Perspectives of arterial gene therapy for the prevention of restenosis

Cardiovascular Research

Volumn 32, Issue 2, 1996, Pages 194-207

  Feldman, Laurent J ^a   Tahlil, Ouafae ^a   Steg, Gabriel ^a  

^a BICHAT HOSPITAL   (France)

Author keywords

Adenovirus; Coronary angioplasty; Gene therapy; Restenosis; Smooth muscle cell; Smooth muscle cell proliferation; Thymidine kinase

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE; THYMIDINE KINASE;

ADENOVIRUS; ANGIOGENESIS; ATHEROSCLEROSIS; CELL PROLIFERATION; CORONARY ARTERY DILATATION; CORONARY ARTERY OBSTRUCTION; GENE THERAPY; GENE TRANSFER; HUMAN; NONHUMAN; PRIORITY JOURNAL; RECURRENT DISEASE; REVIEW; SMOOTH MUSCLE;

ANGIOPLASTY, TRANSLUMINAL, PERCUTANEOUS CORONARY; ANIMALS; ARTERIES; CORONARY DISEASE; CORONARY VESSELS; GENE THERAPY; GENETIC VECTORS; HUMANS; RECURRENCE;

EID: 0030222275     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/0008-6363(96)00099-5     Document Type: Review

References (121)

