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Cancer Causes & Control

, Volume 30, Issue 1, pp 53–62 | Cite as

Active and secondhand smoke exposure throughout life and DNA methylation in breast tumors

  • Catherine L. CallahanEmail author
  • Matthew R. Bonner
  • Jing Nie
  • Youjin Wang
  • Meng-Hua Tao
  • Peter G. Shields
  • Catalin Marian
  • Kevin H. Eng
  • Maurizio Trevisan
  • Jo L. Freudenheim
Original paper
  • 114 Downloads

Abstract

Purpose

Tobacco smoke exposure has been associated with altered DNA methylation. However, there is a paucity of information regarding tobacco smoke exposure and DNA methylation of breast tumors.

Methods

We conducted a case-only analysis using breast tumor tissue from 493 postmenopausal and 225 premenopausal cases in the Western New York Exposures and Breast Cancer (WEB) study. Methylation of nine genes (SFN, SCGB3A1, RARB, GSTP1, CDKN2A, CCND2, BRCA1, FHIT, and SYK) was measured with pyrosequencing. Participants reported their secondhand smoke (SHS) and active smoking exposure for seven time periods. Unconditional logistic regression was used to estimate odds ratios (OR) of having methylation higher than the median.

Results

SHS exposure was associated with tumor DNA methylation among postmenopausal but not premenopausal women. Active smoking at certain ages was associated with increased methylation of GSTP1, FHIT, and CDKN2A and decreased methylation of SCGB3A1 and BRCA1 among both pre- and postmenopausal women.

Conclusion

Exposure to tobacco smoke may contribute to breast carcinogenesis via alterations in DNA methylation. Further studies in a larger panel of genes are warranted.

Keywords

Breast cancer DNA methylation Tobacco Secondhand smoke Epigenetics 

Notes

Disclaimer

This article was prepared while Catherine Callahan and Youjin Wang were employed at the University at Buffalo. The opinions expressed in this article are the authors’ own and do not reflect the view of the National Institutes of Health, the Department of Health and Human Services, or the United States government.

Funding

Catherine L. Callahan was supported by the National Cancer Institute (NCI) Grant R25CA113951.

Compliance with Ethical Standards

Conflict of interest

The authors declare no potential conflict of interest.

