Down-regulation ofmiR-23b induces phenotypic switching of vascular smoothmuscle cells in vitro and in vivo

Cardiovascular Research

Volumn 107, Issue 4, 2015, Pages 522-533

  Iaconetti, Claudio ^a   De Rosa, Salvatore ^a   Polimeni, Alberto ^a   Sorrentino, Sabato ^a   Gareri, Clarice ^a   Carino, Annarita ^a   Sabatino, Jolanda ^a   Colangelo, Maria ^a   Curcio, Antonio ^a   Indolfi, Ciro ^a  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

Author keywords

FoxO4; MicroRNAs; Phenotypic switch; Restenosis; Vascular smooth muscle cells

Indexed keywords

ALPHA ACTIN; GELATINASE B; MICRORNA; MICRORNA 23B; MYOSIN HEAVY CHAIN; MYOSIN HEAVY CHAIN 11; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP4; UNCLASSIFIED DRUG; UROKINASE; MIRN23 MICRORNA, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTERY WALL; ARTICLE; BLOOD VESSEL INJURY; CAROTID ARTERY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GENE OVEREXPRESSION; GENE SWITCHING; GENETIC TRANSFECTION; HYPERPLASIA; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; PHENOTYPE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; VASCULAR SMOOTH MUSCLE CELL; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; GENETICS; METABOLISM; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DOWN-REGULATION; MICRORNAS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; RATS;

EID: 84948129366     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv141     Document Type: Article

References (56)

