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Current Environmental Health Reports

, Volume 5, Issue 4, pp 544–578 | Cite as

The Impact of Air Pollution on Our Epigenome: How Far Is the Evidence? (A Systematic Review)

  • Rossella Alfano
  • Zdenko Herceg
  • Tim S. Nawrot
  • Marc Chadeau-Hyam
  • Akram GhantousEmail author
  • Michelle PlusquinEmail author
Environmental Epigenetics (A Baccarelli and A Cardenas, Section Editors)
  • 340 Downloads
Part of the following topical collections:
  1. Topical Collection on Environmental Epigenetics

Abstract

Purpose of Review

This systematic review evaluated existing evidence linking air pollution exposure in humans to major epigenetic mechanisms: DNA methylation, microRNAs, long noncoding RNAs, and chromatin regulation.

Recent Findings

Eighty-two manuscripts were eligible, most of which were observational (85%), conducted in adults (66%) and based on DNA methylation (79%).

Summary

Most observational studies, except panel, demonstrated modest effects of air pollution on the methylome. Panel and experimental studies revealed a relatively large number of significant methylome alterations, though based on smaller sample sizes. Particulate matter levels were positively associated in several studies with global or LINE-1 hypomethylation, a hallmark of several diseases, and with decondensed chromatin structure. Several air pollution species altered the DNA methylation clock, inducing accelerated biological aging. The causal nature of identified associations is not clear, however, especially that most originate from countries with low air pollution levels. Existing evidence, gaps, and perspectives are highlighted herein.

Keywords

Air pollution Epigenetics DNA methylation MicroRNAs Noncoding RNA Chromatin 

Notes

Funding Information

Support for this work was provided by the project EXPOSOMICS, grant agreement 308610-FP7 European Commission, and by the Plan Cancer-Eva-Inserm research grant.

Compliance with Ethical Standards

Conflict of Interest

Rossella Alfano has a PhD fellowship from Bijzonder Onderzoeksfonds (BOF) Hasselt University.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

40572_2018_218_MOESM1_ESM.docx (105 kb)
ESM 1 (DOCX 105 kb)

