Human Genetics

, Volume 132, Issue 9, pp 1027–1037 | Cite as

Epigenomic association analysis identifies smoking-related DNA methylation sites in African Americans

  • Yan V. SunEmail author
  • Alicia K. Smith
  • Karen N. Conneely
  • Qiuzhi Chang
  • Weiyan Li
  • Alicia Lazarus
  • Jennifer A. Smith
  • Lynn M. Almli
  • Elisabeth B. Binder
  • Torsten Klengel
  • Dorthie Cross
  • Stephen T. Turner
  • Kerry J. Ressler
  • Sharon L. R. Kardia
Original Investigation


Cigarette smoking is an environmental risk factor for many chronic diseases, and disease risk can often be managed by smoking control. Smoking can induce cellular and molecular changes, including epigenetic modification, but the short- and long-term epigenetic modifications caused by cigarette smoking at the gene level have not been well understood. Recent studies have identified smoking-related DNA methylation (DNAm) sites in Caucasians. To determine whether the same DNAm sites associate with smoking in African Americans, and to identify novel smoking-related DNAm sites, we conducted a methylome-wide association study of cigarette smoking using a discovery sample of 972 African Americans, and a replication sample of 239 African Americans with two array-based methods. Among 15 DNAm sites significantly associated with smoking after correction for multiple testing in our discovery sample, 5 DNAm sites are replicated in an independent cohort, and 14 sites in the replication sample have effects in the same direction as in the discovery sample. The top two smoking-related DNAm sites in F2RL3 (factor II receptor-like 3) and GPR15 (G-protein-coupled receptor 15) observed in African Americans are consistent with previous findings in Caucasians. The associations between the replicated DNAm sites and smoking remain significant after adjusting for genetic background. Despite the distinct genetic background between African Americans and Caucasians, the DNAm from the two ethnic groups shares common associations with cigarette smoking, which suggests a common molecular mechanism of epigenetic modification influenced by environmental exposure.


Cigarette Smoking African American Current Smoking Status Replication Sample Discovery Sample 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors gratefully acknowledge the participants of the study. Genetic Epidemiology Network of Arteriopathy (GENOA) study is supported by the National Institutes of Health, Grant numbers HL100185 and HL100245 from National Heart, Lung, Blood Institute. Grady Trauma Project (GTP) is supported, in part, by NIH/NIDA T32 DA15040, and support for AKS was provided by MH085806. The authors thank Richard Barfield and Varun Kilaru for technical assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

439_2013_1311_MOESM1_ESM.xlsx (21 kb)
Supplementary Table 1: Significant smoking-related DNAm sites with FDR q value less than 0.05 (XLSX 21 kb)
439_2013_1311_MOESM2_ESM.xlsx (24 kb)
Supplementary Table 2: Replication of smoking-related DNAm on the level of genes using human methylation 450 k array. (XLSX 23 kb)


  1. Arnett DK, Meyers KJ, Devereux RB, Tiwari HK, Gu CC, Vaughan LK, Perry RT, Patki A, Claas SA, Sun YV, Broeckel U, Kardia SL (2011) Genetic variation in NCAM1 contributes to left ventricular wall thickness in hypertensive families. Circ Res 108:279–283PubMedCrossRefGoogle Scholar
