Clinical applications of epigenetics in cardiovascular disease: The long road ahead

Translational Research

Volumn 165, Issue 1, 2015, Pages 143-153

  Aslibekyan, Stella ^a   Claas, Steven A ^a   Arnett, Donna K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOVASCULAR DISEASE; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC MARKER; GENETIC POLYMORPHISM; HISTONE MODIFICATION; HUMAN; NONHUMAN; PATHOGENESIS; REVIEW; ANIMAL; CARDIOVASCULAR DISEASES; GENETIC EPIGENESIS; GENETICS; TRANSLATIONAL RESEARCH;

GENETIC MARKER;

ANIMALS; CARDIOVASCULAR DISEASES; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION; GENETIC MARKERS; HUMANS; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84919839650     PISSN: 19315244     EISSN: 18781810     Source Type: Journal    
DOI: 10.1016/j.trsl.2014.04.004     Document Type: Review

References (116)

1. E. Di Angelantonio, and A.S. Butterworth Clinical utility of genetic variants for cardiovascular risk prediction: a futile exercise or insufficient data? Circ Cardiovasc Genet 5 2012 387 390
2. G. Egger, G. Liang, and A. Aparicio Epigenetics in human disease and prospects for epigenetic therapy Nature 429 2004 457 463
3. M.U. Kaikkonen, M.T. Lam, and C.K. Glass Non-coding RNAs as regulators of gene expression and epigenetics Cardiovasc Res 90 2011 430 440
4. B. Duygu, E.M. Poels, and P.A. da Costa Martins Genetics and epigenetics of arrhythmia and heart failure Front Genet 4 2013 219
5. S. Udali, P. Guarini, and S. Moruzzi Cardiovascular epigenetics: from DNA methylation to microRNAs Mol Aspects Med 34 2013 883 901
6. A. Baccarelli, M. Rienstra, and E.J. Benjamin Cardiovascular epigenetics: basic concepts and results from animal and human studies Circ Cardiovasc Genet 3 2010 567 573
7. J.M. Ordovas, and C.E. Smith Epigenetics and cardiovascular disease Nat Rev Cardiol 7 2010 510 519
8. A.M. Grabiec, and K.A. Reedquist Histone deacetylases in RA: epigenetics and epiphenomena Arthritis Res Ther 12 2010 142
9. R.R. Ratan Epigenetics and the nervous system: epiphenomenon or missing piece of the neurotherapeutic puzzle? Lancet Neurol 8 2009 975 977
10. S. Gopalakrishnan, B.O. Van Emburgh, and K.D. Robertson DNA methylation in development and human disease Mutat Res 647 2008 30 38
11. K.D. Robertson DNA methylation and human disease Nat Rev Genet 6 2005 597 610
12. P.A. Jones, and S.B. Baylin The fundamental role of epigenetic events in cancer Nat Rev Genet 3 2002 415 428
13. T. Vaissiere, C. Sawan, and Z. Herceg Epigenetic interplay between histone modifications and DNA methylation in gene silencing Mutat Res 659 2008 40 48
14. B.T. Heijmans, D. Kremer, and E.W. Tobi Heritable rather than age-related environmental and stochastic factors dominate variation in DNA methylation of the human IGF2/H19 locus Hum Mol Genet 16 2007 547 554
15. I. Huh, J. Zeng, and T. Park DNA methylation and transcriptional noise Epigenetics Chromatin 6 2013 9
16. D.T. Hsiung, C.J. Marsit, and E.A. Houseman Global DNA methylation level in whole blood as a biomarker in head and neck squamous cell carcinoma Cancer Epidemiol Biomarkers Prev 16 2007 108 114
17. D.E. Handy, R. Castro, and J. Loscalzo Epigenetic modifications: basic mechanisms and role in cardiovascular disease Circulation 123 2011 2145 2156
18. R. Castro, I. Rivera, and E.A. Struys Increased homocysteine and S-adenosylhomocysteine concentrations and DNA hypomethylation in vascular disease Clin Chem 49 2003 1292 1296
19. P. Sharma, J. Kumar, and G. Garg Detection of altered global DNA methylation in coronary artery disease patients DNA Cell Biol 27 2008 357 365
20. P. Stenvinkel, M. Karimi, and S. Johansson Impact of inflammation on epigenetic DNA methylation: a novel risk factor for cardiovascular disease? J Intern Med 261 2007 488 499
21. M.A. Bind, A. Baccarelli, and A. Zanobetti Air pollution and markers of coagulation, inflammation, and endothelial function: associations and epigene-environment interactions in an elderly cohort Epidemiology 23 2012 332 340
