282
Views
38
CrossRef citations to date
0
Altmetric
Review

Regulation of smooth muscle cells in development and vascular disease: current therapeutic strategies

Pages 789-800 | Published online: 10 Jan 2014

References

  • Laporte R, Hui A, Laher I. Pharmacological modulation of sarcoplasmic reticulum function in smooth muscle. Pharmacol. Rev.56, 439–513 (2004).
  • Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev.84, 767–801 (2004).
  • Berk BC. Vascular smooth muscle growth: autocrine growth mechanisms. Physiol. Rev.81, 999–1030 (2001).
  • Libby P. Inflammation in atherosclerosis. Nature420, 868–874 (2002).
  • Thom T, Haase N, Rosamond W et al. Heart Disease and Stroke Statistics – 2006 Update. A Report From the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation113, E85–E151 (2006).
  • Murabito JM, Evans JC, Larson MG, Nieto K, Levy D, Wilson PW. The ankle–brachial index in the elderly and risk of stroke, coronary disease, and death: the Framingham Study. Arch. Intern. Med.163, 1939–1942 (2003).
  • Simosa HF, Conte MS. Genetic therapy for vein bypass graft disease: current perspectives. Vascular12, 213–217 (2004).
  • Woods TC, Marks AR. Drug-eluting stents. Ann. Rev. Med.55, 169–178 (2004).
  • Cutlip DE, Chauhan MS, Baim DS et al. Clinical restenosis after coronary stenting: perspectives from multicenter clinical trials. J. Am. Coll. Cardiol.40, 2082–2089 (2002).
  • Motwani JG, Topol EJ. Aortocoronary saphenous vein graft disease: pathogenesis, predisposition, and prevention. Circulation97, 916–931 (1998).
  • Mohler ER III. Peripheral arterial disease: identification and implications. Arch. Intern. Med.163, 2306–2314 (2003).
  • Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat. Med.8, 1249–1256 (2002).
  • Cai X, Freedman NJ. New therapeutic possibilities for vein graft disease in the post-edifoligide era. Future Cardiol.2, 493–501 (2006).
  • Goldschmidt-Clermont PJ, Creager MA, Lorsordo DW, Lam GK, Wassef M, Dzau VJ. Atherosclerosis 2005: recent discoveries and novel hypotheses. Circulation112, 3348–3353 (2005).
  • Sata M, Saiura A, Kunisato A et al. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat. Med.8, 403–409 (2002).
  • Shimizu K, Sugiyama S, Aikawa M et al. Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Nat. Med.7, 738–741 (2001).
  • Carmeliet P. Angiogenesis in health and disease. Nat. Med.9, 653–660 (2003).
  • Ferrara N, Carver-Moore K, Chen H et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature380, 439–442 (1996).
  • Gittenberger-de Groot AC, DeRuiter MC, Bergwerff M, Poelmann RE. Smooth muscle cell origin and its relation to heterogeneity in development and disease. Arterioscler. Thromb. Vasc. Biol.19, 1589–1594 (1999).
  • Yoshida T, Owens GK. Molecular determinants of vascular smooth muscle cell diversity. Circ. Res.96, 280–291 (2005).
  • Kirby ML, Waldo KL. Neural crest and cardiovascular patterning. Circ. Res.77, 211–215 (1995).
  • Jiang X, Rowitch DH, Soriano P, McMahon AP, Sucov HM. Fate of the mammalian cardiac neural crest. Development127, 1607–1616 (2000).
  • DeRuiter MC, Poelmann RE, VanMunsteren JC, Mironov V, Markwald RR, Gittenberger-de Groot AC. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ. Res.80, 444–451 (1997).
  • Reese DE, Mikawa T, Bader DM. Development of the coronary vessel system. Circ. Res.91, 761–768 (2002).
  • Domenga V, Fardoux P, Lacombe P et al. Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev.18, 2730–2735 (2004).
