Effects of age, sex, and persistent organic pollutants on DNA methylation in children

Environmental and Molecular Mutagenesis

Volumn 55, Issue 3, 2014, Pages 209-222

  Huen, Karen ^a   Yousefi, Paul ^a   Bradman, Asa ^a   Yan, Liying ^b   Harley, Kim G ^a   Kogut, Katherine ^a   Eskenazi, Brenda ^a   Holland, Nina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b EpigenDx   (United States)

Author keywords

Alu; Co exposure; DDE; DDT; Epigenetics; LINE 1; PBDE

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; 2,2',4,4',5,5' HEXABROMODIPHENYL ETHER; BISULFITE; CHLORPHENOTANE; DNA; POLYBROMINATED DIPHENYL ETHER;

AGE DISTRIBUTION; ALU SEQUENCE; ARTICLE; BLOOD SAMPLING; CHILD; CONTROLLED STUDY; DNA ISOLATION; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE; GROUPS BY AGE; HISPANIC; HUMAN; LONG INTERSPERSED REPEAT; MAJOR CLINICAL STUDY; MALE; MATERNAL BLOOD; NEWBORN; ORGANIC POLLUTION; POLLUTANT; PRENATAL EXPOSURE; PYROSEQUENCING; SCHOOL CHILD; SEX DIFFERENCE; THIRD TRIMESTER PREGNANCY; UMBILICAL CORD BLOOD;

ALU; CO-EXPOSURE; DDE; DDT; EPIGENETICS; LINE-1; PBDE;

AGE FACTORS; ALU ELEMENTS; CELL COUNT; CHILD; COHORT STUDIES; DDT; DICHLORODIPHENYL DICHLOROETHYLENE; DNA METHYLATION; ENVIRONMENTAL POLLUTANTS; EPIGENESIS, GENETIC; FEMALE; FETAL BLOOD; HALOGENATED DIPHENYL ETHERS; HUMANS; INFANT, NEWBORN; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MATERNAL EXPOSURE; MEXICAN AMERICANS; ORGANIC CHEMICALS; PREGNANCY; SEX FACTORS;

EID: 84895750493     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.21845     Document Type: Article

References (75)

