Chromatin methylation and cardiovascular aging

Journal of Molecular and Cellular Cardiology

Volumn 83, Issue , 2015, Pages 21-31

  Illi, Barbara ^a   Ciarapica, Roberta ^b   Capogrossi, Maurizio C ^b  

^a CNR   (Italy)

^b LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Aging; Cardiovascular disease; DNA methylation; Histone methylation

Indexed keywords

DNA; HISTONE; POLYCOMB GROUP PROTEIN; CHROMATIN;

AGING; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASE; CHROMATIN; CONGESTIVE CARDIOMYOPATHY; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENETIC DRIFT; HEART ARRHYTHMIA; HEART FAILURE; HEART INFARCTION; HISTONE METHYLATION; HUMAN; HYPERTENSION; MOLECULAR INTERACTION; MYOCARDITIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGERIA; REVIEW; ANIMAL; CHEMISTRY; GENETIC EPIGENESIS; GENETICS; HEART MUSCLE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

AGING; ANIMALS; ARRHYTHMIAS, CARDIAC; ATHEROSCLEROSIS; CHROMATIN; DNA METHYLATION; EPIGENESIS, GENETIC; HEART FAILURE; HISTONES; HUMANS; MYOCARDIUM; POLYCOMB-GROUP PROTEINS; SIGNAL TRANSDUCTION;

EID: 84937973423     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2015.02.011     Document Type: Review

References (178)

1. López-Otín C., Blasco M.A., Partridge L., Serrano M., Kroemer G. The hallmarks of aging. Cell 2013, 153:1194-1217.
2. Berger S.L., Kouzarides T., Shiekhattar R., Shilatifard A. An operational definition of epigenetics. Genes Dev 2009, 23:781-783.
3. Aalami O.O., Fang T.D., Song H.M., Nacamuli R.P. Physiological features of aging persons. Arch Surg 2003, 138:1068-1076.
4. Loscalzo J., Handy D.E. Epigenetic modifications: basic mechanisms and role in cardiovascular disease (2013 Grover Conference series). Pulm Circ 2014, 4:169-174.
5. Napoli C., Palinski W. Hypercholesterolemia during pregnancy influences the later development of atherosclerosis: clinical and pathogenic implications. Eur Heart J 2001, 22:4-9.
6. Barker D.J. The fetal and infant origins of disease. Eur J Clin Invest 1995, 25:457-463.
7. Barker D.J. Fetal origins of cardiovascular disease. Ann Med 1999, 31:3-6.
8. Santos F., Hyslop L., Stojkovic P., Leary C., Murdoch A., Reik W., et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod 2010, 25:2387-2395.
9. Scherrer U., Rimoldi S.F., Rexhaj E., Stuber T., Duplain H., Garcin S., et al. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation 2012, 125:1890-1896.
10. Rexhaj E., Bloch J., Jayet P.Y., Rimoldi S.F., Dessen P., Mathieu C., et al. Fetal programming of pulmonary vascular dysfunction in mice: role of epigenetic mechanisms. Am J Physiol Heart Circ Physiol 2011, 301:H247-H252.
11. Peterson C.L., Laniel M.A. Histones and histone modifications. Curr Biol 2004, 14:R546-R551.
12. Prokhortchouk E., Defossez P.A. The cell biology of DNA methylation in mammals. Biochim Biophys Acta 2008, 1783:2167-2173.
13. Smith B.C., Denu J.M. Chemical mechanism of histone lysine and arginin modifications. Biochim Biophys Acta 2009, 1789:45-57.
14. Carthew R.W., Sontheimer E.J. Origins and mechanisms of miRNAs and siRNAs. Cell 2009, 20:642-655.
15. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 2006, 31:89-97.
16. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 2005, 74:481-514.
17. Jeltsch A., Nellen W., Lyko F. Two substrates are better than one: dual specificities for Dnmt2 methyltransferases. Trends Biochem Sci 2006, 31:306-308.
18. Goll M.G., Kirpekar F., Maggert K.A., Yoder J.A., Hsieh C.L., Zhang X., et al. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 2006, 311:395-398.
19. Jeltsch A. Molecular enzymology of mammalian DNA methyltransferases. Curr Top Microbiol Immunol 2006, 301:203-225.
20. Jones P.L., Veenstra G.J., Wade P.A., Vermaak D., Kass S.U., Landsberger N., et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998, 19:187-191.