  • Hao H, Gabbiani G, Bochaton-Piallat ML. Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development. Arterioscler. Thromb. Vasc. Biol.23, 1510–1520 (2003).
  • Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. Smooth muscle cells isolated from discrete compartments of the mature vascular media exhibit unique phenotypes and distinct growth capabilities. Circ. Res.81, 940–952 (1997).
  • Benzakour O, Kanthou C, Kanse SM, Scully MF, Kakkar VV, Cooper DN. Evidence for cultured human vascular smooth muscle cell heterogeneity: isolation of clonal cells and study of their growth characteristics. Thromb. Haemost.75, 854–858 (1996).
  • Li S, Fan YS, Chow LH et al. Innate diversity of adult human arterial smooth muscle cells: cloning of distinct subtypes from the internal thoracic artery. Circ. Res.89, 517–525 (2001).
  • Bochaton-Piallat ML, Clowes AW, Clowes MM et al. Cultured arterial smooth muscle cells maintain distinct phenotypes when implanted into carotid artery. Arterioscler. Thromb. Vasc. Biol.21, 949–954 (2001).
  • Wang Z, Wang DZ, Hockemeyer D, McAnally J, Nordheim A, Olson EN. Myocardin and ternary complex factors compete for SRF to control smooth muscle gene expression. Nature428, 185–189 (2004).
  • Weiser-Evans MC, Schwartz PE, Grieshaber NA et al. Novel embryonic genes are preferentially expressed by autonomously replicating rat embryonic and neointimal smooth muscle cells. Circ. Res.87, 608–615 (2000).
  • Weiser-Evans MC, Quinn BE, Burkard MR, Stenmark KR. Transient reexpression of an embryonic autonomous growth phenotype by adult carotid artery smooth muscle cells after vascular injury. J. Cell Physiol.182, 12–23 (2000).
  • Wenzlau JM, Garl PJ, Simpson P et al. Embryonic growth-associated protein is one subunit of a novel N-terminal acetyltransferase complex essential for embryonic vascular development. Circ. Res.98, 846–855 (2006).
  • van der Loop FT, Gabbiani G, Kohnen G, Ramaekers FC, van Eys GJ. Differentiation of smooth muscle cells in human blood vessels as defined by smoothelin, a novel marker for the contractile phenotype. Arterioscler. Thromb. Vasc. Biol.17, 665–671 (1997).
  • Feil R, Feil S, Hofmann F. A heretical view on the role of NO and cGMP in vascular proliferative diseases. Trends Mol. Med.11, 71–75 (2005).
  • Lusis AJ, Mar R, Pajukanta P. Genetics of atherosclerosis. Ann. Rev. Genomics Hum. Genet.5, 189–218 (2004).
  • Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med.352, 1685–1695 (2005).
  • Zhang WD, Bai HZ, Sawa Y et al. Association of smooth muscle cell phenotypic modulation with extracellular matrix alterations during neointima formation in rabbit vein grafts. J. Vasc. Surg.30, 169–183 (1999).
  • Meir KS, Leitersdorf E. Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress. Arterioscler. Thromb. Vasc. Biol.24, 1006–1014 (2004).
  • Christen T, Verin V, Bochaton-Piallat M et al. Mechanisms of neointima formation and remodeling in the porcine coronary artery. Circulation103, 882–888 (2001).
  • Aikawa M, Kim HS, Kuro-o M et al. Phenotypic modulation of smooth muscle cells during progression of human atherosclerosis as determined by altered expression of myosin heavy chain isoforms. Ann. NY Acad. Sci.748, 578–585 (1995).
  • Aikawa M, Yamaguchi H, Yazaki Y, Nagai R. Smooth muscle phenotypes in developing and atherosclerotic human arteries demonstrated by myosin expression. J. Atheroscler. Thromb.2, 14–23 (1995).
