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Research Article

Identification of sex-specific DNA methylation changes driven by specific chemicals in cord blood in a Faroese birth cohort

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Pages 290-300 | Received 08 Jan 2018, Accepted 20 Feb 2018, Published online: 16 May 2018

References

  • Ladd-Acosta C. Epigenetic signatures as biomarkers of exposure. Curr Environ Health Rep. 2015;2:117–125. doi:10.1007/s40572-015-0051-2. PMID:26231361
  • Hanna CW, Bloom MS, Robinson WP, et al. DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF. Hum Reprod. 2012;27:1401–1410. doi:10.1093/humrep/des038. PMID:22381621
  • Pilsner JR, Hu H, Ettinger A, et al. Influence of prenatal lead exposure on genomic methylation of cord blood DNA. Environ Health Perspect. 2009;117:1466–1471. doi:10.1289/ehp.0800497. PMID:19750115
  • Lander ES, Linton LM, Birren B, et al. Initial sequencing and analysis of the human genome. Nature. 2001;409:860–921. doi:10.1038/35057062. PMID:11237011
  • Jordan IK, Rogozin IB, Glazko GV, et al. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 2003;19:68–72. doi:10.1016/S0168-9525(02)00006-9. PMID:12547512
  • Ho SM, Johnson A, Tarapore P, et al. Environmental epigenetics and its implication on disease risk and health outcomes. ILAR J. 2012;53:289–305. doi:10.1093/ilar.53.3-4.289. PMID:23744968
  • Ho SM, Cheong A, Adgent MA, et al. Environmental factors, epigenetics, and developmental origin of reproductive disorders. Reprod Toxicol. 2017;68:85–104. doi:10.1016/j.reprotox.2016.07.011. PMID:27421580
  • Perera F, Tang WY, Herbstman J, et al. Relation of DNA methylation of 5'-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS One. 2009;4:e4488. doi:10.1371/journal.pone.0004488. PMID:19221603
  • Tang WY, Levin L, Talaska G, et al. Maternal exposure to polycyclic aromatic hydrocarbons and 5'-CpG methylation of interferon-gamma in cord white blood cells. Environ Health Perspect. 2012;120:1195–1200. doi:10.1289/ehp.1103744. PMID:22562770
  • Joubert BR, Haberg SE, Nilsen RM, et al. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect. 2012;120:1425–1431. doi:10.1289/ehp.1205412. PMID:22851337
  • Joubert BR, Haberg SE, Bell DA, et al. Maternal smoking and DNA methylation in newborns: in utero effect or epigenetic inheritance?. Cancer Epidemiol Biomarkers Prev. 2014;23:1007–1017. doi:10.1158/1055-9965.EPI-13-1256. PMID:24740201
  • Richmond RC, Simpkin AJ, Woodward G, et al. Prenatal exposure to maternal smoking and offspring DNA methylation across the lifecourse: findings from the avon longitudinal study of parents and children (ALSPAC). Hum Mol Genet. 2015;24:2201–2217. doi:10.1093/hmg/ddu739. PMID:25552657
  • Koestler DC, Avissar-Whiting M, Houseman EA, et al. Differential DNA methylation in umbilical cord blood of infants exposed to low levels of arsenic in utero. Environ Health Perspect. 2013;121:971–977. doi:10.1289/ehp.1205925. PMID:23757598
  • Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261:412–417. doi:10.1111/j.1365-2796.2007.01809.x. PMID:17444880
  • Wu S, Hivert MF, Cardenas A, et al. Exposure to low levels of lead in utero and umbilical cord blood DNA methylation in project viva: an epigenome-wide association study. Environ Health Perspect. 2017;125:087019-1–087019-10. doi:10.1289/EHP1246. PMID:28858830
  • Grandjean P, Budtz-Jorgensen E, White RF, et al. Methylmercury exposure biomarkers as indicators of neurotoxicity in children aged 7 years. Am J Epidemiol. 1999;150:301–305. doi:10.1093/oxfordjournals.aje.a010002. PMID:10430235
  • Grandjean P, Weihe P, Burse VW, et al. Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicol Teratol. 2001;23:305–317. doi:10.1016/S0892-0362(01)00155-6. PMID:11485834
  • Weihe P, Joensen HD. Dietary recommendations regarding pilot whale meat and blubber in the Faroe Islands. Int J Circumpolar Health. 2012;71:18594-1–18594-5. doi:10.3402/ijch.v71i0.18594.
