Platelet microRNAs: From platelet biology to possible disease biomarkers and therapeutic targets

Platelets

Volumn 24, Issue 8, 2013, Pages 579-589

  Stakos, Dimitrios A ^a   Gatsiou, Aikaterini ^b,c   Stamatelopoulos, Kimon ^d   Tselepis, Alexandros D ^c   Stellos, Konstantinos ^b  

^a DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF IOANNINA   (Greece)

^d UNIVERSITY OF ATHENS   (Greece)

Author keywords

cardiovascular disease; MiRNAs; platelets

Indexed keywords

BIOLOGICAL MARKER; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; MICRORNA; MICRORNA 107; MICRORNA 200B;

ARTERIOSCLEROSIS; CARDIOVASCULAR DISEASE; DRUG TARGETING; HUMAN; NONHUMAN; PLATELET REACTIVITY; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; THROMBOCYTE; THROMBOCYTE FUNCTION; THROMBOCYTE SHAPE; THROMBOCYTOPOIESIS; VASCULITIS;

ANIMALS; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; BLOOD PLATELETS; HUMANS; MICRORNAS; RNA INTERFERENCE; RNA, MESSENGER; THROMBOSIS;

EID: 84885946027     PISSN: 09537104     EISSN: 13691635     Source Type: Journal    
DOI: 10.3109/09537104.2012.724483     Document Type: Review

References (126)

1. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011;12:861-874.
2. Nagalla S, Shaw C, Kong X, Kondkar AA, Edelstein LC, Ma L, Chen J, McKnight GS, Lopez JA, Yang L, et al. Platelet microRNA-mRNA coexpression profiles correlate with platelet reactivity. Blood 2011;117:5189-5197.
3. 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.
4. Gatsiou A, Boeckel N, Randriamboavonjy V, Stellos K. MicroRNAs in platelet biogenesis and function: Implications in vascular homeostasis and inflammation. Curr Vasc Pharmacol 2012;10:524-531.
5. Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, Volinia S, Bhatt D, Alder H, Marcucci G, et al. MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA 2006;103:5078-5083.
6. Kondkar AA, Bray MS, Leal SM, Nagalla S, Liu DJ, Jin Y, Dong JF, Ren Q, Whiteheart SW, Shaw C, et al. Vamp8/endobrevin is overexpressed in hyperreactive human platelets: Suggested role for platelet microRNA. J Thromb Haemost 2010;8:369-378.
7. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, et al. MicroRNA-21 contributes to myocardial disease by stimulating map kinase signalling in fibroblasts. Nature 2008;456:980-984.
8. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C. MicroRNA expression signature and antisense-mediated depletion reveal an essential role of microRNA in vascular neointimal lesion formation. Circ Res 2007;100:1579-1588.
9. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN. Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 2008;105:13027-13032.
10. Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini P, Gu Y, Dalton ND, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007;13:613-618.
11. Xiao J, Luo X, Lin H, Zhang Y, Lu Y, Wang N, Zhang Y, Yang B, Wang Z. MicroRNA miR-133 represses HERG K channel expression contributing to QT prolongation in diabetic hearts. J Biol Chem 2007;282:12363-12367.
12. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, Sutton GG, Smith HO, Yandell M, Evans CA, Holt RA, et al. The sequence of the human genome. Science 2001;291:1304-1351.
13. Elgar G, Vavouri T. Tuning in to the signals: Noncoding sequence conservation in vertebrate genomes. Trends Genet 2008;24:344-352.
14. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, et al. The transcriptional landscape of the mammalian genome. Science 2005;309:1559-1563.
15. Kapranov P, Drenkow J, Cheng J, Long J, Helt G, Dike S, Gingeras TR. Examples of the complex architecture of the human transcriptome revealed by race and high-density tiling arrays. Genome Res 2005;15:987-997.
16. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 2006;15(Suppl. 1):R17-R29.
17. Kapranov P, Willingham AT, Gingeras TR. Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 2007;8:413-423.
18. Stefani G, Slack FJ. Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 2008;9:219-230.
19. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993;75:843-854.
20. Rajewsky N. MicroRNA target predictions in animals. Nat Genet 2006;38(Suppl):S8-S13.
21. Yi R, Qin Y, Macara IG, Cullen BR. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev 2003;17:3011-3016.
22. Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U. Nuclear export of microRNA precursors. Science 2004;303:95-98.
23. Zamore PD, Tuschl T, Sharp PA, Bartel DP. RNAi: Doublestranded RNA directs the ATP-dependent cleavage of mRNA at to 23 nucleotide intervals. Cell 2000;101:25-33.
24. Vermeulen A, Behlen L, Reynolds A, Wolfson A, Marshall WS, Karpilow J, Khvorova A. The contributions of dsRNA structure to dicer specificity and efficiency. RNA 2005;11: 674-682.
25. Preall JB, He Z, Gorra JM, Sontheimer EJ. Short interfering RNA strand selection is independent of dsRNA processing polarity during RNAi in drosophila. Curr Biol 2006;16:530-535.
26. Siomi H, Siomi MC. On the road to reading the RNA-interference code. Nature 2009;457:396-404.
27. Gregory RI, Chendrimada TP, Cooch N, Shiekhattar R. Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell 2005;123:631-640.
28. Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004;116:281-297.
29. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009;19:92-105.
30. Hennessy E, O'Driscoll L. Molecular medicine of microRNAs: Structure, function and implications for diabetes. Expert Rev Mol Med 2008;10:e24.