1. Adalsteinsson BT, Gudnason H, Aspelund T, Harris TB, Launer LJ, Eiriksdottir G, Smith AV, Gudnason V. 2012. Heterogeneity in white blood cells has potential to confound DNA methylation measurements. PLoS ONE 7:e46705.
2. Al-Saleh I, Al-Doush I, Alsabbaheen A, Mohamed Gel D, Rabbah A. 2012. Levels of DDT and its metabolites in placenta, maternal and cord blood and their potential influence on neonatal anthropometric measures. Sci Total Environ 416:62-74.
3. Alexeeff SE, Baccarelli AA, Halonen J, Coull BA, Wright RO, Tarantini L, Bollati V, Sparrow D, Vokonas P, Schwartz J. 2013. Association between blood pressure and DNA methylation of retrotransposons and pro-inflammatory genes. Int J Epidemiol 42:270-280.
4. Baccarelli A, Bollati V. 2009. Epigenetics and environmental chemicals. Curr Opin Pediatr 21:243-251.
5. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, Zanobetti A, Sparrow D, Vokonas PS, Schwartz J. 2009. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 179:572-578.
6. Barr JR, Maggio VL, Barr DB, Turner WE, Sjodin A, Sandau CD, Pirkle JL, Needham LL, Patterson DG, Jr. 2003. New high-resolution mass spectrometric approach for the measurement of polychlorinated biphenyls and organochlorine pesticides in human serum. J Chromatogr B Analyt Technol Biomed Life Sci 794:137-148.
7. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, Byun HM, Jiang J, Marinelli B, Pesatori AC, Bertazzi PA, Yang AS. 2007. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 67:876-880.
8. Bollati V, Schwartz J, Wright R, Litonjua A, Tarantini L, Suh H, Sparrow D, Vokonas P, Baccarelli A. 2009. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev 130:234-239.
9. Bradman A, Castorina R, Sjodin A, Fenster L, Jones RS, Harley KG, Chevrier J, Holland NT, Eskenazi B. 2012. Factors associated with serum polybrominated diphenyl ether (PBDE) levels among school-age children in the CHAMACOS cohort. Environ Sci Technol 46:7373-7381.
10. Bradman AS, Schwartz JM, Fenster L, Barr DB, Holland NT, Eskenazi B. 2007. Factors predicting organochlorine pesticide levels in pregnant Latina women living in a United States agricultural area. J Expo Sci Environ Epidemiol 17:388-399.
11. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD. 2009. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 180:462-467.
12. Burris HH, Rifas-Shiman SL, Baccarelli A, Tarantini L, Boeke CE, Kleinman K, Litonjua AA, Rich-Edwards JW, Gillman MW. 2012. Associations of LINE-1 DNA methylation with preterm birth in a prospective cohort study. J Dev Orig Health Dis 3:173-181.
13. Byun HM, Motta V, Panni T, Bertazzi PA, Apostoli P, Hou L, Baccarelli AA. 2013. Evolutionary age of repetitive element subfamilies and sensitivity of DNA methylation to airborne pollutants. Part Fibre Toxicol 10:28.
14. Carpenter DO, Arcaro K, Spink DC. 2002. Understanding the human health effects of chemical mixtures. Environ Health Perspect 110:25-42.
15. Casimir GJ, Mulier S, Hanssens L, Zylberberg K, Duchateau J. 2010. Gender differences in inflammatory markers in children. Shock 33:258-262.
16. Castorina R, Bradman A, Sjodin A, Fenster L, Jones RS, Harley KG, Eisen EA, Eskenazi B. 2011. Determinants of serum polybrominated diphenyl ether (PBDE) levels among pregnant women in the CHAMACOS cohort. Environ Sci Technol 45:6553-6560.
17. Chao HR, Tsou TC, Huang HL, Chang-Chien GP. 2011. Levels of breast milk PBDEs from southern Taiwan and their potential impact on neurodevelopment. Pediatr Res 70:596-600.
18. Chevrier J, Harley KG, Bradman A, Gharbi M, Sjodin A, Eskenazi B. 2010. Polybrominated diphenyl ether (PBDE) flame retardants and thyroid hormone during pregnancy. Environ Health Perspect 118:1444-1449.
19. Cohn BA, Wolff MS, Cirillo PM, Sholtz RI. 2007. DDT and breast cancer in young women: New data on the significance of age at exposure. Environ Health Perspect 115:1406-1414.
