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Archives of Toxicology

, Volume 93, Issue 10, pp 2715–2740 | Cite as

A systematic review of smoking-related epigenetic alterations

  • Gagandeep Kaur
  • Rizwana Begum
  • Shilpa Thota
  • Sanjay BatraEmail author
Review Article
  • 120 Downloads

Abstract

The aim of this study is to provide a systematic review of the known epigenetic alterations caused by cigarette smoke; establish an evidence-based perspective of their clinical value for screening, diagnosis, and treatment of smoke-related disorders; and discuss the challenges and ethical concerns associated with epigenetic studies. A well-defined, reproducible search strategy was employed to identify relevant literature (clinical, cellular, and animal-based) between 2000 and 2019 based on AMSTAR guidelines. A total of 80 studies were identified that reported alterations in DNA methylation, histone modifications, and miRNA expression following exposure to cigarette smoke. Changes in DNA methylation were most extensively documented for genes including AHRR, F2RL3, DAPK, and p16 after exposure to cigarette smoke. Likewise, miR16, miR21, miR146, and miR222 were identified to be differentially expressed in smokers and exhibit potential as biomarkers for determining susceptibility to COPD. We also identified 22 studies highlighting the transgenerational effects of maternal and paternal smoking on offspring. This systematic review lists the epigenetic events/alterations known to occur in response to cigarette smoke exposure and identifies the major genes and miRNAs that are potential targets for translational research in associated pathologies. Importantly, the limitations and ethical concerns related to epigenetic studies are also highlighted, as are the effects on the ability to address specific questions associated with exposure to tobacco/cigarette smoke. In the future, improved interpretation of epigenetic signatures will lead to their increased use as biomarkers and/or in drug development.

Keywords

Systematic review Epigenetics Tobacco/cigarette smoking DNA methylation Histone modifications microRNA Maternal/paternal smoking Challenges Ethics 

Notes

Acknowledgements

The funding has been received from FAMRI with Grant No. 123253_YCSA_Faculty; NIH with Grant No. 7 R15 ES023151 02 and SUS Foundation with Grant No. FY 2018-020.

Compliance with ethical standards

Conflict of interest

The employment affiliation of the authors is shown on the cover page of the manuscript. The authors declare no conflict of interest. All the authors participated in the study design and interpretation of the findings. We declare that none of the authors have participated in any regulatory or legal proceedings related to the contents of this paper.

