The role of nitric oxide in the pathophysiology of intimal hyperplasia

Furchgott, 1980, The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine, Nature, 288, 373, 10.1038/288373a0 Palmer, 1987, Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor, Nature, 327, 524, 10.1038/327524a0 Bredt, 1994, Nitric oxide: a physiologic messenger molecule, Annu Rev Biochem, 63, 175, 10.1146/annurev.bi.63.070194.001135 Ignarro, 1981, Mechanism of vascular smooth-muscle relaxation by organic nitrates, nitrites, nitroprusside and nitric-oxide - evidence for the involvement of s-nitrosothiols as active intermediates, J Pharmacol Exp Ther, 218, 739 Arnold, 1977, Nitric-oxide activates guanylate cyclase and increases guanosine 3’-5’-cyclic monophosphate levels in various tissue preparations, Proc Natl Acad Sci U S A, 74, 3203, 10.1073/pnas.74.8.3203 Furchgott, 1993, Introduction to EDRF research, J Cardiovasc Pharmacol, 22, S1, 10.1097/00005344-199300221-00002 Ignarro, 1999, Nitric oxide as a signaling molecule in the vascular system: An overview, J Cardiovasc Pharmacol, 34, 879, 10.1097/00005344-199912000-00016 Murad, 1985, Role of cyclic-GMP in relaxations of vascular smooth muscle, J Cardiovasc Pharmacol, 7, S111 Forstermann, 1994, Nitric oxide synthase isozymes, Hypertension, 23, 1121, 10.1161/01.HYP.23.6.1121 Morris, 1994, New insights into the regulation of inducible nitric oxide synthesis, Am J Physiol, 266, E829 Nathan, 1994, Nitric oxide synthases: roles, tolls, and controls, Cell, 78, 915, 10.1016/0092-8674(94)90266-6 Clowes, 1983, Mechanisms of stenosis after arterial injury, Lab Invest, 49, 208 Fingerle, 1989, Role of platelets in smooth muscle cell proliferation and migration after vascular injury in rat carotid artery, Proc Natl Acad Sci U S A, 86, 8412, 10.1073/pnas.86.21.8412 Ross, 1981, Atherosclerosis—a problem of the biology of arterial-wall cells and their interactions with blood components, Arteriosclerosis, 1, 293, 10.1161/01.ATV.1.5.293 Ross, 1974, Platelet-dependent serum factor that stimulates proliferation of arterial smooth-muscle cells in vitro, Proc Natl Acad Sci U S A, 71, 1207, 10.1073/pnas.71.4.1207 Mitra, 2005, Cells, cytokines and cellular immunity in the pathogenesis of fibroproliferative vasculopathies, Can J Physiol Pharmacol, 83, 701, 10.1139/y05-080 Ross, 1986, The biology of platelet-derived growth-factor, Cell, 46, 155, 10.1016/0092-8674(86)90733-6 Libby, 1988, Interleukin-1: a mitogen for human vascular smooth-muscle cells that induces the release of growth-inhibitory prostanoids, J Clin Invest, 81, 487, 10.1172/JCI113346 Yang, 2006, A novel model of inflammatory neointima formation reveals a role of myeloperoxidase in neointimal hyperplasia, Arterioscler Thromb Vasc Biol, 26, E71 Baldus, 2006, Heparins increase endothelial nitric oxide bioavailability by liberating vessel-immobilized myeloperoxidase, Circulation, 113, 1871, 10.1161/CIRCULATIONAHA.105.590083 Lindner, 1991, Role of basic fibroblast growth factor in vascular lesion formation, Circ Res, 68, 106, 10.1161/01.RES.68.1.106 Clowes, 1986, Kinetics of cellular proliferation after arterial injury, Lab Invest, 54, 295 Chen, 2006, Potent inhibition of platelet-derived growth factor-induced responses in vascular smooth muscle cells by BMS-354825 (dasatinib), Mol Pharmacol, 69, 1527, 10.1124/mol.105.020172 Bendeck, 1994, Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat, Circ Res, 75, 539, 10.1161/01.RES.75.3.539 Hasenstab, 1997, Plasminogen activator inhibitor type 1 and tissue inhibitor of metalloproteinases-2 increase after arterial injury in rats, Circ Res, 80, 490, 10.1161/01.RES.80.4.490 Majesky, 1991, Production of transforming growth factor beta 1 during repair of arterial injury, J Clin Invest, 88, 904, 10.1172/JCI115393 Nabel, 1993, Direct transfer of transforming growth factor beta 1 gene into arteries stimulates fibrocellular hyperplasia, Proc Natl Acad Sci U S A, 90, 10759, 10.1073/pnas.90.22.10759 Anderson, 2000, Cyclic GMP-dependent protein kinase expression in coronary arterial smooth muscle in response to balloon catheter