Emerging role of micrornas in cardiovascular diseases

Circulation Journal

Volumn 78, Issue 3, 2014, Pages 567-575

  De Rosa, Salvatore ^a   Curcio, Antonio ^a   Indolfi, Ciro ^a  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

Aging; Cardiovascular diseases; Circulation; microRNAs

Indexed keywords

MICRORNA; MICRORNA 1; MICRORNA 106; MICRORNA 107; MICRORNA 122; MICRORNA 1248; MICRORNA 126; MICRORNA 133; MICRORNA 134; MICRORNA 146; MICRORNA 16; MICRORNA 2; MICRORNA 200; MICRORNA 21; MICRORNA 215; MICRORNA 217; MICRORNA 22; MICRORNA 26; MICRORNA 27; MICRORNA 29; MICRORNA 290; MICRORNA 30B; MICRORNA 324; MICRORNA 34; MICRORNA 423; MICRORNA 451; MICRORNA 663; MICRORNA 7; MICRORNA 9; UNCLASSIFIED DRUG; UNINDEXED DRUG; BIOLOGICAL MARKER;

ACUTE CORONARY SYNDROME; AGING; BIOGENESIS; BRAIN ISCHEMIA; CALCIFICATION; CARDIOVASCULAR DISEASE; CELL COMMUNICATION; CEREBROVASCULAR ACCIDENT; CONGESTIVE HEART FAILURE; CORONARY ARTERY DISEASE; HEART FAILURE; HEART INFARCTION; HUMAN; NONHUMAN; RESTENOSIS; REVIEW; ANIMAL; CARDIOVASCULAR DISEASES; GENETICS; METABOLISM;

ANIMALS; BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; HUMANS; MICRORNAS;

EID: 84894420502     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-14-0086     Document Type: Review

References (117)

1. Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, et al. Heart Disease and Stroke Statistics-2014 Update: A Report From the American Heart Association. Circulation 2014; 129: e28-e292, doi:10.1161/01.cir.0000441139.02102.80. (accessed 2 January, 2014.)
2. Yeh RW, Sidney S, Chandra M, Sorel M, Selby JV, Go AS. Population trends in the incidence and outcomes of acute myocardial infarction. N Engl J Med 2010; 362: 2155-2165.
3. He J, Gu D, Wu X, Reynolds K, Duan X, Yao C, et al. Major causes of death among men and women in China. N Engl J Med 2005; 353: 1124-1134.
4. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-297.
5. Polimeni A, De Rosa S, Indolfi C. Vascular miRNAs after balloon angioplasty. Trends Cardiovasc Med 2013; 23: 9-14.
6. Curcio A, Torella D, Iaconetti C, Pasceri E, Sabatino J, Sorrentino S, et al. MicroRNA-1 downregulation increases connexin 43 displacement and induces ventricular tachyarrhythmias in rodent hypertrophic hearts. PLoS One 2013; 8: e70158, doi:10.1371/journal. pone.0070158.
7. Stellos K, Dimmeler S. Vascular microRNAs: From disease mechanisms to therapeutic targets. Circ Res 2014; 114: 3-4.
8. Rayner KJ, Moore KJ. MicroRNA control of high-density lipoprotein metabolism and function. Circ Res 2014; 114: 183-192.
9. Ren J, Zhang J, Xu N, Han G, Geng Q, Song J, et al. Signature of circulating microRNAs as potential biomarkers in vulnerable coronary artery disease. PLoS One 2013; 8: e80738, doi:10.1371/journal. pone.0080738.
10. Iaconetti C, Gareri C, Polimeni A, Indolfi C. Non-coding RNAs: The "dark matter" of cardiovascular pathophysiology. Int J Mol Sci 2013; 14: 19987-20018.
11. Zampetaki A, Willeit P, Drozdov I, Kiechl S, Mayr M. Profiling of circulating microRNAs: From single biomarkers to re-wired networks. Cardiovasc Res 2012; 93: 555-562.
12. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 12: 15-20.
13. Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, et al. A uniform system for microRNA annotation. RNA 2003; 9: 277-279.
14. Cheng Y, Liu X, Zhang S, Lin Y, Yang J, Zhang C. MicroRNA-21 protects against the H2O2-induced injury on cardiac myocytes via its target gene PDCD4. J Mol Cell Cardiol 2009; 47: 5-14.
15. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res 2011; 39: 7223-7233.
16. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating miRs independent of vesicles in human plasma. Proc Natl Acad Sci USA 2011; 108: 5003-5008.
17. Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of miRs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 2010; 38: 7248-7259.
18. Ghaeni L, Wagner J, Leistner D, De Rosa S, Fichtlscherer S, Zeiher AM, et al. Characterisation of circulating protein-bound miRNAs. 2012 Annual Congress of the German Cardiac Society. Mannheim, Germany.
19. Wagner J, Riwanto M, Besler C, Knau A, Fichtlscherer S, Röxe T, et al. Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arterioscler Thromb Vasc Biol 2013; 33: 1392-1400.
20. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2: ra81, doi:10.1126/scisignal.2000610.
21. Hergenreider E, Heydt S, Tréguer K, Boettger T, Horrevoets AJ, Zeiher AM, et al. Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs. Nat Cell Biol 2012; 14: 249-256.
22. Ambros V. The functions of animal miRs. Nature 2004; 431: 350-355.
23. Gregory RI, Yan KP, Amuthan G, Chendrimada T, Doratotaj B, Cooch N, et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004; 432: 235-240.
24. Madina BR, Kuppan G, Vashisht AA, Liang YH, Downey KM, Wohlschlegel JA, et al. Guide RNA biogenesis involves a novel RNase III family endoribonuclease in Trypanosoma brucei. RNA 2011; 17: 1821-1830.
25. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005; 123: 631-640.
26. Park JE, Hel I, Tian Y, Simanshu DK, Chang H, Jee D, et al. Dicer recognizes the 5'end of RNA for efficient and accurate processing. Nature 2011; 475: 201-205.
27. Yang JS, Lai EC. Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011; 43: 892-903.
28. Yang JS, Lai EC. Dicer-independent, Ago2-mediated microRNA biogenesis in vertebrates. Cell Cycle 2010; 9: 4455-4460.
