Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury

Basic Research in Cardiology

Volumn 107, Issue 5, 2012, Pages

  Iaconetti, Claudio ^a   Polimeni, Alberto ^a   Sorrentino, Sabato ^a   Sabatino, Jolanda ^a   Pironti, Gianluigi ^b   Esposito, Giovanni ^b   Curcio, Antonio ^a   Indolfi, Ciro ^a  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Endothelial cells; MicroRNAs; Re endothelialization restenosis; Vascular smooth muscle cells

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; KRUPPEL LIKE FACTOR 4; MICRORNA; MICRORNA 92A; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; KRUPPEL LIKE FACTOR; MAP2K4 PROTEIN, HUMAN; MIRN92 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY INTIMA PROLIFERATION; ARTICLE; CAROTID ARTERY INJURY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VITRO STUDY; IN VIVO STUDY; KLF4 GENE; LOSS OF FUNCTION MUTATION; MKK4 GENE; NEOINTIMA; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RESTENOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STENT; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; ANIMAL; BIOSYNTHESIS; BLOOD VESSEL INJURY; CELL CULTURE; CELL MOTION; CYTOLOGY; DRUG ANTAGONISM; GENETICS; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MALE; MAP KINASE KINASE 4; MICRORNAS; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; NITRIC OXIDE; RATS; RATS, WISTAR; VASCULAR SYSTEM INJURIES; VON WILLEBRAND FACTOR;

EID: 84864827128     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0296-y     Document Type: Article