21. Harikrishnan K.N., Chow M.Z., Baker E.K., Pal S., Bassal S., Brasacchio D., et al. Brahma links the SWI/SNF chromatin-remodeling complex with MeCP2-dependent transcriptional silencing. Nat Genet 2005, 37:254-264.
22. Tsutsui T., Fukasawa R., Shynmyouzu K., Nagakawa R., Tobe K., Tanaka A., et al. Mediator complex recruits epigenetic regulators via its two cyclin-dependent kinase subunits to repress transcription of immune response genes. J Biol Chem 2013, 288:20955-20965.
23. Clouaire T., Stancheva I. Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin?. Cell Mol Life Sci 2008, 85:1509-1522.
24. Nan X., Ng H.H., Johnson C.A., Laherty C.D., Turner B.M., Eisenman R.N., et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998, 393:386-389.
25. Prokhortchouk A., Hendrich B., Jørgensen H., Ruzov A., Wilm M., Georgiev G., et al. The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev 2001, 15:1613-1618.
26. Filion G.J., Zhenilo S., Salozhin S., Yamada D., Prokhortchouk E., Defossez P.A. A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol Cell Biol 2006, 26:169-181.
27. Mori T., Ikeda D.D., Yamaguchi Y., Unoki M. NIRF project. NIRF/UHRF2 occupies a central position in the cell cycle network and allows coupling with the epigenetic landscape. FEBS Lett 2012, 586:1570-1583.
28. Bronner C., Fuhrmann G., Chédin F.L., Macaluso M., Dhe-Paganon S. UHRF1 links the histone code and DNA methylation to ensure faithful epigenetic memory inheritance. Genet Epigenet 2009, 2012:29-36.
29. Delaval K., Wagschal A., Feil R. Epigenetic deregulation of imprinting in congenital diseases of aberrant growth. Bioessays 2006, 28:453-459.
30. Schulz W.A., Steinhoff C., Florl A.R. Methylation of endogenous human retroelements in health and disease. Curr Top Microbiol Immunol 2006, 310:211-250.
31. Rakyan V.K., Hildmann T., Novik K.L., Lewin J., Tost J., Cox S.V., et al. DNA methylation profiling of the human major histocompatibility complex: a pilot study for the human epigenome project. PLoS Biol 2004, 2:e405.
32. Illingworth R., Kerr A., Desousa D., Jørgensen H., Ellis P., Stalker J., et al. A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 2008, 6:e22.
33. Macleod D., Charlton J., Mullins J., Bird A.P. Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev 1994, 8:2282-2292.
34. Brandeis M., Frank D., Keshet I., Siegfried Z., Mendelsohn M., Nemes A., et al. Sp1 elements protect a CpG island from de novo methylation. Nature 1994, 371:435-438.
35. Mummaneni P., Yates P., Simpson J., Rose J., Turker M.S. The primary function of a redundant Sp1 binding site in the mouse aprt gene promoter is to block epigenetic gene inactivation. Nucleic Acids Res 1998, 26:5163-5169.
36. Bestor T.H., Edwards J.R., Boulard M. Notes on the role of dynamic DNA methylation in mammalian development. Proc Natl Acad Sci U S A 2014, [pii: 201415301].
37. Lee D.U., Agarwal S., Rao A. Th2 lineage commitment and efficient IL-4 production involves extended demethylation of the IL-4 gene. Immunity 2002, 16:649-660.
38. Gilsbach R., Preissl S., Grüning B.A., Schnick T., Burger L., Benes V., et al. Dynamic DNA methylation orchestrates cardiomyocyte development, maturation and disease. Nat Commun 2014, 5:5288.
39. Lister R., Mukamel E.A., Nery J.R., Urich M., Puddifoot C.A., Johnson N.D., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
40. Levenson J.M., Roth T.L., Lubin F.D., Miller C.A., Huang I.C., Desai P., et al. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 2006, 281:15763-15773.
41. Akbarian S., Beeri M.S., Haroutunian V. Epigenetic determinants of healthy and diseased brain aging and cognition. JAMA Neurol 2013, 70:711-718.
42. Jones P.A., Wolkowicz M.J., Rideout W.M., Gonzales F.A., Marziasz C.M., Coetzee G.A., et al. De novo methylation of the MyoD1 CpG island during the establishment of immortal cell lines. Proc Natl Acad Sci U S A 1990, 87:6117-6121.
