The Aging Epigenome

Molecular Cell

Volumn 62, Issue 5, 2016, Pages 728-744

  Booth, Lauren N ^a   Brunet, Anne ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; TRANSCRIPTION FACTOR; MITOCHONDRIAL DNA; UNTRANSLATED RNA;

CELL AGING; CELL FUNCTION; CELL STRESS; CHROMATIN; DNA METHYLATION; EPIGENETICS; HUMAN; NONHUMAN; REVIEW; TRANSCRIPTION REGULATION; AGE; AGING; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; GENETIC TRANSCRIPTION; GENETICS; GENOMIC INSTABILITY; GENOTYPE; METABOLISM; MITOCHONDRION; NUTRITIONAL STATUS; PATHOLOGY; PHENOTYPE; PROCEDURES; TELOMERE;

AGE FACTORS; AGING; ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DNA, MITOCHONDRIAL; EPIGENESIS, GENETIC; EPIGENOMICS; GENOMIC INSTABILITY; GENOTYPE; HISTONES; HUMANS; MITOCHONDRIA; NUTRITIONAL STATUS; PHENOTYPE; RNA, UNTRANSLATED; TELOMERE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84971441042     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.013     Document Type: Review

References (154)

1. Aguilar-Arnal L., Katada S., Orozco-Solis R., Sassone-Corsi P. NAD(+)-SIRT1 control of H3K4 trimethylation through circadian deacetylation of MLL1. Nat. Struct. Mol. Biol. 2015, 22:312-318.
2. Altarejos J.Y., Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 2011, 12:141-151.
3. Avrahami D., Li C., Zhang J., Schug J., Avrahami R., Rao S., Stadler M.B., Burger L., Schübeler D., Glaser B., Kaestner K.H. Aging-dependent demethylation of regulatory elements correlates with chromatin state and improved β cell function. Cell Metab. 2015, 22:619-632.
4. Baker D.J., Childs B.G., Durik M., Wijers M.E., Sieben C.J., Zhong J., Saltness R.A., Jeganathan K.B., Verzosa G.C., Pezeshki A., et al. Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 2016, 530:184-189.
5. Baumgart M., Groth M., Priebe S., Savino A., Testa G., Dix A., Ripa R., Spallotta F., Gaetano C., Ori M., et al. RNA-seq of the aging brain in the short-lived fish N. furzeri-conserved pathways and novel genes associated with neurogenesis. Aging Cell 2014, 13:965-974.
6. Beerman I., Rossi D.J. Epigenetic control of stem cell potential during homeostasis, aging, and disease. Cell Stem Cell 2015, 16:613-625.
7. Beerman I., Bock C., Garrison B.S., Smith Z.D., Gu H., Meissner A., Rossi D.J. Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell Stem Cell 2013, 12:413-425.
8. Benayoun B.A., Pollina E.A., Ucar D., Mahmoudi S., Karra K., Wong E.D., Devarajan K., Daugherty A.C., Kundaje A.B., Mancini E., et al. H3K4me3 breadth is linked to cell identity and transcriptional consistency. Cell 2014, 158:673-688.
9. Benayoun B.A., Pollina E.A., Brunet A. Epigenetic regulation of ageing: linking environmental inputs to genomic stability. Nat. Rev. Mol. Cell Biol. 2015, 16:593-610.
10. Berger S.L., Sassone-Corsi P. Metabolic signaling to chromatin. Cold Spring Harb. Perspect. Biol. 2015, Published online August 20, 2015. 10.1101/cshperspect.a019463.
11. Blackwell T.K., Steinbaugh M.J., Hourihan J.M., Ewald C.Y., Isik M. SKN-1/Nrf, stress responses, and aging in Caenorhabditis elegans. Free Radic. Biol. Med. 2015, 88(Pt B):290-301.
12. Bochkis I.M., Przybylski D., Chen J., Regev A. Changes in nucleosome occupancy associated with metabolic alterations in aged mammalian liver. Cell Rep. 2014, 9:996-1006.
13. Brandhorst S., Choi I.Y., Wei M., Cheng C.W., Sedrakyan S., Navarrete G., Dubeau L., Yap L.P., Park R., Vinciguerra M., et al. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 2015, 22:86-99.