References

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Cohen AJ, Brauer M, Burnett R, Anderson HR, Frostad J, Estep K, et al. Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: an analysis of data from the Global Burden of Diseases Study 2015. Lancet. 2017;389(10082):1907–18.  https://doi.org/10.1016/S0140-6736(17)30505-6.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    WHO. WHO Global Urban Ambient Air Pollution 2016 Database http://www.who.int/phe/health_topics/outdoorair/databases/cities/en/. 2016.
  3. 3.
    Silva RA, West JJ, Lamarque J-F, Shindell DT, Collins WJ, Faluvegi G, et al. Future global mortality from changes in air pollution attributable to climate change. Nat Clim Chang. 2017;7(9):647–51.  https://doi.org/10.1038/nclimate3354.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Forman HJ, Finch CE. A critical review of assays for hazardous components of air pollution. Free Radic Biol Med. 2018;117:202–17.  https://doi.org/10.1016/j.freeradbiomed.2018.01.030.CrossRefPubMedGoogle Scholar
  5. 5.
    Brook RD, Rajagopalan S, Pope CA 3rd, Brook JR, Bhatnagar A, Diez-Roux AV, et al. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation. 2010;121(21):2331–78.  https://doi.org/10.1161/CIR.0b013e3181dbece1.CrossRefPubMedGoogle Scholar
  6. 6.
    Nawrot TS, Perez L, Kunzli N, Munters E, Nemery B. Public health importance of triggers of myocardial infarction: a comparative risk assessment. Lancet. 2011;377(9767):732–40.  https://doi.org/10.1016/S0140-6736(10)62296-9.CrossRefPubMedGoogle Scholar
  7. 7.
    Fiorito G, Vlaanderen J, Polidoro S, Gulliver J, Galassi C, Ranzi A, et al. Oxidative stress and inflammation mediate the effect of air pollution on cardio- and cerebrovascular disease: a prospective study in nonsmokers. Environ Mol Mutagen. 2018;59(3):234–46.  https://doi.org/10.1002/em.22153.CrossRefPubMedGoogle Scholar
  8. 8.
    Hoek G, Krishnan RM, Beelen R, Peters A, Ostro B, Brunekreef B, et al. Long-term air pollution exposure and cardio- respiratory mortality: a review. Environ Health. 2013;12(1):43.  https://doi.org/10.1186/1476-069X-12-43.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Hamra GB, Guha N, Cohen A, Laden F, Raaschou-Nielsen O, Samet JM, et al. Outdoor particulate matter exposure and lung cancer: a systematic review and meta-analysis. Environ Health Perspect. 2014;122(9):906–11.  https://doi.org/10.1289/ehp.1408092.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Loomis D, Grosse Y, Lauby-Secretan B, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, et al. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013;14(13):1262–3.CrossRefGoogle Scholar
  11. 11.
    Clifford A, Lang L, Chen R, Anstey KJ, Seaton A. Exposure to air pollution and cognitive functioning across the life course—a systematic literature review. Environ Res. 2016;147:383–98.  https://doi.org/10.1016/j.envres.2016.01.018.CrossRefPubMedGoogle Scholar
  12. 12.
    Saenen ND, Plusquin M, Bijnens E, Janssen BG, Gyselaers W, Cox B, et al. In utero fine particle air pollution and placental expression of genes in the brain-derived neurotrophic factor signaling pathway: an ENVIRONAGE birth cohort study. Environ Health Perspect. 2015;123(8):834–40.  https://doi.org/10.1289/ehp.1408549.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Lanki T, Pekkanen J, Aalto P, Elosua R, Berglind N, D'Ippoliti D, et al. Associations of traffic related air pollutants with hospitalisation for first acute myocardial infarction: the HEAPSS study. Occup Environ Med. 2006;63(12):844–51.  https://doi.org/10.1136/oem.2005.023911.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Harris MH, Gold DR, Rifas-Shiman SL, Melly SJ, Zanobetti A, Coull BA, et al. Prenatal and childhood traffic-related air pollution exposure and childhood executive function and behavior. Neurotoxicol Teratol. 2016;57:60–70.  https://doi.org/10.1016/j.ntt.2016.06.008.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Saenen ND, Provost EB, Viaene MK, Vanpoucke C, Lefebvre W, Vrijens K, et al. Recent versus chronic exposure to particulate matter air pollution in association with neurobehavioral performance in a panel study of primary schoolchildren. Environ Int. 2016;95:112–9.  https://doi.org/10.1016/j.envint.2016.07.014.CrossRefPubMedGoogle Scholar
  16. 16.
    Goodson JM, Weldy CS, MacDonald JW, Liu Y, Bammler TK, Chien WM, et al. In utero exposure to diesel exhaust particulates is associated with an altered cardiac transcriptional response to transverse aortic constriction and altered DNA methylation. FASEB Journal. 2017;31(11):4935–45.  https://doi.org/10.1096/fj.201700032R.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    •• Plusquin M, Chadeau-Hyam M, Ghantous A, Alfano R, Bustamante M, Chatzi L, et al. DNA methylome marks of exposure to particulate matter at three time points in early life. Environ Sci Technol. 2018;52(9):5427–37.  https://doi.org/10.1021/acs.est.7b06447 Using longitudinal measurements of blood DNA methylation from birth to adolescence provides evidence that residential PM10 exposure affects methylation of sites involved in neurological and cell division control mechanism. CrossRefPubMedGoogle Scholar
  18. 18.
    Martens DS, Cox B, Janssen BG, Clemente DBP, Gasparrini A, Vanpoucke C, et al. Prenatal air pollution and newborns’ predisposition to accelerated biological aging. JAMA Pediatr. 2017;171(12):1160–7.  https://doi.org/10.1001/jamapediatrics.2017.3024.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–88.  https://doi.org/10.1146/annurev.nutr.27.061406.093705.CrossRefPubMedGoogle Scholar
