Cigarette smoking reduces DNA methylation levels at multiple genomic loci but the effect is partially reversible upon cessation

Epigenetics

Volumn 9, Issue 10, 2014, Pages 1382-1396

  Tsaprouni, Loukia G ^a,b   Yang, Tsun Po ^a,c   Bell, Jordana ^d   Dick, Katherine J ^e,f   Kanoni, Stavroula ^g   Nisbet, James ^a   Viñuela, Ana ^d   Grundberg, Elin ^h   Nelson, Christopher P ^e,f   Meduri, Eshwar ^a,d   Buil, Alfonso ⁱ   Cambien, Francois ^j   Hengstenberg, Christian ^k   Erdmann, Jeanette ^l   Schunkert, Heribert ^m   Goodall, Alison H ^e,f   Ouwehand, Willem H ^a,n   Dermitzakis, Emmanouil ⁱ   Spector, Tim D ^d   Samani, Nilesh J ^e,f   Deloukas, Panos ^a,g,o   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF BEDFORDSHIRE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF LEICESTER   (United Kingdom)

^f GLENFIELD HOSPITAL   (United Kingdom)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^h MCGILL UNIVERSITY   (Canada)

ⁱ UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^j SORBONNE UNIVERSITÉ   (France)

^k Klinik und Poliklinik fur Innere Medizin II   (Germany)

^l UNIVERSITY OF LÜBECK   (Germany)

^m DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

ⁿ UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^o KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

more..

Author keywords

CHRND; CPOX; DNA methylation; Epigenome wide screen; Gene network; metQTLs; rs2697768; Smoking

Indexed keywords

ALKALINE PHOSPHATASE PLACENTA ISOENZYME; ARGIPRESSIN; COPROPORPHYRINOGEN OXIDASE; NICOTINIC RECEPTOR; PRESENILIN 2; S6 KINASE; SERINE PROTEINASE; SERINE PROTEINASE 23; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BLOOD CELL COUNT; CHRND GENE; CONTROLLED STUDY; DNA METHYLATION; FEMALE; GENE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE REPLICATION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC REGULATION; GPR15 GENE; HERITABILITY; HUMAN; MALE; QUANTITATIVE TRAIT LOCUS; QUESTIONNAIRE; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING; SMOKING CESSATION; ADVERSE EFFECTS; CLINICAL TRIAL; CPG ISLAND; GENETIC EPIGENESIS; MIDDLE AGED; MULTICENTER STUDY; SEQUENCE ANALYSIS; STATISTICAL MODEL; TWINS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; LINEAR MODELS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SEQUENCE ANALYSIS, RNA; SMOKING;

EID: 84922021718     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/15592294.2014.969637     Document Type: Article

References (46)

