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Current Vascular Pharmacology

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ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

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General Research Article

Inhibition of miR-223 Expression Using a Sponge Strategy Decreases Restenosis in Rat Injured Carotids

Author(s): Eleonore M’baya-Moutoula, Alexandre Marchand, Isabelle Six, Noura Bahrar, Tanja Celic, Nathalie Mougenot, Pierre Maitrias, Ziad A. Massy, Anne-Marie Lompré, Laurent Metzinger* and Valérie Metzinger-Le Meuth*

Volume 18, Issue 5, 2020

Page: [507 - 516] Pages: 10

DOI: 10.2174/1570161117666190705141152

Price: $65

Abstract

Objective: Restenosis is a frequent complication of angioplasty. It consists of a neointimal hyperplasia resulting from progression and migration of vascular smooth muscle cells (VSMC) into the vessel lumen. microRNA miR-223 has recently been shown to be involved in cardiovascular diseases including atherosclerosis, vascular calcification and arterial thrombosis. In this study, our aim was to assess the impact of miR-223 modulation on restenosis in a rat model of carotid artery after balloon injury.

Methods: The over and down-expression of miR-223 was induced by adenoviral vectors, containing either a pre-miR-223 sequence allowing artificial miR-223 expression or a sponge sequence, trapping the native microRNA, respectively. Restenosis was quantified on stained rat carotid sections.

Results: In vitro, three mRNA (Myocyte Enhancer Factor 2C (MEF2C), Ras homolog gene family, member B (RhoB) and Nuclear factor 1 A-type (NFIA)) reported as miR-223 direct targets and known to be implicated in VSMC differentiation and contractility were studied by RT-qPCR. Our findings showed that down-expression of miR-223 significantly reduced neointimal hyperplasia by 44% in carotids, and was associated with a 2-3-fold overexpression of MEF2C, RhoB and NFIA in a murine monocyte macrophage cell line, RAW 264.7 cells.

Conclusion: Down-regulating miR-223 could be a potential therapeutic approach to prevent restenosis after angioplasty.

Keywords: Restenosis, microRNA, miR-223, rat carotid, vascular smooth muscle cells, angioplasty.

