hernandez AL, Smith AH (2002) Family correlations of arsenic methylation patterns in children and parents exposed to high concentrations of arsenic in drinking water. Environ Health Perspect 110:729-733. https://doi.org/10.1289/ehp.02110729
  21. Buchet JP, Lauwerys R (1987) Study of factors influencing the in vivo methylation of inorganic arsenic in rats. Toxicol Appl Pharmacol 91:65-74. https://doi.org/10.1016/0041-008x(87)90194-3
  22. Marafante E, Vahter M (1984) The effect of methyltransferase inhibition on the metabolism of [ 74As]arseniteinmiceandrabbits. Chem Biol Interact 50:49-57. https://doi.org/10.1016/0009-2797(84)90131-5
  23. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci 99:6053-6058. https://doi.org/10.1073/pnas.092131899
  24. Pierce BL, Kibriya MG, Tong L, Jasmine F, Argos M, Roy S, Brutus RP, Rahaman R, Zaman MR, Parvez F, Ahmed A, Quasem I, Hore SK, Alam S, Islam T, Slavkovich V, Gamble MV, Yunus M, Rahman M, Baron JA, Graziano JH, Ahsan H (2012) Genome-wide association study identifies chromosome 10q24.32 variants associated with arsenic metabolism and toxicity phenotypes in Bangladesh. PLoS Genet 8:e1002522. https://doi.org/10.1371/journal.pgen.1002522
  25. Pierce BL, Tong L, Dean S, Argos M, Jasmine F, RakibuzZaman M, Sarwar G, Islam MT, Shahriar H, Islam T, Rahman M, Yunus M, Lynch VJ, Oglesbee D, Graziano JH, Kibriya MG, Gamble MV, Ahsan H (2019) A missense variant in FTCD is associated with arsenic metabolism and toxicity phenotypes in Bangladesh. PLoS Genet 15:e1007984. https://doi.org/10.1371/journal.pgen.1007984
  26. Tamayo LI, Kumarasinghe Y, Tong L, Balac O, Ahsan H, Gamble M, Pierce BL (2022) Inherited genetic effects on arsenic metabolism: a comparison of effects on arsenic species measured in urine and in blood. Environ Epidemiol 6:e230. https://doi.org/10.1097/EE9.0000000000000230
  27. Banerjee N, Nandy S, Kearns JK, Bandyopadhyay AK, Das JK, Majumder P, Basu S, Banerjee S, Sau TJ, States JC, Giri AK (2011) Polymorphisms in the TNF-α and IL10 gene promoters and risk of arsenic-induced skin lesions and other nondermatological health effects. Toxicol Sci 121:132-139. https://doi.org/10.1093/toxsci/kfr046
  28. Lesseur C, Gilbert-Diamond D, Andrew AS, Ekstrom RM, Li Z, Kelsey KT, Marsit CJ, Karagas MR (2012) A case-control study of polymorphisms in xenobiotic and arsenic metabolism genes and arsenic-related bladder cancer in New Hampshire. Toxicol Lett 210:100-106. https://doi.org/10.1016/j.toxlet.2012.01.015
  29. Lin YC, Chen WJ, Huang CY, Shiue HS, Su CT, Ao PL, Pu YS, Hsueh YM (2018) Polymorphisms of arsenic (+3 oxidation state) methyltransferase and arsenic methylation capacity afect the risk of bladder cancer. Toxicol Sci 164:328-338. https://doi.org/10.1093/toxsci/kfy087
  30. Surenbaatar U, Kim BG, Son HJ, Cho SS, Kim GM, Lim HJ, Kwon JY, Kim KH, Hong YS (2021) MTHFR, As3MT and GSTO1 polymorphisms influencing arsenic metabolism in residents near abandoned metal mines in South Korea. J Environ Health Sci 47:530-539. https://doi.org/10.5668/JEHS.2021.47.6.530