injury, Arterioscler Thromb Vasc Biol, 20, 2192, 10.1161/01.ATV.20.10.2192 Lindner, 1990, Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries, J Clin Invest, 85, 2004, 10.1172/JCI114665 Rudic, 1998, Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling, J Clin Invest, 101, 731, 10.1172/JCI1699 Huang, 1995, Hypertension in mice lacking the gene for endothelial nitric oxide synthase, Nature, 377, 239, 10.1038/377239a0 Zhang, 2006, Endothelial NO synthase deficiency promotes smooth muscle progenitor cells in association with upregulation of stromal cell-derived factor-1 alpha in a mouse model of carotid artery ligation, Arterioscler Thromb Vasc Biol, 26, 765, 10.1161/01.ATV.0000207319.28254.8c Fischer, 2004, Pharmacologic inhibition of nitric oxide synthases and cyclooxygenases enhances intimal hyperplasia in balloon-injured rat carotid arteries, J Vasc Surg, 40, 115, 10.1016/j.jvs.2004.03.037 Radomski, 1987, Endogenous nitric oxide inhibits human platelet adhesion to vascular endothelium, Lancet, 2, 1057, 10.1016/S0140-6736(87)91481-4 Yan, 1996, Expression of inducible nitric oxide synthase inhibits platelet adhesion and restores blood flow in the injured artery, Circ Res, 79, 38, 10.1161/01.RES.79.1.38 Kubes, 1991, Nitric oxide: an endogenous modulator of leukocyte adhesion, Proc Natl Acad Sci U S A, 88, 4651, 10.1073/pnas.88.11.4651 Hickey, 1997, Inducible nitric oxide synthase-deficient mice have enhanced leukocyte-endothelium interactions in endotoxemia, FASEB J, 11, 955, 10.1096/fasebj.11.12.9337148 Garg, 1989, Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells, J Clin Invest, 83, 1774, 10.1172/JCI114081 Sarkar, 1997, Cell cycle effects of nitric oxide on vascular smooth muscle cells, Am J Physiol, 272, H1810 Ishida, 1997, Induction of the cyclin-dependent kinase inhibitor p21(Sdi1/Cip1/Waf1) by nitric oxide-generating vasodilator in vascular smooth muscle cells, J Biol Chem, 272, 10050, 10.1074/jbc.272.15.10050 Kibbe, 2000, Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate, J Vasc Surg, 31, 1214, 10.1067/mva.2000.105006 Tanner, 2000, Nitric oxide modulates expression of cell cycle regulatory proteins: a cytostatic strategy for inhibition of human vascular smooth muscle cell proliferation, Circulation, 101, 1982, 10.1161/01.CIR.101.16.1982 Dubey, 1995, Nitric oxide inhibits angiotensin II-induced migration of rat aortic smooth muscle cell, J Clin Invest, 96, 141, 10.1172/JCI118014 Sarkar, 1996, Nitric oxide reversibly inhibits the migration of cultured vascular smooth muscle cells, Circ Res, 78, 225, 10.1161/01.RES.78.2.225 Pollman, 1996, Vasoactive substances regulate vascular smooth muscle cell apoptosis - Countervailing influences of nitric oxide and angiotensin II, Circ Res, 79, 748, 10.1161/01.RES.79.4.748 Nishio, 1996, Nitric oxide donor SNAP induces apoptosis in smooth muscle cells through cGMP-independent mechanism, Biochem Biophys Res Commun, 221, 163, 10.1006/bbrc.1996.0563 Iwashina, 1998, Transfection of inducible nitric oxide synthase gene causes apoptosis in vascular smooth muscle cells, Circulation, 98, 1212, 10.1161/01.CIR.98.12.1212 Gurjar, 1999, eNOS gene transfer inhibits smooth muscle cell migration and MMP-2 and MMP-9 activity, Arterioscler Thromb Vasc Biol, 19, 2871, 10.1161/01.ATV.19.12.2871 Dupuis, 2004, Profiling of aortic smooth muscle cell gene expression in response to chronic inhibition of nitric oxide synthase in rats, Circulation, 110, 867, 10.1161/01.CIR.0000138850.72900.FE Chaux, 1998, Perivascular delivery of a nitric oxide donor inhibits neointimal hyperplasia in vein grafts implanted in the arterial circulation, J Thorac Cardiovasc Surg, 115, 604, 10.1016/S0022-5223(98)70325-3 Dattilo, 1998, The nitric oxide precursor L-arginine reduces expression of hyaluronan synthase in experimental vein bypass grafts, J Surg Res, 74, 39, 10.1006/jsre.1997.5224 Schmidt, 2003, Exogenous nitric oxide causes overexpression of TGF-beta(1) and overproduction of extracellular matrix in human coronary smooth muscle cells, Cardiovas Res, 58, 671, 10.1016/S0008-6363(03)00322-5 Rizvi, 1997, Nitric oxide