DNA methylation-based measures of biological age: Meta-analysis predicting time to death

Aging

Volumn 8, Issue 9, 2016, Pages 1844-1865

  Chen, Brian H ^a,b,c   Marioni, Riccardo E ^d,e   Colicino, Elena ^f   Peters, Marjolein J ^g   Ward Caviness, Cavin K ^h   Tsai, Pei Chien ⁱ   Roetker, Nicholas S ^j   Just, Allan C ^f   Demerath, Ellen W ^j   Guan, Weihua ^k   Bressler, Jan ^l   Fornage, Myriam ^l,m   Studenski, Stephanie ^a   Vandiver, Amy R ⁿ   Moore, Ann Zenobia ^a   Tanaka, Toshiko ^a   Kiel, Douglas P ^o,p   Liang, Liming ^q   Vokonas, Pantel ^q   Schwartz, Joel ^q   Lunetta, Kathryn L ^b,r   Murabito, Joanne M ^b,s   Bandinelli, Stefania ^t   Hernandez, Dena G ^a   Melzer, David ^u   Nalls, Michael ^a   Pilling, Luke C ^u   Price, Timothy R ^a   Singleton, Andrew B ^a   Gieger, Christian ^h   Holle, Rolf ^h   Kretschmer, Anja ^h   Kronenberg, Florian ^v   Kunze, Sonja ^h   Linseisen, Jakob ^h   Meisinger, Christine ^h   Rathmann, Wolfgang ^w   Waldenberger, Melanie ^h   Visscher, Peter M ^d,e   Shah, Sonia ^e   Wray, Naomi R ^e   McRae, Allan F ^e   Franco, Oscar H ^g   Hofman, Albert ^g,q   Uitterlinden, André G ^g   Absher, Devin ^x   Assimes, Themistocles ^y   Levine, Morgan E ^z   Lu, Ake T ^z   Tsao, Philip S ^y,aa   Hou, Lifang ^ab   Manson, JoAnn E ^ac   Carty, Cara L ^ad   LaCroix, Andrea Z ^ae   Reiner, Alexander P ^af,ag   Spector, Tim D ⁱ   Feinberg, Andrew P ^n,ah   Levy, Daniel ^b,c   Baccarelli, Andrea ^f,q   Meurs, Joyce van ^g   Bell, Jordana T ⁱ   Peters, Annette ^h   Deary, Ian J ^d   Pankow, James S ^j   Ferrucci, Luigi ^a   Horvath, Steve ^z,ai   more..

^a NATIONAL INSTITUTE ON AGING   (United States)

^b FRAMINGHAM HEART STUDY   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f Department of Medicine   (United States)

^g ERASMUS MEDICAL CENTER   (Netherlands)

^h INSTITUTE OF EPIDEMIOLOGY   (Germany)

ⁱ KING'S COLLEGE LONDON   (United Kingdom)

^j UNIVERSITY OF MINNESOTA   (United States)

^k UNIVERSITY OF MINNESOTA   (United States)

^l UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^m BAYLOR COLLEGE OF MEDICINE   (United States)

ⁿ JOHNS HOPKINS UNIVERSITY   (United States)

^o HARVARD MEDICAL SCHOOL   (United States)

^p Hebrew Senior Life   (United States)

^q HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^r BOSTON UNIVERSITY SCHOOL OF PUBLIC HEALTH   (United States)

^s BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^t Medical Physics Unit   (Italy)

^u UNIVERSITY OF EXETER   (United Kingdom)

^v INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^w HEINRICH HEINE UNIVERSITY   (Germany)

^x HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^y STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^z UNIVERSITY OF CALIFORNIA   (United States)

^aa VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^ab NORTHWESTERN UNIVERSITY   (United States)

^ac BRIGHAM AND WOMEN S HOSPITAL   (United States)

^ad GEORGE WASHINGTON UNIVERSITY   (United States)

^ae UNIVERSITY OF CALIFORNIA   (United States)

^af UNIVERSITY OF WASHINGTON   (United States)

^ag Fred Hutchinson Cancer Research Center   (United States)

^ah JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^ai UNIVERSITY OF CALIFORNIA   (United States)

more..

Author keywords

All cause mortality; DNA methylation; Epigenetic clock; Epigenetics; Lifespan; Mortality

Indexed keywords

ACCELERATION; AFRICAN AMERICAN; AGE; BLOOD CELL COUNT; CAUCASIAN; CELL COMPOSITION; DEATH; DNA METHYLATION; EPIGENETICS; ETHNIC GROUP; HUMAN; LIFESPAN; META ANALYSIS; MORTALITY; RISK FACTOR; SAMPLE SIZE; STATISTICAL SIGNIFICANCE; AGING; ANCESTRY GROUP; FEMALE; GENETIC EPIGENESIS; GENETICS; MALE; PHYSIOLOGY; STATISTICAL MODEL; SURVIVAL ANALYSIS; T LYMPHOCYTE SUBPOPULATION;