References

  1. Adenuga D, Yao H, March TH, Seagrave J, Rahman I (2009) Histone deacetylase 2 is phosphorylated, ubiquitinated, and degraded by cigarette smoke. Am J Respir Cell Mol Biol 40(4):464–473PubMedCrossRefGoogle Scholar
  2. Advani J, Subbannayya Y, Patel K et al (2017) Long-term cigarette smoke exposure and changes in MiRNA expression and proteome in non-small-cell lung cancer. OMICS 21(7):390–403PubMedPubMedCentralCrossRefGoogle Scholar
  3. Alkhaled Y, Laqqan M, Tierling S, Lo Porto C, Amor H, Hammadeh ME (2018) Impact of cigarette-smoking on sperm DNA methylation and its effect on sperm parameters. Andrologia.  https://doi.org/10.1111/and.12950 CrossRefPubMedGoogle Scholar
  4. Ambatipudi S, Cuenin C, Hernandez-Vargas H et al (2016) Tobacco smoking-associated genome-wide DNA methylation changes in the EPIC study. Epigenomics 8(5):599–618PubMedCrossRefGoogle Scholar
  5. Andersson BA, Sayardoust S, Lofgren S, Rutqvist LE, Laytragoon-Lewin N (2018) Cigarette smoking affects microRNAs and inflammatory biomarkers in healthy individuals and an association to single nucleotide polymorphisms is indicated. Biomarkers 24(2):180–185PubMedCrossRefGoogle Scholar
  6. Banerjee A, Luettich K (2012) MicroRNAs as potential biomarkers of smoking-related diseases. Biomark Med 6(5):671–684PubMedCrossRefGoogle Scholar
  7. Banerjee A, Waters D, Camacho OM, Minet E (2015) Quantification of plasma microRNAs in a group of healthy smokers, ex-smokers and non-smokers and correlation to biomarkers of tobacco exposure. Biomarkers 20(2):123–131PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21(3):381–395PubMedPubMedCentralCrossRefGoogle Scholar
  9. Barnes PJ (2009) Histone deacetylase-2 and airway disease. Ther Adv Respir Dis 3(5):23543CrossRefGoogle Scholar
  10. Beach SRH, Lei MK, Ong ML, Brody GH, Dogan MV, Philibert RA (2017) MTHFR methylation moderates the impact of smoking on DNA methylation at AHRR for African American young adults. Am J Med Genet B Neuropsychiatr Genet 174(6):608–618PubMedPubMedCentralCrossRefGoogle Scholar
  11. Belinsky SA, Palmisano WA, Gilliland FD et al (2002) Aberrant promoter methylation in bronchial epithelium and sputum from current and former smokers. Cancer Res 62(8):2370–2377PubMedPubMedCentralGoogle Scholar
  12. 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(4):450–457PubMedPubMedCentralCrossRefGoogle Scholar
  13. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD (2009) Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 180(5):462–467PubMedPubMedCentralCrossRefGoogle Scholar
  14. Burton A (2011) Does the smoke ever really clear? Thirdhand smoke exposure raises new concerns. Environ Health Perspect 119(2):A70–A74PubMedPubMedCentralCrossRefGoogle Scholar
  15. Campbell RM, Tummino PJ (2014) Cancer epigenetics drug discovery and development: the challenge of hitting the mark. J Clin Invest 124(1):64–69PubMedPubMedCentralCrossRefGoogle Scholar
  16. Carrozza MJ, Utley RT, Workman JL, Cote J (2003) The diverse functions of histone acetyltransferase complexes. Trends Genet 19(6):321–329PubMedCrossRefPubMedCentralGoogle Scholar
  17. Carvalho RH, Haberle V, Hou J et al (2012) Genome-wide DNA methylation profiling of non-small cell lung carcinomas. Epigenet Chromatin 5(1):9CrossRefGoogle Scholar
  18. Catalano R, Bruckner T, Gould J, Eskenazi B, Anderson E (2005) Sex ratios in California following the terrorist attacks of September 11. Hum Reprod 20(5):1221–1227PubMedCrossRefPubMedCentralGoogle Scholar
  19. Costa LA, da Silva ICB, Mariz B, da Silva MB, Freitas-Ribeiro GM, de Oliveira NFP (2016) Influence of smoking on methylation and hydroxymethylation levels in global DNA and specific sites of KRT14, KRT19, MIR-9-3 and MIR-137 genes of oral mucosa. Arch Oral Biol 72:56–65PubMedCrossRefPubMedCentralGoogle Scholar
  20. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB (2003) Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 370(Pt 3):737–749PubMedPubMedCentralCrossRefGoogle Scholar
