The role of microRNAs in the initiation and progression of stable atheromatous plaque

Current Pharmaceutical Design

Volumn 19, Issue 9, 2013, Pages 1651-1657

  Papageorgiou, Nikolaos ^a   Tousoulis, Dimitris ^a   Androulakis, Emmanuel ^a   Kontogeorgou, Anna ^a   Charakida, Marietta ^a   Giolis, Anastasios ^a   Siama, Katerina ^a   Trikas, Athanasios ^a   Briasoulis, Alexandros ^a   Pitsavos, Christos ^a   Stefanadis, Christodoulos ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Atherosclerosis; miRNAs; Plaque progression

Indexed keywords

BIOLOGICAL MARKER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LOW DENSITY LIPOPROTEIN; MICRORNA; MICRORNA 1; MICRORNA 125A; MICRORNA 126; MICRORNA 126 3P; MICRORNA 12B; MICRORNA 143; MICRORNA 145; MICRORNA 155; MICRORNA 17 3P; MICRORNA 21; MICRORNA 214; MICRORNA 221; MICRORNA 222; MICRORNA 26A; MICRORNA 27B; MICRORNA 30C; MICRORNA 31; MICRORNA 33; MICRORNA 378; MICRORNA 92A; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN LET 7; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANGIOGENESIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BIOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL FEATURE; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DISEASE COURSE; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVITY; GENE EXPRESSION; HEART INFARCTION; HEART PROTECTION; HUMAN; HYPERHOMOCYSTEINEMIA; HYPERLIPIDEMIA; HYPERTENSION; INFLAMMATION; PATHOGENESIS; PRIORITY JOURNAL; SMOKING; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; VASCULAR SMOOTH MUSCLE;

EID: 84876720612     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612811319090012     Document Type: Article

References (101)

