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      Reducing In-Stent Restenosis : Therapeutic Manipulation of miRNA in Vascular Remodeling and Inflammation

      research-article
      Author(s): , PhD ∗ , , MBChB ∗ , , PhD ∗ , , PhD ∗ , , PhD ∗ , , PhD ∗ , , PhD ∗ , , PhD ∗ , , PhD ∗ , , MBChB ∗ , , PhD † , , MD † , , MD ‡ , , PhD ∗ , ∗
      Publication date PMC-release:
      Journal: Journal of the American College of Cardiology
      Publisher: Elsevier Biomedical
      Keywords: late stent thrombosis, miRNA stem loop, neointima, smooth muscle cell, BMDM, bone marrow–derived macrophages, BMS, bare-metal stent(s), CD, cluster of differentiation, DES, drug-eluting stent(s), IL, interleukin, ISR, in-stent restenosis, KO, knockout, LPS, lipopolysaccharide, miRNA, micro–ribonucleic acid, PDCD4, programmed cell death protein 4, PDGF, platelet-derived growth factor, PPAR, peroxisome proliferator–activated receptor, RNA, ribonucleic acid, SMC, smooth muscle cell, WT, wild-type

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          Abstract

          Background

          Drug-eluting stents reduce the incidence of in-stent restenosis, but they result in delayed arterial healing and are associated with a chronic inflammatory response and hypersensitivity reactions. Identifying novel interventions to enhance wound healing and reduce the inflammatory response may improve long-term clinical outcomes. Micro–ribonucleic acids (miRNAs) are noncoding small ribonucleic acids that play a prominent role in the initiation and resolution of inflammation after vascular injury.

          Objectives

          This study sought to identify miRNA regulation and function after implantation of bare-metal and drug-eluting stents.

          Methods

          Pig, mouse, and in vitro models were used to investigate the role of miRNA in in-stent restenosis.

          Results

          We documented a subset of inflammatory miRNAs activated after stenting in pigs, including the miR-21 stem loop miRNAs. Genetic ablation of the miR-21 stem loop attenuated neointimal formation in mice post-stenting. This occurred via enhanced levels of anti-inflammatory M2 macrophages coupled with an impaired sensitivity of smooth muscle cells to respond to vascular activation.

          Conclusions

          MiR-21 plays a prominent role in promoting vascular inflammation and remodeling after stent injury. MiRNA-mediated modulation of the inflammatory response post-stenting may have therapeutic potential to accelerate wound healing and enhance the clinical efficacy of stenting.

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          Most cited references25

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          PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines.

          C. Jiang, A. Ting, B. Seed (1998)
          The peroxisome proliferator-activated receptor-gamma (PPAR-gamma) is a member of the nuclear receptor family of transcription factors, a large and diverse group of proteins that mediate ligand-dependent transcriptional activation and repression. Expression of PPAR-gamma is an early and pivotal event in the differentiation of adipocytes. Several agents that promote differentiation of fibroblast lines into adipocytes have been shown to be PPAR-gamma agonists, including several prostanoids, of which 15-deoxy-delta-prostaglandin J2 is the most potent, as well as members of a new class of oral antidiabetic agents, the thiazolidinediones, and a variety of non-steroidal anti-inflammatory drugs (NSAIDs). Here we show that PPAR-gamma agonists suppress monocyte elaboration of inflammatory cytokines at agonist concentrations similar to those found to be effective for the promotion of adipogenesis. Inhibition of cytokine production may help to explain the incremental therapeutic benefit of NSAIDs observed in the treatment of rheumatoid arthritis at plasma drug concentrations substantially higher than are required to inhibit prostaglandin G/H synthase (cyclooxygenase).
          Article 0 comments Cited 428 times – based on 0 reviews     Review now
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            A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent Study Group.

            Patrick W. Serruys, Peter P.T.h. de Jaegere, Ferdinand Kiemeneij … (1994)
            Balloon-expandable coronary-artery stents were developed to prevent coronary restenosis after coronary angioplasty. These devices hold coronary vessels open at sites that have been dilated. However, it is unknown whether stenting improves long-term angiographic and clinical outcomes as compared with standard balloon angioplasty. A total of 520 patients with stable angina and a single coronary-artery lesion were randomly assigned to either stent implantation (262 patients) or standard balloon angioplasty (258 patients). The primary clinical end points were death, the occurrence of a cerebrovascular accident, myocardial infarction, the need for coronary-artery bypass surgery, or a second percutaneous intervention involving the previously treated lesion, either at the time of the initial procedure or during the subsequent seven months. The primary angiographic end point was the minimal luminal diameter at follow-up, as determined by quantitative coronary angiography. After exclusions, 52 patients in the stent group (20 percent) and 76 patients in the angioplasty group (30 percent) reached a primary clinical end point (relative risk, 0.68; 95 percent confidence interval, 0.50 to 0.92; P = 0.02). The difference in clinical-event rates was explained mainly by a reduced need for a second coronary angioplasty in the stent group (relative risk, 0.58; 95 percent confidence interval, 0.40 to 0.85; P = 0.005). The mean (+/- SD) minimal luminal diameters immediately after the procedure were 2.48 +/- 0.39 mm in the stent group and 2.05 +/- 0.33 mm in the angioplasty group; at follow-up, the diameters were 1.82 +/- 0.64 mm in the stent group and 1.73 +/- 0.55 mm in the angioplasty group (P = 0.09), which correspond to rates of restenosis (diameter of stenosis, > or = 50 percent) of 22 and 32 percent, respectively (P = 0.02). Peripheral vascular complications necessitating surgery, blood transfusion, or both were more frequent after stenting than after balloon angioplasty (13.5 vs. 3.1 percent, P < 0.001). The mean hospital stay was significantly longer in the stent group than in the angioplasty group (8.5 vs. 3.1 days, P < 0.001). Over seven months of follow-up, the clinical and angiographic outcomes were better in patients who received a stent than in those who received standard coronary angioplasty. However, this benefit was achieved at the cost of a significantly higher risk of vascular complications at the access site and a longer hospital stay.
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              MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation.