  21. de Vries M, van der Plaat DA, Nedeljkovic I et al (2018a) From blood to lung tissue: effect of cigarette smoke on DNA methylation and lung function. Respir Res 19(1):212PubMedPubMedCentralCrossRefGoogle Scholar
  22. de Vries M, van der Plaat DA, Vonk JM, Boezen HM (2018b) No association between DNA methylation and COPD in never and current smokers. BMJ Open Respir Res 5(1):e000282PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dogan MV, Shields B, Cutrona C et al (2014) The effect of smoking on DNA methylation of peripheral blood mononuclear cells from African American women. BMC Genomics 15:151PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dogan MV, Beach SRH, Philibert RA (2017) Genetically contextual effects of smoking on genome wide DNA methylation. Am J Med Genet B Neuropsychiatr Genet 174(6):595–607PubMedPubMedCentralCrossRefGoogle Scholar
  25. Edwards JR, Yarychkivska O, Boulard M, Bestor TH (2017) DNA methylation and DNA methyltransferases. Epigenet Chromatin 10:23CrossRefGoogle Scholar
  26. Eissenberg JC, Shilatifard A (2010) Histone H3 lysine 4 (H3K4) methylation in development and differentiation. Dev Biol 339(2):240–249PubMedCrossRefPubMedCentralGoogle Scholar
  27. Elliott HR, Tillin T, McArdle WL et al (2014) Differences in smoking associated DNA methylation patterns in South Asians and Europeans. Clin Epigenet 6(1):4.  https://doi.org/10.1186/1868-7083-6-4 CrossRefGoogle Scholar
  28. El-Zein RA, Young RP, Hopkins RJ, Etzel CJ (2012) Genetic predisposition to chronic obstructive pulmonary disease and/or lung cancer: important considerations when evaluating risk. Cancer Prev Res (Phila) 5(4):522–527CrossRefGoogle Scholar
  29. Fa S, Larsen TV, Bilde K et al (2016) Assessment of global DNA methylation in the first trimester fetal tissues exposed to maternal cigarette smoking. Clin Epigenet 8:128CrossRefGoogle Scholar
  30. Fasanelli F, Baglietto L, Ponzi E et al (2015) Hypomethylation of smoking-related genes is associated with future lung cancer in four prospective cohorts. Nat Commun 6:10192PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gross TJ, Powers LS, Boudreau RL et al (2014) A microRNA processing defect in smokers’ macrophages is linked to SUMOylation of the endonuclease DICER. J Biol Chem 289(18):12823–12834PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gu W, Yuan Y, Yang H et al (2018) Role of miR-195 in cigarette smoke-induced chronic obstructive pulmonary disease. Int Immunopharmacol 55:49–54PubMedCrossRefPubMedCentralGoogle Scholar
  33. Gunes S, Metin Mahmutoglu A, Arslan MA, Henkel R (2018) Smoking-induced genetic and epigenetic alterations in infertile men. Andrologia 50(9):e13124PubMedCrossRefPubMedCentralGoogle Scholar
  34. Gupta R, van Dongen J, Fu Y et al (2019) Epigenome-wide association study of serum cotinine in current smokers reveals novel genetically driven loci. Clin Epigenet 11(1):1CrossRefGoogle Scholar
  35. Gutierrez-Arcelus M, Ongen H, Lappalainen T et al (2015) Tissue-specific effects of genetic and epigenetic variation on gene regulation and splicing. PLoS Genet 11(1):e1004958PubMedPubMedCentralCrossRefGoogle Scholar
  36. Hamad MF, Dayyih WAA, Laqqan M, AlKhaled Y, Montenarh M, Hammadeh ME (2018) The status of global DNA methylation in the spermatozoa of smokers and non-smokers. Reprod Biomed Online 37(5):581–589PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hammons GJ, Yan Y, Lopatina NG et al (1999) Increased expression of hepatic DNA methyltransferase in smokers. Cell Biol Toxicol 15(6):389–394PubMedCrossRefPubMedCentralGoogle Scholar
  38. Harlid S, Xu Z, Panduri V, Sandler DP, Taylor JA (2014) CpG sites associated with cigarette smoking: analysis of epigenome-wide data from the Sister Study. Environ Health Perspect 122(7):673–678PubMedPubMedCentralCrossRefGoogle Scholar
  39. Heffernan T (2016) Editorial: the impact of active and passive smoking upon health and neurocognitive function. Front Psychiatry 7:148PubMedPubMedCentralCrossRefGoogle Scholar
  40. Heijink IH, de Bruin HG, van den Berge M et al (2013) Role of aberrant WNT signalling in the airway epithelial response to cigarette smoke in chronic obstructive pulmonary disease. Thorax 68(8):709–716PubMedCrossRefPubMedCentralGoogle Scholar