  • Mulvihill ER, Jaeger J, Sengupta R et al. Atherosclerotic plaque smooth muscle cells have a distinct phenotype. Arterioscler. Thromb. Vasc. Biol.24, 1283–1289 (2004).
  • Hao H, Gabbiani G, Camenzind E, Bacchetta M, Virmani R, Bochaton-Piallat ML. Phenotypic modulation of intima and media smooth muscle cells in fatal cases of coronary artery lesion. Arterioscler. Thromb. Vasc. Biol.26, 326–332 (2006).
  • Aikawa M, Sakomura Y, Ueda M et al. Redifferentiation of smooth muscle cells after coronary angioplasty determined via myosin heavy chain expression. Circulation96, 82–90 (1997).
  • Liu C, Nath KA, Katusic ZS, Caplice NM. Smooth muscle progenitor cells in vascular disease. Trends Cardiovasc. Med.14, 288–293 (2004).
  • Han CI, Campbell GR, Campbell JH. Circulating bone marrow cells can contribute to neointimal formation. J. Vasc. Res.38, 113–119 (2001).
  • Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ. Res.93, 783–790 (2003).
  • Zhang L, Freedman NJ, Brian L, Peppel K. Graft-extrinsic cells predominate in vein graft arterialization. Arterioscler. Thromb. Vasc. Biol.24, 470–476 (2004).
  • Hu Y, Mayr M, Metzler B, Erdel M, Davison F, Xu Q. Both donor and recipient origins of smooth muscle cells in vein graft atherosclerotic lesions. Circ. Res.91, E13–E20 (2002).
  • Hillebrands JL, Klatter FA, van den Hurk BM, Popa ER, Nieuwenhuis P, Rozing J. Origin of neointimal endothelium and α-actin-positive smooth muscle cells in transplant arteriosclerosis. J. Clin. Invest.107, 1411–1422 (2001).
  • Saiura A, Sata M, Hirata Y, Nagai R, Makuuchi M. Circulating smooth muscle progenitor cells contribute to atherosclerosis. Nat. Med.7, 382–383 (2001).
  • Sata M. Molecular strategies to treat vascular diseases: circulating vascular progenitor cell as a potential target for prophylactic treatment of atherosclerosis. Circ. J67, 983–991 (2003).
  • Hillebrands JL, Onuta G, Rozing J. Role of progenitor cells in transplant arteriosclerosis. Trends Cardiovasc. Med.15, 1–8 (2005).
  • Roberts N, Jahangiri M, Xu Q. Progenitor cells in vascular disease. J. Cell Mol. Med.9, 583–591 (2005).
  • Yamashita J, Itoh H, Hirashima M et al. Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature408, 92–96 (2000).
  • Sainz J, Al Haj Zen A, Caligiuri G et al. Isolation of “side population” progenitor cells from healthy arteries of adult mice. Arterioscler. Thromb. Vasc. Biol.26, 281–286 (2006).
  • Simper D, Stalboerger PG, Panetta CJ, Wang S, Caplice NM. Smooth muscle progenitor cells in human blood. Circulation106, 1199–1204 (2002).
  • Kashiwakura Y, Katoh Y, Tamayose K et al. Isolation of bone marrow stromal cell-derived smooth muscle cells by a human SM22α promoter: in vitro differentiation of putative smooth muscle progenitor cells of bone marrow. Circulation107, 2078–2081 (2003).
  • Sugiyama S, Kugiyama K, Nakamura S et al. Characterization of smooth muscle-like cells in circulating human peripheral blood. Atherosclerosis187, 351–362 (2006).
  • Fukuda D, Shimada K, Tanaka A, Kawarabayashi T, Yoshiyama M, Yoshikawa J. Circulating monocytes and in-stent neointima after coronary stent implantation. J. Am. Coll. Cardiol.43, 18–23 (2004).
  • Minami E, Laflamme MA, Saffitz JE, Murry CE. Extracardiac progenitor cells repopulate most major cell types in the transplanted human heart. Circulation112, 2951–2958 (2005).