  31. Lim JA, Kwon HJ, Ha M, Kim H, Oh SY, Kim JS, Lee SA, Park JD, Hong YS, Sohn SJ, Pyo H, Park KS, Lee KG, Kim YD, Jun S, Hwang MS (2015) Korean research project on the integrated exposure assessment of hazardous substances for food safety. Environ Health Toxicol 30:e2015004. https://doi.org/10.5620/eht.e2015004
  32. Seo MN, Lee SG, Eom SY, Kim J, Oh SY, Kwon HJ, Kim H, Choi BS, Yu IJ, Park JD (2016) Estimation of total and inorganic arsenic intake from the diet in Korean adults. Arch Environ Contam Toxicol 70:647-656. https://doi.org/10.1007/s00244-015-0257-1
  33. WHO (2011) Evaluation of certain contaminants in food: seventy second report of the Joint FAO/WHO Expert Committee on Food Additives. WHO technical report series 959. http://apps.who.int/iris/bitstream/10665/44514/1/WHO_TRS_959_eng.pdf. Accessed 03 Sept 2015
  34. Bae HS, Kang IG, Lee SG, Eom SY, Kim YD, Oh SY, Kwon HJ, Park KS, Kim H, Choi BS, Yu IJ, Park JD (2016) Arsenic exposure and seafood intake in Korean adults. Hum Exp Toxicol 36:451-460. https://doi.org/10.1177/0960327116665673
  35. Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 5:46-51. https://doi.org/10.1080/1047322X.1990.10389587
  36. Eom SY, Lim JA, Kim YD, Choi BS, Hwang MS, Park JD, Kim H, Kwon HJ (2016) Allele frequencies of the single nucleotide polymorphisms related to the body burden of heavy metals in the Korean population and their ethnic differences. Toxicol Res 32:195-205. https://doi.org/10.5487/TR.2016.32.3.195
  37. Ioannidis JP, Patsopoulos NA, Evangelou E (2007) Heterogeneity in meta-analyses of genome-wide association investigations. PLoS One 2:e841. https://doi.org/10.1371/journal.pone.0000841
  38. Gloerich M, Bos JL (2011) Regulating rap small G-proteins in time and space. Trends Cell Biol 21:615-623. https://doi.org/10.1016/j.tcb.2011.07.001
  39. Xu B, Ionita-Laza I, Roos JL, Boone B, Woodrick S, Sun Y, Levy S, Gogos JA, Karayiorgou M (2012) De novo gene mutations highlight patterns of genetic and neural complexity in schizophrenia. Nat Genet 44:1365-1369. https://doi.org/10.1038/ng.2446
  40. Gladwin TE, Derks EM, Rietschel M, Mattheisen M, Breuer R, Schulze TG, Nothen MM, Levinson D, Shi J, Gejman PV, Cichon S, Ophof RA, Genetic Risk and Outcome of Psychosis (GROUP) (2012) Segment-wise genome-wide association analysis identifies a candidate region associated with schizophrenia in three independent samples. PloS One 7:e38828. https://doi.org/10.1371/journal.pone.0038828
  41. Liang J, Song W, Tromp G, Kolattukudy PE, Fu M (2008) Genome-wide survey and expression profiling of CCCH-zinc finger family reveals a functional module in macrophage activation. PLoS One 3:e2880. https://doi.org/10.1371/journal.pone.0002880
  42. Keene KL, Quinlan AR, Hou X, Hall IM, Mychaleckyj JC, Onengut-Gumuscu S, Concannon P (2012) Evidence for two independent associations with type 1 diabetes at the 12q13 locus. Genes Immun 13:66-70. https://doi.org/10.1038/gene.2011.56
  43. Uhlen M, Fagerberg L, Hallstrom BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson A, Kampf C, Sjostedt E, Asplund A, Olsson I, Edlund K, Lundberg E, Navani S, Szigyarto CA, Odeberg J, Djureinovic D, Takanen JO, Hober S, Alm T, Edqvist PH, Berling H, Tegel H, Mulder J, Rockberg J, Nilsson P, Schwenk JM, Hamsten M, von Feilitzen K, Forsberg M, Persson L, Johansson F, Zwahlen M, von Heijne G, Nielsen J, Ponten F (2015) Proteomics. Tissue-based map of the human proteome. Science 347:1260419. https://doi.org/10.1126/science.1260419