References

  1. 1.
    Macacu A, Autier P, Boniol M, Boyle P (2015) Active and passive smoking and risk of breast cancer: a meta-analysis. Breast Cancer Res Treat 154:213–224CrossRefGoogle Scholar
  2. 2.
    Rosenberg L, Boggs DA, Bethea TN, Wise LA, Adams-Campbell LL, Palmer JR (2013) A prospective study of smoking and breast cancer risk among African American women. Cancer Causes Control.  https://doi.org/10.1007/s10552-013-0298-6 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Catsburg C, Miller AB, Rohan TE (2015) Active cigarette smoking and risk of breast cancer. Int J Cancer 136:2204–2209CrossRefGoogle Scholar
  4. 4.
    Dossus L, Boutron-Ruault MC, Kaaks R et al (2014) Active and passive cigarette smoking and breast cancer risk: results from the EPIC cohort. Int J Cancer 134:1871–1888CrossRefGoogle Scholar
  5. 5.
    Gram IT, Park SY, Kolonel LN et al (2015) Smoking and risk of breast cancer in a racially/ethnically diverse population of mainly women who do not drink alcohol: the MEC study. Am J Epidemiol 182:917–925CrossRefGoogle Scholar
  6. 6.
    Hecht SS (2002) Tobacco smoke carcinogens and breast cancer. Environ Mol Mutagen. 39:119–126CrossRefGoogle Scholar
  7. 7.
    MacNicoll A, Easty G, Neville A, Grover P, Sims P (1980) Metabolism and activation of carcinogenic polycyclic hydrocarbons by human mammary cells. Biochem Biophys Res Commun 95:1599–1606CrossRefGoogle Scholar
  8. 8.
    McCabe MT, Brandes JC, Vertino PM (2009) Cancer DNA methylation: molecular mechanisms and clinical implications. Clin Cancer Res 15:3927–3937CrossRefGoogle Scholar
  9. 9.
    Johnson KC, Koestler DC, Cheng C, Christensen BC (2014) Age-related DNA methylation in normal breast tissue and its relationship with invasive breast tumor methylation. Epigenetics 9:268–275CrossRefGoogle Scholar
  10. 10.
    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 124:966–973CrossRefGoogle Scholar
  11. 11.
    Freeman JR, Chu S, Hsu T, Huang YT (2016) Epigenome-wide association study of smoking and DNA methylation in non-small cell lung neoplasms. Oncotarget 7(43):69579CrossRefGoogle Scholar
  12. 12.
    Weisenberger DJ, Levine AJ, Long TI et al (2015) Association of the colorectal CpG island methylator phenotype with molecular features, risk factors, and family history. Cancer Epidemiol Biomark Prev 24:512–519CrossRefGoogle Scholar
  13. 13.
    Limsui D, Vierkant RA, Tillmans LS et al (2010) Cigarette smoking and colorectal cancer risk by molecularly defined subtypes. J Natl Cancer Inst 102:1012–1022CrossRefGoogle Scholar
  14. 14.
    Shui IM, Wong CJ, Zhao S et al (2016) Prostate tumor DNA methylation is associated with cigarette smoking and adverse prostate cancer outcomes. Cancer 122:2168–2177CrossRefGoogle Scholar
  15. 15.
    Reynolds LM, Magid HS, Chi GC et al (2016) Secondhand tobacco smoke exposure associations with DNA methylation of the aryl hydrocarbon receptor repressor. Nicot Tob Res 19:442–451Google Scholar
  16. 16.
    Scesnaite A, Jarmalaite S, Mutanen P et al (2012) Similar DNA methylation pattern in lung tumours from smokers and never-smokers with second-hand tobacco smoke exposure. Mutagenesis 27:423–429CrossRefGoogle Scholar
  17. 17.
    Ambatipudi S, Cuenin C, Hernandez-Vargas H et al (2016) Tobacco smoking-associated genome-wide DNA methylation changes in the EPIC study. Epigenomics 8:599–618CrossRefGoogle Scholar
  18. 18.
    Ivorra C, Fraga MF, Bayon GF et al (2015) DNA methylation patterns in newborns exposed to tobacco in utero. J Trans Med 13:25CrossRefGoogle Scholar
  19. 19.
    Rzehak P, Saffery R, Reischl E et al (2016) Maternal smoking during pregnancy and DNA-methylation in children at age 5.5 years: epigenome-wide-analysis in the European Childhood Obesity Project (CHOP)-Study. PLoS ONE 11:e0155554CrossRefGoogle Scholar
  20. 20.
    Ladd-Acosta C, Shu C, Lee BK et al (2016) Presence of an epigenetic signature of prenatal cigarette smoke exposure in childhood. Environ Res 144:139–148CrossRefGoogle Scholar
  21. 21.
    Lee KW, Richmond R, Hu P et al (2015) Prenatal exposure to maternal cigarette smoking and DNA methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ Health Pers 123:193–199CrossRefGoogle Scholar
  22. 22.
    White AJ, Chen J, Teitelbaum SL et al (2016) Sources of polycyclic aromatic hydrocarbons are associated with gene-specific promoter methylation in women with breast cancer. Environ Res 145:93–100CrossRefGoogle Scholar
  23. 23.
    Pirouzpanah S, Taleban FA, Atri M, Abadi A-R, Mehdipour P (2010) The effect of modifiable potentials on hypermethylation status of retinoic acid receptor-beta2 and estrogen receptor-alpha genes in primary breast cancer. Cancer Causes Control 21:2101–2111CrossRefGoogle Scholar
  24. 24.
    Johnson KC, Koestler DC, Fleischer T et al (2015) DNA methylation in ductal carcinoma in situ related with future development of invasive breast cancer. Clin Epigen 7:015–0094CrossRefGoogle Scholar
  25. 25.
    Muggerud AA, Ronneberg JA, Warnberg F et al (2010) Frequent aberrant DNA methylation of ABCB1, FOXC1, PPP2R2B and PTEN in ductal carcinoma in situ and early invasive breast cancer. Breast Cancer Res 12:7CrossRefGoogle Scholar