  2. Axume J, Smith SS, Pogribny IP, Moriarty DJ, Caudill MA (2007) Global leukocyte DNA methylation is similar in African American and Caucasian women under conditions of controlled folate intake. Epigenetics 2:66–68PubMedCrossRefGoogle Scholar
  3. Barbalic M, Reiner AP, Wu C, Hixson JE, Franceschini N, Eaton CB, Heiss G, Couper D, Mosley T, Boerwinkle E (2011) Genome-wide association analysis of incident coronary heart disease (CHD) in African Americans: a short report. PLoS Genet 7:e1002199PubMedCrossRefGoogle Scholar
  4. Barfield RT, Kilaru V, Smith AK, Conneely KN (2012) CpGassoc: an R function for analysis of DNA methylation microarray data. Bioinformatics 28:1280–1281PubMedCrossRefGoogle Scholar
  5. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, Degner JF, Gilad Y, Pritchard JK (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 12:R10PubMedCrossRefGoogle Scholar
  6. Bouloukaki I, Tsiligianni IG, Tsoumakidou M, Mitrouska I, Prokopakis EP, Mavroudi I, Siafakas NM, Tzanakis N (2011) Sputum and nasal lavage lung-specific biomarkers before and after smoking cessation. BMC Pulm Med 11:35PubMedCrossRefGoogle Scholar
  7. Braber S, Henricks PA, Nijkamp FP, Kraneveld AD, Folkerts G (2010) Inflammatory changes in the airways of mice caused by cigarette smoke exposure are only partially reversed after smoking cessation. Respir Res 11:99PubMedCrossRefGoogle Scholar
  8. Breitling LP, Yang R, Korn B, Burwinkel B, Brenner H (2011) Tobacco-smoking-related differential DNA methylation: 27 K discovery and replication. Am J Hum Genet 88:450–457PubMedCrossRefGoogle Scholar
  9. Breitling LP, Salzmann K, Rothenbacher D, Burwinkel B, Brenner H (2012) Smoking, F2RL3 methylation, and prognosis in stable coronary heart disease. Eur Heart J 33:2841–2848PubMedCrossRefGoogle Scholar
  10. Chen YA, Choufani S, Ferreira JC, Grafodatskaya D, Butcher DT, Weksberg R (2011) Sequence overlap between autosomal and sex-linked probes on the Illumina HumanMethylation27 microarray. Genomics 97:214–222PubMedCrossRefGoogle Scholar
  11. Conen D, Everett BM, Kurth T, Creager MA, Buring JE, Ridker PM, Pradhan AD (2011) Smoking, smoking cessation, [corrected] and risk for symptomatic peripheral artery disease in women: a cohort study. Ann Intern Med 154:719–726PubMedCrossRefGoogle Scholar
  12. Daniels PR, Kardia SL, Hanis CL, Brown CA, Hutchinson R, Boerwinkle E, Turner ST (2004) Familial aggregation of hypertension treatment and control in the Genetic Epidemiology Network of Arteriopathy (GENOA) study. Am J Med 116:676–681PubMedCrossRefGoogle Scholar
  13. Ehret GB, Munroe PB, Rice KM, Bochud M, Johnson AD, Chasman DI, Smith AV, Tobin MD, Verwoert GC, Hwang SJ, Pihur V, Vollenweider P, O’Reilly PF, Amin N, Bragg-Gresham JL, Teumer A, Glazer NL, Launer L, Zhao JH, Aulchenko Y, Heath S, Sober S, Parsa A, Luan J, Arora P, Dehghan A, Zhang F, Lucas G, Hicks AA, Jackson AU, Peden JF, Tanaka T, Wild SH, Rudan I, Igl W, Milaneschi Y, Parker AN, Fava C, Chambers JC, Fox ER, Kumari M, Go MJ, van der Harst P, Kao WH, Sjogren M, Vinay DG, Alexander M, Tabara Y, Shaw-Hawkins S, Whincup PH, Liu Y, Shi G, Kuusisto J, Tayo B, Seielstad M, Sim X, Nguyen KD, Lehtimaki T, Matullo G, Wu Y, Gaunt TR, Onland-Moret NC, Cooper MN, Platou CG, Org E, Hardy R, Dahgam S, Palmen J, Vitart V, Braund PS, Kuznetsova T, Uiterwaal CS, Adeyemo A, Palmas W, Campbell H, Ludwig B, Tomaszewski M, Tzoulaki I, Palmer ND, Aspelund T, Garcia M, Chang YP, O’Connell JR, Steinle NI, Grobbee DE, Arking DE, Kardia SL, Morrison AC, Hernandez D, Najjar S, McArdle WL, Hadley D, Brown MJ, Connell JM, Hingorani AD, Day IN, Lawlor DA, Beilby JP, Lawrence RW, Clarke R et al (2011) Genetic variants in novel pathways influence blood pressure and cardiovascular disease risk. Nature 478:103–109PubMedCrossRefGoogle Scholar
