Tobacco smoking and smoking-related DNA methylation are associated with the development of frailty among older adults

Epigenetics

Volumn 12, Issue 2, 2017, Pages 149-156

  Gao, Xu ^a   Zhang, Yan ^a   Saum, Kai Uwe ^a   Schöttker, Ben ^a,b   Breitling, Lutz Philipp ^a   Brenner, Hermann ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Aging; epigenetic epidemiology; frailty; smoking methylation; whole blood sample

Indexed keywords

BIOLOGICAL MARKER; COTININE;

ADULT; AGED; ALPP GENE; ARTICLE; ASSESSMENT OF HUMANS; BLOOD LEVEL; CPG ISLAND; CPOX GENE; DNA METHYLATION; DNA METHYLATION ASSAY; EPIGENETICS; EXPOSURE; FEMALE; FRAILTY; FRAILTY INDEX; GENE; GENE LOCUS; GENE MAPPING; GENETIC ASSOCIATION; GERIATRIC ASSESSMENT; GERIATRIC DISORDER; GNG12 GENE; GPR15 GENE; HUMAN; MALE; MYO1G GENE; POLK GENE; SERUM COTININE LEVEL; SMOKING; SMOKING CESSATION; ADVERSE EFFECTS; AGING; CASE CONTROL STUDY; FRAIL ELDERLY; GENETICS; GERMANY; MIDDLE AGED; PATHOLOGY;

AGED; AGING; CASE-CONTROL STUDIES; CPG ISLANDS; DNA METHYLATION; FEMALE; FRAIL ELDERLY; GERMANY; HUMANS; MALE; MIDDLE AGED; SMOKING;

EID: 85011290091     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2016.1271855     Document Type: Article

References (57)

