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Select Early-Life Environmental Exposures and DNA Methylation in the Placenta

  • Early Life Environmental Health (H Volk and J Buckley, Section Editors)
  • Published:
Current Environmental Health Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

To summarize recent literature relating early-life environmental exposures on DNA methylation in the placenta, to identify how variation in placental methylation is regulated in an exposure-specific manner, and to encourage additional work in this area.

Recent Findings

Multiple studies have evaluated associations between prenatal environmental exposures and placental methylation in both gene-specific and epigenome-wide frameworks. Specific exposures lead to unique variability in methylation, and cross-exposure assessments have uncovered certain genes that demonstrate consistency in differential placental methylation. Exposure studies that assess methylation effects in a trimester-specific approach tend to find larger effects during the 1st trimester exposure. Earlier studies have more targeted gene-specific approaches to methylation, while later studies have shifted towards epigenome-wide, array-based approaches. Studies focusing on exposures such as air pollution, maternal smoking, environmental contaminants, and trace metals appear to be more abundant, while studies of socioeconomic adversity and circadian disruption are scarce but demonstrate remarkable effects.

Summary

Understanding the impacts of early-life environmental exposures on placental methylation is critical to establishing the link between the maternal environment, epigenetic variation, and long-term health. Future studies into this field should incorporate repeated measures of exposure throughout pregnancy, in order to determine the critical windows in which placental methylation is most heavily affected. Additionally, the use of methylation-based scores and sequencing technology could provide important insights into epigenetic gestational age and uncovering more genomic regions where methylation is affected. Studies examining the impact of other exposures on methylation, including pesticides, alcohol, and other chemicals are also warranted.

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References

  1. Newell-Price J, Clark AJ, King P. DNA methylation and silencing of gene expression. Trends Endocrinol Metab. 2000;11(4):142–8.

    Article  CAS  Google Scholar 

  2. Hannon E, Knox O, Sugden K, Burrage J, Wong CCY, Belsky DW, et al. Characterizing genetic and environmental influences on variable DNA methylation using monozygotic and dizygotic twins. PLoS Genet. 2018;14(8):e1007544.

    Article  Google Scholar 

  3. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.

    Article  CAS  Google Scholar 

  4. Robinson WP, Price EM. The human placental methylome. Cold Spring Harb Perspect Med. 2015;5(5):a023044.

    Article  Google Scholar 

  5. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet. 2007;39(4):457–66.

    Article  CAS  Google Scholar 

  6. Vryer R, Saffery R. What’s in a name? Context-dependent significance of ‘global’ methylation measures in human health and disease. Clin Epigenetics. 2017;9:2.

    Article  Google Scholar 

  7. Stoccoro A, Coppede F. Mitochondrial DNA methylation and human diseases. Int J Mol Sci. 2021;22(9).

  8. Dong Z, Pu L, Cui H. Mitoepigenetics and its emerging roles in cancer. Front Cell Dev Biol. 2020;8:4.

    Article  Google Scholar 

  9. Baccarelli AA, Byun HM. Platelet mitochondrial DNA methylation: a potential new marker of cardiovascular disease. Clin Epigenetics. 2015;7:44.

    Article  Google Scholar 

  10. Tsaprouni LG, Yang TP, Bell J, Dick KJ, Kanoni S, Nisbet J, et al. Cigarette smoking reduces DNA methylation levels at multiple genomic loci but the effect is partially reversible upon cessation. Epigenetics. 2014;9(10):1382–96.

    Article  Google Scholar 

  11. Joubert BR, Felix JF, Yousefi P, Bakulski KM, Just AC, Breton C, et al. DNA methylation in newborns and maternal smoking in pregnancy: genome-wide consortium meta-analysis. Am J Hum Genet. 2016;98(4):680–96.

    Article  CAS  Google Scholar 

  12. Elliott HR, Tillin T, McArdle WL, Ho K, Duggirala A, Frayling TM, et al. Differences in smoking associated DNA methylation patterns in South Asians and Europeans. Clin Epigenetics. 2014;6(1):4.