  41. Heijmans BT, Kremer D, Tobi EW, Boomsma DI, Slagboom PE (2007) Heritable rather than age-related environmental and stochastic factors dominate variation in DNA methylation of the human IGF2/H19 locus. Hum Mol Genet 16(5):547–554PubMedCrossRefPubMedCentralGoogle Scholar
  42. Herberth G, Bauer M, Gasch M et al (2014) Maternal and cord blood miR-223 expression associates with prenatal tobacco smoke exposure and low regulatory T-cell numbers. J Allergy Clin Immunol 133(2):543–550PubMedCrossRefPubMedCentralGoogle Scholar
  43. Hillemacher T, Frieling H, Moskau S et al (2008) Global DNA methylation is influenced by smoking behaviour. Eur Neuropsychopharmacol 18(4):295–298PubMedCrossRefPubMedCentralGoogle Scholar
  44. Huang J, Wu J, Li Y et al (2014) Deregulation of serum microRNA expression is associated with cigarette smoking and lung cancer. Biomed Res Int 2014:364316PubMedPubMedCentralGoogle Scholar
  45. Hyun K, Jeon J, Park K, Kim J (2017) Writing, erasing and reading histone lysine methylations. Exp Mol Med 49(4):e324PubMedPubMedCentralCrossRefGoogle Scholar
  46. Ito K, Lim S, Caramori G, Chung KF, Barnes PJ, Adcock IM (2001) Cigarette smoking reduces histone deacetylase 2 expression, enhances cytokine expression, and inhibits glucocorticoid actions in alveolar macrophages. FASEB J 15(6):1110–1112PubMedCrossRefPubMedCentralGoogle Scholar
  47. Ito K, Caramori G, Lim S et al (2002) Expression and activity of histone deacetylases in human asthmatic airways. Am J Respir Crit Care Med 166(3):392–396PubMedCrossRefPubMedCentralGoogle Scholar
  48. Ito K, Ito M, Elliott WM et al (2005) Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 352(19):1967–1976PubMedCrossRefPubMedCentralGoogle Scholar
  49. Izzotti A, Calin GA, Steele VE, Croce CM, De Flora S (2009) Relationships of microRNA expression in mouse lung with age and exposure to cigarette smoke and light. FASEB J 23(9):3243–3250PubMedPubMedCentralCrossRefGoogle Scholar
  50. Izzotti A, Larghero P, Longobardi M et al (2011) Dose-responsiveness and persistence of microRNA expression alterations induced by cigarette smoke in mouse lung. Mutat Res 717(1–2):9–16PubMedCrossRefPubMedCentralGoogle Scholar
  51. Jamal A, Phillips E, Gentzke AS et al (2018) Current cigarette smoking among adults—United States. MMWR Morb Mortal Wkly Rep 67(2):53–59PubMedPubMedCentralCrossRefGoogle Scholar
  52. Janssen HL, Reesink HW, Lawitz EJ et al (2013) Treatment of HCV infection by targeting microRNA. N Engl J Med 368(18):1685–1694PubMedCrossRefPubMedCentralGoogle Scholar
  53. Jenkins TG, James ER, Alonso DF et al (2017) Cigarette smoking significantly alters sperm DNA methylation patterns. Andrology 5(6):1089–1099PubMedPubMedCentralCrossRefGoogle Scholar
  54. Jin B, Robertson KD (2013) DNA methyltransferases, DNA damage repair, and cancer. Adv Exp Med Biol 754:3–29PubMedPubMedCentralCrossRefGoogle Scholar
  55. Joubert BR, Haberg SE, Nilsen RM et al (2012) 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ Health Perspect 120(10):1425–1431PubMedPubMedCentralCrossRefGoogle Scholar
  56. Joubert BR, Haberg SE, Bell DA et al (2014) Maternal smoking and DNA methylation in newborns: in utero effect or epigenetic inheritance? Cancer Epidemiol Biomark Prev 23(6):1007–1017CrossRefGoogle Scholar
  57. Kaneda M, Okano M, Hata K et al (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429(6994):900–903PubMedCrossRefPubMedCentralGoogle Scholar
  58. Kaur G, Bagam P, Pinkston R, Singh DP, Batra S (2018) Cigarette smoke-induced inflammation: NLRP10-mediated mechanisms. Toxicology 398–399:52–67PubMedCrossRefPubMedCentralGoogle Scholar
  59. Khashan AS, McNamee R, Henriksen TB et al (2011) Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. J Psychiatr Res 45(7):879–885PubMedCrossRefPubMedCentralGoogle Scholar
  60. Knopik VS, Maccani MA, Francazio S, McGeary JE (2012) The epigenetics of maternal cigarette smoking during pregnancy and effects on child development. Dev Psychopathol 24(4):1377–1390PubMedPubMedCentralCrossRefGoogle Scholar
