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The epigenetic tracks of aging

  • Carola Ingrid Weidner EMAIL logo und Wolfgang Wagner EMAIL logo
Veröffentlicht/Copyright: 2. September 2014

Abstract

Aging is associated with the deterioration of biological functions, which is either caused by accumulation of random defects or mediated by a controlled process. This article provides an overview of age-associated epigenetic alterations in the histone code, DNA-methylation (DNAm) pattern, and chromatin structure. In particular, age-related DNAm changes are highly reproducible at specific sites in the genome. The DNAm level at few CpGs facilitates estimation of chronological age and there is evidence that such predictions are indicative for biological age. Overall, aging appears to be associated with a tightly regulated epigenetic process, but the underlying mechanism remains to be elucidated.


Corresponding authors: Carola Ingrid Weidner and Wolfgang Wagner, Helmholtz-Institute for Biomedical Engineering, Stem Cell Biology and Cellular Engineering, RWTH Aachen University Medical School, Pauwelsstrasse 20, D-52074 Aachen, Germany, e-mail: ,

Acknowledgments

This work was supported by the Stem Cell Network North Rhine Westphalia and by the Else-Kröner Fresenius Stiftung.

References

Alisch, R.S., Barwick, B.G., Chopra, P., Myrick, L.K., Satten, G.A., Conneely, K.N., and Warren, S.T. (2012). Age-associated DNA methylation in pediatric populations. Genome Res. 22, 623–632.10.1101/gr.125187.111Suche in Google Scholar PubMed PubMed Central

Armstrong, D.A., Lesseur, C., Conradt, E., Lester, B.M., and Marsit, C.J. (2014). Global and gene-specific DNA methylation across multiple tissues in early infancy: implications for children’s health research. FASEB J. 28, 2088–2097.10.1096/fj.13-238402Suche in Google Scholar PubMed PubMed Central

Berger, S.L. (2007). The complex language of chromatin regulation during transcription. Nature 447, 407–412.10.1038/nature05915Suche in Google Scholar PubMed

Bibikova, M., Barnes, B., Tsan, C., Ho, V., Klotzle, B., Le, J.M., Delano, D., Zhang, L., Schroth, G.P., Gunderson, K.L., et al. (2011). High density DNA methylation array with single CpG site resolution. Genomics 98, 288–295.10.1016/j.ygeno.2011.07.007Suche in Google Scholar PubMed

Bickmore, W.A. and van Steensel, B. (2013). Genome architecture: domain organization of interphase chromosomes. Cell 152, 1270–1284.10.1016/j.cell.2013.02.001Suche in Google Scholar PubMed

Bocker, M.T., Hellwig, I., Breiling, A., Eckstein, V., Ho, A.D., and Lyko, F. (2011). Genome-wide promoter DNA methylation dynamics of human hematopoietic progenitor cells during differentiation and aging. Blood 117, e182–e189.10.1182/blood-2011-01-331926Suche in Google Scholar PubMed

Bocklandt, S., Lin, W., Sehl, M.E., Sanchez, F.J., Sinsheimer, J.S., Horvath, S., and Vilain, E. (2011). Epigenetic predictor of age. PLoS One 6, e14821.10.1371/journal.pone.0014821Suche in Google Scholar PubMed PubMed Central

Bork, S., Pfister, S., Witt, H., Horn, P., Korn, B., Ho, A.D., and Wagner, W. (2010). DNA methylation pattern changes upon long-term culture and aging of human mesenchymal stromal cells. Aging Cell 9, 54–63.10.1111/j.1474-9726.2009.00535.xSuche in Google Scholar PubMed PubMed Central

Boyd-Kirkup, J.D., Green, C.D., Wu, G., Wang, D., and Han, J.D. (2013). Epigenomics and the regulation of aging. Epigenomics 5, 205–227.10.2217/epi.13.5Suche in Google Scholar PubMed

Brown, K., Xie, S., Qiu, X., Mohrin, M., Shin, J., Liu, Y., Zhang, D., Scadden, D.T., and Chen, D. (2013). SIRT3 reverses aging-associated degeneration. Cell Rep. 3, 319–327.10.1016/j.celrep.2013.01.005Suche in Google Scholar PubMed PubMed Central