  20. 20.
    Rakyan VK, Down TA, Balding DJ, Beck S. Epigenome-wide association studies for common human diseases. Nat Rev Genet. 2011;12(8):529–41.  https://doi.org/10.1038/nrg3000.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Jones PA, Liang G. The human epigenome. In: Michels KB, editor. Epigentic epidemiology. 1 ed.: Springer, Dordrecht; 2012. p. 5–20.Google Scholar
  22. 22.
    Herceg Z, Ghantous A, Wild CP, Sklias A, Casati L, Duthie SJ, et al. Roadmap for investigating epigenome deregulation and environmental origins of cancer. Int J Cancer. 2018;142(5):874–82.  https://doi.org/10.1002/ijc.31014.CrossRefPubMedGoogle Scholar
  23. 23.
    von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol. 2008;61(4):344–9.  https://doi.org/10.1016/j.jclinepi.2007.11.008.CrossRefGoogle Scholar
  24. 24.
    Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006–12.  https://doi.org/10.1016/j.jclinepi.2009.06.005.CrossRefPubMedGoogle Scholar
  25. 25.
    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.  https://doi.org/10.1016/j.envint.2018.05.007.CrossRefPubMedGoogle Scholar
  26. 26.
    Gruzieva O, Xu CJ, Breton CV, Annesi-Maesano I, Antó 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.  https://doi.org/10.1289/EHP36.CrossRefPubMedGoogle Scholar
  27. 27.
    Breton CV, Gao L, Yao J, Siegmund KD, Lurmann F, Gilliland F. Particulate matter, the newborn methylome, and cardio-respiratory health outcomes in childhood. Environ Epigenetics. 2016;2(2):dvw005.  https://doi.org/10.1093/eep/dvw005.CrossRefGoogle Scholar
  28. 28.
    Goodrich JM, Reddy P, Naidoo RN, Asharam K, Batterman S, Dolinoy DC. Prenatal exposures and DNA methylation in newborns: a pilot study in Durban, South Africa. Environ Sci. 2016;18(7):908–17.  https://doi.org/10.1039/c6em00074f.CrossRefGoogle Scholar
  29. 29.
    Rossnerova A, Tulupova E, Tabashidze N, Schmuczerova J, Dostal M, Rossner Jr P et al. Factors affecting the 27K DNA methylation pattern in asthmatic and healthy children from locations with various environments. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis. 2013;741–742:18–26. doi: https://doi.org/10.1016/j.mrfmmm.2013.02.003.
  30. 30.
    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.  https://doi.org/10.1371/journal.pone.0199772.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Janssen BG, Byun HM, Gyselaers W, Lefebvre W, Baccarelli AA, Nawrot TS. Placental mitochondrial methylation and exposure to airborne particulate matter in the early life environment: an ENVIRONAGE birth cohort study. Epigenetics. 2015;10(6):536–44.  https://doi.org/10.1080/15592294.2015.1048412.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Herbstman JB, Tang D, Zhu D, Qu L, Sjodin A, Li Z, et al. Prenatal exposure to polycyclic aromatic hydrocarbons, benzo[a]pyrene-DNA adducts, and genomic DNA methylation in cord blood. Environ Health Perspect. 2012;120(5):733–8.  https://doi.org/10.1289/ehp.1104056.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Li Y, Mu Z, Wang H, Liu J, Jiang F. The role of particulate matters on methylation of IFN-γ and IL-4 promoter genes in pediatric allergic rhinitis. Oncotarget. 2018;9(25):17406–19.  https://doi.org/10.18632/oncotarget.24227.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    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.  https://doi.org/10.1016/j.envint.2018.02.034.CrossRefPubMedGoogle Scholar
  35. 35.
    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 Planetary Health. 2018;2(4):e174–e83.  https://doi.org/10.1016/s2542-5196(18)30049-4.CrossRefPubMedGoogle Scholar
  36. 36.
    Prunicki M, Stell L, Dinakarpandian D, de Planell-Saguer M, Lucas RW, Hammond SK, et al. Exposure to NO2, CO, and PM2.5 is linked to regional DNA methylation differences in asthma. Clin Epigenetics. 2018;10:2.  https://doi.org/10.1186/s13148-017-0433-4.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Alvarado-Cruz I, Sanchez-Guerra M, Hernandez-Cadena L, De Vizcaya-Ruiz A, Mugica V, Pelallo-Martinez NA, et al. Increased methylation of repetitive elements and DNA repair genes is associated with higher DNA oxidation in children in an urbanized, industrial environment. Mutat Res. 2017;813:27–36.  https://doi.org/10.1016/j.mrgentox.2016.11.007.CrossRefPubMedGoogle Scholar
  38. 38.
    Cai J, Zhao Y, Liu P, Xia B, Zhu Q, Wang X et al. Exposure to particulate air pollution during early pregnancy is associated with placental DNA methylation. Sci Total Environ. 2017;607–608:1103–8. doi: https://doi.org/10.1016/j.scitotenv.2017.07.029.
  39. 39.
    Lovinsky-Desir S, Jung KH, Jezioro JR, Torrone DZ, de Planell-Saguer M, Yan B, et al. Physical activity, black carbon exposure, and DNA methylation in the FOXP3 promoter. Clin Epigenetics. 2017;9(1):65.  https://doi.org/10.1186/s13148-017-0364-0.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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.  https://doi.org/10.1289/EHP38.CrossRefPubMedGoogle Scholar
  41. 41.
    Breton CV, Yao J, Millstein J, Gao L, Siegmund KD, Mack W, et al. Prenatal air pollution exposures, DNA methyl transferase genotypes, and associations with newborn line1 and Alu methylation and childhood blood pressure and carotid intima-media thickness in the children’s health study. Environ Health Perspect. 2016;124(12):1905–12.  https://doi.org/10.1289/EHP181.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Somineni HK, Zhang X, Biagini Myers JM, Kovacic MB, Ulm A, Jurcak N, et al. Ten-eleven translocation 1 (TET1) methylation is associated with childhood asthma and traffic-related air pollution. J Allergy Clin Immunol. 2016;137(3):797–805.e5.  https://doi.org/10.1016/j.jaci.2015.10.021.CrossRefPubMedGoogle Scholar