  • Grandjean P, Weihe P, Nielsen F, et al. Neurobehavioral deficits at age 7 years associated with prenatal exposure to toxicants from maternal seafood diet. Neurotoxicol Teratol. 2012;34:466–472. doi:10.1016/j.ntt.2012.06.001. PMID:22705177
  • Grandjean P, Weihe P, Jorgensen PJ, et al. Impact of maternal seafood diet on fetal exposure to mercury, selenium, and lead. Arch Environ Health. 1992;47:185–195. doi:10.1080/00039896.1992.9938348. PMID:1596101
  • Johansen T, Olaffson A. The faroe islands: a brief introduction. Copenhagen: Faroese Government Office; 1999.
  • Weihe P, Grandjean P, Debes F, et al. Health implications for Faroe islanders of heavy metals and PCBs from pilot whales. Sci Total Environ. 1996;186:141–148. doi:10.1016/0048-9697(96)05094-2. PMID:8685706
  • Bloch D, Desportes G, Hoydal K, et al. Pilot whaling in the Faroe Islands. North Atlantic Studies. 1990;2:36–44.
  • Borrell A, Aguilar A. Pollution by DDT and PCB in blubber and muscle of long-finned pilot whales from the Faroe Islands. In: Donovan GP, Lockyer CH, Martin AR, editors. Biology of northern hemisphere pilot whales. Cambridge: International Whaling Commission; 1993. p. 351–367.
  • Dam M. Mercury in the Faroe Islands: a review of available data. Frodskaparrit. 2004;52:85–133.
  • Rotander A, Karrman A, van Bavel B, et al. Increasing levels of long-chain perfluorocarboxylic acids (PFCAs) in Arctic and North Atlantic marine mammals, 1984–2009. Chemosphere. 2012;86:278–285. doi:10.1016/j.chemosphere.2011.09.054. PMID:22051347
  • Grandjean P, Henriksen JE, Choi AL, et al. Marine food pollutants as a risk factor for hypoinsulinemia and type 2 diabetes. Epidemiology (Cambridge, Mass). 2011;22:410–417. doi:10.1097/EDE.0b013e318212fab9. PMID:21364465
  • Weihe P, Kato K, Calafat AM, et al. Serum concentrations of polyfluoroalkyl compounds in Faroese whale meat consumers. Environ Sci Technol. 2008;42:6291–6295. doi:10.1021/es800695m. PMID:18767701
  • Aryee MJ, Jaffe AE, Corrada-Bravo H, et al. Minfi: a flexible and comprehensive Bioconductor package for the analysis of Infinium DNA methylation microarrays. Bioinformatics. 2014;30:1363–1369. doi:10.1093/bioinformatics/btu049. PMID:24478339
  • Xu Z, Niu L, Li L, et al. ENmix: a novel background correction method for Illumina HumanMethylation450 BeadChip. Nucleic Acids Res. 2016;44:e20-1–e20-6. doi:10.1093/nar/gkv907. PMID:26384415
  • Xu Z, Langie SA, De Boever P, et al. RELIC: a novel dye-bias correction method for Illumina Methylation BeadChip. BMC Genomics. 2017;18:4, 1–7. doi:10.1186/s12864-016-3426-3. PMID:28049437
  • Niu L, Xu Z, Taylor JA. RCP: a novel probe design bias correction method for Illumina Methylation BeadChip. Bioinformatics. 2016;32:2659–2663. doi:10.1093/bioinformatics/btw285. PMID:27153672
  • Leek JT, Storey JD. Capturing heterogeneity in gene expression studies by surrogate variable analysis. PLoS Genet. 2007;3:1724–1735. doi:10.1371/journal.pgen.0030161. PMID:17907809
  • Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3: Article3, 1–25. doi:10.2202/1544-6115.1027. PMID:16646809
  • McGregor K, Bernatsky S, Colmegna I, et al. An evaluation of methods correcting for cell-type heterogeneity in DNA methylation studies. Genome Biol. 2016;17:84, 1–17. doi:10.1186/s13059-016-0935-y. PMID:27142380
  • Wang H, Ding N, Guo J, et al. Dysregulation of TTP and HuR plays an important role in cancers. Tumour Biol. 2016;37:14451–14461. doi:10.1007/s13277-016-5397-z. PMID:27644249
  • Sandoval J, Heyn H, Moran S, et al. Validation of a DNA methylation microarray for 450,000 CpG sites in the human genome. Epigenetics. 2011;6:692–702. doi:10.4161/epi.6.6.16196. PMID:21593595
