Human adaptation to arsenic-rich environments

Molecular Biology and Evolution

Volumn 32, Issue 6, 2015, Pages 1544-1555

  Schlebusch, Carina M ^a   Gattepaille, Lucie M ^a   Engström, Karin ^b   Vahter, Marie ^c   Jakobsson, Mattias ^a,d   Broberg, Karin ^c  

^a UPPSALA UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

AS3MT; selection; toxic

Indexed keywords

ARSENIC; METHYLTRANSFERASE; RYANODINE RECEPTOR 3; AS3MT PROTEIN, HUMAN;

ADAPTATION; ARTICLE; CHROMOSOME 1; CHROMOSOME 10; CHROMOSOME 12; CHROMOSOME 13; CHROMOSOME 15; CHROMOSOME 21; CHROMOSOME 3; CHROMOSOME 6; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC DRIFT; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; HAPLOTYPE; HOMOZYGOSITY; HUMAN; OXIDATION; PHENOTYPE; POPULATION GROUP; POPULATION STRUCTURE; SELECTIVE SWEEP; SINGLE NUCLEOTIDE POLYMORPHISM; URINALYSIS; ADOLESCENT; ADULT; AGED; ALLELE; ARGENTINA; GENETIC DATABASE; GENETIC SELECTION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MIDDLE AGED; PERU; POPULATION GENETICS; STATISTICAL MODEL; URINE; YOUNG ADULT;

ADAPTATION, PHYSIOLOGICAL; ADOLESCENT; ADULT; AGED; ALLELES; ARGENTINA; ARSENIC; DATABASES, GENETIC; FEMALE; GENETICS, POPULATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HAPLOTYPES; HUMANS; LINEAR MODELS; METHYLTRANSFERASES; MIDDLE AGED; PERU; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; SELECTION, GENETIC; YOUNG ADULT;

EID: 84930715906     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv046     Document Type: Article

References (78)

