Associations of self-reported smoking, cotinine levels and epigenetic smoking indicators with oxidative stress among older adults: a population-based study

European Journal of Epidemiology

Volumn 32, Issue 5, 2017, Pages 443-456

  Gao, Xu ^a   Gào, Xīn ^a,b   Zhang, Yan ^a   Breitling, Lutz Philipp ^a   Schöttker, Ben ^a,b,c   Brenner, Hermann ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c FOM UNIVERSITY OF APPLIED SCIENCES   (Germany)

Author keywords

Aging; Cotinine levels; Epigenetic epidemiology; Oxidative stress; Smoking methylation; Whole blood samples

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; 8 ISOPROSTANE; COTININE; DNA; 8-EPI-PROSTAGLANDIN F2ALPHA; 8-OXO-7-HYDRODEOXYGUANOSINE; BIOLOGICAL MARKER; DEOXYGUANOSINE; PROSTAGLANDIN F2 ALPHA;

ADULT; AGED; ARTICLE; BLOOD SAMPLING; DNA METHYLATION; DRINKING BEHAVIOR; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; FEMALE; GERMANY; HUMAN; LIFESTYLE; MALE; OBESITY; OXIDATIVE STRESS; PHYSICAL ACTIVITY; SELF REPORT; SMOKING; SMOKING CESSATION; URINE LEVEL; AGING; ANALOGS AND DERIVATIVES; BLOOD; EPIDEMIOLOGY; GENETICS; MIDDLE AGED; URINE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; AGING; BIOMARKERS; COTININE; DEOXYGUANOSINE; DINOPROST; DNA; DNA METHYLATION; EPIGENOMICS; FEMALE; GERMANY; HUMANS; MALE; MIDDLE AGED; OXIDATIVE STRESS; SELF REPORT; SMOKING;

EID: 85018801812     PISSN: 03932990     EISSN: 15737284     Source Type: Journal    
DOI: 10.1007/s10654-017-0248-9     Document Type: Article

References (49)