  • Glaser R, Lu MM, Narula N, Epstein JA. Smooth muscle cells, but not myocytes, of host origin in transplanted human hearts. Circulation106, 17–19 (2002).
  • Quaini F, Urbanek K, Beltrami AP et al. Chimerism of the transplanted heart. N. Engl. J. Med.346, 5–15 (2002).
  • Caplice NM, Bunch TJ, Stalboerger PG et al. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc. Natl Acad. Sci. USA100, 4754–4759 (2003).
  • Li J, Han X, Jiang J et al. Vascular smooth muscle cells of recipient origin mediate intimal expansion after aortic allotransplantation in mice. Am. J. Pathol.158, 1943–1947 (2001).
  • Hu Y, Davison F, Ludewig B et al. Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation106, 1834–1839 (2002).
  • Cooley BC. Murine model of neointimal formation and stenosis in vein grafts. Arterioscler. Thromb. Vasc. Biol.24, 1180–1185 (2004).
  • Sata M, Tanaka K, Nagai R. Origin of smooth muscle progenitor cells: different conclusions from different models. Circulation107, E106–E107 (2003).
  • van der Meer J, Hillege HL, Kootstra GJ et al. Prevention of one-year vein-graft occlusion after aortocoronary-bypass surgery: a comparison of low-dose aspirin, low-dose aspirin plus dipyridamole, and oral anticoagulants. The CABADAS Research Group of the Interuniversity Cardiology Institute of The Netherlands. Lancet342, 257–264 (1993).
  • de Gaetano G. Low-dose aspirin and vitamin E in people at cardiovascular risk: a randomised trial in general practice. Collaborative Group of the Primary Prevention Project. Lancet357, 89–95 (2001).
  • Topol EJ, Lincoff AM, Kereiakes DJ et al. Multi-year follow-up of abciximab therapy in three randomized, placebo-controlled trials of percutaneous coronary revascularization. Am. J. Med.113, 1–6 (2002).
  • The effect of aggressive lowering of low-density lipoprotein cholesterol levels and low-dose anticoagulation on obstructive changes in saphenous-vein coronary-artery bypass grafts. The Post Coronary Artery Bypass Graft Trial Investigators. N. Engl. J. Med.336, 153–162 (1997).
  • Sacks FM, Pfeffer MA, Moye LA et al. The effect of pravastatin on coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events Trial investigators. N. Engl. J. Med.335, 1001–1009 (1996).
  • Serruys PW, Ormiston JA, Sianos G et al. Actinomycin-eluting stent for coronary revascularization: a randomized feasibility and safety study: the ACTION trial. J. Am. Coll. Cardiol.44, 1363–1367 (2004).
  • Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation111, 2257–2273 (2005).
  • Fukuda D, Sata M, Tanaka K, Nagai R. Potent inhibitory effect of sirolimus on circulating vascular progenitor cells. Circulation111, 926–931 (2005).
  • Sousa JE, Costa MA, Abizaid A et al. Lack of neointimal proliferation after implantation of sirolimus-coated stents in human coronary arteries: a quantitative coronary angiography and three-dimensional intravascular ultrasound study. Circulation103, 192–195 (2001).
  • Sousa JE, Costa MA, Sousa AG et al. Two-year angiographic and intravascular ultrasound follow-up after implantation of sirolimus-eluting stents in human coronary arteries. Circulation107, 381–383 (2003).
  • Morice MC, Serruys PW, Sousa JE et al. A randomized comparison of a sirolimus-eluting stent with a standard stent for coronary revascularization. N. Engl. J. Med.346, 1773–1780 (2002).
  • Fajadet J, Morice MC, Bode C et al. Maintenance of long-term clinical benefit with sirolimus-eluting coronary stents: three-year results of the RAVEL trial. Circulation111, 1040–1044 (2005).