1. Ingebrigtsen TS, Thomsen SF, van der Sluis S, Miller M, Christensen K, Sigsgaard T, Backer V. Genetic influences on pulmonary function: a large sample twin study. Lung 2011; 189(4): 323-30; PMID:21660583; http://dx.doi.org/10.1007/s00408-011-9306-3
2. Teschendorff AE, Jones A, Fiegl H, Sargent A, Zhuang JJ, Kitchener HC, Widschwendter M. Epigenetic variability in cells of normal cytology is associated with the risk of future morphological transformation. Genome Med 2012; 4(3): 24; PMID:22453031; http://dx.doi. org/10.1186/gm323
3. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, Mangino M, Zhai G, Zhang F, Valdes A, et al. Epigenome- wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Genet 2012; 8(4): e1002629; PMID:22532803; http://dx.doi.org/10.1371/journal. pgen.1002629
4. Soma T, Kaganoi J, Kawabe A, Kondo K, Imamura M, Shimada Y. Nicotine induces the fragile histidine triad methylation in human esophageal squamous epithelial cells. Int J Cancer 2006; 119(5): 1023-27; PMID:16570269; http://dx.doi.org/10.1002/ijc.21948
5. Dammann R, Strunnikova M, Schagdarsurengin U, Rastetter M, Papritz M, Hattenhorst UE, Hofmann HS, Silber RE, Burdach S, Hansen G. CpG island methylation and expression of tumor-associated genes in lung carcinoma. Eur J Cancer 2005; 41(8): 1223-36; PMID:15911247; http://dx.doi.org/10.1016/j.ejca.2005. 02.020
6. Hillemacher T, Frieling H, Moskau S, Muschler MA, Semmler A, Kornhuber J, Klockgether T, Bleich S, Linnebank M. Global DNA methylation is influenced by smoking behaviour. Eur Neuropsychopharmacol 2008; 18(4): 295-98; PMID:18242065; http://dx.doi.org/ 10.1016/j.euroneuro.2007.12.005
7. Smith IM, Mydlarz WK, Mithani SK, Califano JA. DNA global hypomethylation in squamous cell head and neck cancer associated with smoking, alcohol consumption and stage. Int J Cancer 2007; 121(8): 1724-28; PMID:17582607; http://dx.doi.org/10. 1002/ijc.22889
8. Liu Y, Lan Q, Siegfried JM, Luketich JD, Keohavong P. Aberrant promoter methylation of p16 and MGMT genes in lung tumors from smoking and never-smoking lung cancer patients. Neoplasia 2006; 8: 46-51; PMID:16533425; http://dx.doi.org/10.1593/neo.05586
9. Kaur J, Demokan S, Tripathi SC, Macha MA, Begum S, Califano JA, Ralhan R. Promoter hypermethylation in Indian primary oral squamous cell carcinoma. Int J Cancer 2010; 127(10): 2367-73; PMID:20473870; http://dx.doi.org/10.1002/ijc.25377
10. Hsiung DT, Marsit CJ, Houseman EA, Eddy K, Furniss CS, McClean MD, Kelsey KT. Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2007; 16(1): 108-14; PMID:17220338; http://dx.doi.org/10.1158/1055-9965.EPI-06-0636
11. Broms U, Wedenoja J, Largeau MR, Korhonen T, Pitkäniemi J, Keskitalo-Vuokko K, Häppölä A, Heikkilä KH, Heikkilä K, Ripatti S, et al. Analysis of detailed phenotype profiles reveals CHRNA5- CHRNA3-CHRNB4 gene cluster association with several nicotine dependence traits. Nicotine Tob Res 2012; 14(6): 720-33; PMID:22241830; http://dx.doi. org/10.1093/ntr/ntr283
12. Saccone SF, Hinrichs AL, Saccone NL, Chase GA, Konvicka K, Madden PA, Breslau N, Johnson EO, Hatsukami D, Pomerleau O, et al. Cholinergic nicotinic receptor genes implicated in a nicotine dependence association study targeting 348 candidate genes with 3713 SNPs. Hum Mol Genet 2007; 16: 36-49; PMID:17135278; http://dx.doi.org/10.1093/hmg/ ddl438
13. Port JL, Yamaguchi K, Du B, De Lorenzo M, Chang M, Heerdt PM, Kopelovich L, Marcus CB, Altorki NK, Subbaramaiah K, Dannenberg AJ. Tobacco smoke induces CYP1B1 in the aerodigestive tract. Carcinogenesis 2004; 25(11): 2275-81; PMID:15297370; http:// dx.doi.org/10.1093/carcin/bgh243
14. Tang M, Xu W, Wang Q, Xiao W, Xu R. Potential of DNMT and its epigenetic regulation for lung cancer therapy. Curr Genomics 2009; 10(5): 336-52; PMID:20119531; http://dx.doi.org/10.2174/ 138920209788920994
15. Ho SM. Environmental epigenetics of asthma: an update. J Allergy Clin Immunol 2010; 126(3): 453-65; PMID:20816181; http://dx.doi.org/10.1016/j.jaci.20 10.07.030
16. Kerr KM, Galler JS, Hagen JA, Laird PW, Laird-Offringa IA. The role of DNA methylation in the development and progression of lung adenocarcinoma. Dis Markers 2007; 23(1-2): 5-30; PMID:17325423; http://dx.doi.org/10.1155/2007/985474