1. Salminen A, Ojala J, Kaarniranta K, Kauppinen A. Mitochondrial dysfunction and oxidative stress activate inflammasomes: impact on the aging process and age-related diseases. Cell Mol Life Sci. 2012;69(18):2999–3013. doi:10.1007/s00018-012-0962-0.
2. Salmon AB, Richardson A, Perez VI. Update on the oxidative stress theory of aging: does oxidative stress play a role in aging or healthy aging? Free Radic Biol Med. 2010;48(5):642–55. doi:10.1016/j.freeradbiomed.2009.12.015.
3. Schöttker B, Saum KU, Jansen EH, et al. Oxidative stress markers and all-cause mortality at older age: a population-based cohort study. J Gerontol A Biol Sci Med Sci. 2015;70(4):518–24. doi:10.1093/gerona/glu111.
4. Schöttker B, Brenner H, Jansen EH, et al. Evidence for the free radical/oxidative stress theory of ageing from the CHANCES consortium: a meta-analysis of individual participant data. BMC Med. 2015;13(1):300. doi:10.1186/s12916-015-0537-7.
5. Pandey KB, Rizvi SI. Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxid Med Cell Longev. 2010;3(1):2–12. doi:10.4161/oxim.3.1.10476.
6. Stephens JW, Khanolkar MP, Bain SC. The biological relevance and measurement of plasma markers of oxidative stress in diabetes and cardiovascular disease. Atherosclerosis. 2009;202(2):321–9. doi:10.1016/j.atherosclerosis.2008.06.006.
7. Kotani K, Sakane N. C-reactive protein and reactive oxygen metabolites in subjects with metabolic syndrome. J Int Med Res. 2012;40(3):1074–81.
8. Jones DP. Radical-free biology of oxidative stress. Am J Physiol Cell Physiol. 2008;295(4):C849–68. doi:10.1152/ajpcell.00283.2008.
9. Montuschi P, Collins JV, Ciabattoni G, et al. Exhaled 8-isoprostane as an in vivo biomarker of lung oxidative stress in patients with COPD and healthy smokers. Am J Respir Crit Care Med. 2000;162(3 Pt 1):1175–7. doi:10.1164/ajrccm.162.3.2001063.
10. Kinnula VL, Ilumets H, Myllarniemi M, Sovijarvi A, Rytila P. 8-Isoprostane as a marker of oxidative stress in nonsymptomatic cigarette smokers and COPD. Eur Respir J. 2007;29(1):51–5. doi:10.1183/09031936.00023606.
11. Valavanidis A, Vlachogianni T, Fiotakis C. 8-hydroxy-2′-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2009;27(2):120–39. doi:10.1080/10590500902885684.
12. Babizhayev MA, Yegorov YE. Smoking and health: association between telomere length and factors impacting on human disease, quality of life and life span in a large population-based cohort under the effect of smoking duration. Fundam Clin Pharmacol. 2011;25(4):425–42. doi:10.1111/j.1472-8206.2010.00866.x.
13. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med. 2006;3(11):e442. doi:10.1371/journal.pmed.0030442.
14. Csiszar A, Podlutsky A, Wolin MS, Losonczy G, Pacher P, Ungvari Z. Oxidative stress and accelerated vascular aging: implications for cigarette smoking. Front Biosci (Landmark Ed). 2009;14:3128–44.
15. Thorne D, Wilson J, Kumaravel TS, Massey ED, McEwan M. Measurement of oxidative DNA damage induced by mainstream cigarette smoke in cultured NCI-H292 human pulmonary carcinoma cells. Mutat Res. 2009;673(1):3–8. doi:10.1016/j.mrgentox.2008.11.008.
16. Jansen EH, Beekhof P, Ruskovska T. The effect of smoking on biomarkers of (anti) oxidant status. J Mol Biomark Diagn. 2014;5(6):207–210.
17. Ellegaard PK, Poulsen HE. Tobacco smoking and oxidative stress to DNA: a meta-analysis of studies using chromatographic and immunological methods. Scand J Clin Lab Invest. 2016;76(2):151–8. doi:10.3109/00365513.2015.1127407.
18. Philibert RA, Beach SR, Brody GH. The DNA methylation signature of smoking: an archetype for the identification of biomarkers for behavioral illness. Neb Symp Motiv. 2014;61:109–27.
19. Lee KW, Pausova Z. Cigarette smoking and DNA methylation. Front Genet. 2013;4:132. doi:10.3389/fgene.2013.00132.
20. Philibert RA, Beach SR, Lei MK, Brody GH. Changes in DNA methylation at the aryl hydrocarbon receptor repressor may be a new biomarker for smoking. Clin Epigenetics. 2013;5(1):19. doi:10.1186/1868-7083-5-19.
21. Zeilinger S, Kuhnel B, Klopp N, et al. Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS ONE. 2013;8(5):e63812. doi:10.1371/journal.pone.0063812.
22. Breitling LP, Yang R, Korn B, Burwinkel B, Brenner H. Tobacco-smoking-related differential DNA methylation: 27 K discovery and replication. Am J Hum Genet. 2011;88(4):450–7. doi:10.1016/j.ajhg.2011.03.003.
23. Gao X, Jia M, Zhang Y, Breitling LP, Brenner H. DNA methylation changes of whole blood cells in response to active smoking exposure in adults: a systematic review of DNA methylation studies. Clin Epigenetics. 2015;7(1):113. doi:10.1186/s13148-015-0148-3.
24. Teschendorff AE, Yang Z, Wong A, et al. Correlation of smoking-associated DNA methylation changes in buccal cells With DNA methylation changes in epithelial cancer. JAMA Oncol. 2015;1(4):476–85. doi:10.1001/jamaoncol.2015.1053.