  • Weisz G, Leon MB, Holmes DR, Jr. et al. Two-year outcomes after sirolimus-eluting stent implantation: results from the Sirolimus-Eluting Stent in de novo Native Coronary Lesions (SIRIUS) trial. J. Am. Coll. Cardiol.47, 1350–1355 (2006).
  • Ong AT, van Domburg RT, Aoki J, Sonnenschein K, Lemos PA, Serruys PW. Sirolimus-eluting stents remain superior to bare-metal stents at two years: medium-term results from the Rapamycin-Eluting Stent Evaluated at Rotterdam Cardiology Hospital (RESEARCH) registry. J. Am. Coll. Cardiol.47, 1356–1360 (2006).
  • Wessely R, Schomig A, Kastrati A. Sirolimus and Paclitaxel on polymer-based drug-eluting stents: similar but different. J. Am. Coll. Cardiol.47, 708–714 (2006).
  • Patterson C, Mapera S, Li HH et al. Comparative effects of paclitaxel and rapamycin on smooth muscle migration and survival: role of AKT-dependent signaling. Arterioscler. Thromb. Vasc. Biol.26, 1473–1480 (2006).
  • Joner M, Finn AV, Farb A et al. Pathology of drug-eluting stents in humans: delayed healing and late thrombotic risk. J. Am. Coll. Cardiol.48, 193–202 (2006).
  • Jimenez-Quevedo P, Sabate M, Angiolillo DJ et al. Vascular effects of sirolimus-eluting versus bare-metal stents in diabetic patients: three-dimensional ultrasound results of the Diabetes and Sirolimus-Eluting Stent (DIABETES) Trial. J. Am. Coll. Cardiol.47, 2172–2179 (2006).
  • Ge L, Iakovou I, Sangiorgi GM et al. Treatment of saphenous vein graft lesions with drug-eluting stents: immediate and midterm outcome. J. Am. Coll. Cardiol.45, 989–994 (2005).
  • Schachner T, Zou Y, Oberhuber A et al. Local application of rapamycin inhibits neointimal hyperplasia in experimental vein grafts. Ann. Thorac. Surg.77, 1580–1585 (2004).
  • Masaki T, Rathi R, Zentner G et al. Inhibition of neointimal hyperplasia in vascular grafts by sustained perivascular delivery of paclitaxel. Kidney Int.66, 2061–2069 (2004).
  • Stevens C, La Thangue NB. E2F and cell cycle control: a double-edged sword. Arch. Biochem. Biophys.412, 157–169 (2003).
  • Mann MJ. Transcription factor decoys: a new model for disease intervention. Ann. NY Acad. Sci.1058, 128–139 (2005).
  • Miyake T, Aoki M, Shiraya S et al. Inhibitory effects of NFκB decoy oligodeoxynucleotides on neointimal hyperplasia in a rabbit vein graft model. J. Mol. Cell Cardiol.41(3), 431–440 (2006).
  • Kume M, Komori K, Matsumoto T et al. Administration of a decoy against the activator protein-1 binding site suppresses neointimal thickening in rabbit balloon-injured arteries. Circulation105, 1226–1232 (2002).
  • Ehsan A, Mann MJ, Dell’Acqua G, Dzau VJ. Long-term stabilization of vein graft wall architecture and prolonged resistance to experimental atherosclerosis after E2F decoy oligonucleotide gene therapy. J. Thorac. Cardiovasc. Surg.121, 714–722 (2001).
  • Morishita R, Gibbons GH, Horiuchi M et al. A gene therapy strategy using a transcription factor decoy of the E2F binding site inhibits smooth muscle proliferation in vivo. Proc. Natl Acad. Sci. USA92, 5855–5859 (1995).
  • Mann MJ, Whittemore AD, Donaldson MC et al.Ex-vivo gene therapy of human vascular bypass grafts with E2F decoy: the PREVENT single-centre, randomised, controlled trial. Lancet354, 1493–1498 (1999).