  14. Feinberg AP (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447:433–440PubMedCrossRefGoogle Scholar
  15. Feinberg AP (2008) Epigenetics at the epicenter of modern medicine. JAMA 299:1345–1350PubMedCrossRefGoogle Scholar
  16. Feinberg AP, Tycko B (2004) The history of cancer epigenetics. Nat Rev Cancer 4:143–153PubMedCrossRefGoogle Scholar
  17. Ferreira MA, Matheson MC, Duffy DL, Marks GB, Hui J, Le Souef P, Danoy P, Baltic S, Nyholt DR, Jenkins M, Hayden C, Willemsen G, Ang W, Kuokkanen M, Beilby J, Cheah F, de Geus EJ, Ramasamy A, Vedantam S, Salomaa V, Madden PA, Heath AC, Hopper JL, Visscher PM, Musk B, Leeder SR, Jarvelin MR, Pennell C, Boomsma DI, Hirschhorn JN, Walters H, Martin NG, James A, Jones G, Abramson MJ, Robertson CF, Dharmage SC, Brown MA, Montgomery GW, Thompson PJ, Australian Asthma Genetics C (2011) Identification of IL6R and chromosome 11q13.5 as risk loci for asthma. Lancet 378:1006–1014PubMedCrossRefGoogle Scholar
  18. Figueiredo JC, Grau MV, Wallace K, Levine AJ, Shen L, Hamdan R, Chen X, Bresalier RS, McKeown-Eyssen G, Haile RW, Baron JA, Issa JP (2009) Global DNA hypomethylation (LINE-1) in the normal colon and lifestyle characteristics and dietary and genetic factors. Cancer Epidemiol Biomarkers Prev 18:1041–1049PubMedCrossRefGoogle Scholar
  19. Flom JD, Ferris JS, Liao Y, Tehranifar P, Richards CB, Cho YH, Gonzalez K, Santella RM, Terry MB (2011) Prenatal smoke exposure and genomic DNA methylation in a multiethnic birth cohort. Cancer Epidemiol Biomarkers Prev 20:2518–2523PubMedCrossRefGoogle Scholar
  20. Furniss CS, Marsit CJ, Houseman EA, Eddy K, Kelsey KT (2008) Line region hypomethylation is associated with lifestyle and differs by human papillomavirus status in head and neck squamous cell carcinomas. Cancer Epidemiol Biomarkers Prev 17:966–971PubMedCrossRefGoogle Scholar
  21. Gillespie CF, Bradley B, Mercer K, Smith AK, Conneely K, Gapen M, Weiss T, Schwartz AC, Cubells JF, Ressler KJ (2009) Trauma exposure and stress-related disorders in inner city primary care patients. Gen Hosp Psychiatry 31:505–514PubMedCrossRefGoogle Scholar
  22. Giovino GA (2002) Epidemiology of tobacco use in the United States. Oncogene 21:7326–7340PubMedCrossRefGoogle Scholar
  23. Hartigan JA, Hartigan PM (1985) The dip test of unimodality. Ann Stat 13:70–84CrossRefGoogle Scholar
  24. Heiber M, Marchese A, Nguyen T, Heng HH, George SR, O’Dowd BF (1996) A novel human gene encoding a G-protein-coupled receptor (GPR15) is located on chromosome 3. Genomics 32:462–465PubMedCrossRefGoogle Scholar
  25. 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 13:86PubMedCrossRefGoogle Scholar
  26. 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 16:108–114PubMedCrossRefGoogle Scholar
  27. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3:415–428PubMedCrossRefGoogle Scholar
  28. Joubert BR, Haberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK, Huang Z, Hoyo C, Midttun O, Cupul-Uicab LA, Ueland PM, Wu MC, Nystad W, Bell DA, Peddada SD, London SJ (2012) 450 K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect 120:1425–1431PubMedGoogle Scholar