  43. 43.
    Hew KM, Walker AI, Kohli A, Garcia M, Syed A, McDonald-Hyman C, et al. Childhood exposure to ambient polycyclic aromatic hydrocarbons is linked to epigenetic modifications and impaired systemic immunity in T cells. Clin Exp Allergy. 2015;45(1):238–48.  https://doi.org/10.1111/cea.12377.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Breton CV, Salam MT, Wang X, Byun HM, Siegmund KD, Gilliland FD. Particulate matter, DNA methylation in nitric oxide synthase, and childhood respiratory disease. Environ Health Perspect. 2012;120(9):1320–6.  https://doi.org/10.1289/ehp.1104439.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Salam MT, Byun HM, Lurmann F, Breton CV, Wang X, Eckel SP, et al. Genetic and epigenetic variations in inducible nitric oxide synthase promoter, particulate pollution, and exhaled nitric oxide levels in children, J Allergy Clin Immunol. 2012;129(1):232–9.e7.  https://doi.org/10.1016/j.jaci.2011.09.037.
  46. 46.
    Tang WY, Levin L, Talaska G, Cheung YY, Herbstman J, Tang D et al. Maternal exposure to polycyclic aromatic hydrocarbons and 5′-CpG methylation of interferon-γ in cord white blood cells. Environ Health Perspect 2012;120(8):1195–1200. doi: https://doi.org/10.1289/ehp.1103744.
  47. 47.
    Nadeau K, McDonald-Hyman C, Noth EM, Pratt B, Hammond SK, Balmes J, et al. Ambient air pollution impairs regulatory T-cell function in asthma. J Allergy Clin Immunol. 2010;126(4):845–52.e10.  https://doi.org/10.1016/j.jaci.2010.08.008.CrossRefPubMedGoogle Scholar
  48. 48.
    Perera F, Tang WY, Herbstman J, Tang D, Levin L, Miller R 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(2):e4488. doi: https://doi.org/10.1371/journal.pone.0004488.
  49. 49.
    •• Mostafavi N, Vermeulen R, Ghantous A, Hoek G, Probst-Hensch N, Herceg Z, et al. Acute changes in DNA methylation in relation to 24h personal air pollution exposure measurements: a panel study in four European countries. Environ Int. 2018;120:11–21.  https://doi.org/10.1016/j.envint.2018.07.026 Using panel design revealed an association between 24-hour personal exposure to air pollution and DNA-methylation both at single sites and regional clusters. CrossRefPubMedGoogle Scholar
  50. 50.
    Lichtenfels AJFC, Van Der Plaat DA, De Jong K, Van Diemen CC, Postma DS, Nedeljkovic I, et al. Long-term air pollution exposure, genome-wide DNA methylation and lung function in the lifelines cohort study. Environ Health Perspect. 2018;126(2):027004.  https://doi.org/10.1289/EHP2045.CrossRefGoogle Scholar
  51. 51.
    Dai L, Mehta A, Mordukhovich I, Just AC, Shen J, Hou L, et al. Differential DNA methylation and PM2.5 species in a 450K epigenome-wide association study. Epigenetics. 2017;12(2):139–48.  https://doi.org/10.1080/15592294.2016.1271853.CrossRefPubMedGoogle Scholar
  52. 52.
    Nwanaji-Enwerem JC, Dai L, Colicino E, Oulhote Y, Di Q, Kloog I, et al. Associations between long-term exposure to PM2.5 component species and blood DNA methylation age in the elderly: the VA normative aging study. Environ Int. 2017;102:57–65.  https://doi.org/10.1016/j.envint.2016.12.024.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    •• Panni T, Mehta AJ, Schwartz JD, Baccarelli AA, Just AC, Wolf K, et al. Genome-wide analysis of DNA methylation and fine particulate matter air pollution in three study populations: KORA F3, KORA F4, and the Normative Aging Study. Environ Health Perspect. 2016;124(7):983–90.  https://doi.org/10.1289/ehp.1509966 Combining evidence from three independent adult cohorts suggests novel plausible systemic pathways linking ambient PM exposure to adverse health effect through variations in DNA methylation. CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Plusquin M, Guida F, Polidoro S, Vermeulen R, Raaschou-Nielsen O, Campanella G, et al. DNA methylation and exposure to ambient air pollution in two prospective cohorts. Environ Int. 2017;108:127–36.  https://doi.org/10.1016/j.envint.2017.08.006.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Chi GC, Liu Y, MacDonald JW, Barr RG, Donohue KM, Hensley MD, et al. Long-term outdoor air pollution and DNA methylation in circulating monocytes: results from the multi-ethnic study of atherosclerosis (MESA). Environ Health. 2016;15(1):119.  https://doi.org/10.1186/s12940-016-0202-4.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Nwanaji-Enwerem JC, Colicino E, Trevisi L, Kloog I, Just AC, Shen J et al. Long-term ambient particle exposures and blood DNA methylation age: findings from the VA normative aging study. Environ Epigenetics. 2016;2(2). doi: https://doi.org/10.1093/eep/dvw006.
  57. 57.
    Ward-Caviness CK, Nwanaji-Enwerem JC, Wolf K, Wahl S, Colicino E, Trevisi L, et al. Long-term exposure to air pollution is associated with biological aging. Oncotarget. 2016;7(46):74510–25.  https://doi.org/10.18632/oncotarget.12903.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Carmona JJ, Sofer T, Hutchinson J, Cantone L, Coull B, Maity A, et al. Short-term airborne particulate matter exposure alters the epigenetic landscape of human genes associated with the mitogen-activated protein kinase network: a cross-sectional study. Environ Health. 2014;13(1):94.  https://doi.org/10.1186/1476-069X-13-94.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    De Nys S, Duca RC, Nawrot T, Hoet P, Van Meerbeek B, Van Landuyt KL, et al. Temporal variability of global DNA methylation and hydroxymethylation in buccal cells of healthy adults: association with air pollution. Environ Int. 2018;111:301–8.  https://doi.org/10.1016/j.envint.2017.11.002.CrossRefPubMedGoogle Scholar