17. Georgiou E, Valeri R, Tzimagiorgis G, Anzel J, Krikelis D, Tsilikas C, Sarikos G, Destouni C, Dimitriadou A, Kouidou S. Aberrant p16 promoter methylation among Greek lung cancer patients and smokers: correlation with smoking. Eur J Cancer Prev 2007; 16(5): 396- 402; PMID:17923809; http://dx.doi.org/10.1097/01. cej.0000236260.26265.d6
18. Monick MM, Beach SR, Plume J, Sears R, Gerrard M, Brody GH, Philibert RA. Coordinated changes in AHRR methylation in lymphoblasts and pulmonary macrophages from smokers. Am J Med Genet B Neuropsychiatr Genet 2012; 159B(2): 141-51; PMID:22232023; http://dx.doi.org/10.1002/ajmg. b.32021
19. Chang HW, Ling GS, WeiWI, Yuen AP. Smoking and drinking can induce p15 methylation in the upper aerodigestive tract of healthy individuals and patients with head and neck squamous cell carcinoma. Cancer 2004; 101(1): 125-32; PMID:15221997; http://dx.doi.org/ 10.1002/cncr.20323
20. Suga Y, Miyajima K, Oikawa T, Maeda J, Usuda J, Kajiwara N, Ohira T, Uchida O, Tsuboi M, Hirano T, et al. Quantitative p16 and ESR1 methylation in the peripheral blood of patients with non-small cell lung cancer. Oncol Rep 2008; 20(5):1137-42; PMID:18949413
21. Philibert RA, Beach SR, Gunter TD, Brody GH, Madan A, Gerrard M. The effect of smoking on MAOA promoter methylation in DNA prepared from lymphoblasts and whole blood. Am J Med Genet B Neuropsychiatr Genet 2010; 153B(2): 619-28; PMID:19777560
22. Breitling LP, Yang R, Korn B, Burwinkel B, Brenner H. Tobacco-smoking-related differential DNA methylation: 27K discovery and replication. Am J Hum Genet 2011; 88(4): 450-57; PMID:21457905; http://dx.doi. org/10.1016/j.ajhg.2011.03.003
23. Wan ES, Qiu W, Baccarelli A, Carey VJ, Bacherman H, Rennard SI, Agusti A, Anderson W, Lomas DA, Demeo DL. Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet 2012; 21(13): 3073-82; PMID:22492999; http://dx.doi.org/10.1093/hmg/dds135
24. Joubert BR, Håberg SE, Nilsen RM, Wang X, Vollset SE, Murphy SK, Huang Z, Hoyo C, Midttun Ø, Cupul-Uicab LA, et al. 450K Epigenome-Wide Scan Identifies Differential DNA Methylation in Newborns Related to Maternal Smoking during Pregnancy. Environ Health Perspect 2012; 120(10): 1425-31; PMID:22851337; http://dx.doi.org/10.1289/ehp.1205412
25. Shenker NS, Polidoro S, van Veldhoven K, Sacerdote C, Ricceri F, Birrell MA, Belvisi MG, Brown R, Vineis P, Flanagan JM. 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 2013; 22(5): 843-51; PMID:23175441; http://dx.doi.org/ 10.1093/hmg/dds488
26. Zeilinger S, Kuhnel B, Klopp N, Baurecht H, Kleinschmidt A, Gieger C, Weidinger S, Lattka E, Adamski J, Peters A, et al. Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS One 2013; 8(5): e63812; PMID:23691101; http://dx.doi. org/10.1371/journal.pone.0063812
27. Sun YV, Smith AK, Conneely KN, Chang Q, Li W, Lazarus A, Smith JA, Almli LM, Binder EB, Klengel T, et al. Epigenomic association analysis identifies smoking- related DNA methylation sites in African Americans. Hum Genet 2013; 132: 1027-37; PMID:23657504; http://dx.doi.org/10.1007/s00439- 013-1311-6
28. Bibikova M, Barnes B, Tsan C, Ho V, Klotzle B, Le JM, Delano D, Zhang L, Schroth GP, Gunderson KL, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98: 288-95; PMID:21839163; http://dx.doi.org/10.1016/j.ygeno. 2011.07.007
29. The Encode Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489: 57-74; PMID:22955616; http://dx. doi.org/10.1038/nature11247
30. Adalsteinsson BT, Gudnason H, Aspelund T, Harris TB, Launer LJ, Eiriksdottir G, Smith AV, Gudnason V. Heterogeneity in white blood cells has potential to confound DNA methylation measurements. PLoS ONE 2012; 7(10): e46705; PMID:23071618; http:// dx.doi.org/10.1371/journal.pone.0046705
31. Reinius LE, Acevedo N, Joerink M, Pershagen G, Dahlén S-E, Greco D, Söderhäll C, Scheynius A, Kere J. Differential DNA methylation in purified hHuman blood cells: implications for cell lineage and studies on disease usceptibility. PLoS One 2012; 7(7): e41361; PMID:22848472; http://dx.doi.org/10.1371/journal. pone.0041361
