Epigenetic modifications in cardiovascular disease

Basic Research in Cardiology

Volumn 107, Issue 2, 2012, Pages

  Lorenzen, Johan M ^a   Martino, Filippo ^a   Thum, Thomas ^a,b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

Cardiovascular disease; CpG islands; DNA methylation; Long non coding RNAs; MicroRNAs

Indexed keywords

GENOMIC RNA; MICRORNA;

CARDIOVASCULAR DISEASE; CPG ISLAND; DISEASE ACTIVITY; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; EPIGENETICS; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; GENE SWITCHING; HEART FAILURE; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; ISCHEMIC HEART DISEASE; NONHUMAN; PHENOTYPIC VARIATION; REVIEW; RNA GENE; SEQUENCE ANALYSIS; ANIMAL; GENETIC EPIGENESIS; GENETICS;

ANIMALS; CARDIOVASCULAR DISEASES; EPIGENESIS, GENETIC; HUMANS;

EID: 84859731822     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0245-9     Document Type: Review

References (86)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431:350-355. doi:10.1038/nature02871 (Pubitemid 39265675)
2. Balaguer F, Link A, Lozano JJ, Cuatrecasas M, Nagasaka T, Boland CR, Goel A (2010) Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res 70(16):6609-6618. doi:10.1158/0008-5472.CAN-10-0622
3. Bartel DP (2003) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297. doi:10.1016/S0092-8674 (04)00045-5
4. Bauersachs J, Thum T (2011) Biogenesis and regulation of cardiovascular microRNAs. Circ Res 109(3):334-347. doi:10.1161/ CIRCRESAHA.110.228676
5. Bhutani N, Burns DM, Blau HM (2011) DNA demethylation dynamics. Cell 146(6):866-872. doi:10.1016/j.cell.2011.08.042
6. Bird A (2007) Perceptions of epigenetics. Nature 447:396-398. doi:10.1038/nature05913 (Pubitemid 46816744)
7. Bird A (1986) CpG-rich islands and the function of DNA methylation. Nature 321:209-213. doi:10.1038/321209a0 (Pubitemid 16016411)
8. Bird AP (1980) DNA methylation and the frequency of CpG in animal DNA. Nucleic Acids Res 8:1499-1504. doi:10.1093/nar/8. 7.1499
9. Bogdarina I, Welham S, King PJ, Burns SP, Clark AJ (2007) Epigenetic modification of the reninangiotensin system in the fetal programming of hypertension. Circ Res 100:520-526. doi: 10.1161/01.RES.0000258855.60637.58 (Pubitemid 46673261)
10. Breton CV, Byun HM, Wenten M, Pan F, Yang A, Gilliland FD (2009) Prenatal tobacco smoke exposure affects global and genespecific DNA methylation. Am J Respir Crit Care Med 180(5): 462-467. doi:10.1164/rccm.200901-0135OC
11. Broadbent HM, Peden JF, Lorkowski S, Goel A, Ongen H, Green F, Clarke R, Collins R, Franzosi MG, Tognoni G, Seedorf U, Rust S, Eriksson P, Hamsten A, Farrall M, Watkins H, PROCARDIS Consortium (2008) Susceptibility to coronary artery disease and diabetes is encoded by distinct, tightly linked SNPs in the ANRIL locus on chromosome 9p. Hum Mol Genet 17:806-814. doi: 10.1093/hmg/ddm352 (Pubitemid 351359697)
12. Cai X, Hagedorn CH, Cullen BR (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957-1966. doi:10.1261/rna. 7135204 (Pubitemid 39557833)
13. Calin GA, Liu CG, Ferracin M, Hyslop T, Spizzo R, Sevignani C Fabbri M, CimminoA, Lee EJ, Wojcik SE, ShimizuM, Tili E,Rossi S, Taccioli C, Pichiorri F, Liu X, Zupo S, Herlea V, Gramantieri L, Lanza G, Alder H, Rassenti L, Volinia S, Schmittgen TD, Kipps TJ, Negrini M, Croce CM (2007) Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell 12:215-229. doi:10.1016/j.ccr.2007.07.027 (Pubitemid 47333418)
14. Chen L, Hahn H, Wu G, Chen CH, Liron T, Schechtman D, Cavallaro G, Banci L, Guo Y, Bolli R, Dorn GW 2nd, Mochly- Rosen D (2001) Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 98:11114-11119. doi:10.1073/pnas.191369098 (Pubitemid 32928691)
15. Das M, Das S, Lekli I, Das DK (2011) Caveolin induces cardioprotection through epigenetic regulation. J Cell Mol Med (in press). doi:10.1111/j.1582- 4934.2011.01372.x
16. Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25(10):1010-1022. doi:10.1002/bies.201 000057
17. Defossez PA, Stancheva I (2011) Biological functions of methyl- CpG-binding proteins. Prog Mol Biol Transl Sci 101:377-398. doi:10.1016/B978-0- 12-387685-0.00012-3
18. The ENCODE Project Consortium (2004) The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306:636-640. doi: 10.1126/science.1105136 (Pubitemid 39440902)
19. Dixit M, Ansseau E, Tassin A, Winokur S, Shi R, Qian H, Sauvage S, Matteotti C, van Acker AM, Leo O, Figlewicz D, Barro M, Laoudj-Chenivesse D, Belayew A, Coppee F, Chen YW (2007) DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc Natl Acad Sci USA 104:18157-18162. doi:10.1073/pnas. 0708659104 (Pubitemid 350210837)
20. Ferguson LR (2011) RNA silencing: mechanism, biology and responses to environmental stress. Mutat Res 714(1-2):93-94. doi:10.1016/j.mrfmmm.2011.07.007
21. Gama-Sosa MA, Midgett RM, Slagel VA, Githens S, Kuo KC, Gehrke CW, Ehrlich M (1983) Tissue-specific differences in DNA methylation in various mammals. Biochim Biophys Acta 740:212-219. doi:10.1016/0167-4781(83)90079-9 (Pubitemid 13078586)
22. Gardiner-Garden M, Frommer M (1987) CpG islands in vertebrate genomes. J Mol Biol 196:261-282. doi:10.1016/0022-283 6(87)90689-9 (Pubitemid 17122132)
23. Golding MC, Magri LS, Zhang L, Lalone SA, Higgins MJ, Mann MR (2011) Depletion of Kcnq1ot1 non-coding RNA does not affect imprinting maintenance in stem cells. Development 138(17):3667-3678. doi:10.1242/dev.057778
24. Gray MO, Zhou HZ, Schafhalter-Zoppoth I, Zhu P, Mochly- Rosen D, Messing RO (2004) Preservation of base-line hemodynamic function and loss of inducible cardioprotection in adult mice lacking protein kinase Ce. J Biol Chem 279:3596-3604. doi: 10.1074/jbc.M311459200 (Pubitemid 38140600)
25. Godfrey KM, Barker DJ (2001) Fetal programming and adult health. Pub Health Nutr 4:611-624. doi:10.1079/PHN2001145 (Pubitemid 32524581)
26. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, Shiekhattar R (2004) The microprocessor complex mediates the genesis of microRNAs. Nature 432:235-240. doi: 10.1038/nature03120 (Pubitemid 39545855)
27. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466:835-840. doi:10.1038/nature09267
28. Hartmann D, Thum T (2011) MicroRNAs and vascular (dys)function. Vascul Pharmacol (in press). doi:10.1016/j.vph.2011. 07.005
29. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105:17046-17049. doi:10.1073/pnas. 0806560105
30. Helgadottir A, Thorleifsson G, Manolescu A, Gretarsdottir S, Blondal T, Jonasdottir A, Jonasdottir A, Sigurdsson A, Baker A, Palsson A, Masson G, Gudbjartsson DF, Magnusson KP, Andersen K, Levey AI, Backman VM, Matthiasdottir S, Jonsdottir T, Palsson S, Einarsdottir H, Gunnarsdottir S, Gylfason A, Vaccarino V, Hooper WC, Reilly MP, Granger CB, Austin H, Rader DJ, Shah SH, Quyyumi AA, Gulcher JR, Thorgeirsson G, Thorsteinsdottir U, Kong A, Stefansson K (2007) A common variant on chromosome 9p21 affects the risk of myocardial infarction. Science 316:1491-1493. doi:10.1126/science.1142842 (Pubitemid 46906618)
31. Helgadottir A, Thorleifsson G, Magnusson KP, Grétarsdottir S, Steinthorsdottir V, Manolescu A, Jones GT, Rinkel GJ, Blankensteijn JD, Ronkainen A, Jaaskelainen JE, Kyo Y, Lenk GM, Sakalihasan N, Kostulas K, Gottsater A, Flex A, Stefansson H, Hansen T, Andersen G, Weinsheimer S, Borch-Johnsen K, Jorgensen T, Shah SH, Quyyumi AA, Granger CB, Reilly MP, Austin H, Levey AI, Vaccarino V, Palsdottir E, Walters GB, Jonsdottir T, Snorradottir S, Magnusdottir D, Gudmundsson G, Ferrell RE, Sveinbjornsdottir S, Hernesniemi J, Niemela M, Limet R, Andersen K, Sigurdsson G, Benediktsson R, Verhoeven EL, Teijink JA, Grobbee DE, Rader DJ, Collier DA, Pedersen O, Pola R, Hillert J, Lindblad B, Valdimarsson EM, Magnadottir HB, Wijmenga C, Tromp G, Baas AF, Ruigrok YM, van Rij AM, Kuivaniemi H, Powell JT, Matthiasson SE, Gulcher JR, Thorgeirsson G, Kong A, Thorsteinsdottir U, Stefansson K (2008) The same sequence variant on 9p21 associates with myocardial infarction, abdominal aortic aneurysm and intracranial aneurysm. Nat Genet 40:217-224. doi:10.1038/ng.72 (Pubitemid 351171400)