Cahan, P. and Daley, G.Q. (2013). Origins and implications of pluripotent stem cell variability and heterogeneity. Nat. Rev. Mol. Cell Biol. 14, 357–368.10.1038/nrm3584Suche in Google Scholar PubMed PubMed Central

Chen, H., Gu, X., Su, I.H., Bottino, R., Contreras, J.L., Tarakhovsky, A., and Kim, S.K. (2009). Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev. 23, 975–985.10.1101/gad.1742509Suche in Google Scholar PubMed PubMed Central

Christensen, B.C., Houseman, E.A., Marsit, C.J., Zheng, S., Wrensch, M.R., Wiemels, J.L., Nelson, H.H., Karagas, M.R., Padbury, J.F., Bueno, R., et al. (2009). Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet. 5, e1000602.10.1371/journal.pgen.1000602Suche in Google Scholar PubMed PubMed Central

Cruickshanks, H.A., McBryan, T., Nelson, D.M., Vanderkraats, N.D., Shah, P.P., van, T.J., Singh, R.T., Brock, C., Donahue, G., Dunican, D.S., et al. (2013). Senescent cells harbour features of the cancer epigenome. Nat. Cell Biol. 15, 1495–1506.10.1038/ncb2879Suche in Google Scholar PubMed PubMed Central

Day, K., Waite, L.L., Thalacker-Mercer, A., West, A., Bamman, M.M., Brooks, J.D., Myers, R.M., and Absher, D. (2013). Differential DNA methylation with age displays both common and dynamic features across human tissues that are influenced by CpG landscape. Genome Biol. 14, R102.10.1186/gb-2013-14-9-r102Suche in Google Scholar PubMed PubMed Central

Dhawan, S., Tschen, S.I., and Bhushan, A. (2009). Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev. 23, 906–911.10.1101/gad.1742609Suche in Google Scholar PubMed PubMed Central

Feng, Q., Lu, S.J., Klimanskaya, I., Gomes, I., Kim, D., Chung, Y., Honig, G.R., Kim, K.S., and Lanza, R. (2010). Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 28, 704–712.10.1002/stem.321Suche in Google Scholar PubMed

Florath, I., Butterbach, K., Muller, H., Bewerunge-Hudler, M., and Brenner, H. (2014). 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. 23, 1186–1201.10.1093/hmg/ddt531Suche in Google Scholar PubMed PubMed Central

Garagnani, P., Bacalini, M.G., Pirazzini, C., Gori, D., Giuliani, C., Mari, D., Di Blasio, A.M., Gentilini, D., Vitale, G., Collino, S., et al. (2012). Methylation of ELOVL2 gene as a new epigenetic marker of age. Aging Cell 11, 1132–1134.10.1111/acel.12005Suche in Google Scholar PubMed

Gautrey, H.E., van Otterdijk, S.D., Cordell, H.J., Mathers, J.C., and Strathdee, G. (2014). DNA methylation abnormalities at gene promoters are extensive and variable in the elderly and phenocopy cancer cells. FASEB J. 28, 3261–3272.10.1096/fj.13-246173Suche in Google Scholar PubMed

Gentilini, D., Mari, D., Castaldi, D., Remondini, D., Ogliari, G., Ostan, R., Bucci, L., Sirchia, S.M., Tabano, S., Cavagnini, F., et al. (2013). Role of epigenetics in human aging and longevity: genome-wide DNA methylation profile in centenarians and centenarians’ offspring. Age (Dordr.) 35, 1961–1973.10.1007/s11357-012-9463-1Suche in Google Scholar PubMed PubMed Central

Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S., Klotzle, B., Bibikova, M., Fan, J.B., Gao, Y., et al. (2013). Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol. Cell 49, 359–367.10.1016/j.molcel.2012.10.016Suche in Google Scholar PubMed PubMed Central

Heyn, H., Li, N., Ferreira, H.J., Moran, S., Pisano, D.G., Gomez, A., Diez, J., Sanchez-Mut, J.V., Setien, F., Carmona, F.J., et al. (2012). Distinct DNA methylomes of newborns and centenarians. Proc. Natl. Acad. Sci. USA 109, 10522–10527.10.1073/pnas.1120658109Suche in Google Scholar PubMed PubMed Central