29. North BJ, Sinclair DA. The intersection between aging and cardiovascular disease. Circ Res 2012; 110: 1097-1108.
30. Pierce GL, Lesniewski LA, Lawson BR, Beske SD, Seals DR. Nuclear factor-K{green}B activation contributes to vascular endothelial dysfunction via oxidative stress in overweight/obese middle-aged and older humans. Circulation 2009; 119: 1284-1292.
31. Strait JB, Lakatta EG. Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail Clin 2012; 8:143-164.
32. Hackl M, Brunner S, Fortschegger K, Schreiner C, Micutkova L, Mück C, et al. miR-17, miR-19b, miR-20a, and miR-106a are down-regulated in human aging. Aging Cell 2010; 9: 291-296.
33. Menghini R, Casagrande V, Cardellini M, Martelli E, Terrinoni A, Amati F, et al. MicroRNA 217 modulates endothelial cell senescence via silent information regulator 1. Circulation 2009; 120: 1524-1532.
34. Olivieri F, Antonicelli R, Lorenzi M, D'Alessandra Y, Lazzarini R, Santini G, et al. Diagnostic potential of circulating miR-499-5p in elderly patients with acute non ST-elevation myocardial infarction. Int J Cardiol 2013; 167: 531-536.
35. Boon RA, Dimmeler S. MicroRNAs and aneurysm formation. Trends Cardiovasc Med 2011; 21: 172-177.
36. Boon RA, Seeger T, Heydt S, Fischer A, Hergenreider E, Horrevoets AJ, et al. MicroRNA-29 in aortic dilation: Implications for aneurysm formation. Circ Res 2011; 109: 1115-1119.
37. Ugalde AP, Ramsay AJ, de la Rosa J, Varela I, Mariño G, Cadiñanos J, et al. Aging and chronic DNA damage response activate a regulatory pathway involving miR-29 and p53. EMBO J 2011; 30: 2219-2232.
38. Maegdefessel L, Azuma J, Toh R, Merk DR, Deng A, Chin JT, et al. Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Invest 2012; 122: 497-506.
39. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, et al. miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 2012; 110: 312-324.
40. Zhang P, Huang A, Ferruzzi J, Mecham RP, Starcher BC, Tellides G, et al. Inhibition of microRNA-29 enhances elastin levels in cells haploinsufficient for elastin and in bioengineered vessels-brief report. Arterioscler Thromb Vasc Biol 2012; 32: 756-759.
41. Zhao T, Li J, Chen AF. MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab 2010; 299: E110-E116, doi:10.1152/ajpendo.00192.2010. (accessed 2 January, 2014.)
42. Xu Q, Seeger FH, Castillo J, Iekushi K, Boon RA, Farcas R, et al. Micro-RNA-34a contributes to the impaired function of bone marrow- derived mononuclear cells from patients with cardiovascular disease. J Am Coll Cardiol 2012; 59: 2107-2117.
43. Christoffersen NR, Shalgi R, Frankel LB, Leucci E, Lees M, Klausen M, et al. p53-independent upregulation of miR-34a during oncogeneinduced senescence represses MYC. Cell Death Differ 2010; 17: 236-245.
44. Ito T, Yagi S, Yamakuchi M. MicroRNA-34a regulation of endothelial senescence. Biochem Biophys Res Commun 2010; 398: 735-740.
45. Tabuchi T, Satoh M, Itoh T, Nakamura M. MicroRNA-34a regulates the longevity-associated protein SIRT1 in coronary artery disease: Effect of statins on SIRT1 and microRNA-34a expression. Clin Sci (Lond) 2012; 123: 161-171.
46. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Orjalo AV, Rodier F, et al. MicroRNAs miR-146a/b negatively modulate the senescence- associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 2009; 1: 402-411.
47. Olivieri F, Lazzarini R, Recchioni R, Marcheselli F, Rippo MR, Di Nuzzo S, et al. MiR-146a as a marker of senescence-associated pro-inflammatory status in cells involved in vascular remodelling. Age (Dordr) 2013; 35: 1157-1172.
48. Vasa-Nicotera M, Chen H, Tucci P, Yang AL, Saintigny G, Menghini R, et al. miR-146a is modulated in human endothelial cell with aging. Atherosclerosis 2011; 217: 326-330.
49. van Almen GC, Verhesen W, van Leeuwen RE, van de Vrie M, Eurlings C, Schellings MW, et al. MicroRNA-18 and microRNA-19 regulate CTGF and TSP-1 expression in age-related heart failure. Aging Cell 2011; 10: 769-779.
50. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007; 13: 613-618.
51. Jazbutyte V, Fiedler J, Kneitz S, Galuppo P, Just A, Holzmann A, et al. MicroRNA-22 increases senescence and activates cardiac fibroblasts in the aging heart. Age (Dordr) 2013; 35: 747-762.