20. Delespesse G, Yang LP, Ohshima Y, Demeure C, Shu U, Byun DG, Sarfati M. 1998. Maturation of human neonatal CD4+ and CD8+ T lymphocytes into Th1/Th2 effectors. Vaccine 16:1415-1419.
21. Dolinoy DC, Huang D, Jirtle RL. 2007. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA 104:13056-13061.
22. El-Maarri O, Walier M, Behne F, van Uum J, Singer H, Diaz-Lacava A, Nusgen N, Niemann B, Watzka M, Reinsberg J, et al. 2011. Methylation at global LINE-1 repeats in human blood are affected by gender but not by age or natural hormone cycles. PLoS ONE 6:e16252.
23. Eskenazi B, Bradman A, Gladstone E, Jaramillo S, Birch K, Holland N. 2003. CHAMACOS, a longitudinal birth cohort study: Lessons from the fields. J Childrens Health 1:3-27.
24. Eskenazi B, Chevrier J, Rauch SA, Kogut K, Harley KG, Johnson C, Trujillo C, Sjodin A, Bradman A. 2013. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ Health Perspect 121:257-262.
25. Eskenazi B, Chevrier J, Rosas LG, Anderson HA, Bornman MS, Bouwman H, Chen A, Cohn BA, de Jager C, Henshel DS, et al. 2009. The Pine River statement: Human health consequences of DDT use. Environ Health Perspect 117:1359-1367.
26. Eskenazi B, Fenster L, Castorina R, Marks AR, Sjodin A, Rosas LG, Holland N, Guerra AG, Lopez-Carillo L, Bradman A. 2011. A comparison of PBDE serum concentrations in Mexican and Mexican-American children living in California. Environ Health Perspect 119:1442-1448.
27. Eskenazi B, Marks AR, Bradman A, Fenster L, Johnson C, Barr DB, Jewell NP. 2006. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics 118:233-241.
28. Fenster L, Eskenazi B, Anderson M, Bradman A, Harley K, Hernandez H, Hubbard A, Barr DB. 2006. Association of in utero organochlorine pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 114:597-602.
29. Gao Y, Baccarelli A, Shu XO, Ji BT, Yu K, Tarantini L, Yang G, Li HL, Hou L, Rothman N, et al. 2012. Blood leukocyte Alu and LINE-1 methylation and gastric cancer risk in the Shanghai Women's Health Study. Br J Cancer 106:585-591.
30. Gascon M, Fort M, Martinez D, Carsin AE, Forns J, Grimalt JO, Santa Marina L, Lertxundi N, Sunyer J, Vrijheid M. 2012. Polybrominated diphenyl ethers (PBDEs) in breast milk and neuropsychological development in infants. Environ Health Perspect 120:1760-1765.
31. Gregoraszczuk EL, Rak A, Kawalec K, Ropstad E. 2008. Steroid secretion following exposure of ovarian follicular cells to single congeners and defined mixture of polybrominateddibenzoethers (PBDEs), p, p'-DDT and its metabolite p, p'-DDE. Toxicol Lett 178:103-109.
32. Harley KG, Marks AR, Bradman A, Barr DB, Eskenazi B. 2008. DDT exposure, work in agriculture, and time to pregnancy among farmworkers in California. J Occup Environ Med 50:1335-1342.
33. Harley KG, Marks AR, Chevrier J, Bradman A, Sjodin A, Eskenazi B. 2010. PBDE concentrations in women's serum and fecundability. Environ Health Perspect 118:699-704.
34. He P, Wang A, Niu Q, Guo L, Xia T, Chen X. 2011. Toxic effect of PBDE-47 on thyroid development, learning, and memory, and the interaction between PBDE-47 and PCB153 that enhances toxicity in rats. Toxicol Ind Health 27:279-288.
35. Holland N, Furlong C, Bastaki M, Richter R, Bradman A, Huen K, Beckman K, Eskenazi B. 2006. Paraoxonase polymorphisms, haplotypes, and enzyme activity in latino mothers and newborns. Environ Health Perspect 114:985-991.
36. Hou L, Wang H, Sartori S, Gawron A, Lissowska J, Bollati V, Tarantini L, Zhang FF, Zatonski W, Chow WH, et al. 2010. Blood leukocyte DNA hypomethylation and gastric cancer risk in a high-risk Polish population. Int J Cancer 127:1866-1874.
37. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. 2012. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 13:86.
38. Houwen B. 2001. The differential cell count. Lab Hematol 7:89-100.
39. Hsiung DT, Marsit CJ, Houseman EA, Eddy K, Furniss CS, McClean MD, Kelsey KT. 2007. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 16:108-114.