1. Alexander MR, Owens GK. Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol 2012;74: 13-40.
2. Regan CP, Adam PJ, Madsen CS, Owens GK. Molecular mechanisms of decreased smooth muscle differentiation marker expression after vascular injury. J Clin Invest 2000;106:1139-1147.
3. 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.
4. Gomez D, Owens GK. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc Res 2012;95:156-164.
5. Indolfi C, Torella D, Coppola C, Curcio A, Rodriguez F, Bilancio A, Leccia A, Arcucci O, Falco M, Leosco D, Chiariello M. 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.
6. Indolfi C, Avvedimento EV, Di Lorenzo E, Esposito G, Rapacciuolo A, Giuliano P, Grieco D, Cavuto L, Stingone AM, Ciullo I, Condorelli G, Chiariello M. Activation of cAMP-PKA signaling in vivo inhibits smooth muscle cell proliferation induced by vascular injury. Nat Med 1997;3:775-779.
7. Indolfi C, Avvedimento EV, Rapacciuolo A, Di Lorenzo E, Esposito G, Stabile E, Feliciello A, Mele E, Giuliano P, Condorelli G, Chiariello M. Inhibition of cellular ras prevents smooth muscle cell proliferation after vascular injury in vivo. Nat Med 1995;1: 541-545.
8. Polimeni A, De Rosa S, Indolfi C. Vascular miRNAs after balloon angioplasty. Trends Cardiovasc Med 2013;23:9-14.
9. Curcio A, Torella D, Indolfi C. Mechanisms of smooth muscle cell proliferation and endothelial regeneration after vascular injury and stenting: approach to therapy. Circ J 2011;75:1287-1296.
10. De Rosa S, Curcio A, Indolfi C. Emerging role of microRNAs in cardiovascular diseases. Circ J 2014;78:567-575.
11. LatronicoMV, Catalucci D, Condorelli G.Emerging role of microRNAs in cardiovascular biology. Circ Res 2007;101:1225-1236.
12. De Rosa S, Fichtlscherer S, Lehmann R, Assmus B, Dimmeler S, Zeiher AM. Transcoronary concentration gradients of circulating microRNAs. Circulation 2011;124:1936-1944.
13. Fichtlscherer S, De Rosa S, Fox H, Schwietz T, Fischer A, Liebetrau C, Weber M, HammCW, RoxeT, Muller-Ardogan M, Bonauer A, Zeiher AM, Dimmeler S. Circulating microRNAs in patients with coronary artery disease. Circ Res 2010;107:677-684.
14. Kumarswamy R, Thum T. Non-coding RNAs in cardiac remodeling and heart failure. Circ Res 2013;113:676-689.
15. 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.
16. van Rooij E. The art of microRNA research. Circ Res 2011;108:219-234.
17. Li P, Zhu N, Yi B, Wang N, Chen M, You X, Zhao X, Solomides CC, Qin Y, Sun J. MicroRNA-663 regulates human vascular smooth muscle cell phenotypic switch and vascular neointimal formation. Circ Res 2013;113:1117-1127.
18. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009;460:705-710.
19. Torella D, Iaconetti C, Catalucci D, Ellison GM, Leone A, Waring CD, Bochicchio A, Vicinanza C, Aquila I, Curcio A, Condorelli G, Indolfi C. MicroRNA-133 controls vascular smooth muscle cell phenotypic switch in vitro and vascular remodeling in vivo. Circ Res 2011;109:880-893.
20. Iaconetti C, Polimeni A, Sorrentino S, Sabatino J, Pironti G, Esposito G, Curcio A, Indolfi C. 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.
21. Cheng Y, Liu X, Yang J, Lin Y, Xu DZ, Lu Q, Deitch EA, Huo Y, Delphin ES, Zhang C. MicroRNA-145, a novelsmooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res 2009;105:158-166.
22. Wang YS, Wang HY, Liao YC, Tsai PC, Chen KC, Cheng HY, Lin RT, Juo SH. MicroRNA-195 regulates vascular smooth muscle cell phenotype and prevents neointimal formation. Cardiovasc Res 2012;95:517-526.
23. Bang C, Fiedler J, Thum T. Cardiovascular importance of the microRNA-23/27/24 family. Microcirculation 2012;19:208-214.
24. Zhou Q, Gallagher R, Ufret-Vincenty R, Li X, Olson EN, Wang S. Regulation of angiogenesis and choroidal neovascularization by members of microRNA-23-27-24 clusters. Proc Natl Acad Sci 2011;108:8287-8292.
25. Torella D, Ellison GM, Torella M, Vicinanza C, Aquila I, Iaconetti C, Scalise M, Marino F, Henning BJ, Lewis FC, Gareri C, Lascar N, Cuda G, Salvatore T, Nappi G, Indolfi C, Torella R, Cozzolino D, Sasso FC. Carbonic anhydrase activation is associated with worsened pathological remodeling in human ischemic diabetic cardiomyopathy.. J Am Heart Assoc 2014;3:e000434.
26. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G. MicroRNAs modulate the angiogenic properties of HUVECs. Blood 2006;108:3068-3071.
27. Zhang H, Hao Y, Yang J, Zhou Y, Li J, Yin S, Sun C, Ma M, Huang Y, Xi JJ. Genome-wide functional screening of miR-23b as a pleiotropic modulator suppressing cancer metastasis. Nat Commun 2011;2:554.
28. Pellegrino L, Stebbing J, Braga VM, Frampton AE, Jacob J, Buluwela L, Jiao LR, Periyasamy M, Madsen CD, Caley MP, Ottaviani S, Roca-Alonso L, El-Bahrawy M, Coombes RC, Krell J, Castellano L. miR-23b regulates cytoskeletal remodeling, motility and metastasis by directly targeting multiple transcripts. Nucleic Acids Res 2013;41: 5400-5412.
29. Ham O, Song BW, Lee SY, Choi E, Cha MJ, Lee CY, Park JH, Kim IK, Chang W, Lim S, Lee CH, Kim S, Jang Y, Hwang KC. The role of microRNA-23b in the differentiation of MSC into chondrocyte by targeting protein kinase A signaling. Biomaterials 2012;33: 4500-4507.
30. 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.
31. Wamhoff BR, Hoofnagle MH, Burns A, Sinha S, McDonald OG, Owens GK. A G/C element mediates repression of the SM22alpha promoter within phenotypically modulated smooth muscle cells in experimental atherosclerosis. Circ Res 2004;95:981-988.