    Article  Google Scholar 

  13. Gruzieva O, Xu CJ, Breton CV, Annesi-Maesano I, Anto JM, Auffray C, et al. Epigenome-wide meta-analysis of methylation in children related to prenatal NO2 air pollution exposure. Environ Health Perspect. 2017;125(1):104–10.

    Article  CAS  Google Scholar 

  14. Maghbooli Z, Hossein-Nezhad A, Adabi E, Asadollah-Pour E, Sadeghi M, Mohammad-Nabi S, et al. Air pollution during pregnancy and placental adaptation in the levels of global DNA methylation. PLoS ONE. 2018;13(7):e0199772.

    Article  Google Scholar 

  15. Mostafavi N, Vlaanderen J, Portengen L, Chadeau-Hyam M, Modig L, Palli D, et al. Associations between genome-wide gene expression and ambient nitrogen oxides. Epidemiology. 2017;28(3):320–8.

    Article  Google Scholar 

  16. Goodrich JM, Basu N, Franzblau A, Dolinoy DC. Mercury biomarkers and DNA methylation among Michigan dental professionals. Environ Mol Mutagen. 2013;54(3):195–203.

    Article  CAS  Google Scholar 

  17. Tajuddin SM, Amaral AF, Fernandez AF, Rodriguez-Rodero S, Rodriguez RM, Moore LE, et al. Genetic and non-genetic predictors of LINE-1 methylation in leukocyte DNA. Environ Health Perspect. 2013;121(6):650–6.

    Article  Google Scholar 

  18. Tellez-Plaza M, Tang WY, Shang Y, Umans JG, Francesconi KA, Goessler W, et al. Association of global DNA methylation and global DNA hydroxymethylation with metals and other exposures in human blood DNA samples. Environ Health Perspect. 2014;122(9):946–54.

    Article  Google Scholar 

  19. Hanna CW, Bloom MS, Robinson WP, Kim D, Parsons PJ, vom Saal FS, 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(5):1401–10.

    Article  CAS  Google Scholar 

  20. Itoh H, Iwasaki M, Kasuga Y, Yokoyama S, Onuma H, Nishimura H, et al. Association between serum organochlorines and global methylation level of leukocyte DNA among Japanese women: a cross-sectional study. Sci Total Environ. 2014;490:603–9.

    Article  CAS  Google Scholar 

  21. Watkins DJ, Wellenius GA, Butler RA, Bartell SM, Fletcher T, Kelsey KT. Associations between serum perfluoroalkyl acids and LINE-1 DNA methylation. Environ Int. 2014;63:71–6.

    Article  CAS  Google Scholar 

  22. Clark NA, Demers PA, Karr CJ, Koehoorn M, Lencar C, Tamburic L, et al. Effect of early life exposure to air pollution on development of childhood asthma. Environ Health Perspect. 2010;118(2):284–90.

    Article  CAS  Google Scholar 

  23. Lindoso L, Mondal K, Venkateswaran S, Somineni HK, Ballengee C, Walters TD, et al. The effect of early-life environmental exposures on disease phenotype and clinical course of Crohn’s disease in children. Am J Gastroenterol. 2018;113(10):1524–9.

    Article  CAS  Google Scholar 

  24. Pesce G, Sese L, Calciano L, Travert B, Dessimond B, Maesano CN, et al. Foetal exposure to heavy metals and risk of atopic diseases in early childhood. Pediatr Allergy Immunol. 2021;32(2):242–50.

    Article  CAS  Google Scholar 

  25. Lin X, Teh AL, Chen L, Lim IY, Tan PF, MacIsaac JL, et al. Choice of surrogate tissue influences neonatal EWAS findings. BMC Med. 2017;15(1):211.

    Article  Google Scholar 

  26. Lura MP, Gorlanova O, Muller L, Proietti E, Vienneau D, Reppucci D, et al. Response of cord blood cells to environmental, hereditary and perinatal factors: a prospective birth cohort study. PLoS ONE. 2018;13(7):e0200236.