25. Connor Gorber S, Schofield-Hurwitz S, Hardt J, Levasseur G, Tremblay M. The accuracy of self-reported smoking: a systematic review of the relationship between self-reported and cotinine-assessed smoking status. Nicotine Tob Res. 2009;11(1):12–24. doi:10.1093/ntr/ntn010.
26. Schottker B, Haug U, Schomburg L, et al. Strong associations of 25-hydroxyvitamin D concentrations with all-cause, cardiovascular, cancer, and respiratory disease mortality in a large cohort study. Am J Clin Nutr. 2013;97(4):782–93. doi:10.3945/ajcn.112.047712.
27. Gao X, Mons U, Zhang Y, Breitling LP, Brenner H. DNA methylation changes in response to active smoking exposure are associated with leukocyte telomere length among older adults. Eur J Epidemiol. 2016;31(12):1231–41. doi:10.1007/s10654-016-0210-2.
28. Gao X, Zhang Y, Saum KU, Schottker B, Breitling LP, Brenner H. Tobacco smoking and smoking-related DNA methylation are associated with the development of frailty among older adults. Epigenetics. 2017;12(2):149–56. doi:10.1080/15592294.2016.1271855.
29. Zhang Y, Florath I, Saum KU, Brenner H. Self-reported smoking, serum cotinine, and blood DNA methylation. Environ Res. 2016;146:395–403. doi:10.1016/j.envres.2016.01.026.
30. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16(3):1215.
31. Florath I, Butterbach K, Heiss J, et al. Type 2 diabetes and leucocyte DNA methylation: an epigenome-wide association study in over 1,500 older adults. Diabetologia. 2015;59(1):130–8. doi:10.1007/s00125-015-3773-7.
32. Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics. 2012;13:86. doi:10.1186/1471-2105-13-86.
33. Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995;57(1):289–300.
34. Desquilbet L, Mariotti F. Dose-response analyses using restricted cubic spline functions in public health research. Stat Med. 2010;29(9):1037–57. doi:10.1002/sim.3841.
35. Montuschi P, Corradi M, Ciabattoni G, Nightingale J, Kharitonov SA, Barnes PJ. Increased 8-isoprostane, a marker of oxidative stress, in exhaled condensate of asthma patients. Am J Respir Crit Care Med. 1999;160(1):216–20. doi:10.1164/ajrccm.160.1.9809140.
36. Zhang Y, Yang R, Burwinkel B, Breitling LP, Brenner H. F2RL3 methylation as a biomarker of current and lifetime smoking exposures. Environ Health Perspect. 2014;122(2):131–7. doi:10.1289/ehp.1306937.
37. Vassalle C, Botto N, Andreassi MG, Berti S, Biagini A. Evidence for enhanced 8-isoprostane plasma levels, as index of oxidative stress in vivo, in patients with coronary artery disease. Coron Artery Dis. 2003;14(3):213–8. doi:10.1097/01.mca.0000063504.13456.c3.
38. Monnier L, Mas E, Ginet C, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295(14):1681–7. doi:10.1001/jama.295.14.1681.
39. Gao T, Joyce BT, Liu L, et al. DNA methylation of oxidative stress genes and cancer risk in the normative aging study. Am J Cancer Res. 2016;6(2):553–61.
40. Schöttker B, Zhang Y, Heiss JA, et al. Discovery of a novel epigenetic cancer marker related to the oxidative status of human blood. Genes Chromosomes Cancer. 2015;54(9):583–94. doi:10.1002/gcc.22271.
41. Roh SA, Park IJ, Yoon YS, et al. Feasibility of novel PPP1R15A and proposed ANXA11 single nucleotide polymorphisms as predictive markers for bevacizumab regimen in metastatic colorectal cancer. J Cancer Res Clin Oncol. 2016;142(8):1705–14. doi:10.1007/s00432-016-2177-5.
42. Berndt SI, Camp NJ, Skibola CF, et al. Meta-analysis of genome-wide association studies discovers multiple loci for chronic lymphocytic leukemia. Nat Commun. 2016;7:10933. doi:10.1038/ncomms10933.
43. Zhang Y, Schöttker B, Ordonez-Mena J, et al. F2RL3 methylation, lung cancer incidence and mortality. Int J Cancer. 2015;137(7):1739–48. doi:10.1002/ijc.29537.
44. Zhang Y, Yang R, Burwinkel B, et al. F2RL3 methylation in blood DNA is a strong predictor of mortality. Int J Epidemiol. 2014;43(4):1215–25. doi:10.1093/ije/dyu006.
45. Mulero J, Zafrilla P, Martinez-Cacha A. Oxidative stress, frailty and cognitive decline. J Nutr Health Aging. 2011;15(9):756–60. doi:10.1007/s12603-011-0130-5.
46. Chandrasekaran A, Idelchik MD, Melendez JA. Redox control of senescence and age-related disease. Redox Biol. 2016;11:91–102. doi:10.1016/j.redox.2016.11.005.
47. Gao X, Zhang Y, Breitling LP, Brenner H. Relationship of tobacco smoking and smoking-related DNA methylation with epigenetic age acceleration. Oncotarget. 2016;7(30):46878. doi:10.18632/oncotarget.9795.
48. Schwartz J, Weiss ST. Cigarette smoking and peripheral blood leukocyte differentials. Ann Epidemiol. 1994;4(3):236–42.
49. Gutierrez-Arcelus M, Lappalainen T, Montgomery SB, et al. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife. 2013;2:e00523. doi:10.7554/eLife.00523.