1. Tousoulis D, Hatzis G, Papageorgiou N, et al. Assessment of acute coronary syndromes: focus on novel biomarkers. Curr Med Chem 2012; 19: 2572-87.
2. Kampoli AM, Tousoulis D, Papageorgiou N, et al. Clinical utility of biomarkers in premature atherosclerosis. Curr Med Chem 2012; 19: 2521-33.
3. Briasoulis A, Tousoulis D, Androulakis ES, Papageorgiou N, Latsios G, Stefanadis C. Endothelial dysfunction and atherosclerosis: focus on novel therapeutic approaches. Recent Pat Cardiovasc Drug Discov 2012; 7: 21-32.
4. Tousoulis D, Charakida M, Stefanadis C. Endothelial function and inflammation in coronary artery disease. Heart 2006; 92: 441-4.
5. Tousoulis D, Koutsogiannis M, Papageorgiou N, et al. Endothelial dysfunction: potential clinical implications. Minerva Med 2010; 101: 271-84.
6. Tousoulis D, Kampoli AM, Papageorgiou N, et al. Pathophysiology of atherosclerosis: the role of inflammation. Curr Pharm Des 2011; 17: 4089-110.
7. Papageorgiou N, Tousoulis D, Androulakis E, et al. The role of microRNAs in cardiovascular disease. Curr Med Chem 2012; 19: 2605-10.
8. Shyu AB, Wilkinson MF, van Hoof A. Messenger RNA regulation: to translate or to degrade. EMBO J 2008; 27: 471-81.
9. Lee Y, Ahn C, Han J, et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003; 425: 415-419.
10. Gregory RI, Yan K, Amuthan G, et al. The microprocessor complex mediates the genesis of microRNAs. Nature 2004; 432: 235-240.
11. Ono K, Kuwabara Y, Han J. MicroRNAs and cardiovascular diseases. FEBS J 2011; 278: 1619-33.
12. Haver VG, Slart RH, Zeebregts CJ, Peppelenbosch MP, Tio RA. Rupture of vulnerable atherosclerotic plaques: MicroRNAs conducting the orchestra? Trends Cardiovasc Med 2010; 20: 65-71.
13. Wang K, Zhang S, Marzolf B, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA 2009; 106: 4402-440.
14. Alevizos I, Illei GG. MicroRNAs as biomarkers in rheumatic diseases. Nat Rev Rheumatol 2010; 6: 391-398
15. Condorelli G, Latronico MV, Dorn GW 2nd. microRNAs in heart disease: putative novel therapeutic targets? Eur Heart J 2010; 31: 649-58.
16. Borchert GM, Lanier W, Davidson BL. RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 2006; 13: 1097-1101.
17. Bohnsack MT, Czaplinski K, Gorlich D. Exportin 5 is a RanGTPdependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA 2004; 10: 185-191.
18. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004; 303: 95-98.
19. Suarez Y, Sessa WC. 2009. MicroRNAs as novel regulators of angiogenesis. Circ Res 2009; 104: 442-454.
20. Zeng Y. Principles of micro-RNA production and maturation. Oncogene 2006; 25: 6156-6162.
21. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature 2007; 448: 83-86.
22. Zhang C. MicroRNomics: a newly emerging approach for disease biology. Physiol Genomics 2008; 33: 139-47.
23. Davison TS, Johnson CD, Andruss BF. Analyzing micro-RNA expression using microarrays. Methods Enzymol 2006; 411: 14-34.
24. Chen JF, Mandel EM, Thomson JM, et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 2006; 38: 228-233.
25. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Mycregulated microRNAs modulate E2F1 expression. Nature 2005; 435: 839-43.
26. Hutvagner G, McLachlan J, Pasquinelli AE, Balint E, Tuschl T, Zamore PD. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001; 293: 834-8.
27. Zeng Y, Cullen BR. Sequence requirements for micro RNA processing and function in human cells. RNA 2003; 9: 112-23.
28. Lim LP, Lau NC, Garrett-Engele P, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005; 433: 769-73.
29. Kim VN, Nam JW. Genomics of microRNA. Trends Genet 2006; 22: 165-73.
30. Wang Z, Luo X, Lu Y, Yang B. miRNAs at the heart of the matter. J Mol Med (Berl) 2008; 86: 771-83.
31. Hunter MP, Ismail N, Zhang X, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008; 3: e3694.
32. Celermajer DS, Sorensen KE, Bull C, Robinson J, Deanfield JE. Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction. J Am Coll Cardiol 1994; 24: 1468-74.
33. Tousoulis D, Antoniades C, Stefanadis C. Evaluating endothelial function in humans: a guide to invasive and non-invasive techniques. Heart 2005; 91: 553-8.
34. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352: 1685-95.
35. Papageorgiou N, Tousoulis D, Androulakis E, et al. Lifestyle Factors and Endothelial Function. Curr Vasc Pharmacol 2011; 10: 94-106.
36. Stefanadi E, Tousoulis D, Androulakis ES, et al. Inflammatory markers in essential hypertension: potential clinical implications. Curr Vasc Pharmacol 2010; 8: 509-16.