  29. Kawachi I, Colditz GA, Stampfer MJ, Willett WC, Manson JE, Rosner B, Speizer FE, Hennekens CH (1993) Smoking cessation and decreased risk of stroke in women. JAMA 269:232–236PubMedCrossRefGoogle Scholar
  30. Kellogg SH, McHugh PF, Bell K, Schluger JH, Schluger RP, LaForge KS, Ho A, Kreek MJ (2003) The Kreek–McHugh–Schluger–Kellogg scale: a new, rapid method for quantifying substance abuse and its possible applications. Drug Alcohol Depend 69:137–150PubMedCrossRefGoogle Scholar
  31. Kilaru V, Barfield RT, Schroeder JW, Smith AK, Conneely KN (2012) MethLAB: a graphical user interface package for the analysis of array-based DNA methylation data. Epigenetics 7:225–229PubMedCrossRefGoogle Scholar
  32. 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 118:370–374PubMedCrossRefGoogle Scholar
  33. Kocaman SA, Sahinarslan A, Kunak T, Balcioglu S, Cetin M, Cemri M, Timurkaynak T, Boyaci B, Cengel A (2011) The particular interactions of the traditional cardiovascular risk factors with different circulating specific leukocyte subtype counts in blood: an observational study. Anadolu Kardiyol Derg 11:573–581PubMedGoogle Scholar
  34. Koestler DC, Marsit CJ, Christensen BC, Accomando W, Langevin SM, Houseman EA, Nelson HH, Karagas MR, Wiencke JK, Kelsey KT (2012) Peripheral blood immune cell methylation profiles are associated with nonhematopoietic cancers. Cancer Epidemiol Biomarkers Prev 21:1293–1302PubMedCrossRefGoogle Scholar
  35. Kwabi-Addo B, Wang S, Chung W, Jelinek J, Patierno SR, Wang BD, Andrawis R, Lee NH, Apprey V, Issa JP, Ittmann M (2010) Identification of differentially methylated genes in normal prostate tissues from African American and Caucasian men. Clin Cancer Res 16:3539–3547PubMedCrossRefGoogle Scholar
  36. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, Kobor MS (2012) Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci USA 109(Suppl 2):17253–17260PubMedCrossRefGoogle Scholar
  37. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462:315–322PubMedCrossRefGoogle Scholar
  38. Liu Y, Aryee MJ, Padyukov L, Fallin MD, Hesselberg E, Runarsson A, Reinius L, Acevedo N, Taub M, Ronninger M, Shchetynsky K, Scheynius A, Kere J, Alfredsson L, Klareskog L, Ekstrom TJ, Feinberg AP (2013) Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat Biotechnol 31:142–147PubMedCrossRefGoogle Scholar
  39. Luo J, Margolis KL, Wactawski-Wende J, Horn K, Messina C, Stefanick ML, Tindle HA, Tong E, Rohan TE (2011) Association of active and passive smoking with risk of breast cancer among postmenopausal women: a prospective cohort study. BMJ 342:d1016PubMedCrossRefGoogle Scholar
  40. Mani S, Szymanska K, Cuenin C, Zaridze D, Balassiano K, Lima SC, Matos E, Daudt A, Koifman S, Filho VW, Menezes AM, Curado MP, Ferro G, Vaissiere T, Sylla BS, Tommasino M, Pinto LF, Boffetta P, Hainaut P, Brennan P, Herceg Z (2012) DNA methylation changes associated with risk factors in tumors of the upper aerodigestive tract. Epigenetics 7:270–277PubMedCrossRefGoogle Scholar
  41. Manolio TA, Collins FS, Cox NJ, Goldstein DB, Hindorff LA, Hunter DJ, McCarthy MI, Ramos EM, Cardon LR, Chakravarti A, Cho JH, Guttmacher AE, Kong A, Kruglyak L, Mardis E, Rotimi CN, Slatkin M, Valle D, Whittemore AS, Boehnke M, Clark AG, Eichler EE, Gibson G, Haines JL, Mackay TF, McCarroll SA, Visscher PM (2009) Finding the missing heritability of complex diseases. Nature 461:747–753PubMedCrossRefGoogle Scholar