1. Abecasis GR, Auton A, Brooks LD, DePristo MA, Durbin RM, Handsaker RE, Kang HM, Marth GT, McVean GA. 2012. An integrated map of genetic variation from 1, 092 human genomes. Nature 491:56-65.
2. Ahmed S, Ahsan KB, Kippler M, Mily A, Wagatsuma Y, Hoque AM, Ngom PT, El Arifeen S, Raqib R, Vahter M. 2012. In utero arsenic exposure is associated with impaired thymic function in newborns possibly via oxidative stress and apoptosis. Toxicol Sci. 129:305-314.
3. Ahmed S, Mahabbat-e Khoda S, Rekha RS, Gardner RM, Ameer SS, Moore S, Ekstrom EC, Vahter M, Raqib R. 2011. Arsenic-Associated oxidative stress, inflammation, and immune disruption in human placenta and cord blood. Environ Health Perspect. 119:258-264.
4. Ahsan H, Chen Y, KibriyaMG, Slavkovich V, Parvez F, Jasmine F, Gamble MV, Graziano JH. 2007. Arsenic metabolism, genetic susceptibility, and risk of premalignant skin lesions in Bangladesh. Cancer Epidemiol Biomarkers Prev. 16:1270-1278.
5. Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19:1655-1664.
6. Ameur A, Enroth S, Johansson A, Zaboli G, Igl W, Johansson AC, Rivas MA, DalyMJ, Schmitz G, Hicks AA, et al. 2012. Genetic adaptation of fatty-Acid metabolism: A human-specific haplotype increasing the biosynthesis of long-chain omega-3 and omega-6 fatty acids. Am J Hum Genet. 90:809-820.
7. Arriaza B, Amarasiriwardena D, Cornejo L, Standen V, Byrne S, Bartkus L, Bandak B. 2010. Exploring chronic arsenic poisoning in pre-Columbian Chilean mummies. J Archaeol Sci. 37:1274-1278.
8. Aulchenko YS, Ripke S, Isaacs A, van Duijn CM. 2007. GenABEL: An R library for genome-wide association analysis. Bioinformatics 23: 1294-1296.
9. Basu Mallick C, Iliescu FM, Mols M, Hill S, Tamang R, Chaubey G, Goto R, Ho SY, Gallego Romero I, Crivellaro F, et al. 2013. The light skin allele of SLC24A5 in South Asians and Europeans shares identity by descent. PLoS Genet. 9:e1003912.
10. Bertocchini F, Ovitt CE, Conti A, Barone V, Scholer HR, Bottinelli R, Reggiani C, Sorrentino V. 1997. Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles. Embo J. 16:6956-6963.
11. Bhatia G, Patterson N, Sankararaman S, Price AL. 2013. Estimating and interpreting FST: the impact of rare variants. Genome Res. 23: 1514-1521.
12. Broberg K, EngstromK, Ameer S. 2015. Gene-environment formetals. In: Nordberg GF, Fowler B, Nordberg M, editors. Handbook on the toxicology of metals. Oxford: Academic Press. p. 242-247.
13. Bundschuh J, Perez-Carrera A, Litter MI. 2008. Distribucion del arsenico en las regiones Iberica e Iberoamericana. Editorial Programa Iberoamericano de Ciencia y Tecnologia para el Desarrollo, Buenos Aires, Argentina.
14. Bundschuh J, Litter MI, Parvez F, Roman-Ross G, Nicolli HB, Jean JS, Liu CW, Lopez D, Armienta MA, Guilherme LR, et al. 2012. One century of arsenic exposure in Latin America: A review of history and occurrence from 14 countries. Sci Total Environ. 429:2-35.
15. Chen B, Arnold LL, Cohen SM, Thomas DJ, Le XC. 2011. Mouse arsenic (+3 oxidation state) methyltransferase genotype affects metabolism and tissue dosimetry of arsenicals after arsenite administration in drinking water. Toxicol Sci. 124:320-326.
16. Chen H, Slatkin M. 2013. Inferring selection intensity and allele age from multilocus haplotype structure. G3 3:1429-1442.
17. Chung CJ, Hsueh YM, Bai CH, Huang YK, Huang YL, Yang MH, Chen CJ. 2009. Polymorphisms in arsenic metabolism genes, urinary arsenic methylation profile and cancer. Cancer Causes Control 20: 1653-1661.
18. Concha G, Nermell B, VahterM. 2006. Spatial and temporal variations in arsenic exposure via drinking-water in northern Argentina. J Health Popul Nutr. 24:317-326.
19. Cooke CA, Abbott MB. 2008. A paleolimnological perspective on industrial-era metal pollution in the central Andes, Peru. Sci Total Environ. 393:262-272.
20. Drobna Z, Waters SB, Devesa V, Harmon AW, Thomas DJ, Styblo M. 2005. Metabolism and toxicity of arsenic in human urothelial cells expressing rat arsenic (+3 oxidation state)-methyltransferase. Toxicol Appl Pharmacol. 207:147-159.