Horvath, S. (2013). DNA methylation age of human tissues and cell types. Genome Biol. 14, R115.10.1186/gb-2013-14-10-r115Suche in Google Scholar PubMed PubMed Central

Huidobro, C., Fernandez, A.F., and Fraga, M.F. (2013). Aging epigenetics: causes and consequences. Mol. Aspects Med. 34, 765–781.10.1016/j.mam.2012.06.006Suche in Google Scholar PubMed

Johansson, A., Enroth, S., and Gyllensten, U. (2013). Continuous aging of the human DNA methylome throughout the human lifespan. PLoS One 8, e67378.10.1371/journal.pone.0067378Suche in Google Scholar PubMed PubMed Central

Kanfi, Y., Naiman, S., Amir, G., Peshti, V., Zinman, G., Nahum, L., Bar-Joseph, Z., and Cohen, H.Y. (2012). The sirtuin SIRT6 regulates lifespan in male mice. Nature 483, 218–221.10.1038/nature10815Suche in Google Scholar PubMed

Kimura, H. (2013). Histone modifications for human epigenome analysis. J. Hum. Genet. 58, 439–445.10.1038/jhg.2013.66Suche in Google Scholar PubMed

Kirkwood, T.B. (2005). Understanding the odd science of aging. Cell 120, 437–447.10.1016/j.cell.2005.01.027Suche in Google Scholar PubMed

Koch, C.M. and Wagner, W. (2011). Epigenetic-aging-signature to determine age in different tissues. Aging (Albany, NY) 3, 1018–1027.10.18632/aging.100395Suche in Google Scholar PubMed PubMed Central

Koch, C.M., Suschek, C.V., Lin, Q., Bork, S., Goergens, M., Joussen, S., Pallua, N., Ho, A.D., Zenke, M., and Wagner, W. (2011). Specific age-associated DNA methylation changes in human dermal fibroblasts. PLoS One 6, e16679.10.1371/journal.pone.0016679Suche in Google Scholar PubMed PubMed Central

Koch, C.M., Joussen, S., Schellenberg, A., Lin, Q., Zenke, M., and Wagner, W. (2012). Monitoring of cellular senescence by DNA-methylation at specific CpG sites. Aging Cell 11, 366–369.10.1111/j.1474-9726.2011.00784.xSuche in Google Scholar PubMed

Koch, C.M., Reck, K., Shao, K., Lin, Q., Joussen, S., Ziegler, P., Walenda, G., Drescher, W., Opalka, B., May, T., et al. (2013). Pluripotent stem cells escape from senescence-associated DNA methylation changes. Genome Res. 23, 248–259.10.1101/gr.141945.112Suche in Google Scholar PubMed PubMed Central

Lapasset, L., Milhavet, O., Prieur, A., Besnard, E., Babled, A., it-Hamou, N., Leschik, J., Pellestor, F., Ramirez, J.M., De, V.J., et al. (2011). Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev. 25, 2248–2253.10.1101/gad.173922.111Suche in Google Scholar PubMed PubMed Central

Larson, K., Yan, S.J., Tsurumi, A., Liu, J., Zhou, J., Gaur, K., Guo, D., Eickbush, T.H., and Li, W.X. (2012). Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis. PLoS Genet 8, e1002473.10.1371/journal.pgen.1002473Suche in Google Scholar PubMed PubMed Central

Lister, R., Pelizzola, M., Kida, Y.S., Hawkins, R.D., Nery, J.R., Hon, G., ntosiewicz-Bourget, J., O’Malley, R., Castanon, R., Klugman, S., et al. (2011). Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68–73.10.1038/nature09798Suche in Google Scholar PubMed PubMed Central

Liu, L., Cheung, T.H., Charville, G.W., Hurgo, B.M., Leavitt, T., Shih, J., Brunet, A., and Rando, T.A. (2013). Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 4, 189–204.10.1016/j.celrep.2013.05.043Suche in Google Scholar PubMed PubMed Central

Lopez-Otin, C., Blasco, M.A., Partridge, L., Serrano, M., and Kroemer, G. (2013). The hallmarks of aging. Cell 153, 1194–1217.10.1016/j.cell.2013.05.039Suche in Google Scholar PubMed PubMed Central

