Insights into the molecular pathogenesis of atherosclerosis and therapeutic strategies using gene transfer

Vascular Medicine

Volumn 5, Issue 1, 2000, Pages 41-48

  Hiltunen, Mikko O ^a   Turunen, Mikko P ^a   Laitinen, Marja ^a   Ylä Herttuala, Seppo ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Atherogenesis; Gene transfer; Review

Indexed keywords

ANGIOPOIETIN 1; NITRIC OXIDE; PLASMID DNA; PROSTACYCLIN; TUMOR MARKER; VASCULOTROPIN;

ARTICLE; ATHEROSCLEROSIS; CLINICAL TRIAL; EXPRESSION VECTOR; FLUOROSCOPY; GENE THERAPY; GENE TRANSFER; HEART MUSCLE ISCHEMIA; HUMAN; HYPERLIPIDEMIA; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RESTENOSIS; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

EID: 0034058830     PISSN: 1358863X     EISSN: None     Source Type: Journal    
DOI: 10.1177/1358836x0000500107     Document Type: Article

References (129)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993; 362: 801-809.
2. Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL. Beyond cholesterol. Modifications of low-density lipoprotein that increase its alherogenicity. N Engl J Med 1989; 320: 915-24.
3. Ylä-Herttuala S, Luoma J, Kallionpää H, Laukkanen M. Lehtolainen P, Viita H. Pathogenesis of atherosclerosis. Maturitas 1996; 23 (suppl.): S47-S49.
4. Friedmann T. Approaches to gene therapy of complex multigenic diseases: cancer as a model and implications for cardiovascular disease and diabetes. Ann Med 1992; 24: 411-17.
5. Libby P, Schwartz D, Brogi E, Tanaka H, Clinton SK. A cascade model for restenosis. A special case of atherosclerosis progression. Circulation 1992; 86: III47-III52.
6. 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. Benestent Study Group. N Engl J Med 1994; 331: 489-95.
7. Ohno T, Gordon D. San H et al. Gene therapy for vascular smooth muscle cell proliferation after arterial injury. Science 1994; 265: 781-84.
8. Chang MW, Barr E, Seltzer J et al. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the relinoblastoma gene product. Science 1995; 267: 518-22.
9. Pollman MJ, Hall JL, Mann MJ, Zhang L, Gibbons GH. Inhibition of neointimal cell bcl-x expression induces apoptosis and regression of vascular disease. Nut Med 1998; 4: 222-27.
10. 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: 10732-36.
11. Muller DW. The role of proto-oncogenes in coronary restenosis. Prog Cardiovasc Dis 1997; 40: 117-28.
12. Mann MJ, Whittemore AD, Donaldson MC et al. Ex-vivo gene therapy of human vascular bypass grafts with E2F decay: the PREVENT single-centre, randomised, controlled trial. Lancet 1999; 354: 1493-98.
13. Skopicki HA, Lyons GE, Schatteman G et al. Embryonic expression of the Gax homeodomain protein in cardiac, smooth, and skeletal muscle [see comments]. Circ Res 1997; 80: 452-62.
14. Smith RC, Branellec D, Gorski DH et al. p21CIP1-mediated inhibition of cell proliferation by overexpression of the gax homeodomain gene. Genes Dev 1997; 11: 1674-89.
15. Morishita R, Higaki J, Tomita N, Ogihara T. Application of transcription factor 'decoy' strategy as means of gene therapy and study of gene expression in cardiovascular disease. Circ Res 1998; 82: 1023-28.
16. Laitinen M, Pakkanen T, Donetti E et al. Gene transfer into the carotid artery using an adventitial collar: comparison of the effectiveness of the plasmid-liposorne complexes, retroviruses, pseudotyped retroviruses, and adenoviruses. Hum Gene Ther 1997; 8: 1645-50.
17. Steg PG, Feldman LJ, Scoazec JY et al. Arterial gene transfer to rabbit endothelial and smooth muscle cells using percutaneous delivery of an adenoviral vector. Circulation 1994; 90: 1648-56.
18. 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: 2260-68.
19. Chen SJ, Wilson JM, Muller DW. Adenovirus-mediated gene transfer of soluble vascular cell adhesion molecule to porcine interposition vein grafts. Circulation 1994; 89: 1922-28.
20. 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: 2662-71.
21. Harrell RL, Rajanayagam S, Doanes AM et al. Inhibition of vascular smooth muscle cell proliferation and neointimal accumulation by adenovirus-mediated gene transfer of cytosine deaminase. Circulation 1997; 96: 621-27.
22. Guzman RJ, Lemarchand P, Crystal RG, Epstein SE, Finkel T. Efficient and selective adenovirus-mediated gene transfer into vascular neointima. Circulation 1993; 88: 2838-48.
23. Ylä-Herttuala S, Luoma J. Viita H, Hiltunen T, Sisto T, Nikkari T. Transfer of 15-lipoxygenase gene into rabbit iliac arteries results in the appearance of oxidation-specific lipid-protein adducts characteristic of oxidized low density lipoprotein. J Clin Invest 1995; 95: 2692-98.
24. 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: 1137-41.
25. 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. Arterioscter Thromb 1994; 14: 148-61.
26. Nabel EG, Plautz G, Nabel GJ. Site-specific gene expression in vivo by direct gene transfer into the arterial wall. Science 1990; 249: 1285-88.
27. Nabel EG, Nabel GJ. Complex models for the study of gene function in cardiovascular biology. Annu Rev Physiol 1994; 56: 741-61.
28. Laitinen M, Mäkinen K, Manninen H et al. Adenovirus-mediated gene transfer to lower limb artery of patients with chronic critical leg ischemia. Hum Gene Ther 1998; 9: 1481-86.
29. 165 after intramuscular gene transfer promotes collateral vessel development in patients with critical limb ischemia. Circulation 1998; 97: 1114-23.
30. Takeshita S, Tsurumi Y, Couffinahl T et al. Gene transfer of naked DNA encoding for three isofonns of vascular endothelial growth factor stimulates collateral development in vivo. Lab Invest 1996; 75: 487-501.
31. 165, in patient with ischaemic limb. Lancet 1996; 348: 370-74.
32. Tursz T, Cesne AL, Baldeyrou P et al. Phase I study of a recombinant adenovirus-mediated gene transfer in lung cancer patients. J Natl Cancer Inst 1996; 88: 1857-63.
33. Bellon G, Michel-Calemard L, Thouvenot D et al. Aerosol administration of a recombinant adenovirus expressing CFTR to cystic fibrosis patients: a phase 1 clinical trial. Hum Gene Ther 1997; 8: 15-25.
34. Puumalainen AM, Vapalahti M, Agrawal RS et al. Beta-galactosidase gene transfer to human malignant glioma in vivo using replication-deficient retroviruses and adenoviruses. Hum Gene Ther 1998; 9: 1769-74.
35. Turunen MP, Hiltunen MO, Ruponen M et al. Efficient adventitial gene delivery to rabbit carotid artery with cationic polymer-plasmid complexes. Gene Ther 1999; 6: 6-11.
36. Ylä-Herttuala S. Vascular gene transfer. Curr Opin Lipidol 1997; 8: 72-76.
37. Ooboshi H, Toyoda K, Faraci FM, Lang MG, Heistad DD. Improvement of relaxation in an atherosclerotic artery by gene transfer of endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 1998; 18: 1752-58.
38. Shears LL, Kibbe MR, Murdock AD et al. Efficient inhibition of intimal hyperplasia by adenovirus-mediated inducible nitric oxide synthase gene transfer to rats and pigs in vivo. J Am Coll Surg 1998; 187: 295-306.
39. Chang MW, Ohno T, Gordon D et al. Adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene inhibits vascular smooth muscle cell proliferation and neointima formation following balloon angioplasty of the rat carotid artery. Mol Meet 1995; 1: 172-81.
40. Laitinen M, Ylä-Herttuala S. Adventitial gene transfer to arterial wall. Pharmacol Res 1998; 37: 251-54.
41. Wilson JM. Adenoviruses as gene-delivery vehicles. N Engl J Med 1996; 334: 1185-87.
42. Clesham GJ, Adam PJ, Proudfoot D. Flynn PD, Efstathiou S, Weissberg PL. High adenoviral loads stimulate NF kappaB-dependent gene expression in human vascular smooth muscle cells. Gene Ther 1998; 5: 174-80.
43. Ye X. Robinson MB, Batshaw ML, Furth EE, Smith I, Wilson JM. Prolonged metabolic correction in adult ornithine transcarbamylase-deficient mice with adenoviral vectors. J Biol Chem 1996; 271: 3639-46.
44. O'Neal WK, Zhou H, Morral N et al. Toxicological comparison of E2a-deleted and first-generation adenoviral vectors expressing alpha1-antitrypsin after systemic delivery. Hum Gene Ther 1998; 9: 1587-98.
45. Morgan RA, Anderson WF. Human gene therapy. Annu Rev Biochem 1993; 62: 191-217.
46. Yee JK, Miyanohara A, LaPorte P, Bouic K, Burns JC, Friedmann T. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc Natl Acad Sci USA 1994; 91: 9564-68.
47. Linden RM, Ward P, Giraud C, Winocour E, Berns KI. Site-specific integration by adeno-associated virus. Proc Natl Acad Sci USA 1996; 93: 11 288-94.
48. Marconi P, Krisky D, Oligino T et al. Replication-defective herpes simplex virus vectors for gene transfer in vivo. Proc Natl Acad Sci USA 1996; 93: 11319-20.
49. Wang S, Vos JM. A hybrid herpesvirus infectious vector based on Epstein-Barr virus and herpes simplex virus type 1 for gene transfer into human cells in vitro and in vivo. J Virol 1996; 70: 8422-30.
50. Kafri T, Blömer U, Peterson DA, Gage FH, Verma IM. Sustained expression of genes delivered directly into liver and muscle by lenti-viral vectors. Nat Genet 1997; 17: 314-17.
51. Laitinen M, Makinen K, Manninen H et al. Adenovirus-mediated gene transfer to lower limb artery of patients with chronic critical leg ischemia. Hum Gene Ther 1998; 9: 1481-86.
52. 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: 2190-97.
53. Schwartz SM, deBlois D, O'Brien ER. The intima. Soil for atherosclerosis and restenosis. Circ Res 1995; 77: 445-65.
54. Nikol S, Huehns TY, Hofling B. Molecular biology and post-angioplasty restenosis. Atherosclerosis 1996; 123: 17-31.
55. Landau C, Lange RA, Hillis LD. Percutaneous transluminal coronary angioplasty. N Engl J Med 1994; 330: 981-93.
56. Serruys PW, Rutsch W, Heyndrickx GR et al. Prevention of restenosis after percutaneous transluminal coronary angioplasty with thromboxane A2-receptor blockade. A randomized, double-blind, placebo-controlled trial. Coronary Artery Restenosis Prevention on Repeated Thromboxane-Antagonism Study (CARPORT). Circulation 1991; 84: 1568-80.
57. Herrman JP, Hermans WR, Vos J, Serruys PW. Pharmacological approaches to the prevention of restenosis following angioplasty. The search for the Holy Grail? (Part I). Drugs 1993; 46: 18-52.
58. Popma JJ, Califf RM, Topol EJ. Clinical trials of restenosis after coronary angioplasty. Circulation 1991; 84: 1426-36.
59. Califf RM. Restenosis: the cost to society. Am Heart J 1995; 130: 680-84
60. Grondin CM, Campeau L, Lesperance J, Enjalbert M. Bourassa MG. Comparison of late changes in internal mammary artery and saphenous vein grafts in two consecutive series of patients 10 years after operation. Circulation 1984; 70: 1208-12.
61. Narins CR, Holmes DRJ, Topol EJ. A call for provisional stenting: the balbon is back! Circulation 1998; 97: 1298-305.
62. Kornowski R, Hong MK, Tio FO, Bramwell O, Wu H, Leon MB. Instent restenosis: contributions of inflammatory responses and arterial injury to neointimal hyperplasia. J Am Coll Cardiol 1998; 31: 224-30.
63. Bittl JA. Advances in coronary angioplasty [published erratum appears in N Engl J Med 1997; 336: 670]. N Engl J Med 1996; 335: 1290-302.
64. Libby P. Gene therapy of restenosis - Promise and perils. Circ Res 1998; 82: 404-406.
65. Back S, March KL. Gene therapy for restenosis - Getting nearer the heart of the matter. Circ Res 1998; 82: 295-305.
66. Deyoung MB, Dichek DA. Gene therapy for restenosis - Are we ready? Circ Res 1998; 82: 306-13.
67. Camenzind E, Kint PP, Di Mario C et al. Intracoronary heparin delivery in humans. Acute feasibility and long-term results. Circulation 1995; 92: 2463-72.
68. Campbell GR, Chamley-Campbell JH. Invited review: the cellular pathobiology of atherosclerosis. Pathology 1981; 13: 423-40.
69. Marin ML, Gordon RE, Veith FJ, Tulchin N, Panetta TF. Distribution of c-myc oncoprotein in healthy and atherosclerotic human carotid arteries. J Vasc Surg 1993; 18: 170-76.
70. Koster R, Windstetter U, Uberfuhr P, Baumann G, Nikol S, Hofling B. Enhanced migratory activity of vascular smooth muscle cells with high expression of platelet-derived growth factor A and B. Angiology 1995; 46: 99-106.
71. Shi Y, Hutchinson HG, Hall DJ, Zalewski A. Downregulation of c-myc expression by antisense oligonucleotides inhibits proliferation of human smooth muscle cells. Circulation 1993; 88: 1190-95.
72. Steg PG, Tahlil O, Aubailly N et al. Reduction of restenosis after angioplasty in an atheromatous rabbit model by suicide gene therapy. Circulation 1997; 96: 408-11.
73. Suzuki J, Isobe M. Morishita R et al. Prevention of graft coronary arteriosclerosis by antisense cdk2 kinase oligonucleotide [see comments]. Nat Med 1997; 3: 900-903.
74. Baker AH, Zaltsman AB, George SJ, Newhy AC. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. TIMP-3 promotes apoplosis. J Clin Invest 1998; 101: 1478-87.
75. Kullo IJ, Schwartz RS, Pompili VJ et al. Expression and function of recombinant endothelial NO synthase in coronary artery smooth muscle cells. Arterioscler Thromb Vasc Biol 1997; 17: 2405-12.
76. Rutherford C, Martin W, Salame M, Carrier M, Anggard E, Ferns G. Substantial inhibition of neo-intimal response to balloon injury in the rat carotid artery using a combination of antibodies to platelet-derived growth factor-BB and basic tibroblast growth factor. Atherosclerosis 1997; 130: 45-51.
77. Laitinen M, Zachary I, Breier G et al. Vegf gene transfer reduces intimai thickening via increased production of nitric oxide in carotid arteries. Hum Gene Ther 1997; 8: 1737-44.
78. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA 1973; 70: 1753-56.
79. Penn A, Garte SJ, Warren L, Nesta D, Mindich B. Transforming gene in human atherosclerotic plaque DNA. Proc Natl Acad Sci USA 1986; 83: 7951-55.
80. Hartwell L. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 1992; 71: 543-46.
81. Spandidos DA, Ergazaki M, Arvanitis D, Kiaris H. Microsatellite instability in human atherosclerotic plaques. Biochem Biophys Res Commun 1996; 220: 137-40.
82. Hatzistamou J, Kiaris H, Ergazaki M, Spandidos DA. Loss of heterozygosity and microsatellite instability in human atherosclerotic plaques. Biochem Biophys Res Commun 1996; 225: 186-90.
83. McCaffrey TA, Du B, Consigli S et al. Genomic instability in the type II TGF-betal receptor gene in atherosclerotic and restenotic vascular cells [see comments]. J Clin Invest 1997; 100: 2182-88.
84. Greger V, Passarge E, Hopping W, Messmer E, Horsthemke B. Epigenetic changes may contribute to the formation and spontaneous regression of retinoblastoma. Hum Genet 1989; 83: 155-58.
85. Goelz SE, Vogelstein B, Hamilton SR, Feinberg AP. Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 1985; 228: 187-90.
86. Gama-Sosa MA, Slagel VA, Trewyn RW et al. The 5-methylcytosine content of DNA from human tumors. Nucleic Acids Res 1983; 11: 6883-94.
87. Feinberg AP. Genomic imprinting and gene activation in cancer [news: comment]. Nat Genet 1993; 4: 110-13.
88. Counts JL, Goodman JI. Alterations in DNA methylation may play a variety of roles in carcinoaenesis. Cell 1995; 83: 13-15.
89. Laukkanen MO, Aittomaki S, Hiltunen MO et al. Local hypomethylation in atherosclerosis found in rabbit ec-