14. Budovskaya Y.V., Wu K., Southworth L.K., Jiang M., Tedesco P., Johnson T.E., Kim S.K. An elt-3/elt-5/elt-6 GATA transcription circuit guides aging in C. elegans. Cell 2008, 134:291-303.
15. Burgess R.C., Misteli T., Oberdoerffer P. DNA damage, chromatin, and transcription: the trinity of aging. Curr. Opin. Cell Biol. 2012, 24:724-730.
16. Burkewitz K., Zhang Y., Mair W.B. AMPK at the nexus of energetics and aging. Cell Metab. 2014, 20:10-25.
17. Burkewitz K., Morantte I., Weir H.J., Yeo R., Zhang Y., Huynh F.K., Ilkayeva O.R., Hirschey M.D., Grant A.R., Mair W.B. Neuronal CRTC-1 governs systemic mitochondrial metabolism and lifespan via a catecholamine signal. Cell 2015, 160:842-855.
18. Cantó C., Menzies K.J., Auwerx J. NAD(+) metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab. 2015, 22:31-53.
19. Capell B.C., Drake A.M., Zhu J., Shah P.P., Dou Z., Dorsey J., Simola D.F., Donahue G., Sammons M., Rai T.S., et al. MLL1 is essential for the senescence-associated secretory phenotype. Genes Dev. 2016, 30:321-336.
20. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
21. Chang H.W., Shtessel L., Lee S.S. Collaboration between mitochondria and the nucleus is key to long life in Caenorhabditis elegans. Free Radic. Biol. Med. 2015, 78:168-178.
22. Chang J., Wang Y., Shao L., Laberge R.M., Demaria M., Campisi J., Janakiraman K., Sharpless N.E., Ding S., Feng W., et al. Clearance of senescent cells by ABT263 rejuvenates aged hematopoietic stem cells in mice. Nat. Med. 2016, 22:78-83.
23. Chen K., Chen Z., Wu D., Zhang L., Lin X., Su J., Rodriguez B., Xi Y., Xia Z., Chen X., et al. Broad H3K4me3 is associated with increased transcription elongation and enhancer activity at tumor-suppressor genes. Nat. Genet. 2015, 47:1149-1157.
24. Conboy I.M., Conboy M.J., Wagers A.J., Girma E.R., Weissman I.L., Rando T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433:760-764.
25. Dang W., Steffen K.K., Perry R., Dorsey J.A., Johnson F.B., Shilatifard A., Kaeberlein M., Kennedy B.K., Berger S.L. Histone H4 lysine 16 acetylation regulates cellular lifespan. Nature 2009, 459:802-807.
26. Dang W., Sutphin G.L., Dorsey J.A., Otte G.L., Cao K., Perry R.M., Wanat J.J., Saviolaki D., Murakami C.J., Tsuchiyama S., et al. Inactivation of yeast Isw2 chromatin remodeling enzyme mimics longevity effect of calorie restriction via induction of genotoxic stress response. Cell Metab. 2014, 19:952-966.
27. De Cecco M., Criscione S.W., Peckham E.J., Hillenmeyer S., Hamm E.A., Manivannan J., Peterson A.L., Kreiling J.A., Neretti N., Sedivy J.M. Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements. Aging Cell 2013, 12:247-256.
28. De Santa F., Totaro M.G., Prosperini E., Notarbartolo S., Testa G., Natoli G. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 2007, 130:1083-1094.
29. Domcke S., Bardet A.F., Adrian Ginno P., Hartl D., Burger L., Schübeler D. Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 2015, 528:575-579.
30. Dou Z., Xu C., Donahue G., Shimi T., Pan J.A., Zhu J., Ivanov A., Capell B.C., Drake A.M., Shah P.P., et al. Autophagy mediates degradation of nuclear lamina. Nature 2015, 527:105-109.
31. Eijkelenboom A., Burgering B.M. FOXOs: signalling integrators for homeostasis maintenance. Nat. Rev. Mol. Cell Biol. 2013, 14:83-97.
32. Eijkelenboom A., Mokry M., Smits L.M., Nieuwenhuis E.E., Burgering B.M. FOXO3 selectively amplifies enhancer activity to establish target gene regulation. Cell Rep. 2013, 5:1664-1678.