modulates basal and endothelin-induced coronary artery vascular smooth muscle cell proliferation and collagen levels, J Mol Cell Cardiol, 29, 1779, 10.1006/jmcc.1996.0480 Kolpakov, 1995, Nitric oxide-generating compounds inhibit total protein and collagen-synthesis in cultured vascular smooth-muscle cells, Circ Res, 76, 305, 10.1161/01.RES.76.2.305 Guo, 1995, Mechanisms of vascular preservation by a novel NO donor following rat carotid artery intimal injury, Am J Physiol, 269, H1122 Milkiewicz, 2006, Regulators of angiogenesis and strategies for their therapeutic manipulation, Int J Biochem Cell Biol, 38, 333, 10.1016/j.biocel.2005.10.006 Parenti, 1998, Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium, J Biol Chem, 273, 4220, 10.1074/jbc.273.7.4220 Ziche, 1994, Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P, J Clin Invest, 94, 2036, 10.1172/JCI117557 Ziche, 1997, Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis, J Clin Invest, 99, 2625, 10.1172/JCI119451 Murohara, 1998, Nitric oxide synthase modulates angiogenesis in response to tissue ischemia, J Clin Invest, 101, 2567, 10.1172/JCI1560 RayChaudhury, 1996, Inhibition of endothelial cell proliferation and bFGF-induced phenotypic modulation by nitric oxide, J Cell Biochem, 63, 125, 10.1002/(SICI)1097-4644(19961101)63:2<125::AID-JCB1>3.0.CO;2-# Ziche, 1997, Nitric oxide synthase mediates vascular endothelial growth factor but not basic fibroblast growth factor induced angiogenesis, FASEB J, 11, 1137 Dimmeler, 1997, Suppression of apoptosis by nitric oxide via inhibition of interleukin- 1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)- 32-like proteases, J Exp Med, 185, 601, 10.1084/jem.185.4.601 Tzeng, 1997, Adenoviral transfer of the inducible nitric oxide synthase gene blocks endothelial cell apoptosis, Surgery, 122, 255, 10.1016/S0039-6060(97)90016-7 DeMeester, 1998, Nitric oxide inhibits stress-induced endothelial cell apoptosis, Crit Care Med, 26, 1500, 10.1097/00003246-199809000-00016 Lee, 1996, Chronic inhalation of nitric oxide inhibits neointimal formation after balloon-induced arterial injury, Circ Res, 78, 337, 10.1161/01.RES.78.2.337 McNamara, 1993, L-arginine inhibits balloon catheter-induced intimal hyperplasia, Biochem Biophys Res Commun, 193, 291, 10.1006/bbrc.1993.1622 Chen, 1999, Oral administration of L-arginine reduces intimal hyperplasia in balloon-injured rat carotid arteries, J Surg Res, 82, 17, 10.1006/jsre.1998.5476 Groves, 1995, The effects of exogenous nitric oxide on smooth muscle cell proliferation following porcine carotid angioplasty, Cardiovasc Res, 30, 87, 10.1016/0008-6363(95)00009-7 Lablanche, 1997, Effect of the direct nitric oxide donors linsidomine and molsidomine on angiographic restenosis after coronary balloon angioplasty, Circulation, 95, 83, 10.1161/01.CIR.95.1.83 Napoli, 2001, Effects of nitric oxide-releasing aspirin versus aspirin on restenosis in hypercholesterolemic mice, Proc Natl Acad Sci U S A, 98, 2860, 10.1073/pnas.041602898 Wohrle, 2003, No effect of highly dosed nitric oxide donor molsidomine on the angiographic restenosis rate after percutaneous coronary angioplasty: a randomized, placebo controlled, double-blind trial, Can J Cardiol, 19, 495 von der Leyen, 1995, Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene, Proc Natl Acad Sci U S A, 92, 1137, 10.1073/pnas.92.4.1137 Chen, 1998, Overexpression of human endothelial nitric oxide synthase in rat vascular smooth muscle cells and in balloon-injured carotid artery, Circ Res, 82, 862, 10.1161/01.RES.82.8.862 Janssens, 1998, Human endothelial nitric oxide synthase gene transfer inhibits vascular smooth muscle cell proliferation and neointima formation after balloon injury in rats, Circulation, 97, 1274, 10.1161/01.CIR.97.13.1274 Varenne, 1998, Local adenovirus-mediated transfer of human endothelial nitric oxide synthase reduces luminal narrowing after coronary angioplasty in pigs, Circulation, 98, 919, 10.1161/01.CIR.98.9.919 Shears, 1998, Efficient inhibition of intimal hyperplasia by adenovirus-mediated inducible nitric oxide synthase gene