1. Mitnitski AB, Mogilner AJ, Rockwood K. Accumulation of deficits as a proxy measure of aging. Scientific World J 2001; 1:323-36; PMID:12806071; http://dx.doi.org/10.1100/tsw.2001.58
2. Bergman H, Ferrucci L, Guralnik J, Hogan DB, Hummel S, Karunananthan S, Wolfson C. Frailty:an emerging research and clinical paradigm—issues and controversies. J Gerontol A Biol Sci Med Sci 2007; 62:731-7; PMID:17634320; http://dx.doi.org/10.1093/gerona/62.7.731
3. Kim S, Jazwinski SM. Quantitative measures of healthy aging and biological age. Healthy aging research 2015; 4:26; PMID:26005669; http://dx.doi.org/10.12715/har.2015.4.26.
4. Saum KU, Dieffenbach AK, Muller H, Holleczek B, Hauer K, Brenner H. Frailty prevalence and 10-year survival in community-dwelling older adults:results from the ESTHER cohort study. Eur J Epidemiol 2014; 29:171-9; PMID:24671603; http://dx.doi.org/10.1007/s10654-014-9891-6
5. Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. The Lancet 2013; 381:752-62; PMID:23395245; http://dx.doi.org/10.1016/S0140-6736(12)62167-9
6. Kulmala J, Nykanen I, Hartikainen S. Frailty as a predictor of all-cause mortality in older men and women. Geriatr Gerontol Int 2014; 14:899-905; PMID:24666801; http://dx.doi.org/10.1111/ggi.12190
7. Searle SD, Mitnitski A, Gahbauer EA, Gill TM, Rockwood K. A standard procedure for creating a frailty index. BMC Geriatr 2008; 8:24; PMID:18826625; http://dx.doi.org/10.1186/1471-2318-8-24
8. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G. Frailty in older adults evidence for a phenotype. J Gerontol A Biol Sci Med Sci 2001; 56:M146-M57; PMID:11253156; http://dx.doi.org/10.1093/gerona/56.3.M146
9. Mathers CD, Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 2006; 3:e442; PMID:17132052; http://dx.doi.org/10.1371/journal.pmed.0030442
10. Hubbard R, Searle S, Mitnitski A, Rockwood K. Effect of smoking on the accumulation of deficits, frailty and survival in older adults:a secondary analysis from the Canadian Study of Health and Aging. J Nutr Health Aging 2009; 13:468-72; http://dx.doi.org/10.1007/s12603-009-0085-y
11. Romero‐Ortuno R. Frailty Index in Europeans:association with determinants of health. Geriatr Gerontol Int 2014; 14:420-9; PMID:23879634; http://dx.doi.org/10.1111/ggi.12122
12. Gale CR, Cooper C, Deary IJ, Sayer AA. Psychological well-being and incident frailty in men and women:the English Longitudinal Study of Ageing. Psychol Med 2014; 44:697-706; PMID:23822897; http://dx.doi.org/10.1017/S0033291713001384
13. Lee JS, Auyeung T-W, Leung J, Kwok T, Woo J. Transitions in frailty states among community-living older adults and their associated factors. J Am Med Dir Assoc 2014; 15:281-6; PMID:24534517; http://dx.doi.org/10.1016/j.jamda.2013.12.002
14. Etman A, Kamphuis CB, Van der Cammen TJ, Burdorf A, Van Lenthe FJ. Do lifestyle, health and social participation mediate educational inequalities in frailty worsening? Eur J Public Health 2015; 25:345-50; PMID:25061232; http://dx.doi.org/10.1093/eurpub/cku093
15. Kojima G, Iliffe S, Walters K. Smoking as a predictor of frailty:a systematic review. BMC Geriatr 2015; 15:131; PMID:26489757; http://dx.doi.org/10.1186/s12877-015-0134-9
16. Gale CR, Baylis D, Cooper C, Sayer AA. Inflammatory markers and incident frailty in men and women:the English Longitudinal Study of Ageing. Age 2013; 35:2493-501; PMID:23543263; http://dx.doi.org/10.1007/s11357-013-9528-9
17. Puts MT, Visser M, Twisk JW, Deeg DJ, Lips P. Endocrine and inflammatory markers as predictors of frailty. Clin Endocrinol 2005; 63:403-11; PMID:16181232; http://dx.doi.org/10.1111/j.1365-2265.2005.02355.x
18. Lee KW, Pausova Z. Cigarette smoking and DNA methylation. Front Genet 2013; 4:132; PMID:23882278; http://dx.doi.org/10.3389/fgene.2013.00132
19. Philibert RA, Beach SR, Brody GH. The DNA methylation signature of smoking:an archetype for the identification of biomarkers for behavioral illness. Nebr Symp Motiv 2014; 61:109-27; PMID:25306781; http://dx.doi.org/10.1007/978-1-4939-0653-6_6
20. Shenker NS, Ueland PM, Polidoro S, van Veldhoven K, Ricceri F, Brown R, Flanagan JM, Vineis P. DNA methylation as a long-term biomarker of exposure to tobacco smoke. Epidemiology 2013; 24:712-6; PMID:23867811; http://dx.doi.org/10.1097/EDE.0b013e31829d5cb3
21. 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; 122:131-7; PMID:24273234; http://dx.doi.org/10.1289/ehp.1306937