  26. 26.
    Tao MH, Marian C, Shields PG et al (2013) Exposures in early life: associations with DNA promoter methylation in breast tumors. J Dev Orig Health Dis 4:182–190CrossRefGoogle Scholar
  27. 27.
    Bonner MR, Nie J, Han D et al (2005) Secondhand smoke exposure in early life and the risk of breast cancer among never smokers (United States). Cancer Causes Control 16:683–689CrossRefGoogle Scholar
  28. 28.
    Tao MH, Shields PG, Nie J et al (2009) DNA hypermethylation and clinicopathological features in breast cancer: the Western New York Exposures and Breast Cancer (WEB) Study. Breast Cancer Res Treat. 114: 559–568CrossRefGoogle Scholar
  29. 29.
    Callahan CL, Wang Y, Marian C et al (2016) DNA methylation and breast tumor clinicopathological features: The Western New York Exposures and Breast Cancer (WEB) study. Epigenetics. 11:1–10CrossRefGoogle Scholar
  30. 30.
    Xu X, Gammon MD, Jefferson E et al (2011) The influence of one-carbon metabolism on gene promoter methylation in a population-based breast cancer study. Epigenetics 6:1276–1283CrossRefGoogle Scholar
  31. 31.
    Feng W, Orlandi R, Zhao N et al (2010) Tumor suppressor genes are frequently methylated in lymph node metastases of breast cancers. BMC Cancer 10:1471–2407CrossRefGoogle Scholar
  32. 32.
    Jeong YJ, Jeong HY, Lee SM, Bong JG, Park SH, Oh HK (2013) Promoter methylation status of the FHIT gene and Fhit expression: association with HER2/neu status in breast cancer patients. Oncol Rep 30:2270–2278CrossRefGoogle Scholar
  33. 33.
    Marzese DM, Hoon DS, Chong KK et al (2012) DNA methylation index and methylation profile of invasive ductal breast tumors. J Mol Diagn 14:613–622CrossRefGoogle Scholar
  34. 34.
    Hsu NC, Huang YF, Yokoyama KK, Chu PY, Chen FM, Hou MF (2013) Methylation of BRCA1 promoter region is associated with unfavorable prognosis in women with early-stage breast cancer. PLoS ONE 8:6CrossRefGoogle Scholar
  35. 35.
    Klajic J, Fleischer T, Dejeux E et al (2013) Quantitative DNA methylation analyses reveal stage dependent DNA methylation and association to clinico-pathological factors in breast tumors. BMC Cancer 13:1471–2407CrossRefGoogle Scholar
  36. 36.
    Arai T, Miyoshi Y, Kim SJ, Taguchi T, Tamaki Y, Noguchi S (2006) Association of GSTP1 CpG islands hypermethylation with poor prognosis in human breast cancers. Breast Cancer Res Treat 100:169–176CrossRefGoogle Scholar
  37. 37.
    Zhang X, Shrikhande U, Alicie BM, Zhou Q, Geahlen RL (2009) Role of the protein tyrosine kinase Syk in regulating cell–cell adhesion and motility in breast cancer cells. Mol Cancer Res 7:634–644CrossRefGoogle Scholar
  38. 38.
    Cheol Kim D, Thorat MA, Lee MR et al (2012) Quantitative DNA methylation and recurrence of breast cancer: a study of 30 candidate genes. Cancer Biomark 11:75–88CrossRefGoogle Scholar
  39. 39.
    Tao MH, Marian C, Nie J et al (2011) Body mass and DNA promoter methylation in breast tumors in the Western New York Exposures and Breast Cancer Study. Am J Clin Nutr 94:831–838CrossRefGoogle Scholar
  40. 40.
    Tao MH, Marian C, Shields PG et al (2011) Alcohol consumption in relation to aberrant DNA methylation in breast tumors. Alcohol. 45:689–699CrossRefGoogle Scholar
  41. 41.
    Zeilinger S, Kühnel B, Klopp N et al (2013) Tobacco Smoking Leads to Extensive Genome-Wide Changes in DNA Methylation. PLoS ONE 8:e63812CrossRefGoogle Scholar
  42. 42.
    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 Genom 15:151CrossRefGoogle Scholar
  43. 43.
    Gao X, Jia M, Zhang Y, Breitling LP, Brenner H (2015) DNA methylation changes of whole blood cells in response to active smoking exposure in adults: a systematic review of DNA methylation studies. Clin Epigenet 7:113CrossRefGoogle Scholar
  44. 44.
    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 Persp 120:1425–1431CrossRefGoogle Scholar
  45. 45.
    Sadikovic B, Rodenhiser DI (2006) Benzopyrene exposure disrupts DNA methylation and growth dynamics in breast cancer cells. Toxicol Appl Pharmacol. 216:458–468CrossRefGoogle Scholar
  46. 46.
    Peplonska B, Bukowska A, Wieczorek E, Przybek M, Zienolddiny S, Reszka E (2017) Rotating night work, lifestyle factors, obesity and promoter methylation in BRCA1 and BRCA2 genes among nurses and midwives. PLoS One 12:e0178792CrossRefGoogle Scholar
  47. 47.
    Kim H, Kwon YM, Kim JS et al (2004) Tumor-specific methylation in bronchial lavage for the early detection of non-small-cell lung cancer. J Clin Oncol 22:2363–2370CrossRefGoogle Scholar
  48. 48.
    D’Agostini F, Izzotti A, Balansky R, Zanesi N, Croce CM, De Flora S (2006) Early loss of Fhit in the respiratory tract of rodents exposed to environmental cigarette smoke. Cancer Res 66:3936–3941CrossRefGoogle Scholar
  49. 49.
    Savitz DA, Olshan AF (1995) Multiple comparisons and related issues in the interpretation of epidemiologic data. Am J Epidemiol 142:904–908CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2019