    Article  Google Scholar 

  27. Fisher SJ. The placenta dilemma. Semin Reprod Med. 2000;18(3):321–6.

    Article  CAS  Google Scholar 

  28. Maltepe E, Fisher SJ. Placenta: the forgotten organ. Annu Rev Cell Dev Biol. 2015;31:523–52.

    Article  CAS  Google Scholar 

  29. Nugent BM, Bale TL. The omniscient placenta: metabolic and epigenetic regulation of fetal programming. Front Neuroendocrinol. 2015;39:28–37.

    Article  CAS  Google Scholar 

  30. Barker DJ, Thornburg KL. Placental programming of chronic diseases, cancer and lifespan: a review. Placenta. 2013;34(10):841–5.

    Article  CAS  Google Scholar 

  31. Kusuyama J, Alves-Wagner AB, Makarewicz NS, Goodyear LJ. Effects of maternal and paternal exercise on offspring metabolism. Nat Metab. 2020;2(9):858–72.

    Article  Google Scholar 

  32. Mitro SD, Johnson T, Zota AR. Cumulative chemical exposures during pregnancy and early development. Curr Environ Health Rep. 2015;2(4):367–78.

    Article  CAS  Google Scholar 

  33. Robinson JF, Hamilton EG, Lam J, Chen H, Woodruff TJ. Differences in cytochrome p450 enzyme expression and activity in fetal and adult tissues. Placenta. 2020;100:35–44.

    Article  CAS  Google Scholar 

  34. Sachdeva P, Patel BG, Patel BK. Drug use in pregnancy; a point to ponder! Indian J Pharm Sci. 2009;71(1):1–7.

    Article  Google Scholar 

  35. Myatt L. Placental adaptive responses and fetal programming. J Physiol. 2006;572(Pt 1):25–30.

    Article  CAS  Google Scholar 

  36. Saenen ND, Martens DS, Neven KY, Alfano R, Bove H, Janssen BG, et al. Air pollution-induced placental alterations: an interplay of oxidative stress, epigenetics, and the aging phenotype? Clin Epigenetics. 2019;11(1):124.

    Article  CAS  Google Scholar 

  37. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 2009;5(8):e1000602.

    Article  Google Scholar 

  38. Janssen BG, Godderis L, Pieters N, Poels K, Kicinski M, Cuypers A, et al. Placental DNA hypomethylation in association with particulate air pollution in early life. Part Fibre Toxicol. 2013;10:22.

    Article  CAS  Google Scholar 

  39. Sagawa N, Yura S, Itoh H, Kakui K, Takemura M, Nuamah MA, et al. Possible role of placental leptin in pregnancy: a review. Endocrine. 2002;19(1):65–71.

    Article  CAS  Google Scholar 

  40. Saenen ND, Vrijens K, Janssen BG, Roels HA, Neven KY, Vanden Berghe W, et al. Lower placental leptin promoter methylation in association with fine particulate matter air pollution during pregnancy and placental nitrosative stress at birth in the ENVIRONAGE cohort. Environ Health Perspect. 2017;125(2):262–8.

    Article  CAS  Google Scholar 

  41. Nawrot TS, Saenen ND, Schenk J, Janssen BG, Motta V, Tarantini L, et al. Placental circadian pathway methylation and in utero exposure to fine particle air pollution. Environ Int. 2018;114:231–41.

    Article  CAS  Google Scholar 

  42. Neven KY, Saenen ND, Tarantini L, Janssen BG, Lefebvre W, Vanpoucke C, et al. Placental promoter methylation of DNA repair genes and prenatal exposure to particulate air pollution: an ENVIRONAGE cohort study. Lancet Planet Health. 2018;2(4):e174–83.

    Article  Google Scholar 

  43. Zhao Y, Wang P, Zhou Y, Xia B, Zhu Q, Ge W, et al. Prenatal fine particulate matter exposure, placental DNA methylation changes, and fetal growth. Environ Int. 2021;147:106313.