  • Grube E. PRoject of Ex-vivo Vein graft ENgineering via Transfection (PREVENT) II trial. Presented at The Annual American Heart Association Scientific Sessions, Anaheim, CA, USA November 11–14, 2001
  • Conte MS, Bandyk DF, Clowes AW et al. Results of PREVENT III: a multicenter, randomized trial of edifoligide for the prevention of vein graft failure in lower extremity bypass surgery. J. Vasc. Surg.43, 742–751 (2006).
  • Alexander JH, Hafley G, Harrington RA et al. Efficacy and safety of edifoligide, an E2F transcription factor decoy, for prevention of vein graft failure following coronary artery bypass graft surgery: PREVENT IV: a randomized controlled trial. JAMA294, 2446–2454 (2005).
  • Zhang L, Hagen PO, Kisslo J, Peppel K, Freedman NJ. Neointimal hyperplasia rapidly reaches steady state in a novel murine vein graft model. J. Vasc. Surg.36, 824–832 (2002).
  • Sano H, Sudo T, Yokode M et al. Functional blockade of platelet-derived growth factor receptor-β but not of receptor-α prevents vascular smooth muscle cell accumulation in fibrous cap lesions in apolipoprotein E-deficient mice. Circulation103, 2955–2960 (2001).
  • Raj T, Kanellakis P, Pomilio G, Jennings G, Bobik A, Agrotis A. Inhibition of fibroblast growth factor receptor signaling attenuates atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol.26, 1845–1851 (2006).
  • Hart CE, Kraiss LW, Vergel S et al. PDGFβ receptor blockade inhibits intimal hyperplasia in the baboon. Circulation99, 564–569 (1999).
  • Agrotis A, Kanellakis P, Kostolias G et al. Proliferation of neointimal smooth muscle cells after arterial injury. Dependence on interactions between fibroblast growth factor receptor-2 and fibroblast growth factor-9. J. Biol. Chem.279, 42221–42229 (2004).
  • Davies MG, Owens EL, Mason DP et al. Effect of platelet-derived growth factor receptor-a and -b blockade on flow-induced neointimal formation in endothelialized baboon vascular grafts. Circ. Res.86, 779–786 (2000).
  • Levitzki A, Mishani E. Tyrphostins and Other Tyrosine Kinase Inhibitors. Ann. Rev. Biochem.75, 93–109 (2006).
  • Levitzki A. PDGF receptor kinase inhibitors for the treatment of restenosis. Cardiovasc. Res.65, 581–586 (2005).
  • Banai S, Chorny M, Gertz SD et al. Locally delivered nanoencapsulated tyrphostin (AGL-2043) reduces neointima formation in balloon-injured rat carotid and stented porcine coronary arteries. Biomaterials26, 451–461 (2005).
  • Millette E, Rauch BH, Defawe O, Kenagy RD, Daum G, Clowes AW. Platelet-derived growth factor-BB-induced human smooth muscle cell proliferation depends on basic FGF release and FGFR-1 activation. Circ. Res.96, 172–179 (2005).
  • O’Brien SG, Guilhot F, Larson RA et al. Imatinib compared with interferon and low-dose cytarabine for newly diagnosed chronic-phase chronic myeloid leukemia. N. Engl. J. Med.348, 994–1004 (2003).
  • Myllarniemi M, Frosen J, Calderon Ramirez LG, Buchdunger E, Lemstrom K, Hayry P. Selective tyrosine kinase inhibitor for the platelet-derived growth factor receptor in vitro inhibits smooth muscle cell proliferation after reinjury of arterial intima in vivo. Cardiovasc. Drugs Ther.13, 159–168 (1999).
  • Boucher P, Gotthardt M, Li WP, Anderson RG, Herz J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science300, 329–332 (2003).