22. Philibert R, Hollenbeck N, Andersen E, McElroy S, Wilson S, Vercande K, Beach SR, Osborn T, Gerrard M, Gibbons FX, et al. Reversion of AHRR Demethylation Is a Quantitative Biomarker of Smoking Cessation. Front Psychiatry 2016; 7:55; PMID:27092088; http://dx.doi.org/10.3389/fpsyt.2016.00055
23. Breitling LP, Salzmann K, Rothenbacher D, Burwinkel B, Brenner H. Smoking, F2RL3 methylation, and prognosis in stable coronary heart disease. Eur Heart J 2012; 33:2841-8; PMID:22511653; http://dx.doi.org/10.1093/eurheartj/ehs091
24. Zhang Y, Schöttker B, Ordonez-Mena J, Holleczek B, Yang R, Burwinkel B, Butterbach K, Brenner H. F2RL3 methylation, lung cancer incidence and mortality. Int J Cancer 2015; 137:1739-48; PMID:25821117; http://dx.doi.org/10.1002/ijc.29537
25. Teschendorff AE, Yang Z, Wong A, Pipinikas CP, Jiao Y, Jones A, Anjum S, Hardy R, Salvesen HB, Thirlwell C, et al. Correlation of Smoking-Associated DNA Methylation Changes in Buccal Cells With DNA Methylation Changes in Epithelial Cancer. JAMA Oncol 2015; 1:476-85; PMID:26181258; http://dx.doi.org/10.1001/jamaoncol.2015.1053
26. 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; 7:113; PMID:26478754; http://dx.doi.org/10.1186/s13148-015-0148-3
27. Fugate Woods N, LaCroix AZ, Gray SL, Aragaki A, Cochrane BB, Brunner RL, Masaki K, Murray A, Newman AB. Frailty:emergence and consequences in women aged 65 and older in the Women's Health Initiative Observational Study. J Am Geriatr Soc 2005; 53:1321-30; PMID:16078957; http://dx.doi.org/10.1111/j.1532-5415.2005.53405.x
28. Zhang Y, Florath I, Saum KU, Brenner H. Self-reported smoking, serum cotinine, and blood DNA methylation. Environ Res 2016; 146:395-403; PMID:26826776; http://dx.doi.org/10.1016/j.envres.2016.01.026
29. Tsaprouni LG, Yang TP, Bell J, Dick KJ, Kanoni S, Nisbet J, Vinuela A, Grundberg E, Nelson CP, Meduri E, et al. Cigarette smoking reduces DNA methylation levels at multiple genomic loci but the effect is partially reversible upon cessation. Epigenetics 2014; 9:1382-96; PMID:25424692; http://dx.doi.org/10.4161/15592294.2014.969637
30. Collerton J, Gautrey HE, van Otterdijk SD, Davies K, Martin-Ruiz C, von Zglinicki T, Kirkwood TB, Jagger C, Mathers JC, Strathdee G. Acquisition of aberrant DNA methylation is associated with frailty in the very old:findings from the Newcastle 85+ Study. Biogerontology 2014; 15:317-28; PMID:24770842; http://dx.doi.org/10.1007/s10522-014-9500-9
31. Bellizzi D, D'Aquila P, Montesanto A, Corsonello A, Mari V, Mazzei B, Lattanzio F, Passarino G. Global DNA methylation in old subjects is correlated with frailty. Age 2012; 34:169-79; PMID:21336567; http://dx.doi.org/10.1007/s11357-011-9216-6
32. Gerard A, Patino-Lopez G, Beemiller P, Nambiar R, Ben-Aissa K, Liu Y, Totah FJ, Tyska MJ, Shaw S, Krummel MF. Detection of rare antigen-presenting cells through T cell-intrinsic meandering motility, mediated by Myo1g. Cell 2014; 158:492-505; PMID:25083865; http://dx.doi.org/10.1016/j.cell.2014.05.044
33. Koks G, Uudelepp ML, Limbach M, Peterson P, Reimann E, Koks S. Smoking-Induced Expression of the GPR15 Gene Indicates Its Potential Role in the Chronic Inflammatory Pathologies. Am J Pathol 2015; 185:2898-2906; PMID:26348578; http://dx.doi.org/10.1016/j.ajpath.2015.07.006
34. Larson KC, Lipko M, Dabrowski M, Draper MP. Gng12 is a novel negative regulator of LPS-induced inflammation in the microglial cell line BV-2. Inflamm Res 2010; 59:15-22; PMID:19568691; http://dx.doi.org/10.1007/s00011-009-0062-2
35. Zhang Y, Breitling LP, Balavarca Y, Holleczek B, Schöttker B, Brenner H. Comparison and combination of blood DNA methylation at smoking-associated genes and at lung cancer-related genes in prediction of lung cancer mortality. Int J Cancer 2016; 139:2482-92; PMID:27503000; http://dx.doi.org/10.1002/ijc.30374
36. Dai ZJ, Liu XH, Ma YF, Kang HF, Jin TB, Dai ZM, Guan HT, Wang M, Liu K, Dai C, et al. Association Between Single Nucleotide Polymorphisms in DNA Polymerase Kappa Gene and Breast Cancer Risk in Chinese Han Population:A STROBE-Compliant Observational Study. Medicine (Baltimore) 2016; 95:e2466; PMID:26765445; http://dx.doi.org/10.1097/MD.0000000000002466
37. Yadav S, Mukhopadhyay S, Anbalagan M, Makridakis N. Somatic Mutations in Catalytic Core of POLK Reported in Prostate Cancer Alter Translesion DNA Synthesis. Hum Mutat 2015; 36:873-80; PMID:26046662; http://dx.doi.org/10.1002/humu.22820