  • Giorda R, Bonaglia MC, Beri S, et al. Complex segmental duplications mediate a recurrent dup(X)(p11.22-p11.23) associated with mental retardation, speech delay, and EEG anomalies in males and females. Am J Hum Genet. 2009;85:394–400. doi:10.1016/j.ajhg.2009.08.001. PMID:19716111
  • Butler MG, Rafi SK, Manzardo AM. High-resolution chromosome ideogram representation of currently recognized genes for autism spectrum disorders. Int J Mol Sci. 2015;16:6464–6495. doi:10.3390/ijms16036464. PMID:25803107
  • Gutierrez B, Arias B, Gasto C, et al. Association analysis between a functional polymorphism in the monoamine oxidase A gene promoter and severe mood disorders. Psychiatr Genet. 2004;14:203–208. doi:10.1097/00041444-200412000-00007. PMID:15564894
  • Chatila TA, Blaeser F, Ho N, et al. JM2, encoding a fork head-related protein, is mutated in X-linked autoimmunity-allergic disregulation syndrome. J Clin Invest. 2000;106:R75–R81. doi:10.1172/JCI11679. PMID:11120765
  • Bennett CL, Ochs HD. IPEX is a unique X-linked syndrome characterized by immune dysfunction, polyendocrinopathy, enteropathy, and a variety of autoimmune phenomena. Curr Opin Pediatr. 2001;13:533–538. doi:10.1097/00008480-200112000-00007. PMID:11753102
  • Rajender S, Thangaraj K, Gupta NJ, et al. A novel human sex-determining gene linked to Xp11.21-11.23. J Clin Endocrinol Metab. 2006;91:4028–4036. doi:10.1210/jc.2006-0950. PMID:16868052
  • Cardenas A, Koestler DC, Houseman EA, et al. Differential DNA methylation in umbilical cord blood of infants exposed to mercury and arsenic in utero. Epigenetics. 2015;10:508–515. doi:10.1080/15592294.2015.1046026. PMID:25923418
  • Huen K, Yousefi P, Bradman A, et al. Effects of age, sex, and persistent organic pollutants on DNA methylation in children. Environ Mol Mutagen. 2014;55:209–222. doi:10.1002/em.21845. PMID:24375655
  • Kobayashi S, Azumi K, Goudarzi H, et al. Effects of prenatal perfluoroalkyl acid exposure on cord blood IGF2/H19 methylation and ponderal index: the Hokkaido study. J Expo Sci Environ Epidemiol. 2017;27:251–259. doi:10.1038/jes.2016.50. PMID:27553991
  • Reaves DK, Ginsburg E, Bang JJ, et al. Persistent organic pollutants and obesity: are they potential mechanisms for breast cancer promotion?. Endocr Relat Cancer. 2015;22:R69–R86. doi:10.1530/ERC-14-0411. PMID:25624167
  • Deierlein AL, Rock S, Park S. Persistent endocrine-disrupting chemicals and fatty liver disease. Curr Environ Health Rep. 2017;4(4):439–449. doi:10.1007/s40572-017-0166-8. PMID: 28980219
  • Kennedy SM, Koehoorn M. Exposure assessment in epidemiology: does gender matter?. Am J Ind Med. 2003;44:576–583. doi:10.1002/ajim.10297. PMID: 14635234
  • Sharp AJ, Stathaki E, Migliavacca E, et al. DNA methylation profiles of human active and inactive X chromosomes. Genome Res. 2011;21:1592–1600. doi:10.1101/gr.112680.110. PMID: 21862626
  • Deng X, Berletch JB, Nguyen DK, et al. X chromosome regulation: diverse patterns in development, tissues and disease. Nat Rev Genet. 2014;15:367–378. doi:10.1038/nrg3687. PMID: 24733023
  • Pasque V, Plath K. X chromosome reactivation in reprogramming and in development. Curr Opin Cell Biol. 2015;37:75–83. doi:10.1016/j.ceb.2015.10.006. PMID: 26540406
  • Reue K. Sex differences in obesity: X chromosome dosage as a risk factor for increased food intake, adiposity and co-morbidities. Physiol Behav. 2017;176:174–182. doi:10.1016/j.physbeh.2017.02.040. PMID: 28284880
  • Arnold AP, Cassis LA, Eghbali M, et al. Sex hormones and sex chromosomes cause sex differences in the development of cardiovascular diseases. Arterioscler Thromb Vasc Biol. 2017;37:746–756. doi:10.1161/ATVBAHA.116.307301. PMID: 28279969
  • Reed L, Buchner V, Tchounwou PB. Environmental toxicology and health effects associated with hexachlorobenzene exposure. Rev Environ Health. 2007;22:213–243. doi:10.1515/REVEH.2007.22.3.213. PMID: 18078005