31. Guo M, Mao X, Ji Q, Lang M, Li S, Peng Y, Zhou W, Xiong B, Zeng Q. miR-146a in PBMCs modulates Th1 function in patients with acute coronary syndrome. Immunol Cell Biol 2010;88:555-564.
32. Filipowicz W. RNAi: The nuts and bolts of the RISC machine. Cell 2005;122:17-20.
33. Zamore PD, Haley B. Ribo-gnome: The big world of small RNAs. Science 2005;309:1519-1524.
34. Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. Animal microRNAs confer robustness to gene expression and have a significant impact on 30 UTR evolution. Cell 2005;123:1133-1146.
35. Lee CT, Risom T, Strauss WM. Evolutionary conservation of microRNA regulatory circuits: An examination of microRNA gene complexity and conserved microRNA-target interactions through metazoan phylogeny. DNA Cell Biol 2007;26:209-218.
36. Osman A, Falker K. Characterization of human platelet microRNA by quantitative PCR coupled with an annotation network for predicted target genes. Platelets 2011;22:433-441.
37. Denis MM, Tolley ND, Bunting M, Schwertz H, Jiang H, Lindemann S, Yost CC, Rubner FJ, Albertine KH, Swoboda KJ, et al. Escaping the nuclear confines: Signal-dependent premRNA splicing in anucleate platelets. Cell 2005;122:379-391.
38. Dittrich M, Birschmann I, Pfrang J, Herterich S, Smolenski A, Walter U, Dandekar T. Analysis of SAGE data in human platelets: Features of the transcriptome in an anucleate cell. Thromb Haemost 2006;95:643-651.
39. Bruchova H, Merkerova M, Prchal JT. Aberrant expression of microRNA in polycythemia vera. Haematologica 2008;93: 1009-1016.
40. Edelstein LC, Bray PF. MicroRNAs in platelet production and activation. Blood 2011;117:5289-5296.
41. Hussein K, Theophile K, Dralle W, Wiese B, Kreipe H, Bock O. MicroRNA expression profiling of megakaryocytes in primary myelofibrosis and essential thrombocythemia. Platelets 2009; 20:391-400.
42. Sevinsky JR, Whalen AM, Ahn NG. Extracellular signalregulated kinase induces the megakaryocyte GPIIb/CD41 gene through MafB/Kreisler. Mol Cell Biol 2004;24:4534-4545.
43. Wang X, Crispino JD, Letting DL, Nakazawa M, Poncz M, Blobel GA. Control of megakaryocyte-specific gene expression by GATA-1 and FOG-1: Role of Ets transcription factors. EMBO J 2002;21:5225-5234.
44. Kaushansky K. Historical review: Megakaryopoiesis and thrombopoiesis. Blood 2008;111:981-986.
45. Girardot M, Pecquet C, Boukour S, Knoops L, Ferrant A, Vainchenker W, Giraudier S, Constantinescu SN. miR-28 is a thrombopoietin receptor targeting microRNA detected in a fraction of myeloproliferative neoplasm patient platelets. Blood 2010;116:437-445.
46. Dangelmaier C, Jin J, Smith JB, Kunapuli SP. Potentiation of thromboxane A2-induced platelet secretion by Gi signaling through the phosphoinositide-3 kinase pathway. Thromb Haemost 2001;85:341-348.
47. Jin J, Kunapuli SP. Coactivation of two different G proteincoupled receptors is essential for ADP-induced platelet aggregation. Proc Natl Acad Sci USA 1998;95:8070-8074.
48. Jin J, Quinton TM, Zhang J, Rittenhouse SE, Kunapuli SP. Adenosine diphosphate (ADP)-induced thromboxane A(2) generation in human platelets requires coordinated signaling through integrin alpha(IIb)beta(3) and ADP receptors. Blood 2002;99:193-198.
49. Dorsam RT, Kunapuli SP. Central role of the P2Y12 receptor in platelet activation. J Clin Invest 2004;113:340-345.
50. Hollopeter G, Jantzen HM, Vincent D, Li G, England L, Ramakrishnan V, Yang RB, Nurden P, Nurden A, Julius D, et al. Identification of the platelet ADP receptor targeted by antithrombotic drugs. Nature 2001;409:202-207.
51. Haslam RJ, Davidson MM, Davies T, Lynham JA, McClenaghan MD. Regulation of blood platelet function by cyclic nucleotides. Adv Cyclic Nucl Res 1978;9:533-552.
52. Gambaryan S, Kobsar A, Rukoyatkina N, Herterich S, Geiger J, Smolenski A, Lohmann SM, Walter U. Thrombin and collagen induce a feedback inhibitory signaling pathway in platelets involving dissociation of the catalytic subunit of protein kinase a from an NFkappaB-IkappaB complex. J Biol Chem 2010;285: 18352-18363.
53. Hung HC, Maurer C, Zorn D, Chang WL, Weber F. Sequential and compartment-specific phosphorylation controls the life cycle of the circadian clock protein. J Biol Chem 2009;284: 23734-23742.
54. Kondratov RV, Chernov MV, Kondratova AA, Gorbacheva VY, Gudkov AV, Antoch MP. BMAL1-dependent circadian oscillation of nuclear clock: Posttranslational events induced by dimerization of transcriptional activators of the mammalian CLOCK system. Genes Dev 2003;17:1921-1932.