  44. Godbout R, Packer M, Bie W (1998) Overexpression of a DEAD box protein (DDX1) in neuroblastoma and retinoblastoma cell lines. J Biol Chem 273:21161-21168. https://doi.org/10.1074/jbc.273.33.21161
  45. Bleoo S, Sun X, Hendzel MJ, Rowe JM, Packer M, Godbout R (2001) Association of human DEAD box protein DDX1 with a cleavage stimulation factor involved in 3'-end processing of preMRNA. Mol Biol Cell 12:3046-3059. https://doi.org/10.1091/mbc.12.10.3046
  46. Abdelhaleem M (2004) Do human RNA helicases have a role in cancer? Biochim Biophys Acta 1704:37-46. https://doi.org/10.1016/j.bbcan.2004.05.001
  47. Michibata H, Yanaka N, Kanoh Y, Okumura K, Omori K (2001) Human Ca2+/calmodulin-dependent phosphodiesterase PDE1A: novel splice variants, their specifc expression, genomic organization, and chromosomal localization. Biochim Biophys Acta 1517:278-287. https://doi.org/10.1016/s0167-4781(00)00293-1
  48. Tazawa S, Yamato T, Fujikura H, Hiratochi M, Itoh F, Tomae M, Takemura Y, Maruyama H, Sugiyama T, Wakamatsu A, Isogai T, Isaji M (2005) SLC5A9/SGLT4, a new Na+-dependent glucose transporter, is an essential transporter for mannose, 1,5-anhydroD-glucitol, and fructose. Life Sci 76:1039-1050. https://doi.org/10.1016/j.lfs.2004.10.016
  49. Calatayud M, Barrios JA, Velez D, Devesa V (2012) In vitro study of transporters involved in intestinal absorption of inorganic arsenic. Chem Res Toxicol 25:446-453. https://doi.org/10.1021/tx200491f
  50. Shi Q, Song X, Wang J, Gu J, Zhang W, Hu J, Zhou X, Yu R (2015) FRK inhibits migration and invasion of human glioma cells by promoting N-cadherin/β-catenin complex formation. J Mol Neurosci 55:32-41. https://doi.org/10.1007/s12031-014-0355-y
  51. Chen W, Martindale JL, Holbrook NJ, Liu Y (1998) Tumor promoter arsenite activates extracellular signal-regulated kinase through a signaling pathway mediated by epidermal growth factor receptor and Shc. Mol Cell Biol 18:5178-5188. https://doi.org/10.1128/MCB.18.9.5178
  52. Suc I, Meilhac O, Lajoie-Mazenc I, Vandaele J, Jurgens G, Salvayre R, Negre-Salvayre A (1998) Activation of EGF receptor by oxidized LDL. FASEB J 12:665-671. https://doi.org/10.1096/fasebj.12.9.665
  53. Xiong HY, Alipanahi B, Lee LJ, Bretschneider H, Merico D, Yuen RK, Hua Y, Gueroussov S, Najafabadi HS, Hughes TR, Morris Q, Barash Y, Krainer AR, Jojic N, Scherer SW, Blencowe BJ, Frey BJ (2015) RNA splicing. The human splicing code reveals new insights into the genetic determinants of disease. Science 347:1254806. https://doi.org/10.1126/science.1254806
  54. Waters SB, Devesa V, Razo LMD, Styblo M, Thomas DJ (2004) Endogenous reductants support the catalytic function of recombinant rat cyt19, an arsenic methyltransferase. Chem Res Toxicol 17:404-409. https://doi.org/10.1021/tx0342161
  55. Engstrom KS, Nermell B, Concha G, Stromberg U, Vahter M, Broberg K (2009) Arsenic metabolism is influenced by polymorphisms in genes involved in one-carbon metabolism and reduction reactions. Mutat Res 667:4-14. https://doi.org/10.1016/j.mrfmmm.2008.07.003