References (47)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431:350-355. doi:10.1038/nature02871
2. Baker M, Robinson SD, Lechertier T, Barber PR, Tavora B, D'Amico G, Jones DT, Vojnovic B, Hodivala-Dilke K (2011) Use of the mouse aortic ring assay to study angiogenesis. Nat Protoc 22(7):89-104. doi:10.1038/nprot.2011.435
3. Bartel DP (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116:281-297. doi:10.1016/S0092-8674 (04)00045-5
4. Bavry AA, Kumbhani DJ, Helton TJ, Bhatt DL (2005) Risk of thrombosis with the use of sirolimus-eluting stents for percutaneous coronary intervention (from registry and clinical trial data). Am J Cardiol 95:1469-1472. doi:10.1016/j.amjcard.2005.02.015
5. Bonauer A, Carmona G, Iwasaki M, Mione M, Koyanagi M, Fischer A, Burchfield J, Fox H, Doebele C, Ohtani K, Chavakis E, Potente M, Tjwa M, Urbich C, Zeiher AM, Dimmeler S (2009) MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science 324:1710-1713. doi:10.1126/ science.1174381
6. Camenzind E, Steg PG, Wijns W (2007) Stent thrombosis late after implantation of first-generation drug-eluting stents: A cause for concern. Circulation 115:1440-1455. doi:10.1161/CIRCULATIONAHA. 106.666800
7. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 19(473):298-307. doi: 10.1038/nature10144
8. Chai J, Jones MK, Tarnawski AS (2004) Serum response factor is a critical requirement for VEGF signaling in endothelial cells and VEGF-induced angiogenesis. FASEB J 18:1264-1266. doi: 10.1096/fj.03-1232fje
9. Cowan CE, Kohler EE, Dugan TA, Mirza MK, Malik AB, Wary KK (2010) Kruppel-like factor-4 transcriptionally regulates VE-cadherin expression and endothelial barrier function. Circ Res 107:959-966. doi:10.1161/CIRCRESAHA.110. 219592
10. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A (2006) Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 38:1060-1065. doi: 10.1038/ng1855
11. Drexler H (1999) Nitric oxide and coronary endothelial dysfunction in humans. Cardiovasc Res 43:572-579. doi:10.1016/ S0008-6363(99)00152-2
12. Fleming Y, Armstrong CG, Morrice N, Paterson A, Goedert M, Cohen P (2000) Synergistic activation of stress-activated protein kinase 1/c-Jun N-terminal kinase (SAPK1/JNK) isoforms by mitogen-activated protein kinase kinase 4 (MKK4) and MKK7. Biochem J 352:145-154
13. Forough R, Koyama N, Hasenstab D, Lea H, Clowes M, Nikkari ST, Clowes AW (1996) Overexpression of tissue inhibitor of matrix metalloproteinase-1 inhibits vascular smooth muscle cell functions in vitro and in vivo. Circ Res 79:812-820. doi:10.1161/ 01.RES.79.4.812
14. Friedrich EB, Werner C, Walenta K, Bohm M, Scheller B (2009) Role of extracellular signal-regulated kinase for endothelial progenitor cell dysfunction in coronary artery disease. Basic Res Cardiol 104:613-620. doi:10.1007/s00395-009-0022-6
15. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK (2007) Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem 282: 13769-13779. doi:10.1074/jbc. M700078200
16. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM (2005) A microRNA polycistron as a potential human oncogene. Nature 435:828-833. doi:10.1038/nature03552
17. Hoffmann R, Mintz GS, Mehran R, Pichard AD, Kent KM, Satler LF, Popma JJ, Wu H, Leon MB (1998) Intravascular ultrasound predictors of angiographic restenosis in lesions treated with Palmaz-Schatz stents. J Am Coll Cardiol 31:43-49. doi:10.1016/ S0002-9149(99)00769-9
18. Indolfi C, Avvedimento VE, Di Lorenzo E, Esposito G, Rapacciuolo A, Giuliano P, Grieco D, Cavuto L, Stingone AM, Ciullo I, Condorelli G, Chiariello M (1997) Activation of cAMP-PKA signaling in vivo inhibits smooth muscle cell proliferation induced by vascular injury. Nat Med 3:775-779. doi:10.1038/nm0797-775
19. Indolfi C, Avvedimento EV, Rapacciuolo A, Di Lorenzo E, Esposito G, Stabile E, Feliciello A, Mele E, Giuliano P, Condorelli G (1995) Inhibition of cellular Ras prevents smooth muscle cell proliferation after vascular injury in vivo. Nat Med 1:541-545. doi:10.1038/nm0695-541
20. Indolfi C, Avvedimento EV, Rapacciuolo A, Esposito G, Di Lorenzo E, Leccia A, Pisani A, Chieffo A, Coppola A, Chiariello M (1997) In vivo gene transfer: Prevention of neointima formation by inhibition of mitogen-activated protein kinase kinase. Basic Res Cardiol 92:378-384. doi:10.1007/BF00796211
21. Indolfi C, Di Lorenzo E, Rapacciuolo A, Stingone AM, Stabile E, Leccia A, Torella D, Caputo R, Ciardiello F, Tortora G, Chiariello M (2000) 8-chloro-cAMP inhibits smooth muscle cell proliferation in vitro and neointima formation induced by balloon injury in vivo. J Am Coll Cardiol 36:288-293. doi:10.1016/ S0735-1097(00)00679-3
22. Indolfi C, Esposito G, Di Lorenzo E, Rapacciuolo A, Feliciello A, Porcellini A, Avvedimento VE, Condorelli M, Chiariello M (1995) Smooth muscle cell proliferation is proportional to the degree of balloon injury in a rat model of angioplasty. Circulation 92:1230-1235. doi:10.1161/01.CIR.92.5.1230
23. Indolfi C, Esposito G, Stabile E, Cavuto L, Pisani A, Coppola C, Torella D, Perrino C, Di Lorenzo E, Curcio A, Palombini L, Chiariello M (2000) A new rat model of small vessel stenting. Basic Res Cardiol 95:179-185. doi:10.1007/s003950050180