AGING; CONTINENTAL POPULATION GROUPS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; HUMANS; LOGISTIC MODELS; MALE; MORTALITY; RISK FACTORS; SURVIVAL ANALYSIS; T-LYMPHOCYTE SUBSETS;

EID: 84991466905     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.101020     Document Type: Article

References (37)

1. Bocklandt S, Lin W, Sehl ME, Sánchez FJ, Sinsheimer JS, Horvath S, Vilain E. Epigenetic predictor of age. PLoS One. 2011; 6:e14821. doi.org/10.1371/journal. pone.0014821
2. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, Klotzle B, Bibikova M, Fan JB, Gao Y, Deconde R, Chen M, Rajapakse I, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013; 49:359-67. doi.org/10.1016/j.molcel.2012.10.016
3. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013; 14:R115. doi.org/10.1186/gb-2013-14-10-r115
4. Lin Q, Weidner CI, Costa IG, Marioni RE, Ferreira MR, Deary IJ, Wagner W. DNA methylation levels at individual age-associated CpG sites can be indicative for life expectancy. Aging (Albany NY). 2016; 8:394-401.doi.org/10.18632/aging.100908
5. Marioni RE, Shah S, McRae AF, Chen BH, Colicino E, Harris SE, Gibson J, Henders AK, Redmond P, Cox SR, Pattie A, Corley J, Murphy L, et al. DNA methylation age of blood predicts all-cause mortality in later life. Genome Biol. 2015; 16:25. doi.org/10.1186/s13059-015-0584-6
6. Christiansen L, Lenart A, Tan Q, Vaupel JW, Aviv A, McGue M, Christensen K. DNA methylation age is associated with mortality in a longitudinal Danish twin study. Aging Cell. 2016; 15:149-54. doi.org/10.1111/acel.12421
7. Perna L, Zhang Y, Mons U, Holleczek B, Saum K-U, Brenner H. Epigenetic age acceleration predicts cancer, cardiovascular, and all-cause mortality in a German case cohort. Clin Epigenetics. 2016; 8:64. doi.org/10.1186/s13148-016-0228-z
8. Horvath S, Pirazzini C, Bacalini MG, Gentilini D, Di Blasio AM, Delledonne M, Mari D, Arosio B, Monti D, Passarino G, De Rango F, D'Aquila P, Giuliani C, et al. Decreased epigenetic age of PBMCs from Italian semi-supercentenarians and their offspring. Aging (Albany NY). 2015; 7:1159-70. doi.org/10.18632/aging.100861
9. Fagnoni FF, Vescovini R, Passeri G, Bologna G, Pedrazzoni M, Lavagetto G, Casti A, Franceschi C, Passeri M, Sansoni P. Shortage of circulating naive CD8(+) T cells provides new insights on immunodeficiency in aging. Blood. 2000; 95:2860-68.
10. Franceschi C. Inflammaging as a major characteristic of old people: can it be prevented or cured? Nutr Rev. 2007; 65:S173-76. doi.org/10.1301/nr.2007.dec. S173-S176
11. Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci. 2000; 908:244-54. doi.org/10.1111/j.1749-6632.2000.tb06651.x
12. Miller RA. The aging immune system: primer and prospectus. Science. 1996; 273:70-74. doi.org/10.1126/science.273.5271.70
13. Baker GT 3rd, Sprott RL. Biomarkers of aging. Exp Gerontol. 1988; 23:223-39. doi.org/10.1016/0531-5565(88)90025-3
14. Peters MJ, Joehanes R, Pilling LC, Schurmann C, Conneely KN, Powell J, Reinmaa E, Sutphin GL, Zhernakova A, Schramm K, Wilson YA, Kobes S, Tukiainen T, et al, and NABEC/UKBEC Consortium. The transcriptional landscape of age in human peripheral blood. Nat Commun. 2015; 6:8570. doi.org/10.1038/ncomms9570
15. Sanders JL, Newman AB. Telomere length in epidemiology: a biomarker of aging, age-related disease, both, or neither? Epidemiol Rev. 2013; 35:112-31. doi.org/10.1093/epirev/mxs008
16. Sanders J, Boudreau R, Newman A. 2012. Understanding the Aging Process Using Epidemiologic Approaches. (Dordrecht Heidelberg New York: Springer).
17. Roberts-Thomson IC, Whittingham S, Youngchaiyud U, Mackay IR. Ageing, immune response, and mortality. Lancet. 1974; 2:368-70. doi.org/10.1016/S0140-6736(74)91755-3
18. Levine ME, Hosgood HD, Chen B, Absher D, Assimes T, Horvath S. DNA methylation age of blood predicts future onset of lung cancer in the women's health initiative. Aging (Albany NY). 2015; 7:690-700. doi.org/10.18632/aging.100809
19. Marioni RE, Shah S, McRae AF, Ritchie SJ, Muniz-Terrera G, Harris SE, Gibson J, Redmond P, Cox SR, Pattie A, Corley J, Taylor A, Murphy L, 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. doi.org/10.1093/ije/dyu277