Maegawa, S., Hinkal, G., Kim, H.S., Shen, L., Zhang, L., Zhang, J., Zhang, N., Liang, S., Donehower, L.A., and Issa, J.P. (2010). Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res. 20, 332–340.10.1101/gr.096826.109Suche in Google Scholar PubMed PubMed Central

Mallon, B.S., Hamilton, R.S., Kozhich, O.A., Johnson, K.R., Fann, Y.C., Rao, M.S., and Robey, P.G. (2014). Comparison of the molecular profiles of human embryonic and induced pluripotent stem cells of isogenic origin. Stem Cell Res. 12, 376–386.10.1016/j.scr.2013.11.010Suche in Google Scholar PubMed PubMed Central

Marion, R.M., Strati, K., Li, H., Tejera, A., Schoeftner, S., Ortega, S., Serrano, M., and Blasco, M.A. (2009). Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4, 141–154.10.1016/j.stem.2008.12.010Suche in Google Scholar PubMed

McClay, J.L., Aberg, K.A., Clark, S.L., Nerella, S., Kumar, G., Xie, L.Y., Hudson, A.D., Harada, A., Hultman, C.M., Magnusson, P.K., et al. (2014). 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. 23, 1175–1185.10.1093/hmg/ddt511Suche in Google Scholar PubMed PubMed Central

Meissner, C. and Ritz-Timme, S. (2010). Molecular pathology and age estimation. Forensic Sci. Int. 203, 34–43.10.1016/j.forsciint.2010.07.010Suche in Google Scholar PubMed

Pegoraro, G., Kubben, N., Wickert, U., Gohler, H., Hoffmann, K., and Misteli, T. (2009). Ageing-related chromatin defects through loss of the NURD complex. Nat. Cell Biol. 11, 1261–1267.10.1038/ncb1971Suche in Google Scholar PubMed PubMed Central

Pruitt, K., Zinn, R.L., Ohm, J.E., McGarvey, K.M., Kang, S.H., Watkins, D.N., Herman, J.G., and Baylin, S.B. (2006). Inhibition of SIRT1 reactivates silenced cancer genes without loss of promoter DNA hypermethylation. PLoS Genet. 2, e40.10.1371/journal.pgen.0020040Suche in Google Scholar PubMed PubMed Central

Raddatz, G., Hagemann, S., Aran, D., Sohle, J., Kulkarni, P.P., Kaderali, L., Hellman, A., Winnefeld, M., and Lyko, F. (2013). Aging is associated with highly defined epigenetic changes in the human epidermis. Epigenetics & Chromatin 6, 36–48.10.1186/1756-8935-6-36Suche in Google Scholar PubMed PubMed Central

Rai, T.S. and Adams, P.D. (2013). Lessons from senescence: chromatin maintenance in non-proliferating cells. Biochim. Biophys. Acta 1819, 322–331.10.1016/j.bbagrm.2011.07.014Suche in Google Scholar PubMed PubMed Central

Rakyan, V.K., Down, T.A., Maslau, S., Andrew, T., Yang, T.P., Beyan, H., Whittaker, P., McCann, O.T., Finer, S., Valdes, A.M., et al. (2010). Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res. 20, 434–439.10.1101/gr.103101.109Suche in Google Scholar PubMed PubMed Central

Rando, T.A. and Chang, H.Y. (2012). Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 148, 46–57.10.1016/j.cell.2012.01.003Suche in Google Scholar PubMed PubMed Central

Riedel, C.G., Dowen, R.H., Lourenco, G.F., Kirienko, N.V., Heimbucher, T., West, J.A., Bowman, S.K., Kingston, R.E., Dillin, A., Asara, J.M., et al. (2013). DAF-16 employs the chromatin remodeller SWI/SNF to promote stress resistance and longevity. Nat. Cell Biol. 15, 491–501.10.1038/ncb2720Suche in Google Scholar PubMed PubMed Central

Rohani, L., Johnson, A.A., Arnold, A., and Stolzing, A. (2014). The aging signature: a hallmark of induced pluripotent stem cells? Aging Cell 13, 2–7.10.1111/acel.12182Suche in Google Scholar PubMed PubMed Central

Romanov, G.A. and Vanyushin, B.F. (1981). Methylation of reiterated sequences in mammalian DNAs. Effects of the tissue type, age, malignancy and hormonal induction. Biochim. Biophys. Acta 653, 204–218.10.1016/0005-2787(81)90156-8Suche in Google Scholar PubMed