32. Heusch G, Boengler K, Schulz R (2010) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118(19): 1915-1919. doi:10.1161/CIRCULATIONAHA.108.805242
33. Huarte M, Rinn JL (2010) Large non-coding RNAs: missing links in cancer? Hum Mol Genet 19(R2): R152-R161. doi:10.1093/hmg/ddq353
34. Illi B, Nanni S, Scopece A, Farsetti A, Biglioli P, Capogrossi MC, Gaetano C (2003) Shear stress-mediated chromatin remodeling provides molecular basis for flow-dependent regulation of gene expression. Circ Res 25 93(2):155-161. doi:10.1161/01.RES.000 0080933.82105.29 (Pubitemid 36919703)
35. Kaikkonen MU, Lam MT, Glass CK (2011) Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res90(3):430-440. doi:10.1093/cvr/cvr097
36. Kaneda R, Takada S, Yamashita Y, Choi YL, Nonaka-Sarukawa M, Soda M, Misawa Y, Isomura T, Shimada K, Mano H (2009) Genome-wide histone methylation profile for heart failure. Genes Cells 14(1):69-77. doi:10.1111/j.1365-2443. 2008.01252.x
37. Kouzarides T (2007) Chromatin modifications and their function. Cell 128(4):693-705. doi:10.1016/j.cell.2007.02.005 (Pubitemid 46273577)
38. Laird PW (2003) The power and the promise of DNA methylation markers. Nat Rev Cancer 3(4):253-266. doi:10.1038/nrc1045 (Pubitemid 37328861)
39. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843-854. doi:10.1016/0092-867 4(93)90529-Y (Pubitemid 24014542)
40. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051-4060. doi:10.1038/sj.emboj.7600385 (Pubitemid 39472426)
41. Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim VN (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415-419. doi: 10.1038/nature01957 (Pubitemid 37187272)
42. Li E, Beard C, Jaenisch R (1993) Role for DNA methylation in genomic imprinting. Nature 366:362-365. doi:10.1038/366362a0 (Pubitemid 23349366)
43. Li K, Blum Y, Verma A, Liu Z, Pramanik K, Leigh NR, Chun CZ, Samant GV, Zhao B, Garnaas MK, Horswill MA, Stanhope SA, North PE, Miao RQ, Wilkinson GA, Affolter M, Ramchandran R (2010) A noncoding antisense RNA in tie-1 locus regulates tie-1 function in vivo. Blood 115(1):133-139. doi: 10.1182/blood-2009-09-242180
44. Litt MD, Simpson M, Gaszner M, Allis CD, Felsenfeld G (2001) Correlation between histone lysine methylation and developmental changes at the chicken betaglobin locus. Science 293(5539):2453-2455. doi:10.1126/science.1064413 (Pubitemid 32917326)
45. Margariti A, Zampetaki A, Xiao Q, Zhou B, Karamariti E, Martin D, Yin X, Mayr M, Li H, Zhang Z, De Falco E, Hu Y, Cockerill G, Xu Q, Zeng L (2010) Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin. Circ Res 106:1202-1211. doi:10.1161/CIRCRESAHA.109.213165
46. Mathiyalagan P, Chang L, Du XJ, El-Osta A (2010) Cardiac ventricular chambers are epigenetically distinguishable. Cell Cycle 9(3):612-617. http://dx.doi.org/10.4161/cc.9.3.10612
47. McDonald OG, Owens GK (2007) Programming smooth muscle plasticity with chromatin dynamics. Circ Res 100:1428-1441. doi:10.1161/01.RES.0000266448.30370. a0 (Pubitemid 46834755)
48. Meder B, Keller A, Vogel B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, Just S, BorriesA, Rudloff J, Leidinger P,Meese E, Katus HA, Rottbauer W (2011) MicroRNA signatures in total eripheral blood as novel biomarkers for acute myocardial infarction. Basic Res Cardiol 106(1):13-23. doi:10.1002/ijc.26419