22. A. Baccarelli, L. Tarantini, and R.O. Wright Repetitive element DNA methylation and circulating endothelial and inflammation markers in the VA Normative Aging Study Epigenetics 5 2010 222 228
23. A. Baccarelli, R. Wright, and V. Bollati Ischemic heart disease and stroke in relation to blood DNA methylation Epidemiology 21 2010 819 828
24. H.L. Cash, S.T. McGarvey, and E.A. Houseman Cardiovascular disease risk factors and DNA methylation at the LINE-1 repeat region in peripheral blood from Samoan islanders Epigenetics 6 2011 1257 1264
25. V. Turcot, A. Tchernof, and Y. Deshaies LINE-1 methylation in visceral adipose tissue of severely obese individuals is associated with metabolic syndrome status and related phenotypes Clin Epigenetics 4 2012 10
26. C.G. Bell, S. Finer, and C.M. Lindgren Integrated genetic and epigenetic analysis identifies haplotype-specific methylation in the FTO type 2 diabetes and obesity susceptibility locus PLoS One 5 2010 e14040
27. M.S. Almen, J.A. Jacobsson, and G. Moschonis Genome wide analysis reveals association of a FTO gene variant with epigenetic changes Genomics 99 2012 132 137
28. L.P. Breitling, K. Salzmann, and D. Rothenbacher Smoking, F2RL3 methylation, and prognosis in stable coronary heart disease Eur Heart J 33 2012 2841 2848
29. R.P. Talens, J.W. Jukema, and S. Trompet Hypermethylation at loci sensitive to the prenatal environment is associated with increased incidence of myocardial infarction Int J Epidemiol 41 2012 106 115
30. D. Jiang, D. Zheng, and L. Wang Elevated PLA2G7 gene promoter methylation as a gender-specific marker of aging increases the risk of coronary heart disease in females PLoS One 8 2013 e59752
31. E. Perkins, S.K. Murphy, and A.P. Murtha Insulin-like growth factor 2/H19 methylation at birth and risk of overweight and obesity in children J Pediatr 161 2012 31 39
32. A. Deodati, E. Inzaghi, and A. Liguori IGF2 methylation is associated with lipid profile in obese children Horm Res Paediatr 79 2013 361 367
33. J.Y. Yoo, S. Lee, and H.A. Lee Can proopiomelanocortin methylation be used as an early predictor of metabolic syndrome? Diabetes Care 37 2014 734 739
34. S.E. Alexeeff, A.A. Baccarelli, and J. Halonen Association between blood pressure and DNA methylation of retrotransposons and pro-inflammatory genes Int J Epidemiol 42 2013 270 280
35. S. Friso, F. Pizzolo, and S.W. Choi Epigenetic control of 11 beta-hydroxysteroid dehydrogenase 2 gene promoter is related to human hypertension Atherosclerosis 199 2008 323 327
36. S.P. Guay, G. Voisin, and D. Brisson Epigenome-wide analysis in familial hypercholesterolemia identified new loci associated with high-density lipoprotein cholesterol concentration Epigenomics 4 2012 623 639
37. X. Xu, S. Su, and V.A. Barnes A genome-wide methylation study on obesity: differential variability and differential methylation Epigenetics 8 2013 522 533
38. B. Hidalgo, M.R. Irvin, and J. Sha Epigenome-Wide Association Study of Fasting Measures of Glucose, Insulin, and HOMA-IR in the Genetics of Lipid Lowering Drugs and Diet Network Study Diabetes 63 2014 801 807
39. J. Haas, K.S. Frese, and Y.J. Park Alterations in cardiac DNA methylation in human dilated cardiomyopathy EMBO Mol Med 5 2013 413 429
40. M. Movassagh, M.K. Choy, and D.A. Knowles Distinct epigenomic features in end-stage failing human hearts Circulation 124 2011 2411 2422
41. M. Kim, T.I. Long, and K. Arakawa DNA methylation as a biomarker for cardiovascular disease risk PLoS One 5 2010 e9692
42. R. Cordaux, and M.A. Batzer The impact of retrotransposons on human genome evolution Nat Rev Genet 10 2009 691 703
43. Z.Z. Zhu, L. Hou, and V. Bollati Predictors of global methylation levels in blood DNA of healthy subjects: a combined analysis Int J Epidemiol 41 2012 126 139
44. C. Liu, S. Mou, and C. Pan The FTO gene rs9939609 polymorphism predicts risk of cardiovascular disease: a systematic review and meta-analysis PLoS One 8 2013 e71901