24. Indolfi C, Gasparri C, Vicinanza C, De Serio D, Boncompagni D, Mongiardo A, Spaccarotella C, Agosti V, Torella D, Curcio A (2011) Mitogen-activated protein kinases activation in T lymphocytes of patients with acute coronary syndromes. Basic Res Cardiol 106:667-679. doi:10.1007/s00395-011-0172-1
25. Indolfi C, Pavia M, Angelillo IF (2005) Drug-eluting stents versus bare metal stents in percutaneous coronary interventions (a meta-analysis). Am J Cardiol 95:1146-1152. doi:10.1016/ j.amjcard.2005.01.040
26. Indolfi C, Torella D, Coppola C, Curcio A, Rodriguez F, Bilancio A, Leccia A, Arcucci O, Falco M, Leosco D, Chiariello M (2002) Physical training increases eNOS vascular expression and activity and reduces restenosis after balloon angioplasty or arterial stenting in rats. Circ Res 91:1190-1197. doi:10.1161/01.RES. 0000046233.94299.D6
27. Kleinbongard P, Heusch G, Schulz R (2010) TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther 127:295-314. http://dx.doi.org/10.1016/ j.pharmthera.2010.05.002
28. Liang CC, Park AY, Guan JL (2007) In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2:329-333. doi:10.1038/nprot.2007.30
29. Liu MW, Roubin GS, King SB (1989) Restenosis after coronary angioplasty. Potential biologic determinants and role of intimal hyperplasia. Circulation 79:1374-1387. doi:10.1161/01.CIR.79.6. 1374
30. Lorenzen JM, Martino F, Thum T (2012) Epigenetic modifications in cardiovascular disease. Basic Res Cardiol 107:245. doi:10.1007/s00395-012-0245-9
31. Marx SO, Totary-Jain H, Marks AR (2011) Vascular smooth muscle cell proliferation in restenosis. Circ Cardiovasc Interv 4:104-111. doi:10.1161/CIRCINTERVENTIONS.110.957332
32. Meder B, Keller A, Vogel B, Haas J, Sedaghat-Hamedani F, Kayvanpour E, Just S, Borries A, Rudloff J, Leidinger P, Meese E,Katus HA, Rottbauer W (2011) MicroRNA signatures in total peripheral blood as novel biomarkers for acutemyocardial infarction.Basic Res Cardiol 106:13-23. doi:10.1007/s00395-010- 0123-2
33. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H (2009) Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 297:1535-1543. doi:10.1152/ajpheart.00510.2009
34. Oppermann M, Suvorava T, Freudenberger T, Dao VT, Fischer JW, Weber M, Kojda G (2011) Regulation of vascular guanylyl cyclase by endothelial nitric oxide-dependent posttranslational modification. Basic Res Cardiol 106:539-549. doi:10.1007/s00395-011-0160-5
35. Ohtani K, Dimmeler S (2011) Control of cardiovascular differentiation by microRNAs. Basic Res Cardiol 106:5-11. doi: 10.1007/s00395-010-0139-7
36. Qi YX, Jiang J, Jiang XH, Wang XD, Ji SY, Han Y, Long DK, Shen BR, Yan ZQ, Chien S, Jiang ZL (2011) PDGF-BB and TGF-{beta}1 on cross-talk between endothelial and smooth muscle cells in vascular remodeling induced by low shear stress. Proc Natl Acad Sci USA 108:1908-1913. doi:10.1073/pnas. 1019219108
37. Rajewsky N (2006) MicroRNA target predictions in animals. Nat Genet 38:S8-S13. doi:10.1038/ng1798
38. Ross R (1993) The pathogenesis of atherosclerosis: A perspective for the 1990 s. Nature 362:801-809. doi:10.1038/362801a0
39. Salameh A, Galvagni F, Bardelli M, Bussolino F, Oliviero S (2005) Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of Endothelial cells through the activation of ERK, AKT, and JNK pathways. Blood 106:3423-3431. doi:10.1182/blood-2005-04-1388
40. Sivritas D, Becher MU, Ebrahimian T, Arfa O, Rapp S, Bohner A, Mueller CF, Umemura T, Wassmann S, Nickenig G, Wassmann K (2011) Antiproliferative effect of estrogen in vascular smooth muscle cells is mediated by Kruppel-like factor-4 and manganese superoxide dismutase. Basic Res Cardiol 106:563-575. doi:10.1007/s00395-011-0174-z
41. Small EM, Olson EN (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469:336-342. doi:10.1038/nature 09783
42. Suehiro J, Hamakubo T, Kodama T, Aird WC, Minami T (2010) Vascular endothelial growth factor activation of endothelial cells is mediated by early growth response-3. Blood 115:2520-2532. doi:10.1182/blood-2009-07-233478
43. Torella D, Iaconetti C, Catalucci D, Ellison GM, Leone A, Waring CD, Bochicchio A, Vicinanza C, Aquila I, Curcio A, Condorelli G, Indolfi C (2011) MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ Res 109:880-893. doi:10.1161/CIRCRESAHA.111. 240150
44. Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, Tietz AB, Kirchmair R, Silver M, Curry C, Wecker A, Yoon YS, Heidenreich R, Hanley A, Kearney M, Tio FO, Kuenzler P, Isner JM, Losordo DW (2004) Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: An alternative strategy for inhibition of restenosis. Circulation 110:36-45. doi:10.1161/ 01.CIR.0000133324.38115.0A
45. Wu W, Xiao H, Laguna-Fernandez A, Villarreal G Jr, Wang KC, Geary GG, Zhang Y, Wang WC, Huang HD, Zhou J, Li YS, Chien S, Garcia-Cardena G, Shyy JY (2011) Flow-dependent regulation of Kruppel-like factor 2 ismediated byMicroRNA-92a. Circulation 124:633-641. doi:10.1161/CIRCULATIONAHA.110.005108
46. Zhang W, Liu HT (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res 12:9-18. doi:10.1038/sj.cr.7290105
47. Zhang C, Wu J, Xu X, Potter BJ, Gao X (2010) Direct relationship between levels of TNF-alpha expression and endothelial dysfunction in reperfusion injury. Basic Res Cardiol 105:453-464. doi:10.1007/s00395-010-0083-6