49. MicroCosmTargets (2010)Version 5.EMBL-EBI database [online]http://www. ebi.ac.uk/enright-srv/microcosm/htdocs/targets/v5/
50. Mottet D, Bellahcene A, Pirotte S, Waltregny D, Deroanne C, Lamour V, Lidereau R, Castronovo V (2007) Histone deacetylase 7 silencing alters endothelial cell migration, a key step in angiogenesis. Circ Res 101:1237-1246. doi:10.1161/CIRCRESAHA. 107.149377 (Pubitemid 350294640)
51. Movassagh M, Choy MK, Goddard M, Bennett MR, Down TA, Foo RS (2010) Differential DNA methylation correlates with differential expression of angiogenic factors in human heart failure. PLoS One 5(1):e8564. doi:10.1371/journal.pone.0008564
52. Movassagh M, Choy MK, Knowles DA, Cordeddu L, Haider S, Down T, Siggens L, Vujic A, Simeoni I, Penkett C, Goddard M, Lio P, Bennett MR, Foo RS (2011) Distinct epigenomic features in end-stage failing human hearts. Circulation. doi:10.1161/ CIRCULATIONAHA.111.040071
53. Mund C, Brueckner B, Lyko F (2006) Reactivation of epigenetically silenced genes by DNA methyltransferase inhibitors: basic concepts and clinical applications. Epigenetics 1(1):7-13. doi: 10.4161/epi.1.1.2375
54. Murriel CL, Mochly-Rosen D (2003) Opposing roles of delta and epsilon PKC in cardiac ischemia and reperfusion: targeting the apoptotic machinery. Arch Biochem Biophys 420:246-254. doi: 10.1016/j.abb.2003.08.038 (Pubitemid 37491108)
55. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P (2008) The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322:1717-1720. doi:10.1126/science.1163802
56. Ohtani K, Dimmeler S (2011) Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 106(1):5-11. doi:10.1007/s00395-010-0139-7
57. Ohtani K, Vlachojannis GJ, Koyanagi M, Boeckel JN, Urbich C, Farcas R, Bonig H, Marquez VE, Zeiher AM, Dimmeler S (2011) Epigenetic regulation of endothelial lineage committed genes in pro-angiogenic hematopoietic and endothelial progenitor cells. Circ Res doi. doi:10.1161/CIRCRESAHA.111.247304
58. Painter RC, Roseboom TJ, Bleker OP (2005) Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol 20:345-352. doi:10.1016/j.reprotox.2005.04.005 (Pubitemid 40949554)
59. Panning B, Jaenisch R (1996) DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev 10:1991-2002. doi:10.1101/gad.10.16.1991 (Pubitemid 26346108)
60. Pasmant E, Laurendeau I, Héron D, Vidaud M, Vidaud D, Bièche I (2007) Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res 67:3963-3969. doi:10.1158/0008-5472.CAN-06-2004 (Pubitemid 46762186)
61. Patterson AJ, Chen M, Xue Q, Xiao D, Zhang L (2010) Chronic prenatal hypoxia induces epigenetic programming of PKC{epsilon} gene repression in rat hearts. Circ Res 107(3):365-373. doi: 10.1161/CIRCRESAHA.110.221259
62. Pearson CE (2010) FSHD: a repeat contraction disease finally ready to expand (our understanding of its pathogenesis). PLoS Genet 6:e1001180. doi:10.1371/journal.pgen.1001180
63. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629-641. doi:10.1016/j.cell. 2009.02.006
64. Robb GB, Carson AR, Tai SC, Fish JE, Singh S, Yamada T, Scherer SW, Nakabayashi K, Marsden PA (2004) Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J Biol Chem 279(36):37982-37996. doi:10.1074/jbc.M400271200 (Pubitemid 39195514)
65. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, Jones PA (2006) Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 9(6):435-443. doi: 10.1016/j.ccr.2006.04.020 (Pubitemid 43832188)
66. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419(6905):407-411. doi:10.1038/nature01080
67. Saxonov S, Berg P, Brutlag DL (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci USA 103(5):1412-1417. doi:10.1073/pnas.0510310103 (Pubitemid 43191179)
68. Singh N, Trivedi CM, Lu M, Mullican SE, Lazar MA, Epstein JA (2011) Histone deacetylase 3 regulates smooth muscle differentiation in neural crest cells and development of the cardiac outflow Tract. Circ Res. doi:10.1038/nrm3198