  • Lassila M, Allen TJ, Cao Z et al. Imatinib attenuates diabetes-associated atherosclerosis. Arterioscler. Thromb. Vasc. Biol.24, 935–942 (2004).
  • Zohlnhofer D, Hausleiter J, Kastrati A et al. A randomized, double-blind, placebo-controlled trial on restenosis prevention by the receptor tyrosine kinase inhibitor imatinib. J. Am. Coll. Cardiol.46, 1999–2003 (2005).
  • Hausleiter J, Kastrati A, Mehilli J et al. Randomized, double-blind, placebo-controlled trial of oral sirolimus for restenosis prevention in patients with in-stent restenosis: the Oral Sirolimus to Inhibit Recurrent In-stent Stenosis (OSIRIS) trial. Circulation110, 790–795 (2004).
  • Dzau VJ, Gnecchi M, Pachori AS, Morello F, Melo LG. Therapeutic potential of endothelial progenitor cells in cardiovascular diseases. Hypertension46, 7–18 (2005).
  • Dashwood MR, Savage K, Dooley A, Shi-Wen X, Abraham DJ, Souza DS. Effect of vein graft harvesting on endothelial nitric oxide synthase and nitric oxide production. Ann. Thorac. Surg.80, 939–944 (2005).
  • Aicher A, Zeiher AM, Dimmeler S. Mobilizing endothelial progenitor cells. Hypertension45, 321–325 (2005).
  • Dimmeler S, Aicher A, Vasa M et al. HMG-CoA reductase inhibitors (statins) increase endothelial progenitor cells via the PI 3-kinase/Akt pathway. J. Clin. Invest.108, 391–397 (2001).
  • Cho HJ, Kim TY, Cho HJ et al. The effect of stem cell mobilization by granulocyte-colony stimulating factor on neointimal hyperplasia and endothelial healing after vascular injury with bare-metal versus paclitaxel-eluting stents. J. Am. Coll. Cardiol.48, 366–374 (2006).
  • Mayr U, Zou Y, Zhang Z, Dietrich H, Hu Y, Xu Q. Accelerated arteriosclerosis of vein grafts in inducible no synthase-/- mice is related to decreased endothelial progenitor cell repair. Circ. Res.98, 412–440 (2006).
  • Walter DH, Cejna M, Diaz-Sandoval L et al. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation110, 36–45 (2004).
  • Blindt R, Vogt F, Astafieva I et al. A novel drug-eluting stent coated with an integrin-binding cyclic Arg-Gly-Asp peptide inhibits neointimal hyperplasia by recruiting endothelial progenitor cells. J. Am. Coll. Cardiol.47, 1786–1795 (2006).
  • Werner N, Nickenig G. Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy? Arterioscler. Thromb. Vasc. Biol.26, 257–266 (2006).
  • Cai X, Lytton J. The cation/Ca2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol. Biol. Evol.21, 1692–1703 (2004).
  • Wamhoff BR, Bowles DK, Owens GK. Excitation-transcription coupling in arterial smooth muscle. Circ. Res.98, 868–878 (2006).
  • Barlow CA, Rose P, Pulver-Kaste RA, Lounsbury KM. Excitation-transcription coupling in smooth muscle. J. Physiol.570, 59–64 (2006).
  • Choi J, Chiang A, Taulier N, Gros R, Pirani A, Husain M. A calmodulin-binding site on cyclin E mediates Ca2+-sensitive G1/s transitions in vascular smooth muscle cells. Circ. Res.98, 1273–1281 (2006).
  • Mann KM, Ray JL, Moon ES, Sass KM, Benson MR. Calcineurin initiates smooth muscle differentiation in neural crest stem cells. J. Cell Biol.165, 483–491 (2004).
  • Wamhoff BR, Bowles DK, McDonald OG et al. L-type voltage-gated Ca2+ channels modulate expression of smooth muscle differentiation marker genes via a rho kinase/myocardin/SRF-dependent mechanism. Circ. Res.95, 406–414 (2004).