37. Tousoulis D, Papageorgiou N, Androulakis E, Paroutoglou K, Stefanadis C. Novel therapeutic strategies targeting vascular endothelium in essential hypertension. Expert Opin Investig Drugs 2010; 19: 1395-412.
38. Spagnoli LG, Bonanno E, Sangiorgi G, Mauriello A. Role of inflammation in atherosclerosis. J Nucl Med 2007; 48: 1800-15.
39. Li JJ. Inflammation in coronary artery diseases. Chin Med J (Engl) 2011; 124: 3568-75.
40. Kampoli AM, Tousoulis D, Papageorgiou N, et al. Matrix metalloproteinases in acute coronary syndromes: current perspectives. Curr Top Med Chem 2012; 12: 1192-205.
41. Moreno PR, Purushothaman KR, Zias E, Sanz J, Fuster V. Neovascularization in human atherosclerosis. Curr Mol Med 2006; 6: 457-77.
42. Drakopoulou M, Toutouzas K, Michelongona A, Tousoulis D, Stefanadis C. Vulnerable plaque and inflammation: potential clinical strategies. Curr Pharm Des 2011; 17: 4190-209.
43. Babak T, Zhang W, Morris Q, Blencowe BJ, Hughes TR. Probing microRNAs with microarrays: tissue specificity and functional inference. RNA 2004; 10: 1813-9.
44. Barad O, Meiri E, Avniel A, et al. MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 2004; 14: 2486-94.
45. Chen C, Ridzon DA, Broomer AJ, et al. Real-time quantification of microRNAs by stemloop RT-PCR. Nucleic Acids Res 2005; 33: e179.
46. Jamaluddin S, Weakley S, Zhang L, et al. miRNAs: roles and clinical applications in vascular disease, Expert Rev Mol Diagn 2011; 11: 79-89.
47. Qin B, Yang H, Xiao B. Role of microRNAs in endothelial inflammation and senescence, Mol Biol Rep 2012; 39: 4509-18.
48. Santovito D, Mezzetti A, Cipollone F. MicroRNAs and atherosclerosis: New actors for an old movie. Nutr Metab Cardiovasc Dis 2012 [Epub ahead of print].
49. Weber M, Baker MB, Moore JP, Searles CD. MiR-21 is induced in endothelial cells by shear stress and modulates apoptosis and eNOS activity. Biochem Biophys Res Commun 2010; 393: 643-8.
50. Fleissner F, Jazbutyte V, Fiedler J, et al. Short communication: asymmetric dimethylarginine impairs angiogenic progenitor cell function in patients with coronary artery disease through a microRNA-21-dependentmechanism. Circ Res 2010; 107: 138-43.
51. Chan LS, Yue PY, Mak NK, Wong RN. Role of microRNA-214 in ginsenoside-Rg1-induced angiogenesis. Eur J Pharm Sci 2009; 38: 370-7.
52. Ji R, Cheng Y, Yue J, et al. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circ Res 2007; 100: 1579-88.
53. Parmacek MS. MicroRNA-modulated targeting of vascular smooth muscle cells. J Clin Invest 2009; 119: 2526-8
54. Liu X, Cheng Y, Zhang S, et al. A necessary role of miR-222 and miR-221 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res 2009; 104: 476-87.
55. Zhang C. MicroRNA-145 in vascular smooth muscle cell biology: a new therapeutic target for vascular disease. Cell Cycle 2009; 8: 3469-73.
56. Elia L, Quintavalle M, Zhang J, et al. The knockout of miR-143 and-145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 2009; 16: 1590-8.
57. Cordes KR, Sheehy NT, White MP, et al. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009; 460: 705-10.
58. Cheng Y, Liu X, Yang J, et al. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res 2009; 105: 158-66.
59. Xin M, Small EM, Sutherland LB, et al. MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smoothmuscle cells to injury. Genes Dev 2009; 23: 2166-78.
60. Kawai-Kowase K, Owens GK. Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol 2007; 292: C59-69.
61. Boettger T, Beetz N, Kostin S, et al. Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest 2009; 119: 2634-47
62. Quintavalle M, Elia L, Condorelli G, Courtneidge SA. MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J Cell Biol 2010; 189: 13-22.
63. Davis BN, Hilyard AC, Nguyen PH, Lagna G, Hata A. Induction of microRNA-221 by platelet-derived growth factor signaling is critical for modulation of vascular smooth muscle phenotype. J Biol Chem 2009; 284: 3728-38.
64. Martin K, O'Sullivan J, Caplice N. New therapeutic potential of microRNA treatment to target vulnerable atherosclerotic lesions and plaque rupture. Cur Opin Cardiol 2011; 26: 569-75
65. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis, Cardiovasc Res 2008; 79: 581-8.
66. Suarez Y, Fernandez-Hernando C, Yu J, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA 2008; 105: 14082-7.
67. Poliseno L, Tuccoli A, Mariani L, et al. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 2006; 108: 3068-71.