43. Patel S.A., Bhambra U., Charalambous M.P., David R.M., Edwards R.J., Lightfoot T., et al. Interleukin-6 mediated upregulation of CYP1B1 and CYP2E1 in colorectal cancer involves DNA methylation, miR27b and STAT3. Br J Cancer 2014, 111:2287-2296.
44. Chen C.C., Wang K.Y., Shen C.K. The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 2012, 287:33116-33121.
45. Chen C.C., Wang K.Y., Shen C.K. DNA 5-methylcytosine demethylation activities of the mammalian DNA methyltransferases. J Biol Chem 2013, 288:9084-9091.
46. Seisenberger S., Peat J.R., Hore T.A., Santos F., Dean W., Reik W. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Philos Trans R Soc Lond B Biol Sci 2013, 368:20110330.
47. Valinluck V., Sowers L.C. Inflammation-mediated cytosine damage: a mechanistic link between inflammation and the epigenetic alterations in human cancers. Cancer Res 2007, 67:5583-5586.
48. Spruijt C.G., Gnerlich F., Smits A.H., Pfaffeneder T., Jansen P.W., Bauer C., et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 2013, 152:1146-1159.
49. Ma D.K., Jang M.H., Guo J.U., Kitabatake Y., Chang M.L., Pow-Anpongkul N., et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009, 323:1074-1077.
50. Guo J.U., Su Y., Zhong C., Ming G.L., Song H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145:423-434.
51. Zhou L., Cheng X., Connolly B.A., Dickman M.J., Hurd P.J., Hornby D.P. Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases. J Mol Biol 2002, 321:591-599.
52. Oliveira A.M., Hemstedt T.J., Bading H. Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nat Neurosci 2012, 15:1111-1113.
53. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
54. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010, 11:607-620.
55. Issa J.P. Aging and epigenetic drift: a vicious cycle. J Clin Invest 2014, 124:24-29.
56. Johansson A., Enroth S., Gyllensten U. Continuous aging of the human DNA methylome throughout the human lifespan. PLoS One 2013, 8:e67378.
57. Cheung I., Shulha H.P., Jiang Y., Matevossian A., Wang J., Weng Z., et al. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc Natl Acad Sci U S A 2010, 107:8824-8829.
58. Heyn H., Li N., Ferreira H.J., Moran S., Pisano D.G., Gomez A., et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A 2012, 109:10522-10527.
59. 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 Jan 24 2013, 49(2):359-367.
60. 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, 34:169-179.
61. Bollati V., Schwartz J., Wright R., Litonjua A., Tarantini L., Suh H., et al. Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev 2009, 130:234-239.
62. Lister R., Pelizzola M., Dowen R.H., Hawkins R.D., Hon G., Tonti-Filippini J., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
63. Shen L., Kondo Y., Guo Y., Zhang J., Zhang L., Ahmed S., et al. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet 2007, 3:2023-2036.
64. Gordon L., Joo J.E., Powell J.E., Ollikainen M., Novakovic B., Li X., et al. Neonatal DNA methylation profile in human twins is specified by a complex interplay between intrauterine environmental and genetic factors, subject to tissue-specific influence. Genome Res 2012, 22:1395-1406.
65. Bocklandt S., Lin W., Sehl M.E., Sánchez F.J., Sinsheimer J.S., Horvath S., et al. Epigenetic predictor of age. PLoS One 2011, 6:e14821.
66. Mazin A.L. Suicidal function of DNA methylation in age-related genome disintegration. Ageing Res Rev 2009, 8:314-327.
67. Reynolds L.M., Taylor J.R., Ding J., Lohman K., Johnson C., Siscovick D., et al. Age-related variations in the methylome associated with gene expression in human monocytes and T cells. Nat Commun 2014, 5:5366.
68. Shipony Z., Mukamel Z., Cohen N.M., Landan G., Chomsky E., Zeliger S.R., et al. Dynamic and static maintenance of epigenetic memory in pluripotent and somatic cells. Nature 2014, 513:115-119.
69. Estécio M.R., Gallegos J., Vallot C., Castoro R.J., Chung W., Maegawa S., et al. Genome architecture marked by retrotransposons modulates predisposition to DNA methylation in cancer. Genome Res 2010, 20:1369-1382.
70. Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM Predicting aberrant CpG island methylation. Proc Natl Acad Sci U S A 2003, 100:12253-12258.
71. Rakyan V.K., Down T.A., Maslau S., Andrew T., Yang T.P., Beyan H., et al. Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 2010, 20:434-439.
72. Chambers S.M., Shaw C.A., Gatza C., Fisk C.J., Donehower L.A., Goodell M.A. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS Biol 2007, 5:e201.
73. West J., Beck S., Wang X., Teschendorff A.E. An integrative network algorithm identifies age-associated differential methylation interactome hotspots targeting stem-cell differentiation pathways. Sci Rep 2013, 3:1630.
74. van den Boom V., Kooistra S.M., Boesjes M., Geverts B., Houtsmuller A.B., Monzen K., et al. UTF1 is a chromatin-associated protein involved in ES cell differentiation. Cell Biol 2007, 178:913-924.
75. Brack A.S., Conboy M.J., Roy S., Lee M., Kuo C.J., Keller C., et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007, 317:807-810.
76. Taby R., Issa J.P. Cancer epigenetics. CA Cancer J Clin 2010, 60:376-392.
77. Dechat T., Pfleghaar K., Sengupta K., Shimi T., Shumaker D.K., Solimando L., et al. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008, 22:832-853.
78. Gonzalez J.M., Pla D., Perez-Sala D., Andrei V. A-type lamins and Hutchinson-Gilford progeria syndrome: pathogenesis and therapy. Front Biosci (Schol Ed) 2011, 3:1133-1146.
79. Kubben N., Adriaens M., Meuleman W., Voncken J.W., van Steensel B., Misteli T. Mapping of lamin A- and progerin-interacting genome regions. Chromosoma 2012, 121:447-464.
80. Arancio W., Pizzolanti G., Genovese S.I., Pitrone M., Giordano C. Epigenetic involvement in Hutchinson-Gilford progeria syndrome: a mini-review. Gerontology 2014, 60:197-203.
81. Heyn H., Moran S., Esteller M. Aberrant DNA methylation profiles in the premature aging disorders Hutchinson-Gilford Progeria and Werner syndrome. Epigenetics 2013, 8:28-33.
82. Clark J.P., Lau N.C. Piwi proteins and piRNAs step onto the systems biology stage. Adv Exp Med Biol 2014, 825:159-197.
83. Hwang I.K., Moon S.M., Yoo K.Y., Li H., Kwon H.D., Hwang H.S., et al. c-Myb immunoreactivity, protein and mRNA levels significantly increase in the aged hippocampus proper in gerbils. Neurochem Res 2007, 32:1091-1097.
84. Lee Y.H., Lee N.H., Bhattarai G., Hwang P.H., Kim T.I., Jhee E.C., et al. c-myb has a character of oxidative stress resistance in aged human diploid fibroblasts: regulates SAPK/JNK and Hsp60 pathway consequently. Biogerontology 2010, 11:267-274.
85. Kafri T., Ariel M., Brandeis M., Shermer R., Urven L., Mc Carrey J., et al. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germline. Genes Dev 1992, 6:705-714.
86. Ooi S.K., Qiu C., Bernstein E., Li K., Jia D., Yang Z., et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007, 448:714-717.
87. Meissner A., Mikkelsen T.S., Gu H., Wernig M., Hanna J., Sivachenko A., et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770.
88. Okitsu C.Y., Hsieh C.L. DNA methylation dictates histone H3K4 methylation. Mol Cell Biol 2007, 27:2746-2757.
89. Feldman N., Gerson A., Fang J., Li E., Zhang Y., Shinkai Y., et al. G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol 2006, 8:188-194.
90. Lehnertz B., Ueda Y., Derijck A.A., Braunschweig U., Perez-Burgos L., Kubicek S., et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr Biol 2003, 13:1192-1200.
91. Fuks F., Hurd PJ P., Deplus R., Kouzarides T. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res 2003, 31:2305-2312.
92. Estève P.O., Chin H.G., Smallwood A., Feehery G.R., Gangisetty O., Karpf A.R., et al. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 2006, 20:3089-3103.
93. Ordovás J.M., Smith C.E. Epigenetics and cardiovascular disease. Nat Rev Cardiol 2010, 7:510-519.
94. Yideng J., Jianzhong Z., Ying H., Juan S., Jinge Z., Shenglan W., et al. Homocysteine-mediated expression of SAHH, DNMTs, MBD2, and DNA hypomethylation potential pathogenic mechanism in VSMCs. DNA Cell Biol 2007, 26:603-611.