33. Feser J., Truong D., Das C., Carson J.J., Kieft J., Harkness T., Tyler J.K. Elevated histone expression promotes life span extension. Mol. Cell 2010, 39:724-735.
34. Fnu S., Williamson E.A., De Haro L.P., Brenneman M., Wray J., Shaheen M., Radhakrishnan K., Lee S.H., Nickoloff J.A., Hromas R. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining. Proc. Natl. Acad. Sci. USA 2011, 108:540-545.
35. Fontana L., Partridge L. Promoting health and longevity through diet: from model organisms to humans. Cell 2015, 161:106-118.
36. Fu V.X., Dobosy J.R., Desotelle J.A., Almassi N., Ewald J.A., Srinivasan R., Berres M., Svaren J., Weindruch R., Jarrard D.F. Aging and cancer-related loss of insulin-like growth factor 2 imprinting in the mouse and human prostate. Cancer Res. 2008, 68:6797-6802.
37. Garatachea N., Pareja-Galeano H., Sanchis-Gomar F., Santos-Lozano A., Fiuza-Luces C., Morán M., Emanuele E., Joyner M.J., Lucia A. Exercise attenuates the major hallmarks of aging. Rejuvenation Res. 2015, 18:57-89.
38. Gaudet F., Hodgson J.G., Eden A., Jackson-Grusby L., Dausman J., Gray J.W., Leonhardt H., Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science 2003, 300:489-492.
39. Gomes A.P., Price N.L., Ling A.J., Moslehi J.J., Montgomery M.K., Rajman L., White J.P., Teodoro J.S., Wrann C.D., Hubbard B.P., et al. Declining NAD(+) induces a pseudohypoxic state disrupting nuclear-mitochondrial communication during aging. Cell 2013, 155:1624-1638.
40. Graf T. Historical origins of transdifferentiation and reprogramming. Cell Stem Cell 2011, 9:504-516.
41. Grammatikakis I., Panda A.C., Abdelmohsen K., Gorospe M. Long noncoding RNAs(lncRNAs) and the molecular hallmarks of aging. Aging (Albany, N.Y.) 2014, 6:992-1009.
42. Greer E.L., Dowlatshahi D., Banko M.R., Villen J., Hoang K., Blanchard D., Gygi S.P., Brunet A. An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr. Biol. 2007, 17:1646-1656.
43. Greer E.L., Maures T.J., Hauswirth A.G., Green E.M., Leeman D.S., Maro G.S., Han S., Banko M.R., Gozani O., Brunet A. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 2010, 466:383-387.
44. Greer E.L., Maures T.J., Ucar D., Hauswirth A.G., Mancini E., Lim J.P., Benayoun B.A., Shi Y., Brunet A. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 2011, 479:365-371.
45. Greer E.L., Becker B., Latza C., Antebi A., Shi Y. Mutation of C. elegans demethylase spr-5 extends transgenerational longevity. Cell Res. 2016, 26:229-238.
46. Guarente L. Calorie restriction and sirtuins revisited. Genes Dev. 2013, 27:2072-2085.
47. Helin K., Dhanak D. Chromatin proteins and modifications as drug targets. Nature 2013, 502:480-488.
48. Herskowitz I. A regulatory hierarchy for cell specialization in yeast. Nature 1989, 342:749-757.
49. Horvath S. DNA methylation age of human tissues and cell types. Genome Biol. 2013, 14:R115.
50. Houtkooper R.H., Pirinen E., Auwerx J. Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 2012, 13:225-238.
51. Hsin H., Kenyon C. Signals from the reproductive system regulate the lifespan of C. elegans. Nature 1999, 399:362-366.
52. Hu Z., Chen K., Xia Z., Chavez M., Pal S., Seol J.H., Chen C.C., Li W., Tyler J.K. Nucleosome loss leads to global transcriptional up-regulation and genomic instability during yeast aging. Genes Dev. 2014, 28:396-408.
53. Ivanov A., Pawlikowski J., Manoharan I., van Tuyn J., Nelson D.M., Rai T.S., Shah P.P., Hewitt G., Korolchuk V.I., Passos J.F., et al. Lysosome-mediated processing of chromatin in senescence. J. Cell Biol. 2013, 202:129-143.