Sanders, Y.Y., Liu, H., Zhang, X., Hecker, L., Bernard, K., Desai, L., Liu, G., and Thannickal, V.J. (2013). Histone modifications in senescence-associated resistance to apoptosis by oxidative stress. Redox. Biol. 1, 8–16.10.1016/j.redox.2012.11.004Suche in Google Scholar PubMed PubMed Central

Sarg, B., Koutzamani, E., Helliger, W., Rundquist, I., and Lindner, H.H. (2002). Postsynthetic trimethylation of histone H4 at lysine 20 in mammalian tissues is associated with aging. J. Biol. Chem. 277, 39195–39201.10.1074/jbc.M205166200Suche in Google Scholar PubMed

Satoh, A., Brace, C.S., Rensing, N., Cliften, P., Wozniak, D.F., Herzog, E.D., Yamada, K.A., and Imai, S. (2013). Sirt1 extends life span and delays aging in mice through the regulation of Nk2 homeobox 1 in the DMH and LH. Cell Metab. 18, 416–430.10.1016/j.cmet.2013.07.013Suche in Google Scholar PubMed PubMed Central

Scaffidi, P. and Misteli, T. (2005). Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440–445.10.1038/nm1204Suche in Google Scholar PubMed PubMed Central

Schellenberg, A., Lin, Q., Schuler, H., Koch, C.M., Joussen, S., Denecke, B., Walenda, G., Pallua, N., Suschek, C.V., Zenke, M., et al. (2011). Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging (Albany, NY) 3, 873–888.10.18632/aging.100391Suche in Google Scholar PubMed PubMed Central

Shao, K., Koch, C., Gupta, M.K., Lin, Q., Lenz, M., Laufs, S., Denecke, B., Schmidt, M., Linke, M., Hennies, H.C., et al. (2013). Induced pluripotent mesenchymal stromal cell clones retain donor-derived differences in DNA methylation profiles. Mol. Ther. 21, 240–250.10.1038/mt.2012.207Suche in Google Scholar PubMed PubMed Central

Sharma, A., Diecke, S., Zhang, W.Y., Lan, F., He, C., Mordwinkin, N.M., Chua, K.F., and Wu, J.C. (2013). The role of SIRT6 protein in aging and reprogramming of human induced pluripotent stem cells. J. Biol. Chem. 288, 18439–18447.10.1074/jbc.M112.405928Suche in Google Scholar PubMed PubMed Central

Shokhirev, M.N. and Johnson, A.A. (2014). Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS One 9, e86602.10.1371/journal.pone.0086602Suche in Google Scholar PubMed PubMed Central

Shumaker, D.K., Dechat, T., Kohlmaier, A., Adam, S.A., Bozovsky, M.R., Erdos, M.R., Eriksson, M., Goldman, A.E., Khuon, S., Collins, F.S., et al. (2006). Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. USA 103, 8703–8708.10.1073/pnas.0602569103Suche in Google Scholar PubMed PubMed Central

Steegenga, W.T., Boekschoten, M.V., Lute, C., Hooiveld, G.J., de Groot, P.J., Morris, T.J., Teschendorff, A.E., Butcher, L.M., Beck, S., and Muller, M. (2014). Genome-wide age-related changes in DNA methylation and gene expression in human PBMCs. Age (Dordr.) 36, 1523–1540.10.1007/s11357-014-9648-xSuche in Google Scholar PubMed PubMed Central

Sturm, D., Witt, H., Hovestadt, V., Khuong-Quang, D.A., Jones, D.T., Konermann, C., Pfaff, E., Tonjes, M., Sill, M., Bender, S., et al. (2012). Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22, 425–437.10.1016/j.ccr.2012.08.024Suche in Google Scholar PubMed

Tang, Y., Li, T., Li, J., Yang, J., Liu, H., Zhang, X.J., and Le, W. (2014). Jmjd3 is essential for the epigenetic modulation of microglia phenotypes in the immune pathogenesis of Parkinson’s disease. Cell Death Differ. 21, 369–380.10.1038/cdd.2013.159Suche in Google Scholar PubMed PubMed Central