    Article  CAS  Google Scholar 

  44. White V, Jawerbaum A, Mazzucco MB, Gauster M, Desoye G, Hiden U. IGF2 stimulates fetal growth in a sex- and organ-dependent manner. Pediatr Res. 2018;83(1–1):183–9.

    Article  CAS  Google Scholar 

  45. Garcia-Perez C, Roy SS, Naghdi S, Lin X, Davies E, Hajnoczky G. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc Natl Acad Sci U S A. 2012;109(12):4497–502.

    Article  CAS  Google Scholar 

  46. Wang P, Lindsay J, Owens TW, Mularczyk EJ, Warwood S, Foster F, et al. Phosphorylation of the proapoptotic BH3-only protein bid primes mitochondria for apoptosis during mitotic arrest. Cell Rep. 2014;7(3):661–71.

    Article  CAS  Google Scholar 

  47. Yang SI, Lee SH, Lee SY, Kim HC, Kim HB, Kim JH, et al. Prenatal PM2.5 exposure and vitamin D-associated early persistent atopic dermatitis via placental methylation. Ann Allergy Asthma Immunol. 2020;125(6):665-731 e1.

    Article  CAS  Google Scholar 

  48. Hao N, Whitelaw ML. The emerging roles of AhR in physiology and immunity. Biochem Pharmacol. 2013;86(5):561–70.

    Article  CAS  Google Scholar 

  49. Abraham E, Rousseaux S, Agier L, Giorgis-Allemand L, Tost J, Galineau J, et al. Pregnancy exposure to atmospheric pollution and meteorological conditions and placental DNA methylation. Environ Int. 2018;118:334–47.

    Article  CAS  Google Scholar 

  50. Ding H, Dai Y, Lei Y, Wang Z, Liu D, Li R, et al. Upregulation of CD81 in trophoblasts induces an imbalance of Treg/Th17 cells by promoting IL-6 expression in preeclampsia. Cell Mol Immunol. 2019;16(1):302–12.

    Article  Google Scholar 

  51. Novakovic B, Evain-Brion D, Murthi P, Fournier T, Saffery R. Variable DAXX gene methylation is a common feature of placental trophoblast differentiation, preeclampsia, and response to hypoxia. FASEB J. 2017;31(6):2380–92.

    Article  CAS  Google Scholar 

  52. Roberts VH, Webster RP, Brockman DE, Pitzer BA, Myatt L. Post-translational modifications of the P2X(4) purinergic receptor subtype in the human placenta are altered in preeclampsia. Placenta. 2007;28(4):270–7.

    Article  CAS  Google Scholar 

  53. Zhao WX, Huang TT, Jiang M, Feng R, Lin JH. Expression of notch family proteins in placentas from patients with early-onset severe preeclampsia. Reprod Sci. 2014;21(6):716–23.

    Article  Google Scholar 

  54. Ladd-Acosta C, Feinberg JI, Brown SC, Lurmann FW, Croen LA, Hertz-Picciotto I, et al. Epigenetic marks of prenatal air pollution exposure found in multiple tissues relevant for child health. Environ Int. 2019;126:363–76.

    Article  CAS  Google Scholar 

  55. Johannesson S, Andersson EM, Stockfelt L, Barregard L, Sallsten G. Urban air pollution and effects on biomarkers of systemic inflammation and coagulation: a panel study in healthy adults. Inhal Toxicol. 2014;26(2):84–94.

    Article  CAS  Google Scholar 

  56. Ruckerl R, Hampel R, Breitner S, Cyrys J, Kraus U, Carter J, et al. Associations between ambient air pollution and blood markers of inflammation and coagulation/fibrinolysis in susceptible populations. Environ Int. 2014;70:32–49.

    Article  Google Scholar 

  57. Strauss WJ, Ryan L, Morara M, Iroz-Elardo N, Davis M, Cupp M, et al. Improving cost-effectiveness of epidemiological studies via designed missingness strategies. Stat Med. 2010;29(13):1377–87.