  60. 60.
    Liu J, Xie K, Chen W, Zhu M, Shen W, Yuan J, et al. Genetic variants, PM2.5 exposure level and global DNA methylation level: a multi-center population-based study in Chinese. Toxicol Lett. 2017;269:77–82.  https://doi.org/10.1016/j.toxlet.2017.02.003.CrossRefPubMedGoogle Scholar
  61. 61.
    Sanchez-Guerra M, Zheng Y, Osorio-Yanez C, Zhong J, Chervona Y, Wang S, et al. Effects of particulate matter exposure on blood 5-hydroxymethylation: results from the Beijing truck driver air pollution study. Epigenetics. 2015;10(7):633–42.  https://doi.org/10.1080/15592294.2015.1050174.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    De Prins S, Koppen G, Jacobs G, Dons E, Van de Mieroop E, Nelen V, et al. Influence of ambient air pollution on global DNA methylation in healthy adults: a seasonal follow-up. Environ Int. 2013;59:418–24.  https://doi.org/10.1016/j.envint.2013.07.007.CrossRefPubMedGoogle Scholar
  63. 63.
    Wang C, Chen R, Shi M, Cai J, Shi J, Yang C, et al. Possible mediation by methylation in acute inflammation following personal exposure to fine particulate air pollution. Am J Epidemiol. 2018;187(3):484–93.  https://doi.org/10.1093/aje/kwx277.CrossRefPubMedGoogle Scholar
  64. 64.
    Wang C, Chen R, Cai J, Shi J, Yang C, Tse LA, et al. Personal exposure to fine particulate matter and blood pressure: a role of angiotensin converting enzyme and its DNA methylation. Environ Int. 2016;94:661–6.  https://doi.org/10.1016/j.envint.2016.07.001.CrossRefPubMedGoogle Scholar
  65. 65.
    Sofer T, Maity A, Coull B, Baccarelli A, Schwartz J, Lin X. Multivariate gene selection and testing in studying the exposure effects on a gene set. Stat Biosci. 2012;4(2):319–38.  https://doi.org/10.1007/s12561-012-9072-7.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Peng C, Bind MAC, Colicino E, Kloog I, Byun HM, Cantone L, et al. Particulate air pollution and fasting blood glucose in nondiabetic individuals: associations and epigenetic mediation in the normative aging study, 2000-2011. Environ Health Perspect. 2016;124(11):1715–21.  https://doi.org/10.1289/EHP183.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Ouyang B, Baxter CS, Lam HM, Yeramaneni S, Levin L, Haynes E, et al. Hypomethylation of dual specificity phosphatase 22 promoter correlates with duration of service in firefighters and is inducible by low-dose benzo[a]pyrene. J Occup Environ Med. 2012;54(7):774–80.  https://doi.org/10.1097/JOM.0b013e31825296bc.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Madrigano J, Baccarelli A, Mittleman MA, Sparrow D, Spiro A, Vokonas PS, et al. Air pollution and DNA methylation: interaction by psychological factors in the VA normative aging study. Am J Epidemiol. 2012;176(3):224–32.  https://doi.org/10.1093/aje/kwr523.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Madrigano J, Baccarelli A, Mittleman MA, Wright RO, Sparrow D, Vokonas PS, et al. Prolonged exposure to particulate pollution, genes associated with glutathione pathways, and DNA methylation in a cohort of older men. Environ Health Perspect. 2011;119(7):977–82.  https://doi.org/10.1289/ehp.1002773.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Liu Y, Lan Q, Shen M, Jin J, Mumford J, Ren D, et al. Aberrant gene promoter methylation in sputum from individuals exposed to smoky coal emissions. Anticancer Res. 2008;28(4 B):2061–6.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Lepeule J, Bind MA, Baccarelli AA, Koutrakis P, Tarantini L, Litonjua A, et al. Epigenetic influences on associations between air pollutants and lung function in elderly men: the normative aging study. Environ Health Perspect. 2014;122(6):566–72.  https://doi.org/10.1289/ehp.1206458.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Hou L, Zhang X, Zheng Y, Wang S, Dou C, Guo L, et al. Altered methylation in tandem repeat element and elemental component levels in inhalable air particles. Environ Mol Mutagen. 2014;55(3):256–65.  https://doi.org/10.1002/em.21829.CrossRefPubMedGoogle Scholar
  73. 73.
    Guo L, Byun HM, Zhong J, Motta V, Barupal J, Zheng Y, et al. Effects of short-term exposure to inhalable particulate matter on DNA methylation of tandem repeats. Environ Mol Mutagen. 2014;55(4):322–35.  https://doi.org/10.1002/em.21838.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Chen R, Qiao L, Li H, Zhao Y, Zhang Y, Xu W, et al. Fine particulate matter constituents, nitric oxide synthase DNA methylation and exhaled nitric oxide. Environ Sci Technol. 2015;49(19):11859–65.  https://doi.org/10.1021/acs.est.5b02527.CrossRefPubMedGoogle Scholar
  75. 75.
    Cantone L, Iodice S, Tarantini L, Albetti B, Restelli I, Vigna L, et al. Particulate matter exposure is associated with inflammatory gene methylation in obese subjects. Environ Res. 2017;152:478–84.  https://doi.org/10.1016/j.envres.2016.11.002.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Callahan CL, Bonner MR, Nie J, Han D, Wang Y, Tao MH, et al. Lifetime exposure to ambient air pollution and methylation of tumor suppressor genes in breast tumors. Environ Res. 2018;161:418–24.  https://doi.org/10.1016/j.envres.2017.11.040.CrossRefPubMedGoogle Scholar