21. Drobna Z, Xing W, Thomas DJ, Styblo M. 2006. shRNA silencing of AS3MT expression minimizes arsenic methylation capacity of HepG2 cells. Chem Res Toxicol. 19:894-898.
22. Drobna Z, Naranmandura H, Kubachka KM, Edwards BC, Herbin-Davis K, Styblo M, Le XC, Creed JT, Maeda N, Hughes MF, et al. 2009. Disruption of the arsenic (+3 oxidation state) methyltransferase gene in the mouse alters the phenotype for methylation of arsenic and affects distribution and retention of orally administered arsenate. Chem Res Toxicol. 22:1713-1720.
23. Engstrom K, Vahter M, Mlakar SJ, Concha G, Nermell B, Raqib R, Cardozo A, Broberg K. 2011. Polymorphisms in arsenic (+III oxidation state) methyltransferase (AS3MT) predict gene expression of AS3MT as well as arsenic metabolism. Environ Health Perspect. 119: 182-188.
24. Engstrom KS, Hossain MB, Lauss M, Ahmed S, Raqib R, Vahter M, Broberg K. 2013. Efficient arsenicmetabolism-The AS3MT haplotype is associated with DNA methylation and expression of multiple genes around AS3MT. PLoS One 8:e53732.
25. Farzan SF, Korrick S, Li Z, Enelow R, Gandolfi AJ, Madan J, Nadeau K, KaragasMR. 2013. In utero arsenic exposure and infant infection in a United States cohort: A prospective study. Environ Res. 126:24-30.
26. Florea AM, Splettstoesser F, Busselberg D. 2007. Arsenic trioxide (As2O3) induced calciumsignals and cytotoxicity in two human cell lines: SY-5Y neuroblastoma and 293 embryonic kidney (HEK). Toxicol Appl Pharmacol. 220:292-301.
27. Fry RC, Navasumrit P, Valiathan C, Svensson JP, Hogan BJ, Luo M, Bhattacharya S, Kandjanapa K, Soontararuks S, Nookabkaew S, et al. 2007. Activation of inflammation/NF-kappaB signaling in infants born to arsenic-exposed mothers. PLoS Genet. 3:e207.
28. Fujihara J, Fujii Y, Agusa T, Kunito T, Yasuda T, Moritani T, Takeshita H. 2009. Ethnic differences in five intronic polymorphisms associated with arsenic metabolism within human arsenic (+3 oxidation state) methyltransferase (AS3MT) gene. Toxicol Appl Pharmacol. 234: 41-46.
29. Gardner RM, Kippler M, Tofail F, Bottai M, Hamadani J, Grander M, Nermell B, Palm B, Rasmussen KM, Vahter M. 2013. Environmental exposure to metals and children's growth to age 5 years: A prospective cohort study. Am J Epidemiol. 177:1356-1367.
30. Gardner RM, Nermell B, Kippler M, Grander M, Li L, Ekstrom EC, Rahman A, Lonnerdal B, Hoque AM, Vahter M. 2010. Arsenic methylation efficiency increases during the first trimester of pregnancy independent of folate status. Reprod Toxicol. 31: 210-218.
31. Gautier M, Vitalis R. 2012. rehh: An R package to detect footprints of selection in genome-wide SNP data from haplotype structure. Bioinformatics 28:1176-1177.
32. Gomez-Rubio P, Klimentidis YC, Cantu-Soto E, Meza-Montenegro MM, Billheimer D, Lu Z, Chen Z, Klimecki WT. 2012. Indigenous American ancestry is associated with arsenic methylation efficiency in an admixed population of northwest Mexico. J Toxicol Environ Health A. 75:36-49.
33. Gomez-Rubio P, Meza-Montenegro MM, Cantu-Soto E, Klimecki WT. 2010. Genetic association between intronic variants in AS3MT and arsenic methylation efficiency is focused on a large linkage disequilibrium cluster in chromosome 10. J Appl Toxicol. 30: 260-270.
34. Hanikenne M, Talke IN, Haydon MJ, Lanz C, Nolte A, Motte P, Kroymann J, Weigel D, Kramer U. 2008. Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453:391-395.
35. Hopenhayn-Rich C, Biggs ML, Smith AH, Kalman DA, Moore LE. 1996. Methylation study of a population environmentally exposed to arsenic in drinking water. Environ Health Perspect. 104:620-628.
36. IARC. 2012. A review of human carcinogens: Arsenic, metals, fibres, and dusts, IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 100C. Lyon, France: World Health Organization.
37. Idrovo AJ. 2005. [Possible health effects associated with pre-Columbian metallurgy]. Biomedica 25:295-303; discussion 304.
38. Karlsson EK, Harris JB, Tabrizi S, Rahman A, Shlyakhter I, Patterson N, O'Dushlaine C, Schaffner SF, Gupta S, Chowdhury F, et al. 2013. Natural selection in a Bangladeshi population from the cholera-endemic Ganges river delta. Sci Transl Med. 5:192-186.