    Article  Google Scholar 

  58. Janssen BG, Gyselaers W, Byun HM, Roels HA, Cuypers A, Baccarelli AA, et al. Placental mitochondrial DNA and CYP1A1 gene methylation as molecular signatures for tobacco smoke exposure in pregnant women and the relevance for birth weight. J Transl Med. 2017;15(1):5.

    Article  Google Scholar 

  59. Ezzeldin N, El-Lebedy D, Darwish A, El-Bastawisy A, Hassan M, Abd El-Aziz S, et al. Genetic polymorphisms of human cytochrome P450 CYP1A1 in an Egyptian population and tobacco-induced lung cancer. Genes Environ. 2017;39:7.

    Article  Google Scholar 

  60. Fa S, Larsen TV, Bilde K, Daugaard TF, Ernst EH, Lykke-Hartmann K, et al. Changes in first trimester fetal CYP1A1 and AHRR DNA methylation and mRNA expression in response to exposure to maternal cigarette smoking. Environ Toxicol Pharmacol. 2018;57:19–27.

    Article  CAS  Google Scholar 

  61. Vos S, Nawrot TS, Martens DS, Byun HM, Janssen BG. Mitochondrial DNA methylation in placental tissue: a proof of concept study by means of prenatal environmental stressors. Epigenetics. 2021;16(2):121–31.

    Article  Google Scholar 

  62. Sharma H, Singh A, Sharma C, Jain SK, Singh N. Mutations in the mitochondrial DNA D-loop region are frequent in cervical cancer. Cancer Cell Int. 2005;5:34.

    Article  Google Scholar 

  63. van Loon NM, Lindholm D, Zelcer N. The E3 ubiquitin ligase inducible degrader of the LDL receptor/myosin light chain interacting protein in health and disease. Curr Opin Lipidol. 2019;30(3):192–7.

    Article  Google Scholar 

  64. Cardenas A, Lutz SM, Everson TM, Perron P, Bouchard L, Hivert MF. Mediation by placental DNA methylation of the association of prenatal maternal smoking and birth weight. Am J Epidemiol. 2019;188(11):1878–86.

    Article  Google Scholar 

  65. Shorey-Kendrick LE, McEvoy CT, O’Sullivan SM, Milner K, Vuylsteke B, Tepper RS, et al. Impact of vitamin C supplementation on placental DNA methylation changes related to maternal smoking: association with gene expression and respiratory outcomes. Clin Epigenetics. 2021;13(1):177.

    Article  CAS  Google Scholar 

  66. van Otterdijk SD, Binder AM, Michels KB. Locus-specific DNA methylation in the placenta is associated with levels of pro-inflammatory proteins in cord blood and they are both independently affected by maternal smoking during pregnancy. Epigenetics. 2017;12(10):875–85.

    Article  Google Scholar 

  67. Rousseaux S, Seyve E, Chuffart F, Bourova-Flin E, Benmerad M, Charles MA, et al. Immediate and durable effects of maternal tobacco consumption alter placental DNA methylation in enhancer and imprinted gene-containing regions. BMC Med. 2020;18(1):306.

    Article  CAS  Google Scholar 

  68. Dolinoy DC, Weidman JR, Jirtle RL. Epigenetic gene regulation: linking early developmental environment to adult disease. Reprod Toxicol. 2007;23(3):297–307.

    Article  CAS  Google Scholar 

  69. Everson TM, Vives-Usano M, Seyve E, Cardenas A, Lacasana M, Craig JM, et al. Placental DNA methylation signatures of maternal smoking during pregnancy and potential impacts on fetal growth. Nat Commun. 2021;12(1):5095.

    Article  CAS  Google Scholar 

  70. Song X, Wang Z, Zhang Z, Miao M, Liu J, Luan M, et al. Differential methylation of genes in the human placenta associated with bisphenol A exposure. Environ Res. 2021;200:111389.