20. Levine ME, Lu AT, Bennett DA, Horvath S. Epigenetic age of the pre-frontal cortex is associated with neuritic plaques, amyloid load, and Alzheimer's disease related cognitive functioning. Aging (Albany NY). 2015; 7:1198-211. doi.org/10.18632/aging.100 864
21. Horvath S, Garagnani P, Bacalini MG, Pirazzini C, Salvioli S, Gentilini D, Di Blasio AM, Giuliani C, Tung S, Vinters HV, Franceschi C. Accelerated epigenetic aging in Down syndrome. Aging Cell. 2015; 14:491-95 doi.org/10.1111/acel.12325
22. Horvath S, Langfelder P, Kwak S, Aaronson J, Rosinski J, Vogt TF, Eszes M, Faull RL, Curtis MA, Waldvogel HJ, Choi OW, Tung S, Vinters HV, et al. Huntington's disease accelerates epigenetic aging of human brain and disrupts DNA methylation levels. Aging (Albany NY). 2016; 8:1485-512. doi.org/10.18632/aging.101005
23. Horvath S, Ritz BR. Increased epigenetic age and granulocyte counts in the blood of Parkinson's disease patients. Aging (Albany NY). 2015; 7:1130-42 doi.org/10.18632/aging.100859
24. Horvath S, Erhart W, Brosch M, Ammerpohl O, von Schönfels W, Ahrens M, Heits N, Bell JT, Tsai P-C, Spector TD, Deloukas P, Siebert R, Sipos B, et al. Obesity accelerates epigenetic aging of human liver. Proc Natl Acad Sci USA. 2014; 111:15538-43. doi.org/10.1073/pnas.1412759111
25. Horvath S, Levine AJ. HIV-1 infection accelerates age according to the epigenetic clock. J Infect Dis. 2015; 212:1563-73. doi.org/10.1093/infdis/jiv277
26. Levine ME, Lu AT, Chen BH, Hernandez DG, Singleton AB, Ferrucci L, Bandinelli S, Salfati E, Manson JE, Quach A, Kusters CD, Kuh D, Wong A, et al. Menopause accelerates biological aging. Proc Natl Acad Sci USA. 2016; 113:9327-32. doi.org/10.1073/pnas.1604558113
27. Horvath S, Mah V, Lu AT, Woo JS, Choi OW, Jasinska AJ, Riancho JA, Tung S, Coles NS, Braun J, Vinters HV, Coles LS. The cerebellum ages slowly according to the epigenetic clock. Aging (Albany NY). 2015; 7:294-306. doi.org/10.18632/aging.100742
28. Horvath S, Gurven M, Levine ME, Trumble BC, Kaplan H, Allayee H, Ritz BR, Chen B, Lu AT, Rickabaugh TM, Jamieson BD, Sun D, Li S, et al. An epigenetic clock analysis of race/ethnicity, sex, and coronary heart disease. Genome Biol. 2016; 17:171. doi.org/10.1186/s13059-016-1030-0
29. Lowe D, Horvath S, Raj K. Epigenetic clock analyses of cellular senescence and ageing. Oncotarget. 2016; 7:8524-31. doi:10.18632/oncotarget.7383.
30. Spiers H, Hannon E, Schalkwyk LC, Smith R, Wong CC, O'Donovan MC, Bray NJ, Mill J. Methylomic trajectories across human fetal brain development. Genome Res. 2015; 25:338-52. doi.org/10.1101/gr.180273.114
31. Walker RF, Liu JS, Peters BA, Ritz BR, Wu T, Ophoff RA, Horvath S. Epigenetic age analysis of children who seem to evade aging. Aging (Albany NY). 2015; 7:334-39. doi.org/10.18632/aging.100744
32. Klemera P, Doubal S. A new approach to the concept and computation of biological age. Mech Ageing Dev. 2006; 127:240-48. doi.org/10.1016/j.mad.2005.10.004
33. 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. doi.org/10.1186/1471-2105-13-86
34. Viechtbauer W. Conducting Meta-Analyses in R with the metafor Package. J Stat Softw. 2010; 36:1-48. doi.org/10.18637/jss.v036.i03.
35. Curb JD, McTiernan A, Heckbert SR, Kooperberg C, Stanford J, Nevitt M, Johnson KC, Proulx-Burns L, Pastore L, Criqui M, Daugherty S, and WHI Morbidity and Mortality Committee. Outcomes ascertainment and adjudication methods in the Women's Health Initiative. Ann Epidemiol. 2003 (Suppl ); 13:S122-28. doi.org/10.1016/S1047-2797(03)00048-6
36. Deary IJ, Gow AJ, Pattie A, Starr JM. Cohort profile: the Lothian Birth Cohorts of 1921 and 1936. Int J Epidemiol. 2012; 41:1576-84. doi.org/10.1093/ije/dyr197
37. Ferrucci L, Bandinelli S, Benvenuti E, Di Iorio A, Macchi C, Harris TB, Guralnik JM. Subsystems contributing to the decline in ability to walk: bridging the gap between epidemiology and geriatric practice in the InCHIANTI study. J Am Geriatr Soc. 2000; 48:1618-25. doi.org/10.1111/j.1532-5415.2000.tb 03873.x