Teschendorff, A.E., Menon, U., Gentry-Maharaj, A., Ramus, S.J., Weisenberger, D.J., Shen, H., Campan, M., Noushmehr, H., Bell, C.G., Maxwell, A.P., et al. (2010). Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 20, 440–446.10.1101/gr.103606.109Suche in Google Scholar PubMed PubMed Central

Teschendorff, A.E., West, J., and Beck, S. (2013). Age-associated epigenetic drift: implications, and a case of epigenetic thrift? Hum. Mol. Genet. 22, R7–R15.10.1093/hmg/ddt375Suche in Google Scholar PubMed PubMed Central

Vaskova, E.A., Stekleneva, A.E., Medvedev, S.P., and Zakian, S.M. (2013). “Epigenetic memory” phenomenon in induced pluripotent stem cells. Acta Naturae. 5, 15–21.10.32607/20758251-2013-5-4-15-21Suche in Google Scholar

Volle, C. and Dalal, Y. (2014). Histone variants: the tricksters of the chromatin world. Curr. Opin. Genet. Dev. 25C, 8–14.10.1016/j.gde.2013.11.006Suche in Google Scholar PubMed PubMed Central

Wagner, W., Horn, P., Castoldi, M., Diehlmann, A., Bork, S., Saffrich, R., Benes, V., Blake, J., Pfister, S., Eckstein, V., et al. (2008). Replicative senescence of mesenchymal stem cells – a continuous and organized process. PLoS One 5, e2213.10.1371/journal.pone.0002213Suche in Google Scholar PubMed PubMed Central

Wagner, J.R., Busche, S., Ge, B., Kwan, T., Pastinen, T., and Blanchette, M. (2014). The relationship between DNA methylation, genetic and expression inter-individual variation in untransformed human fibroblasts. Genome Biol. 15, R37.10.1186/gb-2014-15-2-r37Suche in Google Scholar PubMed PubMed Central

Wang, C.M., Tsai, S.N., Yew, T.W., Kwan, Y.W., and Ngai, S.M. (2010). Identification of histone methylation multiplicities patterns in the brain of senescence-accelerated prone mouse 8. Biogerontology 11, 87–102.10.1007/s10522-009-9231-5Suche in Google Scholar PubMed

Watanabe, K. and Bloch, W. (2013). Histone methylation and acetylation indicates epigenetic change in the aged cochlea of mice. Eur. Arch. Otorhinolaryngol. 270, 1823–1830.10.1007/s00405-012-2222-1Suche in Google Scholar PubMed

Weidner, C.I., Lin, Q., Koch, C.M., Eisele, L., Beier, F., Ziegler, P., Bauerschlag, D.O., Jockel, K.H., Erbel, R., Muhleisen, T.W., et al. (2014). Aging of blood can be tracked by DNA methylation changes at just three CpG sites. Genome Biol. 15, R24.10.1186/gb-2014-15-2-r24Suche in Google Scholar PubMed PubMed Central

Xu, Z. and Taylor, J.A. (2014). Genome-wide age-related DNA methylation changes in blood and other tissues relate to histone modification, expression and cancer. Carcinogenesis 35, 356–364.10.1093/carcin/bgt391Suche in Google Scholar PubMed PubMed Central

Zhang, R., Poustovoitov, M.V., Ye, X., Santos, H.A., Chen, W., Daganzo, S.M., Erzberger, J.P., Serebriiskii, I.G., Canutescu, A.A., Dunbrack, R.L., et al. (2005). Formation of MacroH2A-containing senescence-associated heterochromatin foci and senescence driven by ASF1a and HIRA. Dev. Cell 8, 19–30.10.1016/j.devcel.2004.10.019Suche in Google Scholar PubMed

Zykovich, A., Hubbard, A., Flynn, J.M., Tarnopolsky, M., Fraga, M.F., Kerksick, C., Ogborn, D., MacNeil, L., Mooney, S.D., and Melov, S. (2014). Genome-wide DNA methylation changes with age in disease-free human skeletal muscle. Aging Cell 13, 360–366.10.1111/acel.12180Suche in Google Scholar PubMed PubMed Central

Received: 2014-4-4
Accepted: 2014-6-18
Published Online: 2014-9-2
Published in Print: 2014-11-1

©2014 by De Gruyter

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