1. [1] Schneider MD, French BA. The advent of adenovirus. Gene therapy for cardiovascular disease. Circulation 1993;88:1937-1942.
2. [2] Nabel EG. Gene therapy for cardiovascular disease. Circulation 1995;91:541-548.
3. [3] Isner JM, Feldman LJ. Gene therapy for arterial disease. Lancet 1994;344:1653-1654.
4. [4] Nabel EG, Plautz G, Nabel GJ. Site-specific gene expression in vivo by direct gene transfer into the arterial wall. Science 1990;249:1285-1288.
5. [5] Riessen R, Isner JM. Prospects for site-specific delivery of pharmacologic and molecular therapies. J Am Coll Cardiol 1994;23:1234-1244.
6. [6] Mulligan RC. The basic science of gene therapy. Science 1993;260:926-932.
7. [7] Hermans WRM, Rensing BJ, Strauss BH, Serruys PW. Prevention of restenosis after percutaneous transluminal coronary angioplasty: the search for a 'magic bullet'. Am Heart J 1991;122:171-187.
8. [8] Popma JJ, Califf RM, Topol EJ. Clinical trials of restenosis after coronary angioplasty. Circulation 1991;84:1426-1436.
9. [9] Feldman LJ, Riessen R, Steg PG. Prevention of restenosis after coronary angioplasty: towards a molecular approach? Fundam Clin Pharmacol 1995:9:8-16.
10. [10] Nabel EJ, Plautz G, Boyce DM, Stanley JC, Nabel GJ. Recombinant gene expression in vivo within endothelial cells of the arterial wall. Science 1989;244:1342-1344.
11. [11] Plautz G, Nabel EG, Nabel GJ. Introduction of vascular smooth muscle cells expressing recombinant genes in vivo. Circulation 1991;83:578-583.
12. [12] Wilson JM, Birinyi LK, Salomon RN, Libby P, Callow AD, Mulligan RC. Implantation of vascular grafts lined with genetically modified endothelial cells. Science 1989;244:1344-1346.
13. [13] Chen S-J, Wilson JM, Muller DWM. Adenovirus-mediated gene transfer of soluble vascular cell adhesion molecule to porcine interposition vein grafts. Circulation 1994;89:1922-1928.
14. [14] Dichek DA, Neville RF, Zwiebel JA, Freeman SM, Leon MB, Anderson WF. Seeding of intravascular stents with genetically engineered endothelial cells. Circulation 1989;80:1347-1353.
15. [15] Flugelman MY, Virmani R, Leon MB, Bowman RL, Dichek DA. Genetically engineered endothelial cells remain adherent and viable after stent deployment and exposure to flow in vitro. Circ Res 1992;70:348-354.
16. [16] Leclerc G. Isner JM. Percutaneous gene therapy for cardiovascular disease. In: Topol EJ, ed. Textbook of Interventional Cardiology. Philadelphia: Saunders, 1993:1019-1029.
17. [17] Losordo DW, Pickering JG, Takeshita S, et al. Use of the rabbit ear artery to serially assess foreign protein secretion after site-specific arterial gene transfer in vivo. Circulation 1994;89:785-792.
18. [18] Danos O, Mulligan RC. Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges. Proc Natl Acad Sci USA 1988;85:6460-6464.
19. [19] Flugelman MY, Jaklitsch MT, Newman KD, Casscells W, Brathauer GL, Dichek DA. Low level in vivo gene transfer into the arterial wall through a perforated balloon catheter. Circulation 1992;85:1110-1117.
20. [20] Pickering JG, Weir L, Jekanowski J, Kearney M, Isner JM. Proliferative activity in peripheral and coronary atherosclerotic plaque among patients undergoing percutaneous revascularization. J Clin Invest 1993;91:1469-1480.
21. [21] O'Brien ER, Alpers CE, Stewart DK, et al. Proliferation in primary and restenotic coronary atherectomy tissue. Implications for antiproliferative therapy. Circ Res 1993;73:223-231.
22. [22] Horwitz MS. Adenoviridae and their replication. In: Fields BN, Knipe DM, eds. Fundamental Virology. New York: Raven Press, 1991:771-813.
23. [23] Stratford-Perricaudet LD, Makeh I, Perricaudet M, Briand P. Widespread long-term gene transfer to mouse skeletal muscles and heart. J Clin Invest 1992;90:626-630.
24. [24] Vincent N, Ragot T, Gilgenkrantz H, et al. Long-term correction of mouse dystrophic degeneration by adenovirus-mediated transfer of a minidystrophin gene. Nature Genet 1993;5:130-134.
25. [25] Akli S, Caillaud C, Vigne E, et al. Transfer of a foreign gene into the brain using adenovirus vectors. Nature Genet 1993;3:224-228.
26. [26] Guzman R, Lemarchand P, Crystal R, Epstein S, Finkel T. Efficient gene transfer into myocardium by direct injection of adenovirus vectors. Circ Res 1993;73:1202-1207.
27. [27] Rosenfeld MA, Chu C-S, Seth P, et al. Gene transfer to freshly isolated human respiratory epithelial cells in vitro using a replication-deficient adenovirus containing the human cystic fibrosis transmembrane conductance regulator cDNA. Hum Gene Ther 1994;5:331-342.