45. K.S. Vimaleswaran, S. Li, and J.H. Zhao Physical activity attenuates the body mass index-increasing influence of genetic variation in the FTO gene Am J Clin Nutr 90 2009 425 428
46. T. Ronn, P. Volkov, and C. Davegardh A six months exercise intervention influences the genome-wide DNA methylation pattern in human adipose tissue PLoS Genet 9 2013 e1003572
47. Y. Fu, G. Jia, and X. Pang FTO-mediated formation of N6-hydroxymethyladenosine and N6-formyladenosine in mammalian RNA Nat Commun 4 2013 1798
48. G. Jia, Y. Fu, and X. Zhao N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO Nat Chem Biol 7 2011 885 887
49. S. Smemo, J.J. Tena, and K.H. Kim Obesity-associated variants within FTO form long-range functional connections with IRX3 Nature 507 2014 371 375
50. J. Zhuang, W. Peng, and H. Li Methylation of p15INK4b and expression of ANRIL on chromosome 9p21 are associated with coronary artery disease PLoS One 7 2012 e47193
51. C.J. Kelsall, S.P. Hoile, and N.A. Irvine Vascular dysfunction induced in offspring by maternal dietary fat involves altered arterial polyunsaturated fatty acid biosynthesis PLoS One 7 2012 e34492
52. S.P. Hoile, N.A. Irvine, and C.J. Kelsall Maternal fat intake in rats alters 20:4n-6 and 22:6n-3 status and the epigenetic regulation of Fads2 in offspring liver J Nutr Biochem 24 2013 1213 1220
53. V.K. Rakyan, T.A. Down, and D.J. Balding Epigenome-wide association studies for common human diseases Nat Rev Genet 12 2011 529 541
54. R. Papait, P. Cattaneo, and P. Kunderfranco Genome-wide analysis of histone marks identifying an epigenetic signature of promoters and enhancers underlying cardiac hypertrophy Proc Natl Acad Sci U S A 110 2013 20164 20169
55. I. Florath, K. Butterbach, and H. Muller 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 2014 1186 1201
56. C.S. Wilhelm-Benartzi, E.A. Houseman, and M.A. Maccani In utero exposures, infant growth, and DNA methylation of repetitive elements and developmentally related genes in human placenta Environ Health Perspect 120 2012 296 302
57. N.S. Shenker, S. Polidoro, and K. van Veldhoven Epigenome-wide association study in the European Prospective Investigation into Cancer and Nutrition (EPIC-Turin) identifies novel genetic loci associated with smoking Hum Mol Genet 22 2013 843 851
58. S. Zeilinger, B. Kuhnel, and N. Klopp Tobacco smoking leads to extensive genome-wide changes in DNA methylation PLoS One 8 2013 e63812
59. D. Zhi, S. Aslibekyan, and M.R. Irvin SNPs located at CpG sites modulate genome-epigenome interaction Epigenetics 8 2013 802 806
60. J.R. Gibbs, M.P. van der Brug, and D.G. Hernandez Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain PLoS Genet 6 2010 e1000952
61. E.L. Meaburn, L.C. Schalkwyk, and J. Mill Allele-specific methylation in the human genome: implications for genetic studies of complex disease Epigenetics 5 2010 578 582
62. J.K. Pickrell, J.C. Marioni, and A.A. Pai Understanding mechanisms underlying human gene expression variation with RNA sequencing Nature 464 2010 768 772
63. N. Sengupta, and E. Seto Regulation of histone deacetylase activities J Cell Biochem 93 2004 57 67
64. K.R. van Eijk, S. de Jong, and M.P. Boks Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects BMC Genomics 13 2012 636
65. D. Zhang, L. Cheng, and J.A. Badner Genetic control of individual differences in gene-specific methylation in human brain Am J Hum Genet 86 2010 411 419
66. C.E. Yu, E. Cudaback, and J. Foraker Epigenetic signature and enhancer activity of the human APOE gene Hum Mol Genet 22 2013 5036 5047
67. J.E. Joo, U. Hiden, and L. Lassance Variable promoter methylation contributes to differential expression of key genes in human placenta-derived venous and arterial endothelial cells BMC Genomics 14 2013 475
68. A. Johansson, S. Enroth, and U. Gyllensten Continuous aging of the human DNA methylome throughout the human lifespan PLoS One 8 2013 e67378