68. Chen Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that downregulates antiangiogenic homeobox genes GAX and HOXA5. Blood 2008; 111: 1217-26.
69. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S. Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 2007; 101: 59-68.
70. Lee DY, Deng Z, Wang CH, Yang BB. MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc Natl Acad Sci USA 2007; 104: 20350-5.
71. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007; 100: 1164-73.
72. Murohara T, Asahara T, Silver M, et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 1998; 101: 2567-2578.
73. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999; 340: 115-26.
74. Silvestre JS, Mallat Z, Tedgui A, Levy BI. Post-ischemic neovascularisation and inflammation. Cardiovasc Res 2008; 78: 242-9.
75. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA 2008; 105: 1516-21.
76. Zhu N, Zhang D, Chen S, et al. Endothelial enriched microRNAs regulate angiotensin II-induced endothelial inflammation and migration. Atherosclerosis 2011; 215: 286-93
77. Fichtlscherer S, De Rosa S, Fox H, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010; 107: 677-84.
78. Minami Y, Satoh M, Maesawa C, et al. Effect of atorvastatin on microRNA 221 / 222 expression in endothelial progenitor cells obtained from patients with coronary artery disease. Eur J Clin Invest 2009; 39: 359-67.
79. Li D, Yang P, Xiong Q, et al. MicroRNA-125a/b-5p inhibits endothelin-1 expression in vascular endothelial cells. J Hypertens 2010; 28: 1646-54
80. Chen T, Huang Z, Wang L, et al. MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/ macrophages. Cardiovasc Res 2009; 83: 131-9
81. Suarez Y, Wang C, Manes TD, Pober JS. Cutting edge: TNFinduced microRNAs regulate TNF-induced expression of Eselectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J Immunol 2010; 184: 21-25.
82. Callis TE, Chen JF, Wang DZ. MicroRNAs in skeletal and cardiac muscle development. DNA Cell Biol 2007; 26: 219-25.
83. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 2005; 436: 214-20.
84. Kwon C, Han Z, Olson EN, Srivastava D. MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc Natl Acad Sci USA 2005; 102: 18986-91.
85. Zhao Y, Ransom JF, Li A, et al. Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 2007; 129: 303-17.
86. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G. Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 2005; 280: 9330-5.
87. Inoue T, Node K. Molecular basis of restenosis and novel issues of drug-eluting stents. Circ J 2009; 73: 615-21.
88. Rader DJ, Puré E. Lipoproteins, macrophage function, and atherosclerosis: beyond the foam cell? Cell Metab 2005; 1: 223-30.
89. Huang RS, Hu GQ, Lin B, Lin ZY, Sun CC. MicroRNA-155 silencing enhances inflammatory response and lipid uptake in oxidized low-density lipoprotein-stimulated human THP-1 macrophages. J Investig Med 2010; 58: 961-7.
90. Najafi-Shoushtari SH. MicroRNAs in cardiometabolic disease. Curr Atheroscler Rep 2011; 13: 202-7.
91. Rayner KJ, Suarez Y, Davalos A, et al. MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010; 328: 1570-3
92. Esau C, Davis S, Murray SF, et al. miR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab 2006; 3: 87-98.
93. Bakogiannis C, Tousoulis D, Androulakis E, et al. Circulating endothelial progenitor cells as biomarkers for prediction of cardiovascular outcomes. Curr Med Chem 2012; 19: 2597-604.
94. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008; 79: 581-8.
95. Chen Y, Banda M, Speyer CL, et al. Regulation of the expression and activity of the antiangiogenic homeobox gene GAX/MEOX2 by ZEB2 and microRNA-221. Mol Cell Biol 2010; 30: 3902-13
96. Zacharowski K, Zacharowski P, Reingruber S, Petzelbauer P. Fibrin(ogen) and its fragments in the pathophysiology and treatment of myocardial infarction. J Mol Med (Berl) 2006; 84: 469-77
97. Margulies KB. MicroRNAs as novel myocardial biomarkers. Cin Chem 2009; 55: 1897-9.
98. 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: 1944-9.
99. Xu J, Zhao J, Evan G, Xiao C, Cheng Y, Xiao J. Circulating microRNAs: novel biomarkers for cardiovascular diseases. J Mol Med (Berl) 2012; 90: 865-75
100. Bonauer A, Carmona G, Iwasaki M, et al. MicroRNA-92a controls angiogenesis an and functional recovery of ischemic tissues in mice. Science 2009; 324: 1710-3.
101. Yin C, Salloum FN, Kukreja RC. A novel role of microRNA in late preconditioning: upregulation of endothelial nitric oxide synthase and heat shock protein 70. Circ Res 2009; 104: 572-5.