39. Kozul CD, Ely KH, Enelow RI, Hamilton JW. 2009. Low-dose arsenic compromises the immune response to influenza A infection in vivo. Environ Health Perspect. 117:1441-1447.
40. Kwiatkowski DP. 2005. How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet. 77:171-192.
41. Lin S, Shi Q, Nix FB, Styblo M, Beck MA, Herbin-Davis KM, Hall LL, Simeonsson JB, Thomas DJ. 2002. A novel S-Adenosyl-L-methionine: Arsenic (III) methyltransferase from rat liver cytosol. J Biol Chem. 277:10795-10803.
42. Lindberg AL, RahmanM, Persson LA, Vahter M. 2008. The risk of arsenic induced skin lesions in Bangladeshi men and women is affected by arsenic metabolism and the age at first exposure. Toxicol Appl Pharmacol. 230:9-16.
43. Maull EA, Ahsan H, Edwards J, Longnecker MP, Navas-Acien A, Pi J, Silbergeld EK, StybloM, Tseng CH, Thayer KA, et al. 2012. Evaluation of the association between arsenic and diabetes: A National Toxicology Program workshop review. Environ Health Perspect. 120:1658-1670.
44. Melnick JG, Parkin G. 2007. Cleaving mercury-Alkyl bonds: A functional model for mercury detoxification by MerB. Science 317:225-227.
45. Meyer M, Kircher M, Gansauge MT, Li H, Racimo F, Mallick S, Schraiber JG, Jay F, Prufer K, de Filippo C, et al. 2012. A high-coverage genome sequence from an archaic Denisovan individual. Science 338: 222-226.
46. Meza MM, Yu L, Rodriguez YY, Guild M, Thompson D, Gandolfi AJ, Klimecki WT. 2005. Developmentally restricted genetic determinants of human arsenic metabolism: Association between urinary methylated arsenic and CYT19 polymorphisms in children. Environ Health Perspect. 113:775-781.
47. Moon K, Guallar E, Navas-Acien A. 2012. Arsenic exposure and cardiovascular disease: An updated systematic review. Curr Atheroscler Rep. 14:542-555.
48. Normando Cruz E. 2011. Historia y Etnicidad en las Yungas de la Argentina. Venezuela: Ediciones Polar.
49. Nunez ALN, Hill HG, Martinez AL. 1991. Gua Museo Arqueologico, Universidad Catolica del Norte Chile. San Pedro de Atacama (II Regon): Instituto de Investigaciones Arqueologicas y Museo RP. Gustavo Le Paige SJ. Antofagasta, Chile: Universidad Catolica del Norte Chile.
50. Ohta T, Kimura M. 1975. The effect of selected linked locus on heterozygosity of neutral alleles (the hitch-hiking effect). Genet Res. 25: 313-326.
51. Parvez F, Chen Y, Yunus M, Olopade C, Segers S, Slavkovich V, Argos M, Hasan R, Ahmed A, Islam T, et al. 2013. Arsenic exposure and impaired lung function. Findings from a large population-based prospective cohort study. Am J Respir Crit Care Med. 188:813-819.
52. Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2:e190.
53. Perez CF, Lopez JR, Allen PD. 2005. Expression levels of RyR1 and RyR3 control resting free Ca2+ in skeletal muscle. Am J Physiol Cell Physiol. 288:C640-C649.
54. Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R, Werner J, Villanea FA, Mountain JL, Misra R, et al. 2007. Diet and the evolution of human amylase gene copy number variation. Nat Genet. 39: 1256-1260.
55. Pierce BL, KibriyaMG, Tong L, Jasmine F, Argos M, Roy S, Paul-Brutus R, Rahaman R, Rakibuz-Zaman M, Parvez F, et al. 2012. Genome-wide association study identifies chromosome 10q24. 32 variants associated with arsenic metabolism and toxicity phenotypes in Bangladesh. PLoS Genet. 8:e1002522.
56. Pierce BL, Tong L, Argos M, Gao J, Farzana J, Roy S, Paul-Brutus R, Rahaman R, Rakibuz-Zaman M, Parvez F, et al. 2013. Arsenic metabolism efficiency has a causal role in arsenic toxicity: Mendelian randomization and gene-environment interaction. Int J Epidemiol. 42:1862-1871.
57. Prufer K, Munch K, Hellmann I, Akagi K, Miller JR, Walenz B, Koren S, Sutton G, Kodira C, Winer R, et al. 2012. The bonobo genome compared with the chimpanzee and human genomes. Nature 486:527-531.
58. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, et al. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559-575.