  61. Konigshoff M, Eickelberg O (2010) WNT signaling in lung disease: a failure or a regeneration signal? Am J Respir Cell Mol Biol 42(1):21–31PubMedCrossRefPubMedCentralGoogle Scholar
  62. Laqqan M, Tierling S, Alkhaled Y, Porto CL, Solomayer EF, Hammadeh ME (2017) Aberrant DNA methylation patterns of human spermatozoa in current smoker males. Reprod Toxicol 71:126–133PubMedCrossRefPubMedCentralGoogle Scholar
  63. Lee KW, Pausova Z (2013) Cigarette smoking and DNA methylation. Front Genet 4:132PubMedPubMedCentralGoogle Scholar
  64. Lee MK, Hong Y, Kim SY, London SJ, Kim WJ (2016) DNA methylation and smoking in Korean adults: epigenome-wide association study. Clin Epigenet. 8:103CrossRefGoogle Scholar
  65. Leng S, Wu G, Collins LB et al (2015) Implication of a Chromosome 15q15.2 Locus in Regulating UBR1 and Predisposing Smokers to MGMT Methylation in Lung. Cancer Res 75(15):3108–3117PubMedPubMedCentralCrossRefGoogle Scholar
  66. Li S, Wong EM, Bui M et al (2018) Causal effect of smoking on DNA methylation in peripheral blood: a twin and family study. Clin Epigenet 10:18CrossRefGoogle Scholar
  67. Lim D, Maher E (2011) DNA methylation: a form of epigenetic control of gene expression. Obstet Gynaecol 12(1):37–42Google Scholar
  68. Lubick N (2011) Global estimate of SHS burden. Environ Health Perspect 119(2):A66–A67PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lyn-Cook L, Word B, George N, Lyn-Cook B, Hammons G (2014) Effect of cigarette smoke condensate on gene promoter methylation in human lung cells. Tob Induc Dis 12(1):15PubMedPubMedCentralCrossRefGoogle Scholar
  70. Maccani MA, Avissar-Whiting M, Banister CE, McGonnigal B, Padbury JF, Marsit CJ (2010) Maternal cigarette smoking during pregnancy is associated with downregulation of miR-16, miR-21, and miR-146a in the placenta. Epigenetics 5(7):583–589PubMedPubMedCentralCrossRefGoogle Scholar
  71. MacKenzie TD, Bartecchi CE, Schrier RW (1994) The human costs of tobacco use (2). N Engl J Med 330(14):975–980PubMedCrossRefGoogle Scholar
  72. Marczylo EL, Amoako AA, Konje JC, Gant TW, Marczylo TH (2012) Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7(5):432–439PubMedCrossRefGoogle Scholar
  73. Markunas CA, Xu Z, Harlid S et al (2014) Identification of DNA methylation changes in newborns related to maternal smoking during pregnancy. Environ Health Perspect 122(10):1147–1153PubMedPubMedCentralCrossRefGoogle Scholar
  74. Marwick JA, Kirkham PA, Stevenson CS et al (2004) Cigarette smoke alters chromatin remodeling and induces proinflammatory genes in rat lungs. Am J Respir Cell Mol Biol 31(6):633–642PubMedCrossRefPubMedCentralGoogle Scholar
  75. McCartney DL, Stevenson AJ, Hillary RF et al (2018) Epigenetic signatures of starting and stopping smoking. EBioMedicine 37:214–220PubMedPubMedCentralCrossRefGoogle Scholar
  76. Milutinovic S, Brown SE, Zhuang Q, Szyf M (2004) DNA methyltransferase 1 knock down induces gene expression by a mechanism independent of DNA methylation and histone deacetylation. J Biol Chem 279(27):27915–27927PubMedCrossRefPubMedCentralGoogle Scholar
  77. Monick MM, Beach SR, Plume J et al (2012) Coordinated changes in AHRR methylation in lymphoblasts and pulmonary macrophages from smokers. Am J Med Genet B Neuropsychiatr Genet 159B(2):141–151PubMedPubMedCentralCrossRefGoogle Scholar
  78. Moodie FM, Marwick JA, Anderson CS et al (2004) Oxidative stress and cigarette smoke alter chromatin remodeling but differentially regulate NF-kappaB activation and proinflammatory cytokine release in alveolar epithelial cells. FASEB J 18(15):1897–1899PubMedCrossRefPubMedCentralGoogle Scholar
  79. Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacology 38(1):23–38PubMedCrossRefPubMedCentralGoogle Scholar
  80. Morales E, Vilahur N, Salas LA et al (2016) Genome-wide DNA methylation study in human placenta identifies novel loci associated with maternal smoking during pregnancy. Int J Epidemiol 45(5):1644–1655PubMedCrossRefPubMedCentralGoogle Scholar