  77. 77.
    Bind MA, Coull BA, Peters A, Baccarelli AA, Tarantini L, Cantone L, et al. Beyond the mean: quantile regression to explore the association of air pollution with gene-specific methylation in the Normative Aging Study. Environ Health Perspect. 2015;123(8):759–65.  https://doi.org/10.1289/ehp.1307824.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Bind MA, Lepeule J, Zanobetti A, Gasparrini A, Baccarelli A, Coull BA, et al. Air pollution and gene-specific methylation in the Normative Aging Study: association, effect modification, and mediation analysis. Epigenetics. 2014;9(3):448–58.  https://doi.org/10.4161/epi.27584.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, et al. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med. 2009;179(7):572–8.  https://doi.org/10.1164/rccm.200807-1097OC.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Zhong J, Karlsson O, Wang G, Li J, Guo Y, Lin X, et al. B vitamins attenuate the epigenetic effects of ambient fine particles in a pilot human intervention trial. Proc Natl Acad Sci U S A. 2017;114(13):3503–8.  https://doi.org/10.1073/pnas.1618545114.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Clifford RL, Jones MJ, MacIsaac JL, McEwen LM, Goodman SJ, Mostafavi S, et al. Inhalation of diesel exhaust and allergen alters human bronchial epithelium DNA methylation. J Allergy Clin Immunol. 2017;139(1):112–21.  https://doi.org/10.1016/j.jaci.2016.03.046.CrossRefPubMedGoogle Scholar
  82. 82.
    Jiang R, Jones MJ, Sava F, Kobor MS, Carlsten C. Short-term diesel exhaust inhalation in a controlled human crossover study is associated with changes in DNA methylation of circulating mononuclear cells in asthmatics. Particle Fibre Toxicol. 2014;11(1):71.  https://doi.org/10.1186/s12989-014-0071-3.CrossRefGoogle Scholar
  83. 83.
    Tobaldini E, Bollati V, Prado M, Fiorelli EM, Pecis M, Bissolotti G, et al. Acute particulate matter affects cardiovascular autonomic modulation and IFN-Γ methylation in healthy volunteers. Environ Res. 2018;161:97–103.  https://doi.org/10.1016/j.envres.2017.10.036.CrossRefPubMedGoogle Scholar
  84. 84.
    Chen R, Meng X, Zhao A, Wang C, Yang C, Li H, et al. DNA hypomethylation and its mediation in the effects of fine particulate air pollution on cardiovascular biomarkers: a randomized crossover trial. Environ Int. 2016;94:614–9.  https://doi.org/10.1016/j.envint.2016.06.026.CrossRefPubMedGoogle Scholar
  85. 85.
    Bellavia A, Urch B, Speck M, Brook RD, Scott JA, Albetti B, et al. DNA hypomethylation, ambient particulate matter, and increased blood pressure: findings from controlled human exposure experiments. J Am Heart Assoc. 2013;2(3):e000212.  https://doi.org/10.1161/JAHA.113.000212.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    •• Krauskopf J, Caiment F, van Veldhoven K, Chadeau-Hyam M, Sinharay R, Chung KF, et al. The human circulating miRNome reflects multiple organ disease risks in association with short-term exposure to traffic-related air pollution. Environ Int. 2018;113:26–34.  https://doi.org/10.1016/j.envint.2018.01.014 Proposes cmiRNA signature comprised of organ-enriched miRNAs as a highly specific candidate for biomarker-based health risk assessment allowing the early detection and prevention of TRAP-induced health outcomes. CrossRefPubMedGoogle Scholar
  87. 87.
    Liu PF, Yan P, Zhao DH, Shi WF, Meng S, Liu Y, et al. The effect of environmental factors on the differential expression of miRNAs in patients with chronic obstructive pulmonary disease: a pilot clinical study. Int J Chronic Obstructive Pulmonary Dis. 2018;13:741–51.  https://doi.org/10.2147/copd.S156865.CrossRefGoogle Scholar
  88. 88.
    Pergoli L, Cantone L, Favero C, Angelici L, Iodice S, Pinatel E, et al. Extracellular vesicle-packaged miRNA release after short-term exposure to particulate matter is associated with increased coagulation. Particle and fibre toxicology. 2017;14(1):32.  https://doi.org/10.1186/s12989-017-0214-4.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Hou L, Barupal J, Zhang W, Zheng Y, Liu L, Zhang X, et al. Particulate air pollution exposure and expression of viral and human microRNAs in blood: the Beijing Truck Driver Air Pollution Study. Environ Health Perspect. 2016;124(3):344–50.  https://doi.org/10.1289/ehp.1408519.CrossRefPubMedGoogle Scholar
  90. 90.
    Motta V, Favero C, Dioni L, Iodice S, Battaglia C, Angelici L, et al. MicroRNAs are associated with blood-pressure effects of exposure to particulate matter: results from a mediated moderation analysis. Environ Res. 2016;146:274–81.  https://doi.org/10.1016/j.envres.2016.01.010.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Rider CF, Yamamoto M, Gunther OP, Hirota JA, Singh A, Tebbutt SJ, et al. Controlled diesel exhaust and allergen coexposure modulates microRNA and gene expression in humans: effects on inflammatory lung markers. J Allergy Clin Immunol. 2016;138(6):1690–700.  https://doi.org/10.1016/j.jaci.2016.02.038.CrossRefPubMedGoogle Scholar
  92. 92.
    Rodosthenous RS, Coull BA, Lu Q, Vokonas PS, Schwartz JD, Baccarelli AA. Ambient particulate matter and microRNAs in extracellular vesicles: a pilot study of older individuals. Particle Fibre Toxicol. 2016;13:13.  https://doi.org/10.1186/s12989-016-0121-0.CrossRefGoogle Scholar
  93. 93.