95. Naeem N., Haneef K., Kabir N., Iqbal H., Jamall S., Salim A. DNA methylation inhibitors, 5-azacytidine and zebularine potentiate the transdifferentiation of rat bone marrow mesenchymal stem cells into cardiomyocytes. Cardiovasc Ther 2013, 31:201-209.
96. Mann J., Oakley F., Akiboye F., Elsharkawy A., Thorne A.W., Mann D.A. Regulation of myofibroblast transdifferentiation by DNA methylation and MeCP2: implications for wound healing and fibrogenesis. Cell Death Differ 2007, 14:275-285.
97. Active and passive tobacco exposure: a serious pediatric health problem. A statement from the Committee on Atherosclerosis and Hypertension in Children, Council on Cardiovascular Disease in the Young, American Heart Association. Circulation 1994, 90:2581-2590.
98. Breton C.V., Byun H.M., Wenten M., Pan F., Yang A., Gilliland F.D. Prenatal tobacco smoke exposure affects global and gene-specific DNA methylation. Am J Respir Crit Care Med 2009, 180:462-467.
99. Yheijmans B.T., Tobi E.W., Stein A.D., Putter H., Blauw G.J., Susser E.S., et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A 2008, 105:17046-17049.
100. Guay S.P., Légaré C., Houde A.A., Mathieu P., Bossé Y., Bouchard L. Acetylsalicylic acid, aging and coronary artery disease are associated with ABCA1 DNA methylation in men. Clin Epigenetics 2014, 6:14.
101. Lund G., Andersson L., Lauria M., Lindholm M., Fraga F., Villar-Garea A., et al. DNA methylation polymorphisms precede any histological sign of atherosclerosis in mice lacking apolipoprotein E. J Biol Chem 2004, 279:29147-29154.
102. Losordo D.W., Kearney M., Kim E.A., Jekanowski J., Isner J.M. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation 1994, 89:1501-1510.
103. Post W.S., Goldschmidt-Clermont P.J, Wilhide C.C., Heldman A.W., Sussman M.S., Ouyang P., et al. Methylation of the estrogen receptor gene is associated with aging and atherosclerosis in the cardiovascular system. Cardiovasc Res 1999, 43:985-991.
104. Kim J., Kim J.Y., Song K.S., Lee Y.H., Seo J.S., Jelinek J., et al. Epigenetic changes in estrogen receptor beta gene in atherosclerotic cardiovascular tissues and in-vitro vascular senescence. Biochim Biophys Acta 2007, 1772:72-80.
105. Connelly J.J., Cherepanova O.A., Cherepanova J.F., Doss J.F., Karaoli T., Lillard T.S., Markunas C.A. Epigenetic regulation of COL15A1 in smooth muscle cell replicative aging and atherosclerosis. Hum Mol Genet 2013, 22:5107-5120.
106. Lowe D., Raj K. Premature aging induced by radiation exhibits proatherosclerotic effects mediated by epigenetic activation of CD44 expression. Aging Cell 2014, 13:900-910.
107. Sharma P., Kumar J., Garg G., Kumar A., Patowary A., Karthikeyan G., et al. Detection of altered global DNA methylation in coronary artery disease patients. DNA Cell Biol 2008, 27:357-365.
108. Zaina S., Heyn H., Carmona F.J., Varol N., Sayols S., Condom E. DNA methylation map of human atherosclerosis. Circ Cardiovasc Genet 2014, 7:692-700.
109. Olson E.N. Gene regulatory networks in the evolution and development of the heart. Science 2006, 313:1922-1927.
110. Haas J., Frese K.S., Park Y.J., Keller A., Vogel B., Lindroth A.M., et al. Alterations in cardiac DNA methylation in human dilated cardiomyopathy. EMBO Mol Med 2013, 5:413-429.
111. Movassagh M., Choy M.K., Knowles D.A., Cordeddu L., Haider S., Down T., et al. Distinct epigenomic features in end-stage failing human hearts. Circulation 2011, 124:2411-2422.
112. Taegtmeyer H., Sen S., Vela D. Return to the fetal gene program: a suggested metabolic link to gene expression in the heart. Ann N Y Acad Sci Feb. 2010, 1188:191-198.