  81. Murphy SK, Adigun A, Huang Z et al (2012) Gender-specific methylation differences in relation to prenatal exposure to cigarette smoke. Gene 494(1):36–43PubMedCrossRefPubMedCentralGoogle Scholar
  82. Nichol JN, Dupere-Richer D, Ezponda T, Licht JD, Miller WH Jr (2016) H3K27 methylation: a focal point of epigenetic deregulation in cancer. Adv Cancer Res 131:59–95PubMedPubMedCentralCrossRefGoogle Scholar
  83. Ostrow KL, Michailidi C, Guerrero-Preston R et al (2013) Cigarette smoke induces methylation of the tumor suppressor gene NISCH. Epigenetics 8(4):383–388PubMedPubMedCentralCrossRefGoogle Scholar
  84. Patil VK, Holloway JW, Zhang H et al (2013) Interaction of prenatal maternal smoking, interleukin 13 genetic variants and DNA methylation influencing airflow and airway reactivity. Clin Epigenet 5(1):22CrossRefGoogle Scholar
  85. Peluso ME, Munnia A, Bollati V et al (2014) Aberrant methylation of hypermethylated-in-cancer-1 and exocyclic DNA adducts in tobacco smokers. Toxicol Sci 137(1):47–54PubMedCrossRefGoogle Scholar
  86. Peters I, Vaske B, Albrecht K, Kuczyk MA, Jonas U, Serth J (2007) Adiposity and age are statistically related to enhanced RASSF1A tumor suppressor gene promoter methylation in normal autopsy kidney tissue. Cancer Epidemiol Biomark Prev 16(12):2526–2532CrossRefGoogle Scholar
  87. Philibert RA, Beach SR, Lei MK, Brody GH (2013) Changes in DNA methylation at the aryl hydrocarbon receptor repressor may be a new biomarker for smoking. Clin Epigenet 5(1):19CrossRefGoogle Scholar
  88. Philibert R, Hollenbeck N, Andersen E et al (2016) Reversion of AHRR demethylation is a quantitative biomarker of smoking cessation. Front Psychiatry 7:55PubMedPubMedCentralCrossRefGoogle Scholar
  89. Portela A, Esteller M (2010) Epigenetic modifications and human disease. Nat Biotechnol 28(10):1057–1068PubMedCrossRefGoogle Scholar
  90. Prince C, Hammerton G, Taylor AE et al (2019) Investigating the impact of cigarette smoking behaviours on DNA methylation patterns in adolescence. Hum Mol Genet 28(1):155–165PubMedPubMedCentralGoogle Scholar
  91. Protano C, Vitali M (2011) The new danger of thirdhand smoke: why passive smoking does not stop at secondhand smoke. Environ Health Perspect 119(10):A422PubMedPubMedCentralCrossRefGoogle Scholar
  92. Qiu W, Baccarelli A, Carey VJ et al (2012) Variable DNA methylation is associated with chronic obstructive pulmonary disease and lung function. Am J Respir Crit Care Med 185(4):373–381PubMedPubMedCentralCrossRefGoogle Scholar
  93. Reynolds LM, Lohman K, Pittman GS et al (2017) Tobacco exposure-related alterations in DNA methylation and gene expression in human monocytes: the Multi-Ethnic Study of Atherosclerosis (MESA). Epigenetics 12(12):1092–1100PubMedCrossRefPubMedCentralGoogle Scholar
  94. Richmond RC, Simpkin AJ, Woodward G et al (2015) Prenatal exposure to maternal smoking and offspring DNA methylation across the lifecourse: findings from the Avon Longitudinal Study of Parents and Children (ALSPAC). Hum Mol Genet 24(8):2201–2217PubMedCrossRefPubMedCentralGoogle Scholar
  95. Richmond RC, Suderman M, Langdon R, Relton CL, Davey Smith G (2018) DNA methylation as a marker for prenatal smoke exposure in adults. Int J Epidemiol 47(4):1120–1130PubMedPubMedCentralCrossRefGoogle Scholar
  96. Rothstein MA, Cai Y, Marchant GE (2009) The ghost in our genes: legal and ethical implications of epigenetics. Health Matrix Clevel 19(1):1–62PubMedPubMedCentralGoogle Scholar
  97. Saha SP, Bhalla DK, Whayne TF Jr, Gairola C (2007) Cigarette smoke and adverse health effects: an overview of research trends and future needs. Int J Angiol 16(3):77–83PubMedPubMedCentralCrossRefGoogle Scholar
  98. Satta R, Maloku E, Zhubi A et al (2008) Nicotine decreases DNA methyltransferase 1 expression and glutamic acid decarboxylase 67 promoter methylation in GABAergic interneurons. Proc Natl Acad Sci USA 105(42):16356–16361PubMedCrossRefPubMedCentralGoogle Scholar
  99. Shabani M, Borry P, Smeers I, Bekaert B (2018) Forensic epigenetic age estimation and beyond: ethical and legal considerations. Trends Genet 34(7):489–491PubMedCrossRefPubMedCentralGoogle Scholar