55. Somanath PR, Podrez EA, Chen J, Ma Y, Marchant K, Antoch M, Byzova TV. Deficiency in core circadian protein BMAL1 is associated with a prothrombotic and vascular phenotype. J Cell Physiol 2011;226:132-140.
56. Ohkura N, Oishi K, Sudo T, Hayashi H, Shikata K, Ishida N, Matsuda J, Horie S. CLOCK regulates circadian platelet activity. Thromb Res 2009;123:523-527.
57. Thurlow PJ, Kenneally DA, Connellan JM. The role of fibronectin in platelet aggregation. Br J Haematol 1990;75:549-556.
58. Tan MH, Sun Z, Opitz SL, Schmidt TE, Peters JH, George EL. Deletion of the alternatively spliced fibronectin EIIIA domain in mice reduces atherosclerosis. Blood 2004;104:11-18.
59. Matuskova J, Chauhan AK, Cambien B, Astrof S, Dole VS, Piffath CL, Hynes RO, Wagner DD. Decreased plasma fibronectin leads to delayed thrombus growth in injured arterioles. Arterioscler Thromb Vasc Biol 2006;26:1391-1396.
60. Ni H, Yuen PS, Papalia JM, Trevithick JE, Sakai T, Fassler R, Hynes RO, Wagner DD. Plasma fibronectin promotes thrombus growth and stability in injured arterioles. Proc Natl Acad Sci USA 2003;100:2415-2419.
61. Cho J, Mosher DF. Impact of fibronectin assembly on platelet thrombus formation in response to type I collagen and von Willebrand factor. Blood 2006;108:2229-2236.
62. Shan SW, Lee DY, Deng Z, Shatseva T, Jeyapalan Z, Du WW, Zhang Y, Xuan JW, Yee SP, Siragam V, et al. MicroRNA miR-17 retards tissue growth and represses fibronectin expression. Nat Cell Biol 2009;11:1031-1038.
63. Cheresh DA, Berliner SA, Vicente V, Ruggeri ZM. Recognition of distinct adhesive sites on fibrinogen by related integrins on platelets and endothelial cells. Cell 1989;58:945-953.
64. Chen CS, Hawiger J. Reactivity of synthetic peptide analogs of adhesive proteins in regard to the interaction of human endothelial cells with extracellular matrix. Blood 1991; 77:2200-2206.
65. Bennett JS, Vilaire G. Exposure of platelet fibrinogen receptors by ADP and epinephrine. J Clin Invest 1979;64:1393-1401.
66. Marguerie GA, Edgington TS, Plow EF. Interaction of fibrinogen with its platelet receptor as part of a multistep reaction in ADP-induced platelet aggregation. J Biol Chem 1980;255: 154-161.
67. Fibrinogen Studies Collaboration, Danesh J, Lewington S, Thompson SG, Lowe GD, Collins R, Kostis JB, Wilson AC, Folsom AR, Wu K, et al. Plasma fibrinogen level and the risk of major cardiovascular diseases and nonvascular mortality: An individual participant meta-analysis. JAMA 2005;294: 1799-1809.
68. Mosesson MW, Siebenlist KR, Meh DA. The structure and biological features of fibrinogen and fibrin. Ann NY Acad Sci 2001;936:11-30.
69. Fort A, Borel C, Migliavacca E, Antonarakis SE, Fish RJ, Neerman-Arbez M. Regulation of fibrinogen production by microRNAs. Blood 2010;116:2608-2615.
70. Fuller GM, Zhang Z. Transcriptional control mechanism of fibrinogen gene expression. Ann NY Acad Sci 2001;936: 469-479.
71. Reed GL. Platelet secretory mechanisms. Semin Thromb Hemost 2004;30:441-450.
72. Coppinger JA, Cagney G, Toomey S, Kislinger T, Belton O, McRedmond JP, Cahill DJ, Emili A, Fitzgerald DJ, Maguire PB. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood 2004;103:2096-2104.
73. Flaumenhaft R. Molecular basis of platelet granule secretion. Arterioscler Thromb Vasc Biol 2003;23:1152-1160.
74. Ungar D, Hughson FM. Snare protein structure and function. Annu Rev Cell Dev Biol 2003;19:493-517.
75. Ren Q, Barber HK, Crawford GL, Karim ZA, Zhao C, Choi W, Wang CC, Hong W, Whiteheart SW. Endobrevin/VAMP-8 is the primary v-SNARE for the platelet release reaction. Mol Biol Cell 2007;18:24-33.
76. Polgar J, Chung SH, Reed GL. Vesicle-associated membrane protein 3 (VAMP-3) and VAMP-8 are present in human platelets and are required for granule secretion. Blood 2002;100: 1081-1083.
77. Shiffman D, Rowland CM, Louie JZ, Luke MM, Bare LA, Bolonick JI, Young BA, Catanese JJ, Stiggins CF, Pullinger CR, et al. Gene variants of VAMP8 and HNRPUL1 are associated with early-onset myocardial infarction. Arterioscler Thromb Vasc Biol 2006;26:1613-1618.
78. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005;120:15-20.
79. Robinson DN, Cooley L. Drosophila kelch is an oligomeric ring canal actin organizer. J Cell Biol 1997;138:799-810.
80. Hartwig JH. Mechanisms of actin rearrangements mediating platelet activation. J Cell Biol 1992;118:1421-1442.