113. Mancini-DiNardo D., Steele S.J., Ingram R.S., Tilghman S.M. A differentially methylated region within the gene Kcnq1 functions as an imprinted promoter and silencer. Hum Mol Genet 2003, 12:283-294.
114. Ritchie M.D., Rowan S., Kucera G., Stubblefield T., Blair M., Carter S., et al. Chromosome 4q25 variants are genetic modifiers of rare ion channel mutations associated with familial atrial fibrillation. J Am Coll Cardiol 2012, 60:1173-1181.
115. Olesen M.S., Andreasen L., Jabbari J., Refsgaard L., Haunsø S., Olesen S.P., et al. Very early-onset lone atrial fibrillation patients have a high prevalence of rare variants in genes previously associated with atrial fibrillation. Heart Rhythm 2014, 11:246-251.
116. El Harchi A., Zhang H., Hancox J.C. The S140G KCNQ1 atrial fibrillation mutation affects 'I(KS)' profile during both atrial and ventricular action potentials. J Physiol Pharmacol 2010, 61:759-764.
117. Fatima N., Schooley J.F., Claycomb W.C., Flagg T.P. Promoter DNA methylation regulates murine SUR1 (Abcc8) and SUR2 (Abcc9) expression in HL-1 cardiomyocytes. PLoS One 2012, 7:e41533.
118. Baccarelli A., Wright R., Bollati V., Litonjua A., Zanobetti A., Tarantini L., et al. Ischemic heart disease and stroke in relation to blood DNA methylation. Epidemiology 2010, 21:819-828.
119. Bannister A.J., Schneider R., Kouzarides T. Histone methylation: dynamic or static?. Cell 2002, 109:801-806.
120. Rea S., Eisenhaber F., O'Carroll D., Strahl B.D., Sun Z.W., Schmid M., et al. Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 2000, 406:593-599.
121. Dillon S.C., Zhang X., Trievel R.C., Cheng X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol 2005, 6:227.
122. Black J.C., Van Rechem C., Whetstine J.R. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell 2012, 48:491-507.
123. Okada Y., Feng Y., Lin Y., Jiang Q., Li Y., Coffield V.M., et al. hDOT1L links histone methylation to leukemogenesis. Cell 2005, 121:167-178.
124. van Leeuwen F., Gafken P.R., Gottschling D.E. Dot1p modulates silencing in yeast by methylation of the nucleosome core. Cell 2002, 109:745-756.
125. Peters A.H., O'Carroll D., Scherthan H., Mechtler K., Sauer S., Schöfer C., et al. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 2001, 107:323-337.
126. Peters A.H., Kubicek S., Mechtler K., O'Sullivan R.J., Derijck A.A., Perez-Burgos L., et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol Cell 2003, 12:1577-1589.
127. Tachibana M., Sugimoto K., Nozaki M., Ueda J., Ohta T., Ohki M., et al. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis. Genes Dev 2002, 16:1779-1791.
128. Nishioka K., Rice J.C., Sarma K., Erdjument-Bromage H., Werner J., Wang Y., et al. PRSet7 is a nucleosome-specific methyltransferase that modifies lysine 20 of histone H4 and is associated with silent chromatin. Mol Cell 2002, 9:1201-1213.
129. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
130. Milne T.A., Briggs S.D., Brock H.W., Martin M.E., Gibbs D., Allis C.D., et al. MLL targets SET domain methyltransferase activity to Hox gene promoters. Mol Cell 2002, 10:1107-1117.
131. Dou Y., Milne T.A., Ruthenburg A.J., Lee S., Lee J.W., Verdine G.L., et al. Regulation of MLL1 H3K4 methyltransferase activity by its core components. Nat Struct Mol Biol 2006, 13:713-779.
132. McCauley B.S., Dang W. Histone methylation and aging: lessons learned from model systems. Biochim Biophys Acta 2014, 1839:1454-1462.
133. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
134. Tsukada Y., Zhang Y. Purification of histone demethylases from HeLa cells. Methods 2006, 40:318-326.
135. Iwase S., Lan F., Bayliss P., de la Torre-Ubieta L., Huarte M., Qi H.H., et al. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007, 128:1077-1088.
136. Cloos P.A., Christensen J., Agger K., Maiolica A., Rappsilber J., Antal T., et al. The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 2006, 442:307-311.