    Fry RC, Rager JE, Bauer R, Sebastian E, Peden DB, Jaspers I, et al. Air toxics and epigenetic effects: ozone altered microRNAs in the sputum of human subjects. Am J Physiol Lung Cell Mol Physiol. 2014;306(12):L1129–L37.  https://doi.org/10.1152/ajplung.00348.2013.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Yamamoto M, Singh A, Sava F, Pui M, Tebbutt SJ, Carlsten C. MicroRNA expression in response to controlled exposure to diesel exhaust: attenuation by the antioxidant N-acetylcysteine in a randomized crossover study. Environ Health Perspect. 2013;121(6):670–5.  https://doi.org/10.1289/ehp.1205963.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Chen R, Li H, Cai J, Wang C, Lin Z, Liu C, et al. Fine particulate air pollution and the expression of microRNAs and circulating cytokines relevant to inflammation, coagulation, and vasoconstriction. Environ Health Perspect. 2018;126(1):017007.  https://doi.org/10.1289/EHP1447.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Tsamou M, Vrijens K, Madhloum N, Lefebvre W, Vanpoucke C, Nawrot TS. Air pollution-induced placental epigenetic alterations in early life: a candidate miRNA approach. Epigenetics. 2018:1–12.  https://doi.org/10.1080/15592294.2016.1155012.
  97. 97.
    Louwies T, Vuegen C, Panis LI, Cox B, Vrijens K, Nawrot TS, et al. miRNA expression profiles and retinal blood vessel calibers are associated with short-term particulate matter air pollution exposure. Environ Res. 2016;147:24–31.  https://doi.org/10.1016/j.envres.2016.01.027.CrossRefPubMedGoogle Scholar
  98. 98.
    Vriens A, Nawrot TS, Saenen ND, Provost EB, Kicinski M, Lefebvre W, et al. Recent exposure to ultrafine particles in school children alters miR-222 expression in the extracellular fraction of saliva. Environ Health. 2016;15(1):80.  https://doi.org/10.1186/s12940-016-0162-8.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Fossati S, Baccarelli A, Zanobetti A, Hoxha M, Vokonas PS, Wright RO, et al. Ambient particulate air pollution and microRNAs in elderly men. Epidemiology (Cambridge, Mass). 2014;25(1):68–78.  https://doi.org/10.1097/EDE.0000000000000026.CrossRefGoogle Scholar
  100. 100.
    Wei MM, Zhou YC, Wen ZS, Zhou B, Huang YC, Wang GZ, et al. Long non-coding RNA stabilizes the Y-box-binding protein 1 and regulates the epidermal growth factor receptor to promote lung carcinogenesis. Oncotarget. 2016;7(37):59556–71.  https://doi.org/10.18632/oncotarget.10006.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Liu C, Xu J, Chen Y, Guo X, Zheng Y, Wang Q, et al. Characterization of genome-wide H3K27ac profiles reveals a distinct PM2.5-associated histone modification signature. Environ Health. 2015;14(1):65.  https://doi.org/10.1186/s12940-015-0052-5.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Zheng Y, Sanchez-Guerra M, Zhang Z, Joyce BT, Zhong J, Kresovich JK, et al. Traffic-derived particulate matter exposure and histone H3 modification: a repeated measures study. Environ Res. 2017;153:112–9.  https://doi.org/10.1016/j.envres.2016.11.015.CrossRefPubMedGoogle Scholar
  103. 103.
    Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013;14(10):R115.  https://doi.org/10.1186/gb-2013-14-10-r115.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013;49(2):359–67.  https://doi.org/10.1016/j.molcel.2012.10.016.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Prins GS, Calderon-Gierszal EL, Hu WY. Stem cells as hormone targets that lead to increased cancer susceptibility. Endocrinology. 2015;156(10):3451–7.  https://doi.org/10.1210/en.2015-1357.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Vineis P, Chatziioannou A, Cunliffe VT, Flanagan JM, Hanson M, Kirsch-Volders M, et al. Epigenetic memory in response to environmental stressors. FASEB Journal. 2017;31(6):2241–51.  https://doi.org/10.1096/fj.201601059RR.CrossRefPubMedGoogle Scholar
  107. 107.
    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.  https://doi.org/10.1016/j.ajhg.2016.02.019.CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Yang AS, Estecio MR, Doshi K, Kondo Y, Tajara EH, Issa JP. A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. Nucleic Acids Res. 2004;32(3):e38.  https://doi.org/10.1093/nar/gnh032.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Price EM, Cotton AM, Penaherrera MS, McFadden DE, Kobor MS, Robinson W. Different measures of “genome-wide” DNA methylation exhibit unique properties in placental and somatic tissues. Epigenetics. 2012;7(6):652–63.  https://doi.org/10.4161/epi.20221.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.  https://doi.org/10.1016/j.cell.2011.02.013.CrossRefGoogle Scholar
  111. 111.
    Felix JF, Joubert BR, Baccarelli AA, Sharp GC, Almqvist C, Annesi-Maesano I, et al. Cohort profile: pregnancy and childhood epigenetics (PACE) consortium. Int J Epidemiol. 2018;47(1):22–3u.  https://doi.org/10.1093/ije/dyx190.CrossRefPubMedGoogle Scholar
  112. 112.
    Vineis P, Chadeau-Hyam M, Gmuender H, Gulliver J, Herceg Z, Kleinjans J, et al. The exposome in practice: design of the EXPOsOMICS project. Int J Hyg Environ Health. 2017;220(2 Pt A):142–51.  https://doi.org/10.1016/j.ijheh.2016.08.001.CrossRefPubMedPubMedCentralGoogle Scholar
  113. 113.
    Yang SJ, Yang SY, Wang DD, Chen X, Shen HY, Zhang XH, et al. The miR-30 family: versatile players in breast cancer. Tumour Biol. 2017;39(3):1010428317692204.  https://doi.org/10.1177/1010428317692204.CrossRefPubMedGoogle Scholar
  114. 114.