              Ruirui Ji, Yunhui Cheng, Junming Yue … (2007)
              MicroRNAs (miRNAs) are a recently discovered class of endogenous, small, noncoding RNAs that regulate about 30% of the encoding genes of the human genome. However, the role of miRNAs in vascular disease is currently completely unknown. Using microarray analysis, we demonstrated for the first time that miRNAs are aberrantly expressed in the vascular walls after balloon injury. The aberrantly expressed miRNAs were further confirmed by Northern blot and quantitative real-time polymerase chain reaction. Modulating an aberrantly overexpressed miRNA, miR-21, via antisense-mediated depletion (knock-down) had a significant negative effect on neointimal lesion formation. In vitro, the expression level of miR-21 in dedifferentiated vascular smooth muscle cells was significantly higher than that in fresh isolated differentiated cells. Depletion of miR-21 resulted in decreased cell proliferation and increased cell apoptosis in a dose-dependent manner. MiR-21-mediated cellular effects were further confirmed in vivo in balloon-injured rat carotid arteries. Western blot analysis demonstrated that PTEN and Bcl-2 were involved in miR-21-mediated cellular effects. The results suggest that miRNAs are novel regulatory RNAs for neointimal lesion formation. MiRNAs may be a new therapeutic target for proliferative vascular diseases such as atherosclerosis, postangioplasty restenosis, transplantation arteriopathy, and stroke.
              Article 0 comments Cited 262 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Andrew H. Baker
                Journal
                Journal ID (nlm-ta): J Am Coll Cardiol
                Journal ID (iso-abbrev): J. Am. Coll. Cardiol
                Title: Journal of the American College of Cardiology
                Publisher: Elsevier Biomedical
                ISSN (Print): 0735-1097
                ISSN (Electronic): 1558-3597
                Publication date PMC-release: 02 June 2015
                Publication date (Print): 02 June 2015
                Volume: 65
                Issue: 21
                Pages: 2314-2327
                Affiliations
                [∗ ]Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, Scotland
                [† ]West of Scotland Regional Heart & Lung Centre, Golden Jubilee National Hospital, Clydebank, Scotland
                [‡ ]Department of Cardiovascular Medicine, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
                Author notes
                [∗ ] Reprint requests and correspondence: Dr. Andrew H. Baker, Institute of Cardiovascular and Medical Sciences, BHF Glasgow Cardiovascular Research Centre, University of Glasgow, 26 University Place, Glasgow, G12 8TA Scotland, United Kingdom. andrew.h.baker@ 123456glasgow.ac.uk
                Article
                Publisher ID: S0735-1097(15)01649-6
                DOI: 10.1016/j.jacc.2015.03.549
                PMC ID: 4444526
                PubMed ID: 26022821
                SO-VID: 4db658b7-01ad-42c2-a95e-98dfe28f88f8
                Copyright © © 2015 Elsevier Inc. All rights reserved.
                History
                Date received : 16 February 2015
                Date accepted : 9 March 2015
                Categories
                Subject: Original Investigation

                ScienceOpen disciplines: Cardiovascular Medicine
                Keywords: late stent thrombosis,mirna stem loop,neointima,smooth muscle cell,bmdm, bone marrow–derived macrophages,bms, bare-metal stent(s),cd, cluster of differentiation,des, drug-eluting stent(s),il, interleukin,isr, in-stent restenosis,ko, knockout,lps, lipopolysaccharide,mirna, micro–ribonucleic acid,pdcd4, programmed cell death protein 4,pdgf, platelet-derived growth factor,ppar, peroxisome proliferator–activated receptor,rna, ribonucleic acid,smc, smooth muscle cell,wt, wild-type
                Data availability:
                ScienceOpen disciplines: Cardiovascular Medicine
                Keywords: late stent thrombosis, mirna stem loop, neointima, smooth muscle cell, bmdm, bone marrow–derived macrophages, bms, bare-metal stent(s), cd, cluster of differentiation, des, drug-eluting stent(s), il, interleukin, isr, in-stent restenosis, ko, knockout, lps, lipopolysaccharide, mirna, micro–ribonucleic acid, pdcd4, programmed cell death protein 4, pdgf, platelet-derived growth factor, ppar, peroxisome proliferator–activated receptor, rna, ribonucleic acid, smc, smooth muscle cell, wt, wild-type

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