  42. Moore LE, Pfeiffer RM, Poscablo C, Real FX, Kogevinas M, Silverman D, Garcia-Closas R, Chanock S, Tardon A, Serra C, Carrato A, Dosemeci M, Garcia-Closas M, Esteller M, Fraga M, Rothman N, Malats N (2008) Genomic DNA hypomethylation as a biomarker for bladder cancer susceptibility in the Spanish Bladder Cancer Study: a case–control study. Lancet Oncol 9:359–366PubMedCrossRefGoogle Scholar
  43. Numata S, Ye T, Hyde TM, Guitart-Navarro X, Tao R, Wininger M, Colantuoni C, Weinberger DR, Kleinman JE, Lipska BK (2012) DNA methylation signatures in development and aging of the human prefrontal cortex. Am J Hum Genet 90:260–272PubMedCrossRefGoogle Scholar
  44. Oka D, Yamashita S, Tomioka T, Nakanishi Y, Kato H, Kaminishi M, Ushijima T (2009) The presence of aberrant DNA methylation in noncancerous esophageal mucosae in association with smoking history: a target for risk diagnosis and prevention of esophageal cancers. Cancer 115:3412–3426PubMedCrossRefGoogle Scholar
  45. Okamoto Y, Shikano S (2011) Phosphorylation-dependent C-terminal binding of 14–3-3 proteins promotes cell surface expression of HIV co-receptor GPR15. J Biol Chem 286:7171–7181PubMedCrossRefGoogle Scholar
  46. Pai AA, Bell JT, Marioni JC, Pritchard JK, Gilad Y (2011) A genome-wide study of DNA methylation patterns and gene expression levels in multiple human and chimpanzee tissues. PLoS Genet 7:e1001316PubMedCrossRefGoogle Scholar
  47. Peto R, Lopez AD, Boreham J, Thun M, Heath C Jr, Doll R (1996) Mortality from smoking worldwide. Br Med Bull 52:12–21PubMedCrossRefGoogle Scholar
  48. Philibert RA, Beach SR, Gunter TD, Brody GH, Madan A, Gerrard M (2010) The effect of smoking on MAOA promoter methylation in DNA prepared from lymphoblasts and whole blood. Am J Med Genet B Neuropsychiatr Genet 153B:619–628PubMedGoogle Scholar
  49. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575PubMedCrossRefGoogle Scholar
  50. Rea TD, Heckbert SR, Kaplan RC, Smith NL, Lemaitre RN, Psaty BM (2002) Smoking status and risk for recurrent coronary events after myocardial infarction. Ann Intern Med 137:494–500PubMedCrossRefGoogle Scholar
  51. 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 116:1547–1552PubMedCrossRefGoogle Scholar
  52. Schwartz J, Weiss ST (1994) Cigarette smoking and peripheral blood leukocyte differentials. Ann Epidemiol 4:236–242PubMedCrossRefGoogle Scholar
  53. Shenker NS, Polidoro S, van Veldhoven K, Sacerdote C, Ricceri F, Birrell MA, Belvisi MG, Brown R, Vineis P, Flanagan JM (2012) Epigenome-wide association study in the European Prospective Investigation into Cancer and Nutrition (EPIC-Turin) identifies novel genetic loci associated with smoking. Hum Mol Genet 22(5):843–851PubMedCrossRefGoogle Scholar
  54. Smith MR, Kinmonth AL, Luben RN, Bingham S, Day NE, Wareham NJ, Welch A, Khaw KT (2003) Smoking status and differential white cell count in men and women in the EPIC-Norfolk population. Atherosclerosis 169:331–337PubMedCrossRefGoogle Scholar
  55. Smith IM, Mydlarz WK, Mithani SK, Califano JA (2007) DNA global hypomethylation in squamous cell head and neck cancer associated with smoking, alcohol consumption and stage. Int J Cancer 121:1724–1728PubMedCrossRefGoogle Scholar