40. Jintaridth P, Mutirangura A. 2010. Distinctive patterns of age-dependent hypomethylation in interspersed repetitive sequences. Physiol Genomics 41:194-200.
41. Kazazian HH, Jr., Goodier JL. 2002. LINE drive. Retrotransposition and genome instability. Cell 110:277-280.
42. Kezios KL, Liu X, Cirillo PM, Cohn BA, Kalantzi OI, Wang Y, Petreas MX, Park JS, Factor-Litvak P. 2013. Dichlorodiphenyltrichloroethane (DDT), DDT metabolites and pregnancy outcomes. Reprod Toxicol 35:156-164.
43. Kim KY, Kim DS, Lee SK, Lee IK, Kang JH, Chang YS, Jacobs DR, Steffes M, Lee DH. 2010. Association of low-dose exposure to persistent organic pollutants with global DNA hypomethylation in healthy Koreans. Environ Health Perspect 118:370-374.
44. Koestler DC, Christensen B, Karagas MR, Marsit CJ, Langevin SM, Kelsey KT, Wiencke JK, Houseman EA. 2013. Blood-based profiles of DNA methylation predict the underlying distribution of cell types: A validation analysis. Epigenetics 8:816-826.
45. Lambrou A, Baccarelli A, Wright RO, Weisskopf M, Bollati V, Amarasiriwardena C, Vokonas P, Schwartz J. 2012. Arsenic exposure and DNA methylation among elderly men. Epidemiology 23:668-676.
46. Lubin JH, Colt JS, Camann D, Davis S, Cerhan JR, Severson RK, Bernstein L, Hartge P. 2004. Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect 112:1691-1696.
47. Lyon MF. 2003. The Lyon and the LINE hypothesis. Semin Cell Dev Biol 14:313-318.
48. Michels KB, Harris HR, Barault L. 2011. Birthweight, maternal weight trajectories and global DNA methylation of LINE-1 repetitive elements. PLoS ONE 6:e25254.
49. Mitchell MM, Woods R, Chi LH, Schmidt RJ, Pessah IN, Kostyniak PJ, LaSalle JM. 2012. Levels of select PCB and PBDE congeners in human postmortem brain reveal possible environmental involvement in 15q11-q13 duplication autism spectrum disorder. Environ Mol Mutagen 53:589-598.
50. Pavanello S, Bollati V, Pesatori AC, Kapka L, Bolognesi C, Bertazzi PA, Baccarelli A. 2009. Global and gene-specific promoter methylation changes are related to anti-B[a]PDE-DNA adduct levels and influence micronuclei levels in polycyclic aromatic hydrocarbon-exposed individuals. Int J Cancer 125:1692-1697.
51. Pellacani C, Tagliaferri S, Caglieri A, Goldoni M, Giordano G, Mutti A, Costa LG. 2012. Synergistic interactions between PBDEs and PCBs in human neuroblastoma cells. Environ Toxicol. doi: 10.1002/tox.21768.
52. Peltier MR, Klimova NG, Arita Y, Gurzenda EM, Murthy A, Chawala K, Lerner V, Richardson J, Hanna N. 2012. Polybrominated diphenyl ethers enhance the production of proinflammatory cytokines by the placenta. Placenta 33:745-749.
53. Perera F, Tang WY, Herbstman J, Tang D, Levin L, Miller R, Ho SM. 2009. Relation of DNA methylation of 5′-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS ONE 4:e4488.
54. Perng W, Rozek LS, Mora-Plazas M, Duchin O, Marin C, Forero Y, Baylin A, Villamor E. 2012. Micronutrient status and global DNA methylation in school-age children. Epigenetics 7:1133-1141.
55. Phillips DL, Pirkle JL, Burse VW, Bernert JT, Jr., Henderson LO, Needham LL. 1989. Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding. Arch Environ Contam Toxicol 18:495-500.
56. Price EM, Cotton AM, Penaherrera MS, McFadden DE, Kobor MS, Robinson W. 2012. Different measures of "genome-wide" DNA methylation exhibit unique properties in placental and somatic tissues. Epigenetics 7:652-663.
57. Rose M, Bennett DH, Bergman A, Fangstrom B, Pessah IN, Hertz-Picciotto I. 2010. PBDEs in 2-5 year-old children from California and associations with diet and indoor environment. Environ Sci Technol 44:2648-2653.
58. Royo JL, Hidalgo M, Ruiz A. 2007. Pyrosequencing protocol using a universal biotinylated primer for mutation detection and SNP genotyping. Nat Protoc 2:1734-1739.