32. Garnier S, Truong V, Brocheton J, Zeller T, Rovital M, Wild PS, Ziegler A; Cardiogenics Consortium, Munzel T, Tiret L, et al. Genome-wide haplotype analysis of cis expression quantitative trait Loci in monocytes. PLoS Genet 2013; 9(1): e1003240; PMID:23382694; http://dx.doi.org/10.1371/journal.pgen.1003240
33. Dimas AS, Deutsch S, Stranger BE, Montgomery SB, Borel C, Attar-Cohen H, Ingle C, Beazley C, Gutierrez Arcelus M, Sekowska M, et al. Common regulatory variation impacts gene expression in a cell type-dependent manner. Science 2009; 325: 1246-50; PMID:19644074; http://dx.doi.org/10.1126/ science.1174148
34. Stranger BE, Montgomery SB, Dimas AS, Parts L, Stegle O, Ingle CE, Sekowska M, Smith GD, Evans D, Gutierrez-Arcelus M, et al. Patterns of cis regulatory variation in diverse human populations. PLoS Genet 2012; 8(4): e1002639; http://dx.doi.org/10.1371/ journal.pgen.1002639
35. Grundberg E, Small KS, Hedman ÅK, Nica AC, Buil A, Keildson S, Bell JT, Yang TP, Meduri E, Barrett A, et al. Mapping cis- and trans-regulatory effects across multiple tissues in twins. Nat Genet 2012; 44(10): 1084-89; PMID:22941192; http://dx.doi.org/ 10.1038/ng.2394
36. Elliott HR, Tillin T, McArdle WL, Ho K, Duggirala A, Frayling TM, Davey Smith G, Hughes AD, Chaturvedi N, Relton CL. Differences in smoking associated DNA methylation patterns in South Asians and Europeans. Clin Epigenetics 2014; 6(1):4; PMID:24485148; http://dx.doi.org/10.1186/1868-7083-6-4
37. Murcray CE, Lewinger JP, Gauderman WJ. Geneenvironment interaction in genome-wide association studies. Am J Epidemiol 2009; 169: 219-26; PMID:19022827; http://dx.doi.org/10.1093/aje/kwn353
38. Tauber S, Jais A, Jeitler M, Haider S, Husa J, Lindroos J, Knöfler M, Mayerhofer M, Pehamberger H, Wagner O, Bilban M. Transcriptome analysis of human cancer reveals a functional role of heme oxygenase-1 in tumor cell adhesion. Mol Cancer 2010; 9: 200; PMID:20667089; http://dx.doi.org/10.1186/1476- 4598-9-200
39. Zöchbauer-Müller S, Lam S, Toyooka S, Virmani AK, Toyooka KO, Seidl S, Minna JD, Gazdar AF. Aberrant methylation of multiple genes in the upper aerodigestive tract epithelium of heavy smokers. Int J Cancer 2003; 107(4): 612-16; PMID:14520700; http://dx. doi.org/10.1002/ijc.11458
40. Bell JT, Spector TD. DNA methylation studies using twins: what are they telling us? Genome Biol 2013; 13 (10): 172; http://dx.doi.org/10.1186/gb-2012-13-10- 172
41. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am J of Hum Genet 2007; 81: 559-75; http://dx.doi.org/ 10.1086/519795
42. Gaffney DJ, Veyrieras J-B, Degner JF, Pique-Regi R, Pai AA, Crawford GE, Stephens M, Gilad Y, Pritchard JK. Dissecting the regulatory architecture of gene expression QTLs. Genome Biol 2012; 13:R7; PMID:22293038; http://dx.doi.org/10.1186/gb-2012- 13-1-r7
43. Visscher PM, Benyamin B, White I. The use of linear mixed models to estimate variance components from data on twin pairs by maximum likelihood. Twin Res 2004; 7(6): 670-74; PMID:15607018; http://dx.doi. org/10.1375/1369052042663742
44. Yang J, Ferreira T, Morris AP, Medland SE, Genetic Investigation of ANthropometric Traits (GIANT) Consortium; DIAbetes Genetics Replication And Meta-analysis (DIAGRAM) Consortium, Madden PA, Heath AC, Martin NG, et al. Conditional and joint multiple SNP analysis of GWAS summary statistics identifies additional variants influencing complex traits. Nat Genet 2011; 44: 369-75; http://dx.doi.org/ 10.1038/ng.2213
45. Yang TP, Beazley C, Montgomery SB, Dimas AS, Gutierrez-Arcelus M, Stranger BE, Deloukas P, Dermitzakis ET. Genevar: a database and Java application for the analysis and visualization of SNP-gene associations in eQTL studies. Bioinformatics 2010; 26(19): 2474-76; PMID:20702402; http://dx.doi.org/ 10.1093/bioinformatics/btq452
46. The CARDIoGRAMplusC4D Consortium, Deloukas P, Kanoni S, Willenborg C, Farrall M, Assimes TL, Thompson JR, Ingelsson E, Saleheen D, Erdmann J, et al. Largescale association analysis identifies new risk loci for coronary artery disease. Nat Genet 2013; 45: 25-33; PMID:23202125; http://dx.doi.org/10.1038/ng.2480