  100. Shea BJ, Grimshaw JM, Wells GA et al (2007) Development of AMSTAR: a measurement tool to assess the methodological quality of systematic reviews. BMC Med Res Methodol 7:10PubMedPubMedCentralCrossRefGoogle Scholar
  101. Shen W, Liu J, Zhao G et al (2017) Repression of Toll-like receptor-4 by microRNA-149-3p is associated with smoking-related COPD. Int J Chron Obstruct Pulmon Dis 12:705–715PubMedPubMedCentralCrossRefGoogle Scholar
  102. Shenker NS, Polidoro S, van Veldhoven K et al (2013) 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):843–851PubMedCrossRefPubMedCentralGoogle Scholar
  103. Shi B, Gao H, Zhang T, Cui Q (2016) Analysis of plasma microRNA expression profiles revealed different cancer susceptibility in healthy young adult smokers and middle-aged smokers. Oncotarget 7(16):21676–21685PubMedPubMedCentralGoogle Scholar
  104. Siedlinski M, Klanderman B, Sandhaus RA et al (2012) Association of cigarette smoking and CRP levels with DNA methylation in alpha-1 antitrypsin deficiency. Epigenetics 7(7):720–728PubMedPubMedCentralCrossRefGoogle Scholar
  105. Sohal SS, Reid D, Soltani A et al (2013) Changes in airway histone deacetylase2 in smokers and COPD with inhaled corticosteroids: a randomized controlled trial. PLoS One 8(5):e64833PubMedPubMedCentralCrossRefGoogle Scholar
  106. Soria JC, Rodriguez M, Liu DD, Lee JJ, Hong WK, Mao L (2002) Aberrant promoter methylation of multiple genes in bronchial brush samples from former cigarette smokers. Cancer Res 62(2):351–355PubMedPubMedCentralGoogle Scholar
  107. Su D, Wang X, Campbell MR et al (2016) Distinct epigenetic effects of tobacco smoking in whole blood and among leukocyte subtypes. PLoS One 11(12):e0166486PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sun YV, Smith AK, Conneely KN et al (2013) Epigenomic association analysis identifies smoking-related DNA methylation sites in African Americans. Hum Genet 132(9):1027–1037PubMedPubMedCentralCrossRefGoogle Scholar
  109. Sundar IK, Rahman I (2016) Gene expression profiling of epigenetic chromatin modification enzymes and histone marks by cigarette smoke: implications for COPD and lung cancer. Am J Physiol Lung Cell Mol Physiol 311(6):L1245–L1258PubMedPubMedCentralCrossRefGoogle Scholar
  110. Sundar IK, Chung S, Hwang JW et al (2012) Mitogen- and stress-activated kinase 1 (MSK1) regulates cigarette smoke-induced histone modifications on NF-kappaB-dependent genes. PLoS One 7(2):e31378PubMedPubMedCentralCrossRefGoogle Scholar
  111. Sundar IK, Nevid MZ, Friedman AE, Rahman I (2014) Cigarette smoke induces distinct histone modifications in lung cells: implications for the pathogenesis of COPD and lung cancer. J Proteome Res 13(2):982–996PubMedCrossRefGoogle Scholar
  112. Sundar IK, Yin Q, Baier BS et al (2017) DNA methylation profiling in peripheral lung tissues of smokers and patients with COPD. Clin Epigenet 9:38CrossRefGoogle Scholar
  113. Suter M, Abramovici A, Showalter L et al (2010) In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism 59(10):1481–1490PubMedPubMedCentralCrossRefGoogle Scholar
  114. Suter M, Ma J, Harris A et al (2011) Maternal tobacco use modestly alters correlated epigenome-wide placental DNA methylation and gene expression. Epigenetics 6(11):1284–1294PubMedPubMedCentralCrossRefGoogle Scholar
  115. Suzuki M, Shigematsu H, Shames DS et al (2007) Methylation and gene silencing of the Ras-related GTPase gene in lung and breast cancers. Ann Surg Oncol 14(4):1397–1404PubMedCrossRefPubMedCentralGoogle Scholar
  116. Szulakowski P, Crowther AJ, Jimenez LA et al (2006) The effect of smoking on the transcriptional regulation of lung inflammation in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 174(1):41–50PubMedCrossRefPubMedCentralGoogle Scholar
  117. Tehranifar P, Wu HC, McDonald JA et al (2018) Maternal cigarette smoking during pregnancy and offspring DNA methylation in midlife. Epigenetics 13(2):129–134PubMedPubMedCentralCrossRefGoogle Scholar