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[1]
Gebert LFR, MacRae IJ. Regulation of microRNA function in animals. Nat Rev Mol Cell Biol 2019; 20(1): 21-37.
[http://dx.doi.org/10.1038/s41580-018-0045-7] [PMID: 30108335]
[2]
Gareri C, De Rosa S, Indolfi C. MicroRNAs for restenosis and thrombosis after vascular injury. Circ Res 2016; 118(7): 1170-84.
[http://dx.doi.org/10.1161/CIRCRESAHA.115.308237] [PMID: 27034278]
[3]
Taibi F, Metzinger-Le Meuth V, Massy ZA, Metzinger L. miR-223: An inflammatory oncomiR enters the cardiovascular field. Biochim Biophys Acta 2014; 1842(7): 1001-9.
[http://dx.doi.org/10.1016/j.bbadis.2014.03.005] [PMID: 24657505]
[4]
Rangrez AY, M’Baya-Moutoula E, Metzinger-Le Meuth V, et al. Inorganic phosphate accelerates the migration of vascular smooth muscle cells: evidence for the involvement of miR-223. PLoS One 2012; 7(10) e47807
[http://dx.doi.org/10.1371/journal.pone.0047807] [PMID: 23094093]
[5]
Taibi F, Metzinger-Le Meuth V, M’Baya-Moutoula E, et al. Possible involvement of microRNAs in vascular damage in experimental chronic kidney disease. Biochim Biophys Acta 2014; 1842(1): 88-98.
[http://dx.doi.org/10.1016/j.bbadis.2013.10.005] [PMID: 24140891]
[6]
Metzinger-Le Meuth V, Fourdinier O, Charnaux N, Massy ZA, Metzinger L. The expanding roles of microRNAs in kidney pathophysiology. Nephrol Dial Transplant 2019; 34(1): 7-15.
[http://dx.doi.org/10.1093/ndt/gfy140] [PMID: 29800482]
[7]
Shi L, Fisslthaler B, Zippel N, et al. MicroRNA-223 antagonizes angiogenesis by targeting β1 integrin and preventing growth factor signaling in endothelial cells. Circ Res 2013; 113(12): 1320-30.
[http://dx.doi.org/10.1161/CIRCRESAHA.113.301824] [PMID: 24044949]
[8]
Elmore JB, Mehanna E, Parikh SA, Zidar DA. restenosis of the coronary arteries: past, present, future directions. Interv Cardiol Clin 2016; 5(3): 281-93.
[PMID: 28582027]
[9]
Tian DY, Jin XR, Zeng X, Wang Y. Notch signaling in endothelial cells: is it the therapeutic target for vascular neointimal hyperplasia? Int J Mol Sci 2017; 18(8)E1615
[http://dx.doi.org/10.3390/ijms18081615] [PMID: 28757591]
[10]
Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362(6423): 801-9.
[http://dx.doi.org/10.1038/362801a0] [PMID: 8479518]
[11]
Thomson DW, Dinger ME. Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet 2016; 17(5): 272-83.
[http://dx.doi.org/10.1038/nrg.2016.20] [PMID: 27040487]
[12]
Luo J, Deng ZL, Luo X, et al. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2007; 2(5): 1236-47.
[http://dx.doi.org/10.1038/nprot.2007.135] [PMID: 17546019]
[13]
Merlet E, Atassi F, Motiani RK, et al. miR-424/322 regulates vascular smooth muscle cell phenotype and neointimal formation in the rat. Cardiovasc Res 2013; 98(3): 458-68.
[http://dx.doi.org/10.1093/cvr/cvt045] [PMID: 23447642]
[14]
M’Baya-Moutoula E, Louvet L, Metzinger-Le Meuth V, Massy ZA, Metzinger L. High inorganic phosphate concentration inhibits osteoclastogenesis by modulating miR-223. Biochim Biophys Acta 2015; 1852(10 Pt A): 2202-12.
[http://dx.doi.org/10.1016/j.bbadis.2015.08.003] [PMID: 26255635]
[15]
Six I, Van Belle E, Bordet R, et al. L-arginine and L-NAME have no effects on the reendothelialization process after arterial balloon injury. Cardiovasc Res 1999; 43(3): 731-8.
[http://dx.doi.org/10.1016/S0008-6363(99)00113-3] [PMID: 10690344]
[16]
Shan Z, Qin S, Li W, et al. An endocrine genetic signal between blood cells and vascular smooth muscle cells: role of MicroRNA-223 in smooth muscle function and atherogenesis. J Am Coll Cardiol 2015; 65(23): 2526-37.
[http://dx.doi.org/10.1016/j.jacc.2015.03.570] [PMID: 26065992]
[17]
Wang H, Wang Q, Kleiman K, Guo C, Eitzman DT. Hematopoietic deficiency of mir-223 attenuates thrombosis in response to photochemical injury in mice. Sci Rep 2017; 7(1): 1606.
[http://dx.doi.org/10.1038/s41598-017-01887-x] [PMID: 28487522]
[18]
Buccheri D, Piraino D, Andolina G, Cortese B. Understanding and managing in-stent restenosis: a review of clinical data, from pathogenesis to treatment. J Thorac Dis 2016; 8(10): E1150-62.
[http://dx.doi.org/10.21037/jtd.2016.10.93] [PMID: 27867580]
[19]
Zhang C. MicroRNAs in vascular biology and vascular disease. J Cardiovasc Transl Res 2010; 3(3): 235-40.
[http://dx.doi.org/10.1007/s12265-010-9164-z] [PMID: 20560045]
[20]
Metzinger-Le Meuth V, Andrianome S, Chillon JM, Bengrine A, Massy ZA, Metzinger L. microRNAs are dysregulated in the cerebral microvasculature of CKD mice. Front Biosci 2014; 6: 80-8.
[http://dx.doi.org/10.2741/E693] [PMID: 24389144]
[21]
Celic T, Metzinger-Le Meuth V, Six I, Massy ZA, Metzinger L. The mir-221/222 cluster is a key player in vascular biology via the fine-tuning of endothelial cell physiology. Curr Vasc Pharmacol 2017; 15(1): 40-6.
[http://dx.doi.org/10.2174/1570161114666160914175149] [PMID: 27633456]
[22]
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(11): 1579-88.
[http://dx.doi.org/10.1161/CIRCRESAHA.106.141986] [PMID: 17478730]
[23]
Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C. A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res 2009; 104(4): 476-87.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.185363] [PMID: 19150885]
[24]
Sun SG, Zheng B, Han M, et al. miR-146a and Krppel-like factor 4 form a feedback loop to participate in vascular smooth muscle cell proliferation. EMBO Rep 2011; 12(1): 56-62.
[http://dx.doi.org/10.1038/embor.2010.172] [PMID: 21109779]
[25]
Pagiatakis C, Gordon JW, Ehyai S, McDermott JC. A novel RhoA/ROCK-CPI-17-MEF2C signaling pathway regulates vascular smooth muscle cell gene expression. J Biol Chem 2012; 287(11): 8361-70.
[http://dx.doi.org/10.1074/jbc.M111.286203] [PMID: 22275376]
[26]
Liu Q, Zhang M, Jiang X, et al. miR-223 suppresses differentiation of tumor-induced CD11b Gr1 myeloid-derived suppressor cells from bone marrow cells. Int J Cancer 2011; 129(11): 2662-73.
[http://dx.doi.org/10.1002/ijc.25921] [PMID: 21213211]
[27]
Johnnidis JB, Harris MH, Wheeler RT, et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451(7182): 1125-9.
[http://dx.doi.org/10.1038/nature06607] [PMID: 18278031]
[28]
Sun G, Li H, Rossi JJ. Sequence context outside the target region influences the effectiveness of miR-223 target sites in the RhoB 3'UTR. Nucleic Acids Res 2010; 38(1): 239-52.
[http://dx.doi.org/10.1093/nar/gkp870] [PMID: 19850724]
[29]
Wojciak-Stothard B, Zhao L, Oliver E, et al. Role of RhoB in the regulation of pulmonary endothelial and smooth muscle cell responses to hypoxia. Circ Res 2012; 110(11): 1423-34.
[http://dx.doi.org/10.1161/CIRCRESAHA.112.264473] [PMID: 22539766]
[30]
Jin C, Zhao Y, Yu L, Xu S, Fu G. MicroRNA-21 mediates the rapamycin-induced suppression of endothelial proliferation and migration. FEBS Lett 2013; 587(4): 378-85.
[http://dx.doi.org/10.1016/j.febslet.2012.12.021] [PMID: 23313253]
[31]
Metzinger-Le Meuth V, Burtey S, Maitrias P, Massy ZA, Metzinger L. microRNAs in the pathophysiology of CKD-MBD: Biomarkers and innovative drugs. Biochim Biophys Acta Mol Basis Dis 2017; 1863(1): 337-45.
[http://dx.doi.org/10.1016/j.bbadis.2016.10.027] [PMID: 27806914]
[32]
Yang J, Zeng P, Yang J, et al. MicroRNA-24 regulates vascular remodeling via inhibiting PDGF-BB pathway in diabetic rat model. Gene 2018; 659: 67-76.
[http://dx.doi.org/10.1016/j.gene.2018.03.056] [PMID: 29559348]

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