transfer to rats and pigs in vivo, J Am Coll Surg, 187, 295, 10.1016/S1072-7515(98)00163-X Kibbe, 2001, Adenovirus-mediated gene transfer of human inducible nitric oxide synthase in porcine vein grafts inhibits intimal hyperplasia, J Vasc Surg, 34, 156, 10.1067/mva.2001.113983 Wang, 2001, Local adenoviral-mediated inducible nitric oxide synthase (iNOS) gene transfer inhibits neointimal formation in the porcine coronary stented model, Am J Cardiol, 88, 51G Marks, 1995, Inhibition of neointimal proliferation in rabbits after vascular injury by a single treatment with a protein adduct of nitric oxide, J Clin Invest, 96, 2630, 10.1172/JCI118328 Schwarzacher, 1997, Local intramural delivery of L-arginine enhances nitric oxide generation and inhibits lesion formation after balloon angioplasty, Circulation, 95, 1863, 10.1161/01.CIR.95.7.1863 Fulton, 1998, Local effects of nitric oxide supplementation and suppression in the development of intimal hyperplasia in experimental vein grafts, Eur J Vasc Endovasc Surg, 15, 279, 10.1016/S1078-5884(98)80030-0 Kaul, 2000, Polymeric-based perivascular delivery of a nitric oxide donor inhibits intimal thickening after balloon denudation arterial injury: role of nuclear factor-kappaB, J Am Coll Cardiol, 35, 493, 10.1016/S0735-1097(99)00543-4 Harnek, 2003, Local infusion of the nitric oxide donor SIN-1 after angioplasty: effects on intimal hyperplasia in porcine coronary arteries, Acta Radiol, 44, 395 Yoon, 2002, Local delivery of nitric oxide from an eluting stent to inhibit neointimal thickening in a porcine coronary injury model, Yonsei Med J, 43, 242, 10.3349/ymj.2002.43.2.242 Do, 2004, In-stent restenosis limitation with stent-based controlled-release nitric oxide: initial results in rabbits, Radiology, 230, 377, 10.1148/radiol.2302020417 Hou, 2005, Stent-based nitric oxide delivery reducing neointimal proliferation in a porcine carotid overstretch injury model, Cardiovasc Intervent Radiol, 28, 60 Rich, 1993, Inhaled nitric-oxide: dose-response and the effects of blood in the isolated rat lung, J Appl Physiol, 75, 1278, 10.1152/jappl.1993.75.3.1278 Cooney, 2006, Adenoviral-mediated gene transfer of nitric oxide synthase isoforms and vascular cell proliferation, J Vasc Res, 43, 462, 10.1159/000095163 Kown, 2001, L-arginine polymers inhibit the development of vein graft neointimal hyperplasia, J Thorac Cardiovasc Surg, 121, 971, 10.1067/mtc.2001.112532 Rolland, 2003, Efficacy of local molsidomine delivery from a hydrogel-coated angioplasty balloon catheter in the atherosclerotic porcine model, Cardiovasc Intervent Radiol, 26, 65, 10.1007/s00270-002-1940-y Verma, 2005, Nitric oxide-eluting polyurethanes–vascular grafts of the future?, N Engl J Med, 353, 730, 10.1056/NEJMcibr052030 Smith, 1996, Nitric oxide-releasing polymers containing the [N(O)NO]- group, J Med Chem, 39, 1148, 10.1021/jm950652b Zhang, 2002, Nitric oxide releasing silicone rubbers with improved blood compatibility: preparation, characterization, and in vivo evaluation, Biomaterials, 23, 1485, 10.1016/S0142-9612(01)00274-5 Batchelor, 2003, More lipophilic dialkyldiamine-based diazeniumdiolates: synthesis, characterization, and application in preparing thromboresistant nitric oxide release polymeric coatings, J Med Chem, 46, 5153, 10.1021/jm030286t Fleser, 2004, Nitric oxide-releasing biopolymers inhibit thrombus formation in a sheep model of arteriovenous bridge grafts, J Vasc Surg, 40, 803, 10.1016/j.jvs.2004.07.007 Jun, 2005, Nitric oxide-producing polyurethanes, Biomacromolecules, 6, 838, 10.1021/bm049419y Bohl, 2000, Nitric oxide-generating polymers reduce platelet adhesion and smooth muscle cell proliferation, Biomaterials, 21, 2273, 10.1016/S0142-9612(00)00153-8 Gappa-Fahlenkamp, 2004, Analysis of immobilized L-cysteine on polymers, J Biomed Mater Res A, 71, 519, 10.1002/jbm.a.30180 Oh, 2004, Catalytic generation of nitric oxide from nitrite at the interface of polymeric films doped with lipophilic Cu(Il)-complex: a potential route to the preparation of thromboresistant coatings, Biomaterials, 25, 283, 10.1016/S0142-9612(03)00530-1