Arsenic exposure in early pregnancy alters genome-wide DNA methylation in cord blood, particularly in boys

Journal of Developmental Origins of Health and Disease

Volumn 5, Issue 4, 2014, Pages 288-298

  Broberg, K ^a,b   Ahmed, S ^a,c   Engstrom K ^b   Hossain, M B ^a,b   Jurkovic Mlakar, S ^d   Bottai, M ^a   Grander M ^a   Raqib, R ^c   Vahter, M ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

450 K; cancer; CpG; development; epigenetic; fetal

Indexed keywords

ARSENIC;

ADVERSE EFFECTS; BLOOD; CHEMISTRY; CPG ISLAND; DNA METHYLATION; DRUG EFFECTS; ENVIRONMENTAL EXPOSURE; FEMALE; FETOMATERNAL TRANSFUSION; FETUS BLOOD; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MALE; MASS SPECTROMETRY; NEWBORN; NONPARAMETRIC TEST; PHYSIOLOGY; PREGNANCY; PRINCIPAL COMPONENT ANALYSIS; SEXUAL DEVELOPMENT; STATISTICAL MODEL; URINE;

ARSENIC; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CPG ISLANDS; DNA METHYLATION; FEMALE; FETAL BLOOD; HUMANS; INFANT, NEWBORN; LINEAR MODELS; MALE; MASS SPECTROMETRY; MATERNAL EXPOSURE; MATERNAL-FETAL EXCHANGE; PREGNANCY; PRINCIPAL COMPONENT ANALYSIS; SEX CHARACTERISTICS; STATISTICS, NONPARAMETRIC;

EID: 84903271988     PISSN: 20401744     EISSN: 20401752     Source Type: Journal    
DOI: 10.1017/S2040174414000221     Document Type: Article

References (53)