38. Michiels S, Danoy P, Dessen P, Bera A, Boulet T, Bouchardy C, Lathrop M, Sarasin A, Benhamou S. Polymorphism discovery in 62 DNA repair genes and haplotype associations with risks for lung and head and neck cancers. Carcinogenesis 2007; 28:1731-9; PMID:17494052; http://dx.doi.org/10.1093/carcin/bgm111
39. Ravenni N, Weber M, Neri D. A human monoclonal antibody specific to placental alkaline phosphatase, a marker of ovarian cancer. MAbs 2014; 6:86-94; PMID:24247025; http://dx.doi.org/10.4161/mabs.27230
40. Benton MC, Johnstone A, Eccles D, Harmon B, Hayes MT, Lea RA, Griffiths L, Hoffman EP, Stubbs RS, Macartney-Coxson D. An analysis of DNA methylation in human adipose tissue reveals differential modification of obesity genes before and after gastric bypass and weight loss. Genome Biol 2015; 16:1; PMID:25583448; http://dx.doi.org/10.1186/s13059-014-0569-x
41. Hubbard RE, Lang IA, Llewellyn DJ, Rockwood K. Frailty, body mass index, and abdominal obesity in older people. J Gerontol A Biol Sci Med Sci 2010; 65:377-81; PMID:19942592; http://dx.doi.org/10.1093/gerona/glp186
42. Fulop T, Larbi A, Witkowski JM, McElhaney J, Loeb M, Mitnitski A, Pawelec G. Aging, frailty and age-related diseases. Biogerontology 2010; 11:547-63; PMID:20559726; http://dx.doi.org/10.1007/s10522-010-9287-2
43. Saum KU, Dieffenbach AK, Muezzinler A, Muller H, Holleczek B, Stegmaier C, Butterbach K, Schick M, Canzian F, Stammer H, et al. Frailty and telomere length:cross-sectional analysis in 3537 older adults from the ESTHER cohort. Exp Gerontol 2014; 58:250-5; PMID:25150678; http://dx.doi.org/10.1016/j.exger.2014.08.009
44. Woo J, Tang NL, Suen E, Leung JC, Leung PC. Telomeres and frailty. Mech Ageing Dev 2008; 129:642-8; PMID:18809425; http://dx.doi.org/10.1016/j.mad.2008.08.003
45. Breitling LP, Saum KU, Perna L, Schöttker B, Holleczek B, Brenner H. Frailty is associated with the epigenetic clock but not with telomere length in a German cohort. Clin Epigenetics 2016; 8:21; PMID:26925173; http://dx.doi.org/10.1186/s13148-016-0186-5
46. Marioni RE, Shah S, McRae AF, Ritchie SJ, Muniz-Terrera G, Harris SE, Gibson J, Redmond P, Cox SR, Pattie A, et al. The epigenetic clock is correlated with physical and cognitive fitness in the Lothian Birth Cohort 1936. Int J Epidemiol 2015; 44:1388-96; PMID:25617346; http://dx.doi.org/10.1093/ije/dyu277
47. Gao X, Zhang Y, Breitling LP, Brenner H. Relationship of tobacco smoking and smoking-related DNA methylation with epigenetic age acceleration. Oncotarget 2016; PMID:27276709; http://dx.doi.org/10.18632/oncotarget.9795
48. Schwartz J, Weiss ST. Cigarette smoking and peripheral blood leukocyte differentials. Ann Epidemiol 1994; 4:236-42; PMID:8055125; http://dx.doi.org/10.1016/1047-2797(94)90102-3
49. Houseman EA, Accomando WP, Koestler DC, Christensen BC, Marsit CJ, Nelson HH, Wiencke JK, Kelsey KT. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinformatics 2012; 13:86; PMID:22568884; http://dx.doi.org/10.1186/1471-2105-13-86
50. Gutierrez-Arcelus M, Lappalainen T, Montgomery SB, Buil A, Ongen H, Yurovsky A, Bryois J, Giger T, Romano L, Planchon A. Passive and active DNA methylation and the interplay with genetic variation in gene regulation. Elife 2013; 2:e00523; PMID:23755361; http://dx.doi.org/10.7554/eLife.00523
51. Davey Smith G, Hemani G. Mendelian randomization:genetic anchors for causal inference in epidemiological studies. Hum Mol Genet 2014; 23:R89-98; PMID:25064373; http://dx.doi.org/10.1093/hmg/ddu328
52. Schöttker B, Haug U, Schomburg L, Kohrle J, Perna L, Muller H, Holleczek B, Brenner H. 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; 97:782-93; PMID:23446902; http://dx.doi.org/10.3945/ajcn.112.047712
53. 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; 31:1231-1241; PMID:27832427; http://dx.doi.org/10.1007/s10654-016-0210-2
54. Gao X, Zhang Y, Breitling LP, Brenner H. Tobacco smoking and methylation of genes related to lung cancer development. Oncotarget 2016; 7:59017; PMID:27323854; http://dx.doi.org/10.18632/oncotarget.10007
55. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 1988; 16:1215; PMID:3344216; http://dx.doi.org/10.1093/nar/16.3.1215
56. Florath I, Butterbach K, Heiss J, Bewerunge-Hudler M, Zhang Y, Schöttker B, Brenner H. Type 2 diabetes and leucocyte DNA methylation:an epigenome-wide association study in over 1,500 older adults. Diabetologia 2015; 59:130-8; PMID:26433941; http://dx.doi.org/10.1007/s00125-015-3773-7
57. 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; 57:289-300.