28. [28] Ragot T, Vincent N, Chafey P, et al. Efficient adenovirus-mediated transfer of a human minidystrophin gene to skeletal muscle of mdx mice. Nature 1993;361:647-650.
29. [29] Mastrangeli A, Danel C, Rosenfeld MA, et al. Diversity of airway epithelial cell targets for in vivo recombinant adenovirus-mediated gene transfer. J Clin Invest 1993;91:225-234.
30. [30] Lemarchand P, Jones M, Yamada I, Crystal RG. In vivo gene transfer and expression in normal uninjured blood vessels using replication-deficient recombinant adenovirus vectors. Circ Res 1993;72:1132-1138.
31. [31] Lee SW, Trapnell BC, Rade JJ, Virmani R, Dichek DA. In vivo adenoviral vector-mediated gene transfer into balloon-injured rat carotid arteries. Circ Res 1993;73:797-807.
32. [32] Guzman R, Lemarchand P, Crystal RG, Epstein SE, Finkel T. Efficient and selective adenovirus-mediated gene transfer into vascular neointima. Circulation 1993;88:2838-2848.
33. [33] Schulick AH, Newman KD, Virmani R, Dichek DA. In vivo gene transfer into injured carotid arteries. Optimization and evaluation of acute toxicity. Circulation 1995;91:2407-2414.
34. [34] Schulick AH, Dong G, Newman KD, Virmani R, Dichek DA. Endothelium-specific in vivo gene transfer. Circ Res 1995;77:475-485.
35. [35] Willard JE, Landau C, Glamann DB, et al. Genetic modification of the vessel wall. Comparison of surgical and catheter-based techniques for delivery of recombinant adenovirus. Circulation 1994;89:2190-2197.
36. [36] Rome JJ, Shayani V, Flugelman MY, et al. Anatomic barriers influence the distribution of in vivo gene transfer into the arterial wall. Modeling with microscopic tracer particles and verification with a recombinant adenoviral vector. Arterioscler Thromb 1994;14:148-161.
37. [37] March KL, Gradus-Pizlo I, Wilensky RL, Yei S, Trapnell BC. Cardiovascular gene therapy using adenoviral vectors: distant transduction following local delivery using a porous balloon catheter. J Am Coll Cardiol 1994;23:177A(Abstract).
38. [38] Steg PG, Feldman LJ, Scoazec J-Y, et al. Arterial gene transfer to rabbit endothelial and smooth muscle cells using percutaneous delivery of an adenoviral vector. Circulation 1994;90:1648-1656.
39. [39] French BA, Mazur W, Ali NM, et al. Percutaneous transluminal in vivo gene transfer by recombinant adenovirus in normal porcine coronary arteries, atherosclerotic arteries, and two models of coronary restenosis. Circulation 1994;90:2402-2413.
40. [40] Feldman LJ, Steg PG, Zheng LP, et al. Low-efficiency of percutaneous adenovirus-mediated arterial gene transfer in the atherosclerotic rabbit. J Clin Invest 1995;95:2662-2671.
41. [41] Feldman LJ, Steg PG, Zheng LP, Barry JJ, Perricaudet M, Isner JM. Efficient percutaneous adenovirus-mediated arterial gene transfer using a channeled angioplasty balloon catheter. Circulation 1994;90:1-20(Abstract).
42. [42] March K, Madison JE, Trapnell BC. Pharmacokinetics of adenoviral vector-mediated gene delivery to vascular smooth muscle cells: modulation by Poloxamer 407 and implications for cardiovascular gene therapy. Hum Gene Ther 1995;6:41-53.
43. [43] Pastore C, Feldman LJ, Perricaudet M, Steg PG. Intraluminal delivery of a pluronic gel enhances adenovirus-mediated arterial gene transfer: a morphometric study. Circulation 1994;90:I-517( Abstract).
44. [44] Maillard L, Ziol M, Le Feuvre C, et al. Improved efficiency of percutaneous adenoviral-mediated arterial gene transfer by pre-treatment with elastase. J Am Coll Cardiol 1996:in press(Abstract).
45. [45] Yang Y, Nunes FA, Berencsi K, Furth EE, Gönczöl E, Wilson JM. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc Natl Acad Sci USA 1994;91:4407-4411.
46. [46] Newman KD, Dunn PF, Owens JW, et al. Adenovirus-mediated gene transfer into normal rabbit arteries results in prolonged vascular cell activation, inflammation, and neointimal hyperplasia. J Clin Invest 1995;96:2955-2965.
47. [47] Knowles MR, Hohneker KW, Zhou Z, et al. A controlled study of adenoviral-mediated gene transfer in the nasal epithelium of patients with cystic fibrosis. N Engl J Med 1995;333:823-831.
48. [48] Zabner J, Petersen D, Puga A, et al. Safety and efficacy of repetitive adenovirus-mediated transfer of CFTR cDNA to airway epithelia of primates and cotton rats. Nature Genet 1994;6:75-83.
49. [49] Yang Y, Li Q, Ertl HCJ, Wilson JW. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J Virol 1995;69:2004-2015.
50. [50] Daï Y, Schwarz HM, Gu D, Zhang W-W, Sarvetnick N, Verma IM. Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: tolerization of factor IX and vector antigens allows for long-term expression. Proc Natl Acad Sci USA 1995;92:1401-1405.
51. [51] Engelhardt JF, Ye X, Doranz B, Wilson JM. Ablation of E2A in recombinant adenoviruses improves transgene persistence and decreases inflammatory response in mouse liver. Proc Natl Acad Sci USA 1994:91:6196-6200.
52. [52] Yeh P, Dedieu J-F, Orsini C, Vigne E, Denefle P, Perricaudet P. Efficient dual transcomplementation of adenovirus E1 and E4 regions from a 293-derived cell line expressing a minimal E4 functional unit. J Virol 1996;70:559-565.
53. [53] Clowes A, Reidy M, Clowes M. Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest 1983;49:327-333.
54. [54] Simons M, Edelman ER, DeKeyser J-L, Langer R, Rosenberg RD. Antisense c-myb oligonucleotides inhibit intimal arterial smooth muscle cell accumulation in vivo. Nature 1992;359:67-70.
55. [55] Chapman GD, Lim CS, Gammon RS, et al. Gene transfer into coronary arteries of intact animals with a percutaneous balloon catheter. Circ Res 1992;71:27-33.
56. [56] Riessen R, Rahimizadeh H, Takeshita S, Gal D, Barry JJ, Isner JM. Successful vascular gene transfer using a hydrogel coated balloon angioplasty catheter. Hum Gene Ther 1993;4:749-758.
57. [57] Felgner PL, Gadek TR, Holm M, et al. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci USA 1987;84:7413-7417.
58. [58] Takeshita S, Gal D, Leclerc G, et al. Increased gene expression after liposome-mediated arterial gene transfer associated with intimal smooth muscle cell proliferation. In vitro and in vivo findings in a rabbit model of vascular injury. J Clin Invest 1994;93:652-661.
59. [59] Lim CS, Chapman GD, Gammon JB, et al. Direct in vivo gene transfer into the coronary and peripheral vasculatures of the intact dog. Circulation 1991;83:2007-2011.
60. [60] Leclerc G, Gal D, Takeshita S, Nikol S, Weir L, Isner JM. Percutaneous arterial gene transfer in a rabbit model. Efficiency in normal and balloon-dilated atherosclerotic arteries. J Clin Invest 1992;90:936-944.
61. [61] Nabel EG, Gordon D, Xang ZY, et al. Gene transfer in vivo with DNA-liposome complexes: lack of autoimmunity and gonadal localization. Hum Gene Ther 1992;3:649-656.
62. [62] Zhu N, Liggit D, Liu Y, Debs R. Systemic gene expression after intravenous DNA delivery into adult mice. Science 1993;261:209-211.
63. [63] Pastore CJ, Feldman LJ, Losordo DW, Gorman C, Kim EA, Isner JM. Novel liposome mediates preferential gene transfer of the vascular endothelium in vivo. Circulation 1995;92:1-382(Abstract).
64. [64] Michael SI, Curiel DT. Strategies to achieve targeted gene delivery via the receptor-mediated endocytosis pathway. Gene Ther 1994;1:223-232.
65. [65] Wagner E, Zatloukal K, Cotten M, et al. Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes. Proc Natl Acad Sci USA 1992;89:6099-6103.
66. [66] Kupfer JM, Ruan XM, Liu G, Matloff J, Forrester J, Chaux A. High-efficiency gene transfer to autologous rabbit jugular vein grafts using adenovirus-transferrin/polylysine-DNA complexes. Hum Gene Ther 1994;5:1437-1443.
67. [67] Morishita R, Gibbons G, Kaneda Y, Ogihara T, Dzau V. Novel and effective gene transfer technique for study of vascular renin-angiotensin system. J Clin Invest 1993;91:2580-2585.
68. [68] Morishita R, Gibbons GH, Ellison KE, et al. Single intraluminal delivery of antisense cdc2 kinase and proliferating-cell nuclear antigen oligonucleotides results in chronic inhibition of neointimal hyperplasia. Proc Natl Acad Sci USA 1993;90:8474-8478.
69. [69] von der Leyen HE, Gibbons GH, Morishita R, et al. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci USA 1995;92:1137-1141.
70. [70] Barbee RW, Stapleton DD, Perrry BD, et al. Prior arterial injury enhances luciferase expression following in vivo gene transfer. Biochem Biophys Res Commun 1993;190:70-78.
71. [71] Wilensky RL, March KL, Gradus-Pizlo I, Spaedy AJ, Hathaway DR. Methods and devices for local drug delivery in coronary and peripheral arteries. Trends Cardiovasc Med 1993;3:163-170.
72. [72] Lincoff AM, Topol EJ, Ellis SG. Local drug delivery for the prevention of restenosis. Fact, fancy, and future. Circulation 1994;90:2070-2084.
73. [73] March KL. Derivation of smooth muscle cell lineages from transgenic mice expressing a temperature-sensitive simian virus 40 T-antigen targeted to smooth muscle: conditional growth and phenotype. Circulation 1994;90:1-626(Abstract).
74. [74] Harats D, Kurihara H, Belloni P, et al. Targeting gene expression to the vascular wall in transgenic mice using the murine preproendothelin-1 promoter. J Clin Invest 1995;95:1335-1344.
75. [75] Wu GY, Zhan P, Sze LL, Rosenberg AR, Wu CH. Incorporation of adenovirus into a ligand-based DNA carrier system results in retention of original receptor specificity and enhances targeted gene expression. J Biol Chem 1994;269:11542-11546.
76. [76] Camenzind E, Kint P-P, Di Mario C, et al. Intracoronary heparin delivery in humans. Circulation 1995;92:2463-2472.
77. [77] Fernandez-Ortiz A, Meyer BJ, Mailhac A, et al. A new approach for local intravascular drug delivery. Iontophoretic balloon. Circulation 1994;89:1518-1522.
78. [78] Clowes AW, Reidy MA, Clowes MM. Mechanisms of stenosis after arterial injury. Lab Invest 1983;49:208-215.
79. [79] Lafont A, Guzman LA, Whitlow PL, Goormastic M, Cornhill JF, Chisolm GM. Restenosis after experimental angioplasty. Intimal, medial, and adventitial changes associated with constrictive remodeling. Circ Res 1995;76:996-1002.
80. [80] Post MJ, Borst C. Kuntz RE. The relative importance of arterial remodeling compared with intimal hyperplasia in lumen renarrowing after balloon angioplasty. A study in the normal rabbit and the hypercholesterolemic Yucatan micropig. Circulation 1994;89:2816-2821.
81. [81] Kakuta T, Currier JW, Haudenschild CC, Ryan TJ, Faxon DP. Differences in compensatory vessel enlargement, not intimal formation, account for restenosis after angiolasty in the hypercholesterolemic rabbit model. Circulation 1994;89:2809-2815.
82. [82] Gertz SD, Gimple LW, Banai S. et al. Geometric remodeling is not the principal pathogenetic process in restenosis after balloon angioplasty. Evidence from correlative angiographic-histomorphometric studies of atherosclerotic arteries in rabbits. Circulation 1994;90:3001-3008.
83. [83] Lafont A, Guerot C, Lemarchand P. Which gene for which restenosis? Lancet 1995;346:1442-1443.
84. [84] Kimura T, Kaburagi S, Tashima Y, Nobuyoshi M, Mintz GS, Popma JM. Geometric remodeling and intimal regrowth as mechanisms of restenosis: observations from serial ultrasound analysis of restenosis (SURE) trial. Circulation 1995;92:1-76(Abstract).
85. [85] Braden GA, Young TM, Utley L, Kutcher MA, Applegate RL, Herrington DM. Fibro-intimal hyperplasia is the predominant mechanism of late lumen loss in symptomatic patients with coronary restenosis. Circualtion 1995;92:1-148 (Abstract).
86. [86] Gibbons GH, Dzau VJ. The emerging concept of vascular remodeling. N Engl J Med 1994;330:1431-1438.
87. [87] Epstein SE, Speir E, Unger EF, Guzman RJ, Finkel T. The basis of molecular strategies for treating coronary restenosis after angioplasty. J Am Coll Cardiol 1994;23:1278-1288.
88. [88] Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993;362:801-809.
89. [89] Borrelli E, Heyman ER, Hsi M, Evans RM. Targeting of an inducible toxic phenotype in animal cells. Proc Natl Acad Sci USA 1988;85:7572-7576.
90. [90] Culver KW, Ram Z, Wallvridfe S, Ishii H, Oldfield EH, Blaese RM. In vivo gene transfer with retroviral vector-producer cells for treatment of experimental brain tumors. Science 1992;256:1550-1552.
91. [91] Guzman RJ, Hirschowitz EA, Brody SL, Crystal RG, Epstein SE, Finkel T. In vivo suppression of injury-induced vascular smooth muscle cell accumulation using adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene. Proc Natl Acad Sci USA 1994;91:10732-10736.
92. [92] Ohno T, Gordon D, San H, et al. Gene therapy for vascular smooth muscle cell proliferation after arterial injury. Science 1994;265:781-784.
93. [93] Simari RD, San H, Ohno T, Gordon D, Nabel GJ, Nabel EG. Regulation of cellular proliferation and intimal formation following balloon injury in hyperlipidemic rabbit arteries. Circulation 1995;92:1-501(Abstract).
94. [94] Tahlil O, Branellec D, Aubailly N, et al. Reduction of restenosis after angioplasty by gene therapy with HSV-tk and ganciclovir. Results from a double injury model in the hypercholesterolemic rabbit. Circulation 1995;92:1-295(Abstract).
95. [95] Epstein SE, Speir E, Finkel T. Do antisense approaches to the problem of restenosis make sense? Circulation 1993;88:1351-1354.
96. [96] Bennett MR, Schwartz SM. Antisense therapy for angioplasty restenosis. Some critical considerations. Circulation 1995;92:1981-1993.
97. [97] Bennett MR, Anglin S, McEwan JR, Jagoe R, Newby AC, Evan G. Inhibition of vascular smooth muscle cell proliferation in vitro and in vivo by c-myc antisense oligodeoxynucleotides. J Clin Invest 1994;93:820-828.
98. [98] Stein CA, Cheng Y-C. Antisense oligonucleotides as therapeutic agents. Is the bullet really magical? Science 1993;261:1004-1012.
99. [99] Villa AE, Guzman LA, Poptic EJ, et al. Effects of antisense c-myb oligonucleotides on vascular smooth muscle cell proliferation and reponse to vessel wall injury. Circ Res 1995;76:505-513.
100. [100] Chang MW, Barr E, Seltzer J, et al. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the retinoblastoma gene product. Science 1995;267:518-522.
101. [101] Chang MW, Barr E, Lu MM, Barton K, Leiden JM. Adenovirus-mediated over-expression of the cyclin/cyclin-dependent kinase inhibitor, p21 inhibits vascular smooth muscle cell proliferation and neointima formation in the rat carotid artery model of balloon angioplasty. J Clin Invest 1995:96:2260-2268.
102. [102] Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989;83:1774-1777.
103. [103] Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med 1993;329:2002-2012.
104. [104] Hamon M, Vallet B, Bauters C, et al. Long-term oral administration of L-arginine reduces intimal thickening and enhances neoendothelium-dependent acethylcholine-induced relaxation after arterial injury. Circulation 1994;90:1357-1362.
105. 1 transition in vascular smooth muscle cells. Mol Cell Biol 1993;13:3722-3733.
106. [106] Weir L, Chen D, Pastore C, Kearney M, Isner JM, Walsh K. Gax is rapidly down-regulated in rat carotid arteries following balloon injury: in vivo demonstration of a growth-arrest transcription factor. Circulation 1994;90:1-511(Abstract).
107. [107] Branellec D, Pastore C, Dedieu J-F. et al. A recombinant adenovirus encoding gax can efficiently block vascular smooth muscle cell proliferation. Circulation 1995;92:1-634(Abstract).
108. [108] Ip JH, Fuster V, Israel D, Badimon L, Badimon J, Chesebro JH. The role of platelets, thrombin, and hyperplasia in restenosis after coronary angioplasty. J Am Coll Cardiol 1991;16:77B-88B.
109. [109] McNamara CA, Sarembock IJ, Gimple LW, Fenton JW, Coughlin SR, Owens GK. Thrombin stimulates proliferation of cultured rat aortic smooth muscle cells by a proteolytically activated receptor. J Clin Invest 1993;91:94-98.
110. [110] Schwartz RS, Holmes DR, Topol EJ. The restenosis paradigm revisited: an alternative proposal for cellular mechanisms. J Am Coll Cardiol 1992;20:1284-1296.
111. [111] Feldman LJ, Isner JM. Gene therapy for the vulnerable plaque. J Am Coll Cardiol 1995;26:826-835.
112. [112] Zoldhelyi P, McNatt J, Xu X-M, et al. Prevention of arterial thrombosis by adenovirus-mediated transfer of cyclooxygenase gene. Circulation 1996;93:10-17.
113. [113] Asahara T, Bauters C, Pastore C, et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation 1995;91:2793-2801.
114. [114] Clowes AW, Collazo RE, Karnovsky MJ. A morphologic and permeability study of luminal smooth muscle cells after arterial injury in the rat. Lab Invest 1978;39:141-150.
115. [115] Scott-Burden T, Vanhoutte PM. The endothelium as a regulator of vascular smooth muscle proliferation. Circulation 1993;87(suppl V):V-51-V-55.
116. [116] Takeshita S, Zheng LP, Asahara T, et al. In vivo evidence of enhanced angiogenesis following direct arterial gene transfer of the plasmid encoding vascular endothelial growth factor. Circulation 1994;88:1-476(Abstract).
117. [117] Isner JM, Walsh K, Symes J, et al. Arterial gene therapy for therapeutic angiogenesis in patients with peripheral artery disease. Circulation 1995;91:2687-2691.
118. [118] Shi Y, Pieniek M, Fard A, O'Brien J, Mannion JD, Zalewski A. Adventitial remodeling after coronary arterial injury. Circulation 1996;93:340-348.
119. [119] Fischman D, Leon M, Baim D, et al. A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease. N Engl J Med 1994;331:496-501.
120. [120] Serruys PW, de Jaegere P, Kiemeneij F, et al. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. N Engl J Med 1994;331:489-495.
121. [121] Serruys PW, Emanuelsson H, van der Giessen W, et al. Heparincoated Palmaz-Schatz stents in human coronary arteries. Early outcome of the Benestent-II pilot study. Circulation 1996;93:412-422.