32. Indolfi C, Torella D, Cavuto L, Davalli AM, Coppola C, Esposito G, Carriero MV, Rapacciuolo A, Di Lorenzo E, Stabile E, Perrino C, Chieffo A, Pardo F, Chiariello M. Effects of balloon injury on neointimal hyperplasia in streptozotocin-induced diabetes and in hyperinsulinemic nondiabetic pancreatic islet-Transplanted rats. Circulation 2001; 103:2980-2986.
33. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009;136: 215-233.
34. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-Transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008;9:102-114.
35. Menshikov M, Plekhanova O, Cai H, Chalupsky K, Parfyonova Y, Bashtrikov P, TkachukV, Berk BC. Urokinase plasminogen activator stimulates vascular smooth muscle cell proliferation via redox-dependent pathways. Arterioscler Thromb Vasc Biol 2006;26:801-807.
36. Kiyan Y, Limbourg A, Kiyan R, Tkachuk S, Limbourg FP, Ovsianikov A, Chichkov BN, Haller H, Dumler I. Urokinase receptor associates with myocardin to control vascular smooth muscle cells phenotype in vascular disease. Arterioscler Thromb Vasc Biol 2012; 32:110-122.
37. Tsai S, Hollenbeck ST, Ryer EJ, Edlin R, Yamanouchi D, Kundi R, Wang C, Liu B, Kent KC. TGF-beta through Smad3 signaling stimulates vascular smooth muscle cell proliferation and neointimal formation. Am J Physiol Heart Circ Physiol 2009;297:H540-H549.
38. Suwanabo PA, Kent KC, Liu B. TGF-b and restenosis revisited: a Smad link. J Surg Res 2011;167:287-297.
39. Li H, Liang J, Castrillon DH, DePinho RA, Olson EN, Liu ZP. FoxO4 regulates tumor necrosis factor alpha-directed smooth muscle cell migration by activating matrix metalloproteinase 9 gene transcription. Mol Cell Biol 2007;27:2676-2686.
40. Moon SK, Cha BY, Kim CH. ERK1/2 mediates TNF-Alpha-induced matrix metalloproteinase-9 expression in human vascular smooth muscle cells via the regulation of NF-kappaB and AP-1: involvement of the ras dependent pathway. J Cell Physiol 2004;198:417-427.
41. Rastogi S, Rizwani W, Joshi B, Kunigal S, Chellappan SP. TNF-A response of vascular endothelial and vascular smooth muscle cells involve differential utilization of ASK1 kinase and p73. Cell Death Differ 2012;19:274-283.
42. Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB. The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 2012;95: 194-204.
43. Merlet E, Atassi F, Motiani RK, Mougenot N, Jacquet A, Nadaud S, Capiod T, Trebak M, Lompre AM, Marchand A. miR-424/322 regulates vascular smooth muscle cell phenotype and neointimal formation in the rat. Cardiovasc Res 2013;98:458-468.
44. Zampetaki A, Mayr M. MicroRNAs in vascular and metabolic disease. Circ Res 2012;110: 508-522.
45. Majid S, Dar AA, Saini S, Deng G, Chang I, Greene K, Tanaka Y, Dahiya R, Yamamura S. MicroRNA-23b functions as a tumor suppressor by regulating Zeb1 in bladder cancer. PLoS ONE 2013;8:e67686.
46. Majid S, Dar AA, Saini S, Arora S, ShahryariV, Zaman MS, Chang I, Yamamura S, TanakaY, Deng G, Dahiya R. miR-23b represses proto-oncogene Src kinase and functions as methylation-silenced tumor suppressor with diagnostic and prognostic significance in prostate cancer. Cancer Res 2012;72:6435-6446.
47. Zhu S, Pan W, Song X, Liu Y, Shao X, Tang Y, Liang D, He D, Wang H, Liu W, Shi Y, Harley JB, Shen N, Qian Y. The microRNA miR-23b suppresses IL-17-Associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-A. Nat Med 2012;18: 1077-1086.
48. Plekhanova OS, Parfyonova YV, Bibilashvily R, Stepanova VV, Erne P, Bobik A, Tkachuk VA. Urokinase plasminogen activator enhances neointima growth and reduces lumen size in injured carotid arteries. J Hypertens 2000;18:1065-1069.
49. ClowesAW, Clowes MM, Au YPT, Reidy MA, Belin D. Smooth muscle cells express urokinase during mitogenesis and tissue-Type plasminogen activator during migration in injured rat carotid artery. Circ Res 1990;67:61-67.
50. Parfyonova Y, Plekhanova O, Solomatina M, Naumov V, Bobik A, Berk B, Tkachuk V. Contrasting effects of urokinase and tissue-Type plasminogen activators on neointima formation and vessel remodeling after arterial injury. J Vasc Res 2004;41:268-276.
51. Kundi R, Hollenbeck ST, Yamanouchi D, Herman BC, Edlin R, Ryer EJ, Wang C, Tsai S, Liu B, Kent KC. Arterial gene transfer of the TGF-b signaling protein Smad3 induces adaptive remodelling following angioplasty: a role for CTGF. Cardiovasc Res 2009;84: 326-335.
52. Liu ZP, Wang Z, Yanagisawa H, Olson EN. Phenotypic modulation of smooth muscle cells through interaction of FoxO4 and myocardin. Dev Cell 2005;9:261-270.
53. Ding M, Xie Y, Wagner RJ, Jin Y, Carrao AC, Liu LS, Guzman AK, Powell RJ, Hwa J, Rzucidlo EM, Martin KA. Adiponectin induces vascular smooth muscle cell differentiation via repression ofmammalian target of rapamycin complex 1 and FoxO4. Arterioscler Thromb Vasc Biol 2011;31:1403-1410.
54. Yang X, Gong Y, Tang Y, Li H, He Q, Gower L, Liaw L, Friesel RE. Spry1 and Spry4 differentially regulate human aortic smooth muscle cell phenotype via Akt/FoxO/myocardin signaling. PLoS ONE 2013;8:e58746.
55. Talasila A, Yu H, Ackers-Johnson M, Bot M, van BerkelT, Bennett MR, Bot I, Sinha S. Myocardin regulates vascular response to injury through miR-24/-29a and platelet-derived growth factor receptor-b. Arterioscler Thromb Vasc Biol 2013;33:2355-2365.
56. Maegdefessel L, Spin JM, Raaz U, Eken SM, Toh R, Azuma J, Adam M, Nagakami F, Heymann HM, Chernugobova E, Jin H, Roy J, Hultgren R, Caidahl Kenneth, Schrepfer S, Hamsten A, Eriksson P, McConnell MV, Dalman RL, Tsao Philip S. miR-24 limits aortic vascular inflammation and murine abdominal aneurysm development. Nat Commun 2014;5; doi: 10.1038/ncomms6214.