Authors and Affiliations

  • Catherine L. Callahan
    • 1
    • 2
    Email author
  • Matthew R. Bonner
    • 2
  • Jing Nie
    • 2
  • Youjin Wang
    • 2
    • 3
  • Meng-Hua Tao
    • 4
  • Peter G. Shields
    • 5
  • Catalin Marian
    • 5
    • 6
  • Kevin H. Eng
    • 7
  • Maurizio Trevisan
    • 8
  • Jo L. Freudenheim
    • 2
  1. 1.Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and GeneticsNational Cancer InstituteBethesdaUSA
  2. 2.Department of Epidemiology and Environmental Health, School of Public Health and Health ProfessionsUniversity at BuffaloBuffaloUSA
  3. 3.Clinical Genetics Branch, Division of Cancer Epidemiology and GeneticsNational Cancer InstituteBethesdaUSA
  4. 4.Department of Biostatistics and EpidemiologyUniversity of North Texas Health Science CenterFort WorthUSA
  5. 5.Division of Cancer Prevention and ControlCollege of Medicine and The Ohio State University Comprehensive Cancer CenterColumbusUSA
  6. 6.Department of Biochemistry and PharmacologyUniversity of Medicine and Pharmacy TimisoaraTimisoaraRomania
  7. 7.Department of Biostatistics and BioinformaticsRoswell Park Cancer InstituteBuffaloUSA
  8. 8.City College of New YorkNew YorkUSA

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