  • Karlsen M, Grandjean P, Weihe P, et al. Early-life exposures to persistent organic pollutants in relation to overweight in preschool children. Reprod Toxicol. 2017;68:145–153. doi:10.1016/j.reprotox.2016.08.002. PMID: 27496715
  • Valvi D, Mendez MA, Garcia-Esteban R, et al. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy. Obesity (Silver Spring). 2014;22:488–496. doi:10.1002/oby.20603. PMID: 23963708
  • Jarrell JF, Gocmen A, Akyol D, et al. Hexachlorobenzene exposure and the proportion of male births in Turkey 1935–1990. Reprod Toxicol. 2002;16:65–70. doi:10.1016/S0890-6238(01)00196-4. PMID: 11934533
  • Kelce WR, Wilson EM. Environmental antiandrogens: developmental effects, molecular mechanisms, and clinical implications. J Mol Med (Berl). 1997;75:198–207. doi:10.1007/s001090050104. PMID: 9106076
  • De Jager C, Farias P, Barraza-Villarreal A, et al. Reduced seminal parameters associated with environmental DDT exposure and p,p'-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl. 2006;27:16–27. doi:10.2164/jandrol.05121. PMID: 16400073
  • Charlier CJ, Foidart JM. Comparative study of dichlorodiphenyldichloroethylene in blood and semen of two young male populations: lack of relationship to infertility, but evidence of high exposure of the mothers. Reprod Toxicol. 2005;20:215–220. doi:10.1016/j.reprotox.2005.03.007. PMID: 15907656
  • Quan C, Shi Y, Wang C, et al. p,p'-DDE damages spermatogenesis via phospholipid hydroperoxide glutathione peroxidase depletion and mitochondria apoptosis pathway. Environ Toxicol. 2016;31:593–600. PMID: 25410718
  • Eskenazi B, Marks AR, Bradman A, et al. In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Pediatrics. 2006;118:233–241. doi:10.1542/peds.2005-3117. PMID: 16818570
  • Ribas-Fito N, Cardo E, Sala M, et al. Breastfeeding, exposure to organochlorine compounds, and neurodevelopment in infants. Pediatrics. 2003;111:e580–e585. doi:10.1542/peds.111.5.e580. PMID: 12728113
  • Torres-Sanchez L, Rothenberg SJ, Schnaas L, et al. In utero p,p'-DDE exposure and infant neurodevelopment: a perinatal cohort in Mexico. Environ Health Perspect. 2007;115:435–439. doi:10.1289/ehp.9566. PMID: 17431495
  • Torres-Sanchez L, Schnaas L, Rothenberg SJ, et al. Prenatal p,p -DDE exposure and neurodevelopment among children 3.5-5 years of age. Environ Health Perspect. 2013;121:263–268. PMID: 23151722
  • Wnuk A, Rzemieniec J, Litwa E, et al. The crucial involvement of retinoid X receptors in DDE neurotoxicity. Neurotox Res. 2016;29:155–172. doi:10.1007/s12640-015-9572-6. PMID: 26563996
  • Richardson JR, Roy A, Shalat SL, et al. Elevated serum pesticide levels and risk for Alzheimer disease. JAMA Neurol. 2014;71:284–290. doi:10.1001/jamaneurol.2013.6030. PMID: 24473795
  • Valvi D, Oulhote Y, Weihe P, et al. Gestational diabetes and offspring birth size at elevated environmental pollutant exposures. Environ Int. 2017;107:205–215. doi:10.1016/j.envint.2017.07.016. PMID: 28753482
  • Betts K. PFOS and PFOA in humans: new study links prenatal exposure to lower birth weight. Environ Health Perspect. 2007;115:A550. doi:10.1289/ehp.115-a550a. PMID: 18007977
  • Chen MH, Ha EH, Wen TW, et al. Perfluorinated compounds in umbilical cord blood and adverse birth outcomes. PLoS One. 2012;7:e42474-1–e42474-8. doi:10.1371/journal.pone.0042474. PMID: 22879996
  • Apelberg BJ, Witter FR, Herbstman JB, et al. Cord serum concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in relation to weight and size at birth. Environ Health Perspect. 2007;115:1670–1676. doi:10.1289/ehp.10334. PMID: 18008002

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