Ageing-associated changes in the human DNA methylome: Genomic locations and effects on gene expression

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Marttila, Saara ^a,b   Kananen, Laura ^a,b   Häyrynen, Sergei ^a   Jylhävä, Juulia ^a,b   Nevalainen, Tapio ^a,b   Hervonen, Antti ^a,b   Jylhä, Marja ^a,b   Nykter, Matti ^a   Hurme, Mikko ^a,b,c  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b Jyvaskyla University   (Finland)

^c FIMLAB LABORATORIES   (Finland)

Author keywords

Ageing; DNA methylation; Epigenetics; Gene expression; Hypermethylation; Hypomethylation; Methylome; Molecular ageing; PBMCs

Indexed keywords

AGING; CPG ISLAND; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENETICS; HUMAN; HUMAN GENOME; MALE; MOLECULAR GENETICS; SEX DIFFERENCE; VERY ELDERLY;

AGED, 80 AND OVER; AGING; CPG ISLANDS; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENOME, HUMAN; HUMANS; MALE; MOLECULAR SEQUENCE ANNOTATION; SEX FACTORS;

EID: 84928012878     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1381-z     Document Type: Article

References (63)

1. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell. 2013;153:1194-217.
2. Arnold CR, Wolf J, Brunner S, Herndler-Brandstetter D, Grubeck-Loebenstein B. Gain and loss of T cell subsets in old age - age-related reshaping of the T cell repertoire. J Clin Immunol. 2011;31:137-46.
3. Blagosklonny MV. Aging is not programmed: genetic pseudo-program is a shadow of developmental growth. Cell Cycle. 2013;12:3736-42.
4. de Magalhães JP. Programmatic features of aging originating in development: aging mechanisms beyond molecular damage? FASEB J. 2012;26:4821-6.
5. Kirkwood TB, Melov S. On the programmed/non-programmed nature of ageing within the life history. Curr Biol. 2011;21:R701-7.
6. Bacalini MG, Friso S, Olivieri F, Pirazzini C, Giuliani C, Capri M, et al. Present and future of anti-ageing epigenetic diets. Mech Ageing Dev. 2014;136:101-15.
7. Johnson AA, Akman K, Calimport SR, Wuttke D, Stolzing A, de Magalhães JP. The role of DNA methylation in aging, rejuvenation, and age-related disease. Rejuvenation Res. 2012;15:483-94.
8. Brooks-Wilson AR. Genetics of healthy aging and longevity. Hum Genet. 2013;132:1323-38.
9. Riggs AD. X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet. 1975;14:9-25.
10. Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science. 1975;187:226-32.
11. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25:1010-22.
12. Illingworth RS, Bird AP. CpG islands-'a rough guide'. FEBS Lett. 2009;583:1713-20.
13. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484-92.
14. Bogdanović O, Veenstra GJ. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma. 2009;118:549-65.
15. Cedar H, Bergman Y. Programming of DNA methylation patterns. Annu Rev Biochem. 2012;81:97-117.
16. Christensen BC, Houseman EA, Marsit CJ, Zheng S, Wrensch MR, Wiemels JL, et al. Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 2009;5:e1000602.
17. Bell JT, Tsai PC, Yang TP, Pidsley R, Nisbet J, Glass D, et al. Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population. PLoS Gene. 2012;8:e1002629.
18. Gentilini D, Mari D, Castaldi D, Remondini D, Ogliari G, Ostan R, et al. Role of epigenetics in human aging and longevity: genome-wide DNA methylation profile in centenarians and centenarians' offspring. Age (Dordr). 2013;35:1961-73.
19. Rakyan VK, Down TA, Maslau S, Andrew T, Yang TP, Beyan H, et al. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 2010;20:434-9.
20. TeschendorffAE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, Shen H, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010;20:440-6.
21. Xu Z, Taylor JA. Genome-wide age-related DNA methylation changes in blood and other tissues relate to histone modification, expression and cancer. Carcinogenesis. 2014;35:356-64.
22. Weidner CI, Lin Q, Koch CM, Eisele L, Beier F, Ziegler P, et al. Aging of blood can be tracked by DNA methylation changes at just three CpG sites. Genome Biol. 2014;15:R24.
23. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013;14:R115.
24. Steegenga WT, Boekschoten MV, Lute C, Hooiveld GJ, de Groot PJ, Morris TJ, et al. Genome-wide age-related changes in DNA methylation and gene expression in human PBMCs. Age (Dordr). 2014;36:9648.
25. Florath I, Butterbach K, Muller H, Bewerunge-Hudler M, Brenner H. Cross-sectional and longitudinal changes in DNA methylation with age: an epigenome-wide analysis revealing over 60 novel age-associated CpG sites. Hum Mol Genet. 2013;23:1186-201.
26. Garagnani P, Bacalini MG, Pirazzini C, Gori D, Giuliani C, Mari D, et al. Methylation of ELOVL2 gene as a new epigenetic marker of age. Aging Cell. 2012;11:1132-4.
27. Hannum G, Guinney J, Zhao L, Zhang L, Hughes G, Sadda S, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2012;49:359-67.
28. Heyn H, Li N, Ferreira HJ, Moran S, Pisano DG, Gomez A, et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A. 2012;109:10522-7.
29. Jaffe AE, Irizarry RA. Accounting for cellular heterogeneity is critical in epigenome-wide association studies. Genome Biol. 2014;15:R31.