59. Rahman A, Persson LA, Nermell B, El Arifeen S, Ekstrom EC, Smith AH, Vahter M. 2010. Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology 21:797-804.
60. Rahman A, Vahter M, Ekstrom EC, Persson LA. 2010. Arsenic exposure in pregnancy increases the risk of lower respiratory tract infection and diarrhea during infancy in Bangladesh. Environ Health Perspect. 119: 719-724.
61. Rahman A, Vahter M, Ekstrom EC, Persson LA. 2011. Arsenic exposure in pregnancy increases the risk of lower respiratory tract infection and diarrhea during infancy in Bangladesh. Environ Health Perspect. 119: 719-724.
62. Sabbagh A, Marin J, Veyssiere C, Lecompte E, Boukouvala S, Poloni ES, Darlu P, Crouau-Roy B. 2013. Rapid birth-And-death evolution of the xenobiotic metabolizing NAT gene family in vertebrates with evidence of adaptive selection. BMC Evol Biol. 13:62.
63. Schlawicke Engstrom K, Broberg K, Concha G, Nermell B, Warholm M, Vahter M. 2007. Genetic polymorphisms influencing arsenic metabolism: evidence from Argentina. Environ Health Perspect. 115: 599-605.
64. Schlebusch CM, Lewis CM Jr., Vahter M, Engstrom K, Tito RY, Obregon-Tito AJ, Huerta D, Polo SI, Medina AC, Brutsaert TD, et al. 2013. Possible positive selection for an arsenic-protective haplotype in humans. Environ Health Perspect. 121:53-58.
65. Shriver MD, Kennedy GC, Parra EJ, Lawson HA, Sonpar V, Huang J, Akey JM, Jones KW. 2004. The genomic distribution of population substructure in four populations using 8, 525 autosomal SNPs. Hum Genomics 1:274-286.
66. Simonson TS, Yang Y, Huff CD, Yun H, Qin G, Witherspoon DJ, Bai Z, Lorenzo FR, Xing J, Jorde LB, et al. 2010. Genetic evidence for highaltitude adaptation in Tibet. Science 329:72-75.
67. Smith AH, Marshall G, Yuan Y, Ferreccio C, Liaw J, von Ehrenstein O, Steinmaus C, Bates MN, Selvin S. 2006. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ Health Perspect. 114: 1293-1296.
68. Song WY, Park J, Mendoza-Cozatl DG, Suter-Grotemeyer M, Shim D, Hortensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, et al. 2010. Arsenic tolerance in Arabidopsis is mediated by two ABCCtype phytochelatin transporters. Proc Natl Acad Sci U S A. 107: 21187-21192.
69. Takei Y, Swietlik M, Tanoue A, Tsujimoto G, Kouzarides T, Laskey R. 2001. MCM3AP, a novel acetyltransferase that acetylates replication protein MCM3. EMBO Rep. 2:119-123.
70. Tellez-Plaza M, Gribble MO, Voruganti VS, Francesconi KA, Goessler W, Umans JG, Silbergeld EK, Guallar E, Franceschini N, North KE, et al. 2013. Heritability and preliminary genome-wide linkage analysis of arsenic metabolites in urine. Environ Health Perspect. 121:345-351.
71. Thoma R, Schulz-Gasch T, D'Arcy B, Benz J, Aebi J, Dehmlow H, Hennig M, Stihle M, Ruf A. 2004. Insight into steroid scaffold formation from the structure of human oxidosqualene cyclase. Nature 432:118-122.
72. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC, Silverman JS, Powell K, Mortensen HM, Hirbo JB, Osman M, et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet. 39:31-40.
73. Vahter M. 2002. Mechanisms of arsenic biotransformation. Toxicology 181-182:211-217.
74. Vahter M, Concha G, Nermell B, Nilsson R, Dulout F, Natarajan AT. 1995. A unique metabolism of inorganic arsenic in native Andean women. Eur J Pharmacol. 293:455-462.
75. Van Den Bergh K, Du Laing G, Montoya JC, De Deckere E, Tack FM. 2010. Arsenic in drinking water wells on the Bolivian high plain: field monitoring and effect of salinity on removal efficiency of ironoxides-containing filters. J Environ Sci Health A Tox Hazard Subst Environ Eng. 45:1741-1749.
76. Voight BF, Kudaravalli S, Wen X, Pritchard JK. 2006. A map of recent positive selection in the human genome. PLoS Biol. 4:e72.
77. Williams AL, Patterson N, Glessner J, Hakonarson H, Reich D. 2012. Phasing of many thousands of genotyped samples. Am J Hum Genet. 91:238-251.
78. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW, et al. 2010. Common SNPs explain a large proportion of the heritability for human height. Nat Genet. 42:565-569.