69. H. Heyn, N. Li, and H.J. Ferreira Distinct DNA methylomes of newborns and centenarians Proc Natl Acad Sci U S A 109 2012 10522 10527
70. Z.A. Kaminsky, T. Tang, and S.C. Wang DNA methylation profiles in monozygotic and dizygotic twins Nat Genet 41 2009 240 245
71. E.L. Marczylo, A.A. Amoako, and J.C. Konje Smoking induces differential miRNA expression in human spermatozoa: a potential transgenerational epigenetic concern? Epigenetics 7 2012 432 439
72. J. Laubenthal, O. Zlobinskaya, and K. Poterlowicz Cigarette smoke-induced transgenerational alterations in genome stability in cord blood of human F1 offspring FASEB J 26 2012 3946 3956
73. S. Zaina, and G. Lund Epigenetics: a tool to understand diet-related cardiovascular risk? J Nutrigenet Nutrigenomics 4 2011 261 274
74. K. Szarc vel Szic, M.N. Ndlovu, and G. Haegeman Nature or nurture: let food be your epigenetic medicine in chronic inflammatory disorders Biochem Pharmacol 80 2010 1816 1832
75. P.E. Newman Can reduced folic acid and vitamin B12 levels cause deficient DNA methylation producing mutations which initiate atherosclerosis? Med Hypotheses 53 1999 421 424
76. M. Esteller Epigenetics in biology and medicine 2008: CRC Press Boca Raton, FL 212
77. M. Fang, D. Chen, and C.S. Yang Dietary polyphenols may affect DNA methylation J Nutr 137 2007 223s 228s
78. W.J. Lee, J.Y. Shim, and B.T. Zhu Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids Mol Pharmacol 68 2005 1018 1030
79. J.R. Pilsner, M.N. Hall, and X. Liu Associations of plasma selenium with arsenic and genomic methylation of leukocyte DNA in Bangladesh Environ Health Perspect 119 2011 113 118
80. A. Crescenti, R. Sola, and R.M. Valls Cocoa consumption alters the global DNA methylation of peripheral leukocytes in humans with cardiovascular disease risk factors: a randomized controlled trial PLoS One 8 2013 e65744
81. F.I. Milagro, J. Campion, and P. Cordero A dual epigenomic approach for the search of obesity biomarkers: DNA methylation in relation to diet-induced weight loss FASEB J 25 2011 1378 1389
82. A. Moleres, J. Campion, and F.I. Milagro Differential DNA methylation patterns between high and low responders to a weight loss intervention in overweight or obese adolescents: the EVASYON Study FASEB J 27 2013 2504 2512
83. P. Lopez-Legarrea, M.L. Mansego, and M.A. Zulet SERPINE1, PAI-1 protein coding gene, methylation levels and epigenetic relationships with adiposity changes in obese subjects with metabolic syndrome features under dietary restriction J Clin Biochem Nutr 53 2013 139 144
84. J.T. Bell, P.C. Tsai, and T.P. Yang Epigenome-wide scans identify differentially methylated regions for age and age-related phenotypes in a healthy ageing population PLoS Genet 8 2012 e1002629
85. E.W. Tobi, L.H. Lumey, and R.P. Talens DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific Hum Mol Genet 18 2009 4046 4053
86. A.B. Csoka, and M. Szyf Epigenetic side-effects of common pharmaceuticals: a potential new field in medicine and pharmacology Med Hypotheses 73 2009 770 780
87. C. Napoli, T. Infante, and A. Casamassimi Maternal-foetal epigenetic interactions in the beginning of cardiovascular damage Cardiovasc Res 92 2011 367 374
88. C. Arce, B. Segura-Pacheco, and E. Perez-Cardenas Hydralazine target: from blood vessels to the epigenome J Transl Med 4 2006 10
89. B.H. Lee, S. Yegnasubramanian, and X. Lin Procainamide is a specific inhibitor of DNA methyltransferase 1 J Biol Chem 280 2005 40749 40756
90. E. Cornacchia, J. Golbus, and J. Maybaum Hydralazine and procainamide inhibit T cell DNA methylation and induce autoreactivity J Immunol 140 1988 2197 2200
91. Y. Zhou, and Q. Lu DNA methylation in T cells from idiopathic lupus and drug-induced lupus patients Autoimmun Rev 7 2008 376 383
92. V. Singh, P. Sharma, and N. Capalash DNA methyltransferase-1 inhibitors as epigenetic therapy for cancer Curr Cancer Drug Targets 13 2013 379 399
93. Y.C. Lin, J.H. Lin, and C.W. Chou Statins increase p21 through inhibition of histone deacetylase activity and release of promoter-associated HDAC1/2 Cancer Res 68 2008 2375 2383