69. Spin JM, Quertermous T, Tsao PS (2010) Chromatin remodeling pathways in smooth muscle cell differentiation, and evidence for an integral role for p300. PLoS One 5(12):e14301. doi: 10.1371/journal.pone.0014301
70. Stein AB, Jones TA, Herron TJ, Patel SR, Day SM, Noujaim SF, Milstein ML, Klos M, Furspan PB, Jalife J, Dressler GR (2011) Loss of H3K4 methylation destabilizes gene expression patterns and physiological functions in adult murine cardiomyocytes. J Clin Invest 121(7):2641-2650. doi:10.1172/JCI44641
71. Takai D, Jones PA (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci USA 99:3740-3745. doi:10.1073/pnas. 052410099 (Pubitemid 34252176)
72. Thrash-Bingham CA, Tartof KD (1999) aHIF: a natural antisense transcript overexpressed in human renal cancer and during hypoxia. J Natl Cancer Inst 91:143-151. doi:10.1093/jnci/91.2.143 (Pubitemid 29042691)
73. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, Castoldi M, Soutschek J, Koteliansky V, Rosenwald A, Basson MA, Licht JD, Pena JT,Rouhanifard SH, Muckenthaler MU, Tuschl T, Martin GR, Bauersachs J, Engelhardt S (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456:980-984. doi:10.1038/nature07511
74. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, Doevendans PA, Mummery CL, Borlak J, Haverich A, Gross C, Engelhardt S, Ertl G, Bauersachs J (2007) MicroRNAs in the human heart: a clue to fetal gene reprogramming in heart failure. Circulation 116:258-267. doi:10.1161/CIRCULATIONAHA.107.687947 (Pubitemid 47196561)
75. Tsutsumi YM, Horikawa YT, Jennings MM, Kidd MW, Niesman IR, Yokoyama U, Head BP, Hagiwara Y, Ishikawa Y, Miyanohara A, Patel PM, Insel PA, Patel HH, Roth DM (2008) Cardiacspecific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 118(19):1979-1988. doi:10.1161/CIRCULATIONAHA.108.78 8331
76. Urbich C, Kuehbacher A, Dimmeler S (2008) Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 79(4):581-588. doi:10.1093/cvr/cvn156
77. Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev 20:515-524. doi:10.1101/gad.1399806 (Pubitemid 43345317)
78. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 105:13027-13032. doi:10.1073/pnas.0805038105
79. Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20:116-117. doi:10.1038/2413 (Pubitemid 28455441)
80. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, Schubeler D (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat Genet 39:457-466. doi:10.1038/ng1990 (Pubitemid 46514772)
81. Yang F, Zhang L, Huo XS, Yuan JH, Xu D, Yuan SX, Zhu N, Zhou WP, Yang GS, Wang YZ, Shang JL, Gao CF, Zhang FR, Wang F, Sun SH (2011) Long non-coding RNA high expressed in hepatocellular carcinoma (lncRNA-HEIH) facilitates tumor growth through enhancer of zeste homolog 2. Hepatology (in press). doi:10.1002/hep.24563
82. Yap KL, Li S, Muñoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38(5):662-674. doi:10.1016/j.molcel.2010.03.021
83. Yu W, Gius D, Onyango P, Muldoon-Jacobs K, Karp J, Feinberg AP, Cui H (2008) Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA. Nature 451:202-206. doi:10.1038/ nature06468
84. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322(5902):750-756. doi:10.1126/science. 1163045
85. Zhang H, Darwanto A, Linkhart TA, Sowers LC, Zhang L (2007) Maternal cocaine administration causes an epigenetic modification of protein kinase Cepsilon gene expression in fetal rat heart. Mol Pharmacol 71(5):1319-1328. doi:10.1124/mol.106.032011 (Pubitemid 46658685)
86. Zhang QJ, Chen HZ, Wang L, Liu DP, Hill JA, Liu ZP (2011) The histone trimethyllysine demethylase JMJD2A promotes cardiac hypertrophy in response to hypertrophic stimuli in mice. J Clin Invest 121(6):2447-2456. doi:10.1172/JCI46277