    Qu K, Lin T, Pang Q, Liu T, Wang Z, Tai M, et al. Extracellular miRNA-21 as a novel biomarker in glioma: evidence from meta-analysis, clinical validation and experimental investigations. Oncotarget. 2016;7(23):33994–4010.  https://doi.org/10.18632/oncotarget.9188.CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Sweeney CL, Teng R, Wang H, Merling RK, Lee J, Choi U, et al. Molecular analysis of neutrophil differentiation from human induced pluripotent stem cells delineates the kinetics of key regulators of hematopoiesis. Stem Cells. 2016;34(6):1513–26.  https://doi.org/10.1002/stem.2332.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Paterson MR, Kriegel AJ. MiR-146a/b: a family with shared seeds and different roots. Physiol Genomics. 2017;49(4):243–52.  https://doi.org/10.1152/physiolgenomics.00133.2016.CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Ding S, Huang H, Xu Y, Zhu H, Zhong C. MiR-222 in cardiovascular diseases: physiology and pathology. Biomed Res Int. 2017;2017:4962426.  https://doi.org/10.1155/2017/4962426.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Testa U, Pelosi E, Castelli G, Labbaye C. miR-146 and miR-155: two key modulators of immune response and tumor development. Noncoding RNA. 2017;3(3). doi: https://doi.org/10.3390/ncrna3030022.
  119. 119.
    Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, et al. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature. 2008;456(7224):980–4.  https://doi.org/10.1038/nature07511.CrossRefPubMedGoogle Scholar
  120. 120.
    Huarte M. The emerging role of lncRNAs in cancer. Nat Med. 2015;21(11):1253–61.  https://doi.org/10.1038/nm.3981.CrossRefPubMedGoogle Scholar
  121. 121.
    Bartonicek N, Maag JL, Dinger ME. Long noncoding RNAs in cancer: mechanisms of action and technological advancements. Mol Cancer. 2016;15(1):43.  https://doi.org/10.1186/s12943-016-0530-6.CrossRefPubMedPubMedCentralGoogle Scholar
  122. 122.
    Jantsch MF, Quattrone A, O'Connell M, Helm M, Frye M, Macias-Gonzales M, et al. Positioning Europe for the EPITRANSCRIPTOMICS challenge. RNA Biol. 2018:1–3.  https://doi.org/10.1080/15476286.2018.1460996.
  123. 123.
    Baccarelli A, Bollati V. Epigenetics and environmental chemicals. Curr Opin Pediatr. 2009;21(2):243–51.  https://doi.org/10.1097/MOP.0b013e32832925cc.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Chervona Y, Costa M. The control of histone methylation and gene expression by oxidative stress, hypoxia, and metals. Free Radic Biol Med. 2012;53(5):1041–7.  https://doi.org/10.1016/j.freeradbiomed.2012.07.020.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Bayarsaihan D. Epigenetic mechanisms in inflammation. J Dent Res. 2011;90(1):9–17.  https://doi.org/10.1177/0022034510378683.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Byun HM, Colicino E, Trevisi L, Fan T, Christiani DC, Baccarelli AA. Effects of air pollution and blood mitochondrial DNA methylation on markers of heart rate variability. J Am Heart Assoc. 2016;5(4).  https://doi.org/10.1161/JAHA.116.003218.
  127. 127.
    McCreanor J, Cullinan P, Nieuwenhuijsen MJ, Stewart-Evans J, Malliarou E, Jarup L, et al. Respiratory effects of exposure to diesel traffic in persons with asthma. N Engl J Med. 2007;357(23):2348–58.  https://doi.org/10.1056/NEJMoa071535.CrossRefPubMedGoogle Scholar
  128. 128.
    Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86.  https://doi.org/10.1186/1471-2105-13-86.CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Bakulski KM, Feinberg JI, Andrews SV, Yang J, Brown S, McKenney SL, et al. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenetics. 2016;11(5):354–62.  https://doi.org/10.1080/15592294.2016.1161875.CrossRefPubMedPubMedCentralGoogle Scholar
  130. 130.
    Houseman EA, Kile ML, Christiani DC, Ince TA, Kelsey KT, Marsit CJ. Reference-free deconvolution of DNA methylation data and mediation by cell composition effects. BMC Bioinformatics. 2016;17:259.  https://doi.org/10.1186/s12859-016-1140-4.CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Bauer M, Linsel G, Fink B, Offenberg K, Hahn AM, Sack U, et al. A varying T cell subtype explains apparent tobacco smoking induced single CpG hypomethylation in whole blood. Clin Epigenetics. 2015;7(1):81.  https://doi.org/10.1186/s13148-015-0113-1.CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Green BB, Karagas MR, Punshon T, Jackson BP, Robbins DJ, Houseman EA, et al. Epigenome-wide assessment of DNA methylation in the placenta and arsenic exposure in the New Hampshire Birth Cohort Study (USA). Environ Health Perspect. 2016;124(8):1253–60.  https://doi.org/10.1289/ehp.1510437.CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Langie SA, Szarc Vel Szic K, Declerck K, Traen S, Koppen G, Van Camp G, et al. Whole-genome saliva and blood DNA methylation profiling in individuals with a respiratory allergy. PLoS One. 2016;11(3):e0151109.  https://doi.org/10.1371/journal.pone.0151109.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Rossella Alfano
    • 1
  • Zdenko Herceg
    • 2
  • Tim S. Nawrot
    • 1
    • 3
  • Marc Chadeau-Hyam
    • 4
  • Akram Ghantous
    • 2
    Email author
  • Michelle Plusquin
    • 1
    Email author
  1. 1.Centre for Environmental SciencesHasselt UniversityHasseltBelgium
  2. 2.Epigenetics GroupInternational Agency for Research on Cancer (IARC)LyonFrance
  3. 3.Environment & Health UnitLeuven UniversityLeuvenBelgium
  4. 4.Department of Epidemiology and Biostatistics, The School of Public HealthImperial College LondonLondonUK

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