94. N. Mitro, C. Godio, and E. De Fabiani Insights in the regulation of cholesterol 7alpha-hydroxylase gene reveal a target for modulating bile acid synthesis Hepatology 46 2007 885 897
95. M. Haberland, R.L. Montgomery, and E.N. Olson The many roles of histone deacetylases in development and physiology: implications for disease and therapy Nat Rev Genet 10 2009 32 42
96. L.H. Lehmann, B.C. Worst, and D.A. Stanmore Histone deacetylase signaling in cardioprotection Cell Mol Life Sci 71 2014 1673 1690
97. M.C. Choi, T.J. Cohen, and T. Barrientos A direct HDAC4-MAP kinase crosstalk activates muscle atrophy program Mol Cell 47 2012 122 132
98. T.A. McKinsey Therapeutic potential for HDAC inhibitors in the heart Annu Rev Pharmacol Toxicol 52 2012 303 319
99. T.C. Zhao, J. Du, and S. Zhuang HDAC inhibition elicits myocardial protective effect through modulation of MKK3/Akt-1 PLoS One 8 2013 e65474
100. T.C. Zhao, L.X. Zhang, and G. Cheng gp-91 mediates histone deacetylase inhibition-induced cardioprotection Biochim Biophys Acta 1803 2010 872 880
101. X. Meng, K. Zhang, and J. Li Statins induce the accumulation of regulatory T cells in atherosclerotic plaque Mol Med 18 2012 598 605
102. H. Tao, K.H. Shi, and J.J. Yang Histone deacetylases in cardiac fibrosis: current perspectives for therapy Cell Signal 26 2014 521 527
103. E. Verdin, F. Dequiedt, and H.G. Kasler Class II histone deacetylases: versatile regulators Trends Genet 19 2003 286 293
104. J. Vojinovic, and N. Damjanov HDAC inhibition in rheumatoid arthritis and juvenile idiopathic arthritis Mol Med 17 2011 397 403
105. P. Dje N'Guessan, F. Riediger, and K. Vardarova Statins control oxidized LDL-mediated histone modifications and gene expression in cultured human endothelial cells Arterioscler Thromb Vasc Biol 29 2009 380 386
106. J.B. Chen, T.R. Chern, and T.T. Wei Design and synthesis of dual-action inhibitors targeting histone deacetylases and 3-hydroxy-3-methylglutaryl coenzyme A reductase for cancer treatment J Med Chem 56 2013 3645 3655
107. J. Hanai, P. Cao, and P. Tanksale The muscle-specific ubiquitin ligase atrogin-1/MAFbx mediates statin-induced muscle toxicity J Clin Invest 117 2007 3940 3951
108. C. Buettner, and S.H. Lecker Molecular basis for statin-induced muscle toxicity: implications and possibilities Pharmacogenomics 9 2008 1133 1142
109. D. Bailey, R. Jahagirdar, and A. Gordon RVX-208: a small molecule that increases apolipoprotein A-I and high-density lipoprotein cholesterol in vitro and in vivo J Am Coll Cardiol 55 2010 2580 2589
110. P. Anand, J.D. Brown, and C.Y. Lin BET bromodomains mediate transcriptional pause release in heart failure Cell 154 2013 569 582
111. S.J. Nicholls, A. Gordon, and J. Johannson ApoA-I induction as a potential cardioprotective strategy: rationale for the SUSTAIN and ASSURE studies Cardiovasc Drugs Ther 26 2012 181 187
112. Resverlogix Corp. Resverlogix's BET protein inhibitor RVX-208 meets primary endpoint in SUSTAIN clinical trial in patients with high risk cardiovascular disease. 2012. Available at: http://www.resverlogix.com/media/press-release.html?id=475. Accessed on January 16, 2014.
113. S.J. Nicholls, and J. Chapman ASSURE: effect of an oral agent inducing Apo A-I synthesis on progression of coronary atherosclerosis: results of the ASSURE study 2013 European Society of Cardiology Congress Amsterdam
114. Resverlogix Corp. Resverlogix announces combined RVX-208 findings from SUSTAIN & ASSURE phase 2b trials. 2014. Available at: http://www.resverlogix.com/media/press-release.html?id=497. Accessed on January 16, 2014.
115. M. Jaguszewski, J. Osipova, and J.R. Ghadri A signature of circulating microRNAs differentiates Takotsubo cardiomyopathy from acute myocardial infarction Eur Heart J 35 2014 999 1006
116. J.E. Raizman, E.P. Diamandis, and K. Rayner Novel biomarkers for acute myocardial infarction: is microRNA the new kid on the block? Clin Chem 2013