    Article  CAS  Google Scholar 

  71. Steinhart Z, Angers S. Wnt signaling in development and tissue homeostasis. Development. 2018;145(11).

  72. Ye Y, Tang Y, Xiong Y, Feng L, Li X. Bisphenol A exposure alters placentation and causes preeclampsia-like features in pregnant mice involved in reprogramming of DNA methylation of WNT2. FASEB J. 2019;33(2):2732–42.

    Article  CAS  Google Scholar 

  73. Jedynak P, Tost J, Calafat AM, Bourova-Flin E, Busato F, Forhan A, et al. Pregnancy exposure to synthetic phenols and placental DNA methylation - an epigenome-wide association study in male infants from the EDEN cohort. Environ Pollut. 2021;290:118024.

    Article  CAS  Google Scholar 

  74. Cao X, Hua X, Wang X, Chen L. Exposure of pregnant mice to triclosan impairs placental development and nutrient transport. Sci Rep. 2017;7:44803.

    Article  CAS  Google Scholar 

  75. Wang X, Chen X, Feng X, Chang F, Chen M, Xia Y, et al. Triclosan causes spontaneous abortion accompanied by decline of estrogen sulfotransferase activity in humans and mice. Sci Rep. 2015;5:18252.

    Article  CAS  Google Scholar 

  76. Kim S, Cho YH, Lee I, Kim W, Won S, Ku JL, et al. Prenatal exposure to persistent organic pollutants and methylation of LINE-1 and imprinted genes in placenta: a CHECK cohort study. Environ Int. 2018;119:398–406.

    Article  CAS  Google Scholar 

  77. St-Pierre J, Hivert MF, Perron P, Poirier P, Guay SP, Brisson D, et al. IGF2 DNA methylation is a modulator of newborn’s fetal growth and development. Epigenetics. 2012;7(10):1125–32.

    Article  CAS  Google Scholar 

  78. Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature. 2002;417(6892):945–8.

    Article  CAS  Google Scholar 

  79. Zhao Y, Song Q, Ge W, Jin Y, Chen S, Zhao Y, et al. Associations between in utero exposure to polybrominated diphenyl ethers, pathophysiological state of fetal growth and placental DNA methylation changes. Environ Int. 2019;133(Pt B):105255.

    Article  CAS  Google Scholar 

  80. Bro-Rasmussen F, Buus O, Trolle D. Ratio cortisone/cortisol in mother and infant at birth. Acta Endocrinol (Copenh). 1962;40:579–83.

    CAS  Google Scholar 

  81. Alikhani-Koopaei R, Fouladkou F, Frey FJ, Frey BM. Epigenetic regulation of 11 beta-hydroxysteroid dehydrogenase type 2 expression. J Clin Invest. 2004;114(8):1146–57.

    Article  CAS  Google Scholar 

  82. Zhao Y, Gong X, Chen L, Li L, Liang Y, Chen S, et al. Site-specific methylation of placental HSD11B2 gene promoter is related to intrauterine growth restriction. Eur J Hum Genet. 2014;22(6):734–40.

    Article  CAS  Google Scholar 

  83. Appleton AA, Jackson BP, Karagas M, Marsit CJ. Prenatal exposure to neurotoxic metals is associated with increased placental glucocorticoid receptor DNA methylation. Epigenetics. 2017;12(8):607–15.

    Article  Google Scholar 

  84. Bromer C, Marsit CJ, Armstrong DA, Padbury JF, Lester B. Genetic and epigenetic variation of the glucocorticoid receptor (NR3C1) in placenta and infant neurobehavior. Dev Psychobiol. 2013;55(7):673–83.

    CAS  Google Scholar 

  85. Monk C, Feng T, Lee S, Krupska I, Champagne FA, Tycko B. Distress during pregnancy: epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. Am J Psychiatry. 2016;173(7):705–13.

    Article  Google Scholar 

  86. Seckl JR. Glucocorticoids, feto-placental 11 beta-hydroxysteroid dehydrogenase type 2, and the early life origins of adult disease. Steroids. 1997;62(1):89–94.

    Article  CAS  Google Scholar 

  87. Gundacker C, Hengstschlager M. The role of the placenta in fetal exposure to heavy metals. Wien Med Wochenschr. 2012;162(9–10):201–6.