1. Gluckman PD. Epigenetics and metabolism in 2011: epigenetics, the life-course and metabolic disease. Nat Rev Endocrinol. 2011; 8, 74-76.
2. Attig L, Gabory A, Junien C. Early nutrition and epigenetic programming: chasing shadows. Curr Opin Clin Nutr Metab Care. 2010; 13, 284-293.
3. Barker DJ. Fetal growth and adult disease. Br J Obstet Gynaecol. 1992; 99, 275-276.
4. Bergman Y, Cedar H. DNA methylation dynamics in health and disease. Nat Struct Mol Biol. 2013; 20, 274-281.
5. Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007; 27, 363-388.
6. Baccarelli A, Bollati V. Epigenetics and environmental chemicals. Curr Opin Pediatr. 2009; 21, 243-251.
7. Kippler M, Engström K, Mlakar SJ, et al. Sex-specific effects of early life cadmium exposure on DNA methylation and implications for birth weight. Epigenetics. 2013; 8, 494-503.
8. Perera F, Herbstman J. Prenatal environmental exposures, epigenetics, and disease. Reprod Toxicol. 2011; 31, 363-373
9. EFSA. Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on cadmium in food. EFSA J. 2009; 980, 1-139
10. IARC. A Review of Human Carcinogens: Arsenic, Metals, Fibres, and Dusts. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 2012. International Agency for Research on Cancer: Lyon.
11. Hamadani JD, Tofail F, Nermell B, et al. Critical windows of exposure for arsenic-associated impairment of cognitive function in pre-school girls and boys: a population-based cohort study. Int J Epidemiol. 2011; 40, 1593-1604.
12. Rahman A, Persson LA, Nermell B, et al. Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology. 2010; 21, 797-804.
13. Rahman A, Vahter M, Ekstrom EC, Persson LA. Arsenic exposure in pregnancy increases the risk of lower respiratory tract infection and diarrhea during infancy in Bangladesh. Environ Health Perspect. 2011; 119, 719-724.
14. Saha KK, Engstrom A, Hamadani JD, et al. Pre-and postnatal arsenic exposure and body size to two years of age: a cohort study in rural Bangladesh. Environ Health Perspect. 2012; 120, 1208-1214.
15. Liaw J, Marshall G, Yuan Y, et al. Increased childhood liver cancer mortality and arsenic in drinking water in northern Chile. Cancer Epidemiol Biomarkers Prev. 2008; 17, 1982-1987.
16. Smith AH, Marshall G, Yuan Y, et al. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ Health Perspect. 2006; 114, 1293-1296.
17. Smith AH, Marshall G, Liaw J, et al. Mortality in young adults following in utero and childhood exposure to arsenic in drinking water. Environ Health Perspect. 2012; 120, 1527-1531.
18. Tokar EJ, Diwan BA, Waalkes MP. Arsenic exposure in utero and nonepidermal proliferative response in adulthood in Tg.AC mice. Int J Toxicol. 2010; 29, 291-296.
19. Xie Y, Liu J, Benbrahim-Tallaa L, et al. Aberrant DNA methylation and gene expression in livers of newborn mice transplacentally exposed to a hepatocarcinogenic dose of inorganic arsenic. Toxicology. 2007; 236, 7-15.
20. Yorifuji T, Tsuda T, Grandjean P. Unusual cancer excess after neonatal arsenic exposure from contaminated milk powder. J Natl Cancer Inst. 2010; 102, 360-361.
21. Bhattacharjee P, Banerjee M, Giri AK. Role of genomic instability in arsenic-induced carcinogenicity. A review. Environ Int. 2013; 53, 29-40.
22. Du J, Zhou N, Liu H, et al. Arsenic induces functional re-expression of estrogen receptor alpha by demethylation of DNA in estrogen receptor-negative human breast cancer. PLoS One. 2012; 7, e35957.
23. Hansen KD, Timp W, Bravo HC, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet. 2011; 43, 768-775.
24. Hossain MB, Vahter M, Concha G, Broberg K. Environmental arsenic exposure and DNA methylation of the tumor suppressor gene p16 and the DNA repair gene MLH1: effect of arsenic metabolism and genotype. Metallomics. 2012; 4, 1167-1175.
25. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002; 3, 415-428.
26. Smeester L, Rager JE, Bailey KA, et al. Epigenetic changes in individuals with arsenicosis. Chem Res Toxicol. 2011; 24, 165-167.
27. Intarasunanont P, Navasumrit P, Waraprasit S, et al. Effects of arsenic exposure on DNA methylation in cord blood samples from newborn babies and in a human lymphoblast cell line. Environ Health. 2012; 11, 31.
28. Kile ML, Baccarelli A, Hoffman E, et al. Prenatal arsenic exposure and DNA methylation in maternal and umbilical cord blood leukocytes. Environ Health Perspect. 2012; 120, 1061-1066.