59. Rusiecki JA, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgensen EC. 2008. Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit. Environ Health Perspect 116:1547-1552.
60. Singer H, Walier M, Nusgen N, Meesters C, Schreiner F, Woelfle J, Fimmers R, Wienker T, Kalscheuer VM, Becker T, et al. 2012. Methylation of L1Hs promoters is lower on the inactive X, has a tendency of being higher on autosomes in smaller genomes and shows inter-individual variability at some loci. Hum Mol Genet 21:219-235.
61. Sjodin A, Jones RS, Lapeza CR, Focant JF, McGahee EE, 3rd, Patterson DG, Jr. 2004. Semiautomated high-throughput extraction and cleanup method for the measurement of polybrominated diphenyl ethers, polybrominated biphenyls, and polychlorinated biphenyls in human serum. Anal Chem 76:1921-1927.
62. Tarantini L, Bonzini M, Apostoli P, Pegoraro V, Bollati V, Marinelli B, Cantone L, Rizzo G, Hou L, Schwartz J, et al. 2009. Effects of particulate matter on genomic DNA methylation content and iNOS promoter methylation. Environ Health Perspect 117:217-222.
63. Tobi EW, Slagboom PE, van Dongen J, Kremer D, Stein AD, Putter H, Heijmans BT, Lumey LH. 2012. Prenatal famine and genetic variation are independently and additively associated with DNA methylation at regulatory loci within IGF2/H19. PLoS ONE 7:e37933.
64. Uekert SJ, Akan G, Evans MD, Li Z, Roberg K, Tisler C, Dasilva D, Anderson E, Gangnon R, Allen DB, et al. 2006. Sex-related differences in immune development and the expression of atopy in early childhood. J Allergy Clin Immunol 118:1375-1381.
65. Wang L, Wang F, Guan J, Le J, Wu L, Zou J, Zhao H, Pei L, Zheng X, Zhang T. 2010. Relation between hypomethylation of long interspersed nucleotide elements and risk of neural tube defects. Am J Clin Nutr 91:1359-1367.
66. Warner M, Schall RA, Harley KG, Bradman A, Barr D, Eskenazi B. 2013. In utero DDT and DDE exposure and obesity status of 7-year-old Mexican-American children in the CHAMACOS cohort. Environ Health Perspect 121:631-636.
67. Weldon RH, Webster M, Harley KG, Bradman A, Fenster L, Davis MD, Hubbard A, Barr DB, Holland N, Eskenazi B. 2010. Serum persistent organic pollutants and duration of lactation among Mexican-American women. J Environ Public Health 2010:861757.
68. Wilhelm CS, Kelsey KT, Butler R, Plaza S, Gagne L, Zens MS, Andrew AS, Morris S, Nelson HH, Schned AR, et al. 2010. Implications of LINE1 methylation for bladder cancer risk in women. Clin Cancer Res 16:1682-1689.
69. Windham GC, Pinney SM, Sjodin A, Lum R, Jones RS, Needham LL, Biro FM, Hiatt RA, Kushi LH. 2010. Body burdens of brominated flame retardants and other persistent organo-halogenated compounds and their descriptors in US girls. Environ Res 110:251-257.
70. Woodruff TJ, Zota AR, Schwartz JM. 2011. Environmental chemicals in pregnant women in the United States: NHANES 2003-2004. Environ Health Perspect 119:878-885.
71. Wright RO, Schwartz J, Wright RJ, Bollati V, Tarantini L, Park SK, Hu H, Sparrow D, Vokonas P, Baccarelli A. 2010. Biomarkers of lead exposure and DNA methylation within retrotransposons. Environ Health Perspect 118:790-795.
72. Wu HC, John EM, Ferris JS, Keegan TH, Chung WK, Andrulis I, Delgado-Cruzata L, Kappil M, Gonzalez K, Santella RM, et al. 2011. Global DNA methylation levels in girls with and without a family history of breast cancer. Epigenetics 6:29-33.
73. Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. 2004. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res 32:e38.
74. Zhang FF, Cardarelli R, Carroll J, Fulda KG, Kaur M, Gonzalez K, Vishwanatha JK, Santella RM, Morabia A. 2011. Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood. Epigenetics 6:623-629.
75. Zhu ZZ, Hou L, Bollati V, Tarantini L, Marinelli B, Cantone L, Yang AS, Vokonas P, Lissowska J, Fustinoni S, et al. 2012. Predictors of global methylation levels in blood DNA of healthy subjects: A combined analysis. Int J Epidemiol 41:126-139.