81. Ezzell RM, Kenney DM, Egan S, Stossel TP, Hartwig JH. Localization of the domain of actin-binding protein that binds to membrane glycoprotein Ib and actin in human platelets. J Biol Chem 1988;263:13303-13309.
82. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC. Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007;100:1164-1173.
83. 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;280:9330-9335.
84. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D. miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 2008;15:272-284.
85. Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 2008;3:e3694.
86. 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;105:1516-1521.
87. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelialspecific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 2008;15:261-271.
88. Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, Tsuneoka M, Komiya S, Baron R, Yoshimura A. Spred is a sprouty-related suppressor of ras signalling. Nature 2001;412:647-651.
89. Stellos K, Langer H, Daub K, Schoenberger T, Gauss A, Geisler T, Bigalke B, Mueller I, Schumm M, Schaefer I, et al. Platelet-derived stromal cell-derived factor-1 regulates adhesion and promotes differentiation of human CD34 cells to endothelial progenitor cells. Circulation 2008;117:206-215.
90. Stellos K, Langer H, Gnerlich S, Panagiota V, Paul A, Schonberger T, Ninci E, Menzel D, Mueller I, Bigalke B, et al. Junctional adhesion molecule a expressed on human CD34 cells promotes adhesion on vascular wall and differentiation into endothelial progenitor cells. Arterioscler Thromb Vasc Biol 2010;30:1127-1136.
91. Stellos K, Bigalke B, Langer H, Geisler T, Schad A, Kogel A, Pfaff F, Stakos D, Seizer P, Muller I, et al. Expression of stromal-cell-derived factor-1 on circulating platelets is increased in patients with acute coronary syndrome and correlates with the number of CD34 progenitor cells. Eur Heart J 2009;30:584-593.
92. Stellos K, Rahmann A, Kilias A, Ruf M, Sopova K, Stamatelopoulos K, Jorbenadze R, Weretka S, Geisler T, Gawaz M, et al. Expression of platelet-bound stromal cellderived factor-1 in patients with non-valvular atrial fibrillation and ischemic heart disease. J Thromb Haemost 2012;10:49-55.
93. Stellos K, Seizer P, Bigalke B, Daub K, Geisler T, Gawaz M. Platelet aggregates-induced human cd34 progenitor cell proliferation and differentiation to macrophages and foam cells is mediated by stromal cell derived factor 1 in vitro. Semin Thromb Hemost 2010;36:139-145.
94. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Koppel T, Jahantigh MN, Lutgens E, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009;2:ra81.
95. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: Evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006;20:847-856.
96. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-659.
97. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 2010;285:17442-17452.
98. Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 2011;13:423-433.
99. Stellos K, Sauter R, Fahrleitner M, Grimm J, Stakos D, Emschermann F, Panagiota V, Gnerlich S, Perk A, Schonberger T, et al. Binding of oxidized low-density lipoprotein on circulating platelets is increased in patients with acute coronary syndromes and induces platelet adhesion to vascular wall in vivo - Brief report. Arterioscler Thromb Vasc Biol 2012;32:2017-2020.
100. Daub K, Seizer P, Stellos K, Kramer BF, Bigalke B, Schaller M, Fateh-Moghadam S, Gawaz M, Lindemann S. Oxidized LDL-activated platelets induce vascular inflammation. Semin Thromb Hemost 2010;36:146-156.
101. Alaiti MA, Ishikawa M, Masuda H, Simon DI, Jain MK, Asahara T, Costa MA. Up-regulation of miR-210 by vascular endothelial growth factor in ex vivo expanded CD34 cells enhances cell-mediated angiogenesis. J Cell Mol Med 2012.
102. Hu S, Huang M, Li Z, Jia F, Ghosh Z, Lijkwan MA, Fasanaro P, Sun N, Wang X, Martelli F, et al. MicroRNA-210 as a novel therapy for treatment of ischemic heart disease. Circulation 2010;122:S124-S131.
103. Fasanaro P, D'Alessandra Y, Di Stefano V, Melchionna R, Romani S, Pompilio G, Capogrossi MC, Martelli F. MicroRNA-modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand ephrin-A3. J Biol Chem 2008;283:15878-15883.