29. Pilsner JR, Hall MN, Liu X, et al. Influence of prenatal arsenic exposure and newborn sex on global methylation of cord blood DNA. PLoS One. 2012; 7, e37147.
30. Koestler DC, Avissar-Whiting M, Houseman EA, Karagas MR, Marsit CJ. Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic in utero. Environ Health Perspect. 2013; 121, 971-977.
31. Gabory A, Attig L, Junien C. Developmental programming and epigenetics. Am J Clin Nutr. 2011; 94, 1943S-1952S.
32. Nohara K, Baba T, Murai H, et al. Global DNA methylation in the mouse liver is affected by methyl deficiency and arsenic in a sex-dependent manner. Arch Toxicol. 2011; 85, 653-661.
33. Rahman M, Vahter M, Wahed MA, et al. Prevalence of arsenic exposure and skin lesions. A population based survey in Matlab, Bangladesh. J Epidemiol Community Health. 2006; 60, 242-248.
34. Winston JJ, Escamilla V, Perez-Heydrich C, et al. Protective benefits of deep tube wells against childhood diarrhea in Matlab, Bangladesh. Am J Public Health. 2013; 103, 1287-1291.
35. Persson LÅ, Arifeen S, Ekström EC, et al. Effects of prenatal micronutrient and early food supplementation on maternal hemoglobin, birth weight, and infant mortality among children in Bangladesh: the MINIMat randomized trial. JAMA. 2012; 307, 2050-2059.
36. Saha KK, Frongillo EA, Alam DS, et al. Household food security is associated with infant feeding practices in rural Bangladesh. J Nutr. 2008; 138, 1383-1390.
37. Vahter M, Li L, Nermell B, et al. Arsenic exposure in pregnancy-a population based study in Matlab, Bangladesh. J Health Popul Nutr. 2006; 24, 236-245.
38. Gardner RM, Nermell B, Kippler M, et al. Arsenic methylation efficiency increases during the first trimester of pregnancy independent of folate status. Reprod Toxicol. 2011; 31, 210-218.
39. Vahter M. Effects of arsenic on maternal and fetal health. Annu Rev Nutr. 2009; 29, 381-399.
40. Li H, Engström K, Vahter M, et al. Arsenic exposure through drinking water is associated with longer telomeres in peripheral blood. Chem Res Toxicol. 2012; 25, 2333-2339.
41. Pierce BL, Kibriya MG, Tong L, et al. Genome-wide association study identifies chromosome 10q24.32 variants associated with arsenic metabolism and toxicity phenotypes in Bangladesh. PLoS Genet. 2012; 8, e1002522.
42. Engström KS, Hossain MB, Lauss M, et al. Efficient arsenic metabolism-the AS3MT haplotype is associated with DNA methylation and expression of multiple genes around AS3MT. PLoS One. 2013; 8, e53732.
43. Hossain MB, Vahter M, Concha G, Broberg K. Low-level environmental cadmium exposure is associated with DNA hypomethylation in Argentinean women. Environ Health Perspect. 2012; 120, 879-884.
44. Waalkes MP, Liu J, Diwan BA. Transplacental arsenic carcinogenesis in mice. ToxicolApplPharmacol. 2007; 222, 271-280.
45. Tokar EJ, Diwan BA, Ward JM, Delker DA, Waalkes MP. Carcinogenic effects of 'whole-life' exposure to inorganic arsenic in CD1 mice. Toxicol Sci. 2011; 119, 73-83.
46. Kippler M, Wagatsuma Y, Rahman A, et al. Environmental exposure to arsenic and cadmium during pregnancy and fetal size: a longitudinal study in rural Bangladesh. Reprod Toxicol. 2012; 34, 504-511.
47. Waalkes MP, Liu J, Chen H, et al. Estrogen signaling in livers of male mice with hepatocellular carcinoma induced by exposure to arsenic in utero. J Natl Cancer Inst. 2004; 96, 466-474.
48. Bosma M, Sparks LM, Hooiveld GJ, et al. Overexpression of PLIN5 in skeletal muscle promotes oxidative gene expression and intramyocellular lipid content without compromising insulin sensitivity. Biochim Biophys Acta. 2013; 1831, 844-852.
49. Wang H, Sreenivasan U, Gong DW, et al. Cardiomyocyte-specific perilipin 5 overexpression leads to myocardial steatosis and modest cardiac dysfunction. J Lipid Res. 2013; 54, 953-965.
50. Liu XF, Xiang L, Zhang Y, et al. CAPC negatively regulates NF-KB activation and suppresses tumor growth and metastasis. Oncogene. 2012; 31, 1673-1682.
51. Slattery ML, Lundgreen A, HerrickJS, Wolff RK. Genetic variation in RPS6KA1, RPS6KA2, RPS6KB1, RPS6KB2, and PDK1 and risk of colon or rectal cancer. Mutat Res. 2011; 706, 13-20.
52. Chiba N, Comaills V, Shiotani B, et al. Homeobox B9 induces epithelial-to-mesenchymal transition-associated radioresistance by accelerating DNA damage responses. Proc Natl Acad Sci. 2012; 109, 2760-2765.
53. Harper KN, Peters BA, Gamble MV. Batch effects and pathway analysis: two potential perils in cancer studies involving DNA methylation array analysis. Cancer Epidemiol Biomarkers Prev. 2013; 22, 1052-1060.