30. Marttila S, Jylhävä J, Pesu M, Hämäläinen S, Jylhä M, Hervonen A, et al. IL-7 concentration is increased in nonagenarians but is not associated with markers of T cell immunosenescence. Exp Gerontol. 2011;46:1000-2.
31. Eden E, Lipson D, Yogev S, Yakhini Z. Discovering motifs in ranked lists of DNA sequences. PLoS Comput Biol. 2007;3:e39.
32. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009;10:48.
33. Zambelli F, Pesole G, Pavesi G. Pscan: finding over-represented transcription factor binding site motifs in sequences from co-regulated or co-expressed genes. Nucleic Acids Res. 2009;37:W247-52.
34. Ingenuity Systems®, www.ingenuity.com.
35. Marttila S, Jylhävä J, Nevalainen T, Nykter M, Jylhä M, Hervonen A, et al. Transcriptional analysis reveals gender-specific changes in the aging of the human immune system. PLoS One. 2013;8:e66229.
36. Johansson A, Enroth S, Gyllensten U. Continuous aging of the human DNA methylome throughout the human lifespan. PLoS One. 2013;8:e67378.
37. McClay JL, Aberg KA, Clark SL, Nerella S, Kumar G, Xie LY, et al. A methylome-wide study of aging using massively parallel sequencing of the methyl-CpG-enriched genomic fraction from blood in over 700 subjects. Hum Mol Genet. 2014;23:1175-85.
38. D'Aquila P, Rose G, Bellizzi D, Passarino G. Epigenetics and aging. Maturitas. 2013;74:130-6.
39. Pawelec G, Larbi A, Derhovanessian E. Senescence of the human immune system. J Comp Pathol. 2010;142 Suppl 1:S39-44.
40. Zilbauer M, Rayner TF, Clark C, Coffey AJ, Joyce CJ, Palta P, et al. Genome-wide methylation analyses of primary human leukocyte subsets identifies functionally important cell-type-specific hypomethylated regions. Blood. 2013;122:e52-60.
41. Kondilis-Mangum HD, Wade PA. Epigenetics and the adaptive immune response. Mol Aspects Med. 2013;34:813-25.
42. Lam LL, Emberly E, Fraser HB, Neumann SM, Chen E, Miller GE, et al. Factors underlying variable DNA methylation in a human community cohort. Proc Natl Acad Sci U S A. 2012;109 Suppl 2:17253-60.
43. Lleras RA, Adrien LR, Smith RV, Brown B, Jivraj N, Keller C, et al. Hypermethylation of a cluster of Krüppel-type zinc finger protein genes on chromosome 19q13 in oropharyngeal squamous cell carcinoma. Am J Pathol. 2011;178:1965-74.
44. Lukic S, Nicolas JC, Levine AJ. The diversity of zinc-finger genes on human chromosome 19 provides an evolutionary mechanism for defense against inherited endogenous retroviruses. Cell Death Differ. 2014;21:381-7.
45. Gaubatz JW, Arcement B, Cutler RG. Gene expression of an endogenous retrovirus-like element during murine development and aging. Mech Ageing Dev. 1991;57:71-85.
46. Wada Y, Tsukada M, Kamiyama S, Koizumi A. Retroviral gene expression as a possible biomarker of aging. Int Arch Occup Environ Health. 1993;65(1 Suppl):S235-9.
47. Romanish MT, Cohen CJ, Mager DL. Potential mechanisms of endogenous retroviral-mediated genomic instability in human cancer. Semin Cancer Biol. 2010;20:246-53.
48. Sharif R, Thomas P, Zalewski P, Fenech M. The role of zinc in genomic stability. Mutat Res. 2012;733:111-21.
49. Mocchegiani E, Costarelli L, Giacconi R, Cipriano C, Muti E, Malavolta M. Zinc-binding proteins (metallothionein and alpha-2 macroglobulin) and immunosenescence. Exp Gerontol. 2006;41:1094-107.
50. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature. 2010;466:253-7.
51. Fenteany G, Glogauer M. Cytoskeletal remodeling in leukocyte function. Curr Opin Hematol. 2004;11:15-24.
52. Zykovich A, Hubbard A, Flynn JM, Tarnopolsky M, Fraga MF, Kerksick C, et al. Genome-wide DNA methylation changes with age in disease-free human skeletal muscle. Aging Cell. 2014;13:360-6.
53. Bhutani N, Burns DM, Blau HM. DNA demethylation dynamics. Cell. 2011;146:866-72.
54. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet. 2009;10:805-11.
55. Bellizzi D, D'Aquila P, Montesanto A, Corsonello A, Mari V, Mazzei B, et al. Global DNA methylation in old subjects is correlated with frailty. Age (Dordr). 2012;34:169-79.
56. Goebeler S, Jylhä M, Hervonen A. Medical history, cognitive status and mobility at the age of 90. A population based study in Tampere, Finland. Aging Clin Exp Res. 2003;15:154-61.
57. Pidsley R, Wong CC Y, Volta M, Lunnon K, Mill J, Schalkwyk LC. A data-driven approach to preprocessing Illumina 450K methylation array data. BMC Genomics. 2013;14:293.
58. Chen YA, Lemire M, Choufani S, Butcher DT, Grafodatskaya D, Zanke BW, et al. Discovery of cross-reactive probes and polymorphic CpGs in the Illumina Infinium HumanMethylation450 microarray. Epigenetics. 2013;8:203-9.
59. TeschendorffAE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, et al. A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data. Bioinformatics. 2013;29:189-96.
60. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007;8:118-27.
61. Du P, Kibbe WA, Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics. 2008;24:1547-8.
62. Cribari-Neto F, Zeileis A. Beta regression in R. JSS. 2010;34:1-24.
63. Ferrari C. Beta regression for modelling rates and proportions. J Appl Stat. 2004;31:799-15.