52. Casscells W. Migration of smooth muscle and endothelial cells. Critical events in restenosis. Circulation 1992; 86: 723-729.
53. Indolfi C, Torella D, Cavuto L, Davalli AM, Coppola C, Esposito G, et al. Effects of balloon injury on neointimal hyperplasia in streptozotocin-induced diabetes and in hyperinsulinemic nondiabetic pancreatic islet-transplanted rats. Circulation 2001; 103: 2980-2986.
54. Indolfi C, Avvedimento EV, Rapacciuolo A, Di Lorenzo E, Esposito G, Stabile E, et al. Inhibition of cellular ras prevents smooth muscle cell proliferation after vascular injury in vivo. Nat Med 1995; 1: 541-545.
55. Indolfi C, Di Lorenzo E, Rapacciuolo A, Stingone AM, Stabile E, Leccia A, et al. 8-Chloro-cAMP inhibits smooth muscle cell proliferation in vitro and neointima formation induced by balloon injury in vivo. J Am Coll Cardiol 2000; 36: 288-293.
56. Indolfi C, Torella D, Coppola C, Stabile E, Esposito G, Curcio A, et al. Rat carotid artery dilation by PTCA balloon catheter induces neointima formation in presence of IEL rupture. Am J Physiol Heart Circ Physiol 2002; 283: H760-H767.
57. Indolfi C, Mongiardo A, Curcio A, Torella D. Molecular mechanisms of in-stent restenosis and approach to therapy with eluting stents. Trends Cardiovasc Med 2003; 13: 142-148.
58. Chan D, Ng LL. Biomarkers in acute myocardial infarction. BMC Med 2010; 8: 34.
59. Indolfi C, Avvedimento EV, Di Lorenzo E, Esposito G, Rapacciuolo A, Giuliano P. Activation of cAMP-PKA signaling in vivo inhibits smooth muscle cell proliferation induced by vascular injury. Nat Med 1997; 3: 775-779.
60. Indolfi C, Stabile E, Coppola C, Gallo A, Perrino C, Allevato G. Membrane-bound protein kinase A inhibits smooth muscle cell proliferation in vitro and in vivo by amplifying cAMP-protein kinase A signals. Circ Res 2001; 88: 319-324.
61. Indolfi C, Torella D, Coppola C, Curcio A, Rodriguez F, Bilancio A. Physical training increases eNOS vascular expression and activity and reduces restenosis after balloon angioplasty or arterial stenting in rats. Circ Res 2002; 91: 1190-1197.
62. Iaconetti C, Polimeni A, Sorrentino S, Sabatino J, Pironti G, Esposito G, et al. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res Cardiol 2012; 107: 296-309.
63. Torella D, Iaconetti C, Catalucci D, Ellison GM, Leone A, Waring CD, et al. MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ Res 2011; 109: 880-893.
64. De Rosa S, Fichtlscherer S, Lehmann R, Assmus B, Dimmeler S, Zeiher AM. Transcoronary concentration gradients of circulating miRs. Circulation 2011; 124: 1936-1944.
65. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010; 39: 133-144.
66. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, et al. Circulating miRs in patients with coronary artery disease. Circ Res 2010; 107: 677-684.
67. Rixe J, Rolf A, Fichtlscherer S, Moellmann H, Nef H, Liebetrau C, et al. Plasma levels of circulating MicroRNAs correlate with coronary plaque burden as assessed by cardiac computed tomography. Circulation 2011; 124: A15162.
68. Leistner DM, Fichtlscherer S, Thome C, Boeckel N, Roexe T, Müller-Ardogan M, et al. Eur Heart J 2013; 34(Suppl 1): P5445, doi:10.1093/eurheartj/eht310.P5445.
69. Dong S, Cheng Y, Yang J, Li J, Liu X, Wang X, et al. MicroRNA expression signature and the role of microRNA-21 in the early phase of acute myocardial infarction. J Biol Chem 2009; 284: 29514-29525.
70. Ji X, Takahashi R, Hiura Y, Hirokawa G, Fukushima Y, Iwai N. Plasma miR-208 as a biomarker of myocardial injury. Clin Chem 2009; 55: 1944-1949.
71. Wang R, Li N, Zhang Y, Ran Y, Pu J. Circulating MiRs are promis ing novel biomarkers of acute myocardial infarction. Intern Med 2011; 50: 1789-1795.
72. Corsten MF, Dennert R, Jochems S, Kuznetsova T, Devaux Y, Hofstra L, et al. Circulating MicroRNA-208b and MicroRNA 499 reflect myocardial damage in cardiovascular disease. Circ Cardiovasc Genet 2010; 3: 499-506.
73. Bostjancic E, Zidar N, Stajer D, Glavac D. MiRs miR-1, miR-133a, miR-133b and miR-208 are dysregulated in human myocardial infarction. Cardiology 2010; 115: 163-169.
74. Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, et al. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochem Biophys Res Commun 2010; 391: 73-77.
75. Cheng Y, Tan N, Yang J, Liu X, Cao X, He P, et al. A translational study of circulating cell-free microRNA-1 in acute myocardial infarction. Clin Sci (Lond) 2010; 119: 87-95.
76. D'Alessandra Y, Devanna P, Limana F, Straino S, Di Carlo A, Brambilla PG, et al. Circulating miRs are new and sensitive biomarkers of myocardial infarction. Eur Heart J 2010; 31: 2765-2773.
77. Gidlof O, Andersson P, van der Pals J, Gotberg M, Erlinge D. Cardiospecific microRNA plasma levels correlate with troponin and cardiac function in patients with ST elevation myocardial infarction, are selectively dependent on renal elimination, and can be detected in urine samples. Cardiology 2011; 118: 217-226.
78. Devaux Y, Vausort M, Goretti E, Nazarov PV, Azuaje F, Gilson G, et al. Use of circulating miRs to diagnose acute myocardial infarction. Clin Chem 2012; 58: 559-567.
79. Widera C, Gupta SK, Lorenzen JM, Bang C, Bauersachs J, Bethmann K, et al. Diagnostic and prognostic impact of six circulating miRs in acute coronary syndrome. J Mol Cell Cardiol 2011; 51: 872-875.
80. Meder B, Keller A, Vogel B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, et al. MicroRNA signatures in total peripheral blood as novel biomarkers for acute myocardial infarction. Basic Res Cardiol 2011; 106: 13-23.
81. Indolfi C, Gasparri C, Vicinanza C, De Serio D, Boncompagni D, Mongiardo A, et al. Mitogen-activated protein kinases activation in T lymphocytes of patients with acute coronary syndromes. Basic Res Cardiol 2011; 106: 667-679.
82. Flammer AJ, Gössl M, Widmer RJ, Reriani M, Lennon R, Loeffler D, et al. Osteocalcin positive CD133+/CD34-/KDR+ progenitor cells as an independent marker for unstable atherosclerosis. Eur Heart J 2012; 33: 2963-2969.
83. Moon JH, Chae MK, Kim KJ, Kim HM, Cha BS, Lee HC, et al. Decreased endothelial progenitor cells and increased serum glycated albumin are independently correlated with plaque-forming carotid artery atherosclerosis in type 2 diabetes patients without documented ischemic disease. Circ J 2012; 76: 2273-2279.
84. Wang GK, Zhu JQ, Zhang JT, Li Q, Li Y, He J, et al. Circulating microRNA: A novel potential biomarker for early diagnosis of acute myocardial infarction in humans. Eur Heart J 2010; 31: 659-666.
85. Sanchis J, Bardají A, Bosch X, Loma-Osorio P, Marín F, Sánchez PL, et al. Usefulness of high-sensitivity troponin T for the evaluation of patients with acute chest pain and no or minimal myocardial damage. Am Heart J 2012; 164: 194-200.
86. Tijsen AJ, Creemers EE, Moerland PD, de Windt LJ, van der Wal AC, Kok WE, et al. MiR423-5p as a circulating biomarker for heart failure. Circ Res 2010; 106: 1035-1039.
87. Xiao J, Jing ZC, Ellinor PT, Liang D, Zhang H, Liu Y, et al. MicroRNA-134 as a potential plasma biomarker for the diagnosis of acute pulmonary embolism. J Transl Med 2011; 9: 159.
88. Willerson JT, Golino P, Eidt J, Campbell WB, Buja LM. Specific platelet mediators and unstable coronary artery lesions. Experimental evidence and potential clinical implications. Circulation 1989; 80: 198-205.
89. Cirillo P, Golino P, Calabrò P, Ragni M, Forte L, Piro O, et al. Activated platelets stimulate tissue factor expression in smooth muscle cells. Thromb Res 2003; 112: 51-57.
90. Landry P, Plante I, Ouellet DL, Perron MP, Rousseau G, Provost P. Existence of a microRNA pathway in anucleate platelets. Nat Struct Mol Biol 2009; 16: 961-966.
91. Sondermeijer BM, Bakker A, Halliani A, de Ronde MW, Marquart AA, Tijsen AJ, et al. Platelets in patients with premature coronary artery disease exhibit upregulation of miRNA340 and miRNA624. PLoS One 2011; 6: e25946, doi:10.1371/journal.pone.0025946. (accessed 2 January, 2014.)
92. Nagalla S, Shaw C, Kong X, Kondkar AA, Edelstein LC, Ma L, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011; 117: 5189-5197.
93. Edelstein LC, Bray PF. MicroRNAs in platelet production and ac- tivation. Blood 2011; 117: 5289-5296.