54. Jin C., Li J., Green C.D., Yu X., Tang X., Han D., Xian B., Wang D., Huang X., Cao X., et al. Histone demethylase UTX-1 regulates C. elegans life span by targeting the insulin/IGF-1 signaling pathway. Cell Metab. 2011, 14:161-172.
55. Kaeberlein M., McVey M., Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev. 1999, 13:2570-2580.
56. Katewa S.D., Akagi K., Bose N., Rakshit K., Camarella T., Zheng X., Hall D., Davis S., Nelson C.S., Brem R.B., et al. Peripheral circadian clocks mediate dietary restriction-dependent changes in lifespan and fat metabolism in Drosophila. Cell Metab. 2016, 23:143-154.
57. Kawahara T.L., Michishita E., Adler A.S., Damian M., Berber E., Lin M., McCord R.A., Ongaigui K.C., Boxer L.D., Chang H.Y., Chua K.F. SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span. Cell 2009, 136:62-74.
58. Kaya A., Lobanov A.V., Gladyshev V.N. Evidence that mutation accumulation does not cause aging in Saccharomyces cerevisiae. Aging Cell 2015, 14:366-371.
59. Kennedy B.K., Berger S.L., Brunet A., Campisi J., Cuervo A.M., Epel E.S., Franceschi C., Lithgow G.J., Morimoto R.I., Pessin J.E., et al. Geroscience: linking aging to chronic disease. Cell 2014, 159:709-713.
60. Kim J.Y., Kwak P.B., Weitz C.J. Specificity in circadian clock feedback from targeted reconstitution of the NuRD corepressor. Mol. Cell 2014, 56:738-748.
61. Kim J., Sturgill D., Tran A.D., Sinclair D.A., Oberdoerffer P. Controlled DNA double-strand break induction in mice reveals post-damage transcriptome stability. Nucleic Acids Res. 2016, 44:e64.
62. Kirchman P.A., Kim S., Lai C.Y., Jazwinski S.M. Interorganelle signaling is a determinant of longevity in Saccharomyces cerevisiae. Genetics 1999, 152:179-190.
63. Kondratov R.V. A role of the circadian system and circadian proteins in aging. Ageing Res. Rev. 2007, 6:12-27.
64. Kowalczyk M.S., Tirosh I., Heckl D., Rao T.N., Dixit A., Haas B.J., Schneider R.K., Wagers A.J., Ebert B.L., Regev A. Single-cell RNA-seq reveals changes in cell cycle and differentiation programs upon aging of hematopoietic stem cells. Genome Res. 2015, 25:1860-1872.
65. Labbadia J., Morimoto R.I. Proteostasis and longevity: when does aging really begin?. F1000Prime Rep. 2014, 6:7.
66. Labbadia J., Morimoto R.I. Repression of the heat shock response is a programmed event at the onset of reproduction. Mol. Cell 2015, 59:639-650.
67. Lapasset L., Milhavet O., Prieur A., Besnard E., Babled A., Aït-Hamou N., Leschik J., Pellestor F., Ramirez J.M., De Vos J., et al. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev. 2011, 25:2248-2253.
68. Larrieu D., Britton S., Demir M., Rodriguez R., Jackson S.P. Chemical inhibition of NAT10 corrects defects of laminopathic cells. Science 2014, 344:527-532.
69. Larson K., Yan S.J., Tsurumi A., Liu J., Zhou J., Gaur K., Guo D., Eickbush T.H., Li W.X. Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis. PLoS Genet. 2012, 8:e1002473.
70. Lauberth S.M., Nakayama T., Wu X., Ferris A.L., Tang Z., Hughes S.H., Roeder R.G. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013, 152:1021-1036.
71. Lee S.S., Kennedy S., Tolonen A.C., Ruvkun G. DAF-16 target genes that control C. elegans life-span and metabolism. Science 2003, 300:644-647.
72. Li L., Greer C., Eisenman R.N., Secombe J. Essential functions of the histone demethylase lid. PLoS Genet. 2010, 6:e1001221.
73. Li W., Prazak L., Chatterjee N., Grüninger S., Krug L., Theodorou D., Dubnau J. Activation of transposable elements during aging and neuronal decline in Drosophila. Nat. Neurosci. 2013, 16:529-531.