  56. Sun YV, Turner ST, Smith JA, Hammond PI, Lazarus A, Van De Rostyne JL, Cunningham JM, Kardia SL (2010) Comparison of the DNA methylation profiles of human peripheral blood cells and transformed B-lymphocytes. Hum Genet 127:651–658PubMedCrossRefGoogle Scholar
  57. Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9:465–476PubMedCrossRefGoogle Scholar
  58. Tekpli X, Zienolddiny S, Skaug V, Stangeland L, Haugen A, Mollerup S (2012) DNA methylation of the CYP1A1 enhancer is associated with smoking-induced genetic alterations in human lung. Int J Cancer 131(7):1509–1516PubMedCrossRefGoogle Scholar
  59. Terry MB, Ferris JS, Pilsner R, Flom JD, Tehranifar P, Santella RM, Gamble MV, Susser E (2008) Genomic DNA methylation among women in a multiethnic New York City birth cohort. Cancer Epidemiol Biomarkers Prev 17:2306–2310PubMedCrossRefGoogle Scholar
  60. van der Maarel SM (2008) Epigenetic mechanisms in health and disease. Ann Rheum Dis 67 Suppl 3:iii97–iii100PubMedCrossRefGoogle Scholar
  61. Wan ES, Qiu W, Baccarelli A, Carey VJ, Bacherman H, Rennard SI, Agusti A, Anderson W, Lomas DA, Demeo DL (2012) Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet 21(13):3073–3082PubMedCrossRefGoogle Scholar
  62. Wilhelm-Benartzi CS, Christensen BC, Koestler DC, Andres Houseman E, Schned AR, Karagas MR, Kelsey KT, Marsit CJ (2011) Association of secondhand smoke exposures with DNA methylation in bladder carcinomas. Cancer Causes Control 22:1205–1213PubMedCrossRefGoogle Scholar
  63. Willemse BW, ten Hacken NH, Rutgers B, Lesman-Leegte IG, Postma DS, Timens W (2005) Effect of 1-year smoking cessation on airway inflammation in COPD and asymptomatic smokers. Eur Respir J 26:835–845PubMedCrossRefGoogle Scholar
  64. Xu Q, Ma JZ, Payne TJ, Li MD (2010) Determination of methylated CpG Sites in the promoter region of catechol-O-methyltransferase (COMT) and their involvement in the etiology of tobacco smoking. Front Psychiatry 1:16PubMedGoogle Scholar
  65. 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 6:623–629PubMedCrossRefGoogle Scholar
  66. Zhu ZZ, Hou L, Bollati V, Tarantini L, Marinelli B, Cantone L, Yang AS, Vokonas P, Lissowska J, Fustinoni S, Pesatori AC, Bonzini M, Apostoli P, Costa G, Bertazzi PA, Chow WH, Schwartz J, Baccarelli A (2012) Predictors of global methylation levels in blood DNA of healthy subjects: a combined analysis. Int J Epidemiol 41:126–139PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Yan V. Sun
    • 1
    • 2
    Email author
  • Alicia K. Smith
    • 3
  • Karen N. Conneely
    • 4
  • Qiuzhi Chang
    • 1
  • Weiyan Li
    • 1
  • Alicia Lazarus
    • 5
  • Jennifer A. Smith
    • 5
  • Lynn M. Almli
    • 3
  • Elisabeth B. Binder
    • 3
    • 6
  • Torsten Klengel
    • 6
  • Dorthie Cross
    • 3
  • Stephen T. Turner
    • 7
  • Kerry J. Ressler
    • 3
  • Sharon L. R. Kardia
    • 5
  1. 1.Department of Epidemiology, Rollins School of Public HealthEmory UniversityAtlantaUSA
  2. 2.Department of Biomedical Informatics, School of MedicineEmory UniversityAtlantaUSA
  3. 3.Departments of Psychiatry and Behavioral Sciences, School of MedicineEmory UniversityAtlantaUSA
  4. 4.Department of Human Genetics, School of MedicineEmory UniversityAtlantaUSA
  5. 5.Department of Epidemiology, School of Public HealthUniversity of MichiganAnn ArborUSA
  6. 6.Max-Planck Institute of PsychiatryMunichGermany
  7. 7.Division of Nephrology and HypertensionMayo ClinicRochesterUSA

Personalised recommendations