    Article  Google Scholar 

  88. Everson TM, Punshon T, Jackson BP, Hao K, Lambertini L, Chen J, et al. Cadmium-associated differential methylation throughout the placental genome: epigenome-wide association study of two U.S. birth cohorts. Environ Health Perspect. 2018;126(1):017010.

    Article  Google Scholar 

  89. Tian FY, Everson TM, Lester B, Punshon T, Jackson BP, Hao K, et al. Selenium-associated DNA methylation modifications in placenta and neurobehavioral development of newborns: an epigenome-wide study of two U.S. birth cohorts. Environ Int. 2020;137:105508.

    Article  CAS  Google Scholar 

  90. Kennedy E, Everson TM, Punshon T, Jackson BP, Hao K, Lambertini L, et al. Copper associates with differential methylation in placentae from two US birth cohorts. Epigenetics. 2020;15(3):215–30.

    Article  Google Scholar 

  91. Le A, Shibata NM, French SW, Kim K, Kharbanda KK, Islam MS, et al. Characterization of timed changes in hepatic copper concentrations, methionine metabolism, gene expression, and global DNA methylation in the Jackson toxic milk mouse model of Wilson disease. Int J Mol Sci. 2014;15(5):8004–23.

    Article  Google Scholar 

  92. Santos HP Jr, Bhattacharya A, Martin EM, Addo K, Psioda M, Smeester L, et al. Epigenome-wide DNA methylation in placentas from preterm infants: association with maternal socioeconomic status. Epigenetics. 2019;14(8):751–65.

    Article  Google Scholar 

  93. Appleton AA, Armstrong DA, Lesseur C, Lee J, Padbury JF, Lester BM, et al. Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS ONE. 2013;8(9):e74691.

    Article  CAS  Google Scholar 

  94. Clarkson-Townsend DA, Everson TM, Deyssenroth MA, Burt AA, Hermetz KE, Hao K, et al. Maternal circadian disruption is associated with variation in placental DNA methylation. PLoS ONE. 2019;14(4):e0215745.

    Article  CAS  Google Scholar 

  95. Martin EM, Fry RC. A cross-study analysis of prenatal exposures to environmental contaminants and the epigenome: support for stress-responsive transcription factor occupancy as a mediator of gene-specific CpG methylation patterning. Environ Epigenet. 2016;2(1).

  96. Doi M, Hirayama J, Sassone-Corsi P. Circadian regulator CLOCK is a histone acetyltransferase. Cell. 2006;125(3):497–508.

    Article  CAS  Google Scholar 

  97. Lyons AB, Moy L, Moy R, Tung R. Circadian rhythm and the skin: a review of the literature. J Clin Aesthet Dermatol. 2019;12(9):42–5.

    Google Scholar 

  98. Yuan V, Price EM, Del Gobbo G, Mostafavi S, Cox B, Binder AM, et al. Accurate ethnicity prediction from placental DNA methylation data. Epigenetics Chromatin. 2019;12(1):51.

    Article  Google Scholar 

  99. Lee Y, Choufani S, Weksberg R, Wilson SL, Yuan V, Burt A, et al. Placental epigenetic clocks: estimating gestational age using placental DNA methylation levels. Aging (Albany NY). 2019;11(12):4238–53.

    Article  CAS  Google Scholar 

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Funding

This work was supported by the National Institutes of Health (NIH-NIGMS T32GM008490, NIH-NIEHS R24ES028507, NIH-NIEHS R01ES025145, and NIH-NIEHS P30 ES019776).

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  1. Gangarosa Department of Environmental Health, Rollins School of Public Health, Emory University, Atlanta, USA

    Michael Mortillo & Carmen J. Marsit

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Mortillo, M., Marsit, C.J. Select Early-Life Environmental Exposures and DNA Methylation in the Placenta. Curr Envir Health Rpt 10, 22–34 (2023). https://doi.org/10.1007/s40572-022-00385-1

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