74. Lim J.P., Brunet A. Bridging the transgenerational gap with epigenetic memory. Trends Genet. 2013, 29:176-186.
75. Liu X., Secombe J. The histone demethylase KDM5 activates gene expression by recognizing chromatin context through its PHD reader motif. Cell Rep. 2015, 13:2219-2231.
76. Liu L., Cheung T.H., Charville G.W., Hurgo B.M., Leavitt T., Shih J., Brunet A., Rando T.A. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013, 4:189-204.
77. Lohse M.B., Zordan R.E., Cain C.W., Johnson A.D. Distinct class of DNA-binding domains is exemplified by a master regulator of phenotypic switching in Candida albicans. Proc. Natl. Acad. Sci. USA 2010, 107:14105-14110.
78. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
79. Lu T., Pan Y., Kao S.Y., Li C., Kohane I., Chan J., Yankner B.A. Gene regulation and DNA damage in the ageing human brain. Nature 2004, 429:883-891.
80. Lu T., Aron L., Zullo J., Pan Y., Kim H., Chen Y., Yang T.H., Kim H.M., Drake D., Liu X.S., et al. REST and stress resistance in ageing and Alzheimer's disease. Nature 2014, 507:448-454.
81. Luo G.Z., Blanco M.A., Greer E.L., He C., Shi Y. DNA N(6)-methyladenine: a new epigenetic mark in eukaryotes?. Nat. Rev. Mol. Cell Biol. 2015, 16:705-710.
82. Mahat D.B., Salamanca H.H., Duarte F.M., Danko C.G., Lis J.T. Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol. Cell 2016, 62:63-78.
83. Mair W., Morantte I., Rodrigues A.P., Manning G., Montminy M., Shaw R.J., Dillin A. Lifespan extension induced by AMPK and calcineurin is mediated by CRTC-1 and CREB. Nature 2011, 470:404-408.
84. Maures T.J., Greer E.L., Hauswirth A.G., Brunet A. The H3K27 demethylase UTX-1 regulates C. elegans lifespan in a germline-independent, insulin-dependent manner. Aging Cell 2011, 10:980-990.
85. Maures T.J., Booth L.N., Benayoun B.A., Izrayelit Y., Schroeder F.C., Brunet A. Males shorten the life span of C. elegans hermaphrodites via secreted compounds. Science 2014, 343:541-544.
86. McColl G., Killilea D.W., Hubbard A.E., Vantipalli M.C., Melov S., Lithgow G.J. Pharmacogenetic analysis of lithium-induced delayed aging in Caenorhabditis elegans. J. Biol. Chem. 2008, 283:350-357.
87. Mercken E.M., Carboneau B.A., Krzysik-Walker S.M., de Cabo R. Of mice and men: the benefits of caloric restriction, exercise, and mimetics. Ageing Res. Rev. 2012, 11:390-398.
88. Merkwirth C., Jovaisaite V., Durieux J., Matilainen O., Jordan S.D., Quiros P.M., Steffen K.K., Williams E.G., Mouchiroud L., Tronnes S.U., et al. Two conserved histone demethylases regulate mitochondrial stress-induced longevity. Cell 2016, Published online April 27, 2016. 10.1016/j.cell.2016.04.012.
89. Mertens J., Paquola A.C., Ku M., Hatch E., Böhnke L., Ladjevardi S., McGrath S., Campbell B., Lee H., Herdy J.R., et al. Directly reprogrammed human neurons retain aging-associated transcriptomic signatures and reveal age-related nucleocytoplasmic defects. Cell Stem Cell 2015, 17:705-718.
90. Michishita E., McCord R.A., Berber E., Kioi M., Padilla-Nash H., Damian M., Cheung P., Kusumoto R., Kawahara T.L., Barrett J.C., et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 2008, 452:492-496.
91. Mochida K., Oikawa Y., Kimura Y., Kirisako H., Hirano H., Ohsumi Y., Nakatogawa H. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 2015, 522:359-362.
92. Monnier P., Martinet C., Pontis J., Stancheva I., Ait-Si-Ali S., Dandolo L. H19 lncRNA controls gene expression of the imprinted gene network by recruiting MBD1. Proc. Natl. Acad. Sci. USA 2013, 110:20693-20698.
93. Mostoslavsky R., Chua K.F., Lombard D.B., Pang W.W., Fischer M.R., Gellon L., Liu P., Mostoslavsky G., Franco S., Murphy M.M., et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 2006, 124:315-329.
94. Ni Z., Ebata A., Alipanahiramandi E., Lee S.S. Two SET domain containing genes link epigenetic changes and aging in Caenorhabditis elegans. Aging Cell 2012, 11:315-325.
95. O'Brown Z.K., Van Nostrand E.L., Higgins J.P., Kim S.K. The inflammatory transcription factors NFκB, STAT1 and STAT3 drive age-associated transcriptional changes in the human kidney. PLoS Genet. 2015, 11:e1005734.
96. O'Sullivan R.J., Kubicek S., Schreiber S.L., Karlseder J. Reduced histone biosynthesis and chromatin changes arising from a damage signal at telomeres. Nat. Struct. Mol. Biol. 2010, 17:1218-1225.
97. Oberdoerffer P., Sinclair D.A. The role of nuclear architecture in genomic instability and ageing. Nat. Rev. Mol. Cell Biol. 2007, 8:692-702.
98. Oberdoerffer P., Michan S., McVay M., Mostoslavsky R., Vann J., Park S.K., Hartlerode A., Stegmuller J., Hafner A., Loerch P., et al. SIRT1 redistribution on chromatin promotes genomic stability but alters gene expression during aging. Cell 2008, 135:907-918.
99. Orozco-Solis R., Sassone-Corsi P. Circadian clock: linking epigenetics to aging. Curr. Opin. Genet. Dev. 2014, 26:66-72.
100. Pombo A., Dillon N. Three-dimensional genome architecture: players and mechanisms. Nat. Rev. Mol. Cell Biol. 2015, 16:245-257.
101. Prieur A., Besnard E., Babled A., Lemaitre J.M. p53 and p16(INK4A) independent induction of senescence by chromatin-dependent alteration of S-phase progression. Nat. Commun. 2011, 2:473.
102. Pu M., Ni Z., Wang M., Wang X., Wood J.G., Helfand S.L., Yu H., Lee S.S. Trimethylation of Lys36 on H3 restricts gene expression change during aging and impacts life span. Genes Dev. 2015, 29:718-731.
103. Rahman M.M., Sykiotis G.P., Nishimura M., Bodmer R., Bohmann D. Declining signal dependence of Nrf2-MafS-regulated gene expression correlates with aging phenotypes. Aging Cell 2013, 12:554-562.
104. Rai T.S., Adams P.D. Lessons from senescence: chromatin maintenance in non-proliferating cells. Biochim. Biophys. Acta 2012, 1819:322-331.
105. Rando T.A., Chang H.Y. Aging, rejuvenation, and epigenetic reprogramming: resetting the aging clock. Cell 2012, 148:46-57.
106. Rera M., Bahadorani S., Cho J., Koehler C.L., Ulgherait M., Hur J.H., Ansari W.S., Lo T., Jones D.L., Walker D.W. Modulation of longevity and tissue homeostasis by the Drosophila PGC-1 homolog. Cell Metab. 2011, 14:623-634.
107. 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., Ruvkun G. DAF-16 employs the chromatin remodeller SWI/SNF to promote stress resistance and longevity. Nat. Cell Biol. 2013, 15:491-501.
108. Rinn J.L., Chang H.Y. Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 2012, 81:145-166.
109. Rodier F., Campisi J. Four faces of cellular senescence. J. Cell Biol. 2011, 192:547-556.
110. Rufini A., Tucci P., Celardo I., Melino G. Senescence and aging: the critical roles of p53. Oncogene 2013, 32:5129-5143.
111. Salih D.A., Brunet A. FoxO transcription factors in the maintenance of cellular homeostasis during aging. Curr. Opin. Cell Biol. 2008, 20:126-136.
112. Salminen A., Huuskonen J., Ojala J., Kauppinen A., Kaarniranta K., Suuronen T. Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging. Ageing Res. Rev. 2008, 7:83-105.
113. Scaffidi P., Misteli T. Lamin A-dependent nuclear defects in human aging. Science 2006, 312:1059-1063.
114. Schmutte C., Yang A.S., Beart R.W., Jones P.A. Base excision repair of U:G mismatches at a mutational hotspot in the p53 gene is more efficient than base excision repair of T:G mismatches in extracts of human colon tumors. Cancer Res. 1995, 55:3742-3746.