  • Mason RP, Marche P, Hintze TH. Novel vascular biology of third-generation L-type calcium channel antagonists: ancillary actions of amlodipine. Arterioscler. Thromb. Vasc. Biol.23, 2155–2163 (2003).
  • Arakawa E, Hasegawa K. Benidipine, a calcium channel blocker, regulates proliferation and phenotype of vascular smooth muscle cells. J. Pharmacol. Sci.100, 149–156 (2006).
  • Kohler R, Wulff H, Eichler I et al. Blockade of the intermediate-conductance calcium-activated potassium channel as a new therapeutic strategy for restenosis. Circulation108, 1119–1125 (2003).
  • Kumar B, Dreja K, Shah S et al. Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia. Circ. Res.98, 557–563 (2006).
  • Lipskaia L, del Monte F, Capiod T et al. Sarco/endoplasmic reticulum Ca2+- ATPase gene transfer reduces vascular smooth muscle cell proliferation and neointima formation in the rat. Circ. Res.97, 488–495 (2005).
  • Hata JA, Petrofski JA, Schroder JN et al. Modulation of phosphatidylinositol 3-kinase signaling reduces intimal hyperplasia in aortocoronary saphenous vein grafts. J. Thorac. Cardiovasc. Surg.129, 1405–1413 (2005).
  • Huang J, Niu XL, Pippen AM, Annex BH, Kontos CD. Adenovirus-mediated intraarterial delivery of PTEN inhibits neointimal hyperplasia. Arterioscler. Thromb. Vasc. Biol.25, 354–358 (2005).
  • Barbato JE, Tzeng E. iNOS gene transfer for graft disease. Trends Cardiovasc. Med.14, 267–272 (2004).
  • Johnson TW, Wu YX, Herdeg C et al. Stent-based delivery of tissue inhibitor of metalloproteinase-3 adenovirus inhibits neointimal formation in porcine coronary arteries. Arterioscler. Thromb. Vasc. Biol.25, 754–759 (2005).
  • Zhang L, Peppel K, Brian L, Chien L, Freedman NJ. Vein graft neointimal hyperplasia is exacerbated by tumor necrosis factor receptor-1 signaling in graft-intrinsic cells. Arterioscler. Thromb. Vasc. Biol.24, 2277–2283 (2004).
  • Zou Y, Hu Y, Mayr M, Dietrich H, Wick G, Xu Q. Reduced neointima hyperplasia of vein bypass grafts in intercellular adhesion molecule-1-deficient mice. Circ. Res.86, 434–440. (2000).
  • Schepers A, Eefting D, Bonta PI et al. Anti-MCP-1 gene therapy inhibits vascular smooth muscle cells proliferation and attenuates vein graft thickening both in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol.26, 2063–2069 (2006).
  • George SJ, Beeching CA. Cadherin:catenin complex: A novel regulator of vascular smooth muscle cell behaviour. Atherosclerosis188, 1–11 (2006).
  • Leppanen O, Rutanen J, Hiltunen MO et al. Oral imatinib mesylate (STI571/gleevec) improves the efficacy of local intravascular vascular endothelial growth factor-C gene transfer in reducing neointimal growth in hypercholesterolemic rabbits. Circulation109, 1140–1146 (2004).
  • Dykxhoorn DM, Lieberman J. Knocking down Disease with siRNAs. Cell126, 231–235 (2006).
  • Seo D, Ginsburg GS, Goldschmidt-Clermont PJ. Gene expression analysis of cardiovascular diseases: novel insights into biology and clinical applications. J. Am. Coll. Cardiol.48, 227–235 (2006).
  • Blanco-Colio LM, Martin-Ventura JL, Vivanco F, Michel JB, Meilhac O, Egido J. Biology of atherosclerotic plaques: what we are learning from proteomic analysis. Cardiovasc. Res.72, 18–29 (2006).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.