137. Klose R.J., Yamane K., Bae Y., Zhang D., Erdjument-Bromage H., Tempst P., et al. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 2006, 442:312-316.
138. Trojer P., Zhang J., Yonezawa M., Schmidt A., Zheng H., Jenuwein T., et al. Dynamic histone H1 isotype 4 methylation and demethylation by histone lysine methyltransferase G9a/KMT1C and the Jumonji domain-containing JMJD2/KDM4 proteins. J Biol Chem 2009, 284:8395-8405.
139. Whetstine J.R., Nottke A., Lan F., Huarte M., Smolikov S., Chen Z., et al. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 2006, 125:467-481.
140. Gayatri S., Bedford M.T. Readers of histone methylarginine marks. Biochim Biophys Acta 1839, 2014:702-710.
141. Chang B., Chen Y., Zhao Y., Bruick R.K. JMJD6 is a histone arginine demethylase. Science 2007, 318:444-447.
142. Hyllus D., Stein C., Schnabel K., Schiltz E., Imhof A., Dou Y., et al. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev 2007, 21:3369-3380.
143. Iberg A.N., Espejo A., Cheng D., Kim D., Michaud-Levesque J., Richard S., et al. Arginine methylation of the histone H3 tail impedes effector binding. J Biol Chem 2008, 283:3006-3010.
144. Zhan M., Yamaza H., Sun Y., Sinclair J., Li H., Zou S. Temporal and spatial transcriptional profiles of aging in Drosophila melanogaster. Genome Res 2007, 17:1236-1243.
145. Feser J., Tyler J. Chromatin structure as a mediator of aging. FEBS Lett 2011, 585:2041-2048.
146. Tsurumi A., Li W.X. Global heterochromatin loss: a unifying theory of aging?. Epigenetics 2012, 7:680-688.
147. Shelton D.N., Chang E., Whittier P.S., Choi D., Funk W.D. Microarray analysis of replicative senescence. Curr Biol 1999, 9:939-945.
148. Narita M., Nũnez S., Heard Narita M., Lin A.W., Hearn S.A. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003, 133:703-716.
149. Chandra T., Narita M. High-order chromatin structure and the epigenome in SAHFs. Nucleus 2013, 4:23-28.
150. Shumaker D.K., Dechat T., Kohlmaier A., Adam S.A., Bozovsky M.R., Erdos M.R., et al. Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci U S A 2006, 103:8703-8708.
151. Larson K., Yan S.-J., Tsurumi A., Liu J., Zhou J., Gaur K., et al. Heterochromatin formation promotes longevity and represses ribosomal RNA synthesis. PLoS Genet 2012, 8:e1002473.
152. Wood J.G., Hillenmeyer S., Lawrence C., Chang C., Hosier S., Lightfoot W., et al. Chromatin remodeling in the aging genome of Drosophila. Aging Cell 2010, 9:971-978.
153. Han Y., Han D., Yan Z., Boyd-Kirkup J.D., Green C.D., Khaitovich P., et al. Stress associated H3K4 methylation accumulates during postnatal development and aging of rhesus macaque brain. Aging Cell 2012, 11:1055-1064.
154. Greer E.L., Maures T.J., Hauswirth A.G., Green E.M., Leeman D.S., Maro G.S., et al. Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 2010, 466:383-387.
155. Kourtis N., Tavernarakis N. Cellular stress response pathways and ageing: intricate molecular relationships. EMBO J 2011, 30:2520-2531.
156. Williams J.S.Y., Adler G.K., Khalil R.A., Romero J.R., Sinha S., Ponnuchamy B., et al. Genetic alteration of a histone demethylase is associated with altered aldosterone and vascular responsiveness: an intermediate phenotype of human hypertension. Hypertension 2007, 52:E38.
157. Pojoga L.H., Williams J.S., Yao T.M., Kumar A., Raffetto J.D., do Nascimento G.R., et al. Histone demethylase LSD1 deficiency during high-salt diet is associated with enhanced vascular contraction, altered NO-cGMP relaxation pathway, and hypertension. Am J Physiol Heart Circ Physiol 2011, 301:H1862-H1871.
158. Pamukcu B., Lip G.Y., Shantsila E. The nuclear factor-kappa B pathway in atherosclerosis: a potential therapeutic target for atherothrombotic vascular disease. Thromb Res 2011, 128:117-123.