115. Schroeder E.A., Raimundo N., Shadel G.S. Epigenetic silencing mediates mitochondria stress-induced longevity. Cell Metab. 2013, 17:954-964.
116. Schulz A.M., Haynes C.M. UPR(mt)-mediated cytoprotection and organismal aging. Biochim. Biophys. Acta 2015, 1847:1448-1456.
117. Sen P., Dang W., Donahue G., Dai J., Dorsey J., Cao X., Liu W., Cao K., Perry R., Lee J.Y., et al. H3K36 methylation promotes longevity by enhancing transcriptional fidelity. Genes Dev. 2015, 29:1362-1376.
118. Shah P.P., Donahue G., Otte G.L., Capell B.C., Nelson D.M., Cao K., Aggarwala V., Cruickshanks H.A., Rai T.S., McBryan T., et al. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev. 2013, 27:1787-1799.
119. Shi C., Murphy C.T. Mating induces shrinking and death in Caenorhabditis mothers. Science 2014, 343:536-540.
120. 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. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc. Natl. Acad. Sci. USA 2006, 103:8703-8708.
121. Siebold A.P., Banerjee R., Tie F., Kiss D.L., Moskowitz J., Harte P.J. Polycomb Repressive Complex 2 and Trithorax modulate Drosophila longevity and stress resistance. Proc. Natl. Acad. Sci. USA 2010, 107:169-174.
122. Simola D.F., Graham R.J., Brady C.M., Enzmann B.L., Desplan C., Ray A., Zwiebel L.J., Bonasio R., Reinberg D., Liebig J., Berger S.L. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 2016, 351:aac6633.
123. Sinclair D.A., Mills K., Guarente L. Molecular mechanisms of yeast aging. Trends Biochem. Sci. 1998, 23:131-134.
124. Sinha M., Jang Y.C., Oh J., Khong D., Wu E.Y., Manohar R., Miller C., Regalado S.G., Loffredo F.S., Pancoast J.R., et al. Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 2014, 344:649-652.
125. Slotkin R.K., Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 2007, 8:272-285.
126. Sun D., Luo M., Jeong M., Rodriguez B., Xia Z., Hannah R., Wang H., Le T., Faull K.F., Chen R., et al. Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal. Cell Stem Cell 2014, 14:673-688.
127. Sun N., Youle R.J., Finkel T. The mitochondrial basis of aging. Mol. Cell 2016, 61:654-666.
128. Sykiotis G.P., Bohmann D. Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev. Cell 2008, 14:76-85.
129. Tamayo A.G., Duong H.A., Robles M.S., Mann M., Weitz C.J. Histone monoubiquitination by Clock-Bmal1 complex marks Per1 and Per2 genes for circadian feedback. Nat. Struct. Mol. Biol. 2015, 22:759-766.
130. Taylor R.C. Aging and the UPR(ER). Brain Res. 2016, Published online April 8, 2016. 10.1016/j.brainres.2016.04.017.
131. Tebay L.E., Robertson H., Durant S.T., Vitale S.R., Penning T.M., Dinkova-Kostova A.T., Hayes J.D. Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic. Biol. Med. 2015, 88(Pt B):108-146.
132. 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. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010, 20:440-446.
133. Tian Y., Garcia G., Bian Q., Steffen K.K., Joe L., Wolff S., Meyer B.J., Dillin A. Mitochondrial stress induces chromatin reorganization to promote longevity and UPR(mt). Cell 2016, Published online April 28, 2016. 10.1016/j.cell.2016.04.011.
134. Tilstra J.S., Clauson C.L., Niedernhofer L.J., Robbins P.D. NF-κB in aging and disease. Aging Dis. 2011, 2:449-465.
135. Toiber D., Erdel F., Bouazoune K., Silberman D.M., Zhong L., Mulligan P., Sebastian C., Cosentino C., Martinez-Pastor B., Giacosa S., et al. SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Mol. Cell 2013, 51:454-468.
136. Tullet J.M., Hertweck M., An J.H., Baker J., Hwang J.Y., Liu S., Oliveira R.P., Baumeister R., Blackwell T.K. Direct inhibition of the longevity-promoting factor SKN-1 by insulin-like signaling in C. elegans. Cell 2008, 132:1025-1038.
137. Varela I., Cadiñanos J., Pendás A.M., Gutiérrez-Fernández A., Folgueras A.R., Sánchez L.M., Zhou Z., Rodríguez F.J., Stewart C.L., Vega J.A., et al. Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature 2005, 437:564-568.
138. Venkatraman A., He X.C., Thorvaldsen J.L., Sugimura R., Perry J.M., Tao F., Zhao M., Christenson M.K., Sanchez R., Yu J.Y., et al. Maternal imprinting at the H19-Igf2 locus maintains adult haematopoietic stem cell quiescence. Nature 2013, 500:345-349.
139. Vijg J., Suh Y. Genome instability and aging. Annu. Rev. Physiol. 2013, 75:645-668.
140. Wang Y., Navin N.E. Advances and applications of single-cell sequencing technologies. Mol. Cell 2015, 58:598-609.
141. Webb A.E., Pollina E.A., Vierbuchen T., Urbán N., Ucar D., Leeman D.S., Martynoga B., Sewak M., Rando T.A., Guillemot F., et al. FOXO3 shares common targets with ASCL1 genome-wide and inhibits ASCL1-dependent neurogenesis. Cell Rep. 2013, 4:477-491.
142. Webb A.E., Kundaje A., Brunet A. Characterization of the direct targets of FOXO transcription factors throughout evolution. Aging Cell 2016, Published online April 8, 2016. 10.1111/acel.12479.
143. Welch J.S., Ley T.J., Link D.C., Miller C.A., Larson D.E., Koboldt D.C., Wartman L.D., Lamprecht T.L., Liu F., Xia J., et al. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
144. Welstead G.G., Creyghton M.P., Bilodeau S., Cheng A.W., Markoulaki S., Young R.A., Jaenisch R. X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc. Natl. Acad. Sci. USA 2012, 109:13004-13009.
145. Willcox B.J., Donlon T.A., He Q., Chen R., Grove J.S., Yano K., Masaki K.H., Willcox D.C., Rodriguez B., Curb J.D. FOXO3A genotype is strongly associated with human longevity. Proc. Natl. Acad. Sci. USA 2008, 105:13987-13992.
146. Wood J.G., Hillenmeyer S., Lawrence C., Chang C., Hosier S., Lightfoot W., Mukherjee E., Jiang N., Schorl C., Brodsky A.S., et al. Chromatin remodeling in the aging genome of Drosophila. Aging Cell 2010, 9:971-978.
147. Yan H., Bonasio R., Simola D.F., Liebig J., Berger S.L., Reinberg D. DNA methylation in social insects: how epigenetics can control behavior and longevity. Annu. Rev. Entomol. 2015, 60:435-452.
148. Yuan T., Jiao Y., de Jong S., Ophoff R.A., Beck S., Teschendorff A.E. An integrative multi-scale analysis of the dynamic DNA methylation landscape in aging. PLoS Genet. 2015, 11:e1004996.
149. Zahn J.M., Poosala S., Owen A.B., Ingram D.K., Lustig A., Carter A., Weeraratna A.T., Taub D.D., Gorospe M., Mazan-Mamczarz K., et al. AGEMAP: a gene expression database for aging in mice. PLoS Genet. 2007, 3:e201.
150. Zampieri M., Ciccarone F., Calabrese R., Franceschi C., Bürkle A., Caiafa P. Reconfiguration of DNA methylation in aging. Mech. Ageing Dev. 2015, 151:60-70.
151. Zaret K.S., Carroll J.S. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 2011, 25:2227-2241.
152. Zhang J., Ohta T., Maruyama A., Hosoya T., Nishikawa K., Maher J.M., Shibahara S., Itoh K., Yamamoto M. BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress. Mol. Cell. Biol. 2006, 26:7942-7952.
153. Zhang R., Chen H.-Z., Liu D.-P. The four layers of aging. Cell Syst. 2015, 1:180-186.
154. Zhang W., Li J., Suzuki K., Qu J., Wang P., Zhou J., Liu X., Ren R., Xu X., Ocampo A., et al. Aging stem cells. a Werner syndrome stem cell model unveils heterochromatin alterations as a driver of human aging. Science 2015, 348:1160-1163.