94. Kondkar AA, Bray MS, Leal SM, Nagalla S, Liu DJ, Jin Y, et al. VAMP8/endobrevin is overexpressed in hyperreactive human platelets: Suggested role for platelet microRNA. J Thromb Haemost 2010; 8: 369-378.
95. Thum T, Galuppo P, Wolf C, Fiedler J, Kneitz S, van Laake LW, et al. MiRs in the human heart: A clue to fetal gene reprogramming in heart failure. Circulation 2007; 116: 258-267.
96. Dirkx E, Gladka MM, Philippen LE, Armand AS, Kinet V, Leptidis S, et al. Nfat and miR-25 cooperate to reactivate the transcription factor Hand2 in heart failure. Nat Cell Biol 2013; 15: 1282-1293.
97. Sucharov C, Bristow MR, Port JD. MiRNA expression in the failing human heart: Functional correlates. J Mol Cell Cardiol 2008; 45: 185-192.
98. Montgomery RL, Hullinger TG, Semus HM, Dickinson BA, Seto AG, Lynch JM, et al. Therapeutic inhibition of miR-208a improves cardiac function and survival during heart failure. Circulation 2011; 124: 1537-1547.
99. Limana F, Esposito G, D'Arcangelo D, Di Carlo A, Romani S, Melillo G, et al. HMGB1 attenuates cardiac remodelling in the failing heart via enhanced cardiac regeneration and miR-206-mediated inhibition of TIMP-3. PLoS One 2011; 6: e19845, doi:10.1371/ journal.pone.0019845. (accessed 2 January, 2014.)
100. Naga Prasad SV, Duan ZH, Gupta MK, Surampudi VS, Volinia S, Calin GA, et al. Unique microRNA profile in end-stage heart failure indicates alterations in specific cardiovascular signaling networks. J Biol Chem 2009; 284: 27487-27499.
101. Fukushima Y, Nakanishi M, Nonogi H, Goto Y, Iwai N. Assessment of plasma miRs in congestive heart failure. Circ J 2011; 75: 336-340.
102. Voellenkle C, van Rooij J, Cappuzzello C, Greco S, Arcelli D, Di Vito L, et al. MicroRNA signatures in peripheral blood mononuclear cells of chronic heart failure patients. Physiol Genomics 2010; 42: 420-426.
103. Goren Y, Kushnir M, Zafrir B, Tabak S, Lewis BS, Amir O. Serum levels of miRs in patients with heart failure. Eur J Heart Fail 2012; 14: 147-154.
104. Qureshi IA, Mehler MF. The emerging role of epigenetics in stroke: II. RNA regulatory circuitry. Arch Neurol 2010; 67: 1435-1441.
105. Jeyaseelan K, Lim KY, Armugam A. MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 2008; 39: 959-966.
106. Laterza OF, Lim L, Garrett-Engele PW, Vlasakova K, Muniappa N, Tanaka WK, et al. Plasma MiRs as sensitive and specific biomarkers of tissue injury. Clin Chem 2009; 55: 1977-1983.
107. Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J Cereb Blood Flow Metab 2009; 29: 675-687.
108. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, et al. Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J Cereb Blood Flow Metab 2010; 30: 92-101.
109. Tan KS, Armugam A, Sepramaniam S, Lim KY, Setyowati KD, Wang CW, et al. Expression profile of MiRs in young stroke patients. PLoS One 2009; 4: e7689, doi:10.1371/journal. pone.0007689.
110. Rink C, Khanna S. MicroRNA in ischemic stroke etiology and pathology. Physiol Genomics 2011; 43: 521-528.
111. Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Front Biosci (Elite Ed) 2011; 3: 1265-1272.
112. Yin KJ, Deng Z, Huang H, Hamblin M, Xie C, Zhang J, et al. miR- 497 regulates neuronal death in mouse brain after transient focal cerebral ischemia. Neurobiol Dis 2010; 38: 17-26.
113. Selvamani A, Sathyan P, Miranda RC, Sohrabji F. An antagomir to microRNA Let7f promotes neuroprotection in an ischemic stroke model. PLoS One 2012; 7: e32662, doi:10.1371/journal. pone.0032662.
114. Ouyang YB, Lu Y, Yue S, Giffard RG. miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion 2012; 12: 213-219.
115. Ouyang YB, Lu Y, Yue S, Xu LJ, Xiong XX, White RE, et al. miR- 181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis 2012; 45: 555-563.
116. Budde H, Schmitt S, Fitzner D, Opitz L, Salinas-Riester G, Simons M. Control of oligodendroglial cell number by the miR-17-92 cluster. Development 2010; 137: 2127-2132.
117. Chen J, Yang T, Yu H, Sun K, Shi Y, Song W. A functional variant in the 3-UTR of angiopoietin-1 might reduce stroke risk by interfering with the binding efficiency of microRNA 211. Hum Mol Genet 2010; 19: 2524-2533.