104. Parikh VN, Jin RC, Rabello S, Gulbahce N, White K, Hale A, Cottrill KA, Shaik RS, Waxman AB, Zhang YY, et al. MicroRNA-21 integrates pathogenic signaling to control pulmonary hypertension: Results of a network bioinformatics approach. Circulation 2012;125:1520-1532.
105. Guduric-Fuchs J, O'Connor A, Cullen A, Harwood L, Medina RJ, O'Neill CL, Stitt AW, Curtis TM, Simpson DA. Deep sequencing reveals predominant expression of miR-21 amongst the small non-coding RNAs in retinal microvascular endothelial cells. J Cell Biochem 2012;113:2098-2111.
106. Fleissner F, Jazbutyte V, Fiedler J, Gupta SK, Yin X, Xu Q, Galuppo P, Kneitz S, Mayr M, Ertl G, et al. Short communication: Asymmetric dimethylarginine impairs angiogenic progenitor cell function in patients with coronary artery disease through a microRNA-21-dependent mechanism. Circ Res 2010;107:138-143.
107. Gill JG, Langer EM, Lindsley RC, Cai M, Murphy TL, Murphy KM. Snail promotes the cell-autonomous generation of Flk1() endothelial cells through the repression of the microRNA-200 family. Stem Cells Dev 2012;21: 167-176.
108. Li YX, Liu DQ, Zheng C, Zheng SQ, Liu M, Li X, Tang H. miR-200a modulate HUVECs viability and migration. IUBMB Life 2011;63:553-559.
109. Choi YC, Yoon S, Jeong Y, Yoon J, Baek K. Regulation of vascular endothelial growth factor signaling by miR-200b. Mol Cells 2011;32:77-82.
110. McArthur K, Feng B, Wu Y, Chen S, Chakrabarti S. MicroRNA-200b regulates vascular endothelial growth factormediated alterations in diabetic retinopathy. Diabetes 2011;60: 1314-1323.
111. Chan YC, Khanna S, Roy S, Sen CK. miR-200b targets Ets-1 and is down-regulated by hypoxia to induce angiogenic response of endothelial cells. J Biol Chem 2011;286:2047-2056.
112. Stratz C, Nuhrenberg TG, Binder H, Valina CM, Trenk D, Hochholzer W, Neumann FJ, Fiebich BL. Micro-array profiling exhibits remarkable intra-individual stability of human platelet micro-RNA. Thromb Haemost 2012;107:634-641.
113. Kai ZS, Pasquinelli AE. MicroRNA assassins: Factors that regulate the disappearance of miRNAs. Nat Struct Mol Biol 2010;17:5-10.
114. Scholer N, Langer C, Dohner H, Buske C, Kuchenbauer F. Serum microRNAs as a novel class of biomarkers: A comprehensive review of the literature. Exp Hematol 2010;38:1126-1130.
115. Sondermeijer BM, Bakker A, Halliani A, de Ronde MW, Marquart AA, Tijsen AJ, Mulders TA, Kok MG, Battjes S, Maiwald S, et al. Platelets in patients with premature coronary artery disease exhibit upregulation of miRNA340.and miRNA624.. PLoS One 2011;6:e25946.
116. Fichtlscherer S, de Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, Hamm CW, Roxe T, Muller-Ardogan M, et al. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010;107:677-684.
117. Meder B, Keller A, Vogel B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, Just S, Borries A, Rudloff J, Leidinger P, et al. MicroRNA signatures in total peripheral blood as novel biomarkers for acute myocardial infarction. Basic Res Cardiol 2011;106:13-23.
118. Krutzfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, Stoffel M. Silencing of microRNAs in vivo with 'antagomiRs'. Nature 2005;438:685-689.
119. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: Competitive inhibitors of small RNAs in mammalian cells. Nat Methods 2007;4:721-726.
120. Xiao J, Yang B, Lin H, Lu Y, Luo X, Wang Z. Novel approaches for gene-specific interference via manipulating actions of microRNAs: Examination on the pacemaker channel genes HCN2 and HCN4. J Cell Physiol 2007;212:285-292.
121. Obad S, Dos Santos CO, Petri A, Heidenblad M, Broom O, Ruse C, Fu C, Lindow M, Stenvang J, Straarup EM, et al. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet 2011;43:371-378.
122. Condorelli G, Latronico MV, Dorn II GW. MicroRNAs in heart disease: Putative novel therapeutic targets? Eur Heart J 2010;31:649-658.
123. Okamura K, Phillips MD, Tyler DM, Duan H, Chou YT, Lai EC. The regulatory activity of microRNA.species has substantial influence on microRNA and 30 UTR evolution. Nat Struct Mol Biol 2008;15:354-363.
124. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 2009;460:479-486.
125. Iguchi H, Kosaka N, Ochiya T. Versatile applications of microRNA in anti-cancer drug discovery: From therapeutics to biomarkers. Curr Drug Discov Technol 2010;7:95-105.
126. Ambros V. The functions of animal microRNAs. Nature 2004;431:350-355. Platelet microRNAs 589