  118. Terzikhan N, Verhamme KM, Hofman A, Stricker BH, Brusselle GG, Lahousse L (2016) Prevalence and incidence of COPD in smokers and non-smokers: the Rotterdam Study. Eur J Epidemiol 31(8):785–792PubMedPubMedCentralCrossRefGoogle Scholar
  119. UniProt (2019a) UniProtKB - Q8NFU7 (TET1_HUMAN). In. https://www.uniprot.org/uniprot/Q8NFU7. Accessed Jan 4 2019Google Scholar
  120. UniProt (2019b) UniProtKB - Q9UBC3 (DNM3B_HUMAN). In. https://www.uniprot.org/uniprot/Q9UBC3. Accessed Jan 4 2019Google Scholar
  121. Van Pottelberge GR, Mestdagh P, Bracke KR et al (2011) MicroRNA expression in induced sputum of smokers and patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 183(7):898–906PubMedCrossRefPubMedCentralGoogle Scholar
  122. Wahid F, Shehzad A, Khan T, Kim YY (2010) MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochim Biophys Acta 11:1231–1243CrossRefGoogle Scholar
  123. Wan ES, Qiu W, Baccarelli A et al (2012) Cigarette smoking behaviors and time since quitting are associated with differential DNA methylation across the human genome. Hum Mol Genet 21(13):3073–3082PubMedPubMedCentralCrossRefGoogle Scholar
  124. Wang G, Wang R, Strulovici-Barel Y et al (2015) Persistence of smoking-induced dysregulation of miRNA expression in the small airway epithelium despite smoking cessation. PLoS One 10(4):e0120824PubMedPubMedCentralCrossRefGoogle Scholar
  125. Weinhold B (2006) Epigenetics: the science of change. Environ Health Perspect 114(3):A160–A167PubMedPubMedCentralCrossRefGoogle Scholar
  126. Willinger CM, Rong J, Tanriverdi K et al (2017) MicroRNA signature of cigarette smoking and evidence for a putative causal role of microRNAs in smoking-related inflammation and target organ damage. Circ Cardiovasc Genet 10(5):e001678PubMedPubMedCentralCrossRefGoogle Scholar
  127. Wilson R, Wahl S, Pfeiffer L et al (2017) The dynamics of smoking-related disturbed methylation: a two time-point study of methylation change in smokers, non-smokers and former smokers. BMC Genom 18(1):805CrossRefGoogle Scholar
  128. 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 1:16PubMedPubMedCentralGoogle Scholar
  129. Xu W, Fang P, Zhu Z et al (2013) Cigarette smoking exposure alters pebp1 DNA methylation and protein profile involved in MAPK signaling pathway in mice testis. Biol Reprod 89(6):142PubMedCrossRefPubMedCentralGoogle Scholar
  130. Yang IV, Schwartz DA (2011) Epigenetic control of gene expression in the lung. Am J Respir Crit Care Med 183(10):1295–1301PubMedPubMedCentralCrossRefGoogle Scholar
  131. Yang SR, Chida AS, Bauter MR et al (2006) Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 291(1):L46–L57PubMedCrossRefPubMedCentralGoogle Scholar
  132. Yao H, Hwang JW, Moscat J et al (2010) Protein kinase C zeta mediates cigarette smoke/aldehyde- and lipopolysaccharide-induced lung inflammation and histone modifications. J Biol Chem 285(8):5405–5416PubMedCrossRefPubMedCentralGoogle Scholar
  133. Zaghlool SB, Al-Shafai M, Al Muftah WA, Kumar P, Falchi M, Suhre K (2015) Association of DNA methylation with age, gender, and smoking in an Arab population. Clin Epigenet 7:6CrossRefGoogle Scholar
  134. Zhang Y, Yang R, Burwinkel B et al (2014) F2RL3 methylation in blood DNA is a strong predictor of mortality. Int J Epidemiol 43(4):1215–1225PubMedPubMedCentralCrossRefGoogle Scholar
  135. Zheleznyakova GY, Piket E, Marabita F et al (2017) Epigenetic research in multiple sclerosis: progress, challenges, and opportunities. Physiol Genom 49(9):447–461CrossRefGoogle Scholar
  136. Zhu X, Li J, Deng S et al (2016) Genome-wide analysis of DNA methylation and cigarette smoking in a Chinese population. Environ Health Perspect 124(7):966–973PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Gagandeep Kaur
    • 1
  • Rizwana Begum
    • 1
  • Shilpa Thota
    • 1
  • Sanjay Batra
    • 1
    Email author
  1. 1.Laboratory of Pulmonary Immuno-toxicology, Department of Environmental Toxicology, 129 Health Research CentreSouthern University and A&M CollegeBaton RougeUSA

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