159. Reddy MA M.A., Villeneuve L.M., Wang M., Lanting L., Natarajan R. Role of the lysine-specific demethylase 1 in the proinflammatory phenotype of vascular smooth muscle cells of diabetic mice. Circ Res 2008, 103:615-623.
160. De Santa F., Totano M.G., Prosperino 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.
161. Chen X., Niroomand F., Liu Z., Zankl A., Katus H.A., Jahn L., et al. Expression of nitric oxide related enzymes in coronary heart disease. Basic Res Cardiol 2006, 101:346-353.
162. Schwartz B., Pirrotta V. A new world of Polycombs: unexpected partnerships and emerging functions. Nat Rev Genet 2013, 14:853-864.
163. Delgado-Olguín P., Huang Y., Li X., Christodoulou D., Seidman C.E., Seidman J., et al. Epigenetic repression of cardiac progenitor gene expression by Ezh2 is required for postnatal cardiac homeostasis. Nat Genet 2012, 44:343-347.
164. He A., Ma Q., Cao J., von Gise A., Zhou P., Xie H., et al. Polycomb repressive complex 2 regulates normal development of the mouse heart. Circ Res 2012, 110:406-415.
165. Yang T., Zhang G.F., Chen X.F., Gu H.H., Fu S.Z., Xu H.F., et al. MicroRNA-214 provokes cardiac hypertrophy via repression of EZH2. Biochem Biophys Res Commun 2013, 436:578-584.
166. Lai H.L., Grachoff M., McGinley A.L., Khan F.F., Warren C.M., Chowdhury S.A., et al. Maintenance of adult cardiac function requires the chromatin factor Asxl2. J Mol Cell Cardiol 2012, 53:734-741.
167. Villeneuve L.M., Reddy M.A., Lanting L.L., Wang M., Meng L., Natarajan R. Epigenetic histone H3 lysine 9 methylation in metabolic memory and inflammatory phenotype of vascular smooth muscle cells in diabetes. Proc Natl Acad Sci U S A 2008, 105:9047-9052.
168. El Osta A., Brasacchio D., Yao D., Pocai A., Jones P.L., Roeder R.G., et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008, 205:2409-2417.
169. Kumar A., Kumar S., Vikram A., Hoffman T.A., Naqvi A., Lewarchik C.M., et al. Histone and DNA methylation-mediated epigenetic downregulation of endothelial Kruppel-like factor 2 by low-density lipoprotein cholesterol. Arterioscler Thromb Vasc Biol 2012, 33:1936-1942.
170. Bracken A.P., Kleine-Kohlbrecher D., Dietrich N., Pasini D., Gargiulo G., Beekman C., et al. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev 2007, 21:525-530.
171. Sdek P., Zhao P., Wang Y., Huang C.J., Ko C.Y., Butler P.C., et al. Rb and p130 control cell cycle gene silencing to maintain the postmitotic phenotype in cardiac myocytes. J Cell Biol 2011, 194:407-423.
172. Gil J., Peters G. Regulation of the INK4b-ARF-INK4a tumour suppressor locus: all for one or one for all. Nat Rev Mol Cell Biol 2006, 7:667-677.
173. Jacobs J.J., Kieboom K., Marino S., DePinho R.A., van Lohuizen M.T. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999, 397:164-168.
174. Chen H., Gu X., Su I.H., Bottino R., Contreras J.L., Tarakhovsky A., et al. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 2009, 23:975-985.
175. Zhou J.X., Dhawan S., Fu H., Snyder E., Bottino R., Kundu S., et al. Combined modulation of Polycomb and trithorax genes rejuvenates β cell replication. J Clin Invest 2013, 123:4849-4858.
176. Nicholls S.J., Gordon A., Johannson J., Ballantyne C.M., Barter P.J., Brewer H.B., et al. ApoA-I induction as a potential cardioprotective strategy: rationale for the SUSTAIN and ASSURE studies. Cardiovasc Drugs Ther 2012, 26:181-187.
177. Aslibekyan S., Claas S.A., Arnett D.K. Clinical applications of epigenetics in cardiovascular disease: the long road ahead. Transl Res 2015, 165:143-153.
178. Liu Y., Liu K., Qin S., Xu C., Min J. Epigenetic targets and drug discovery: part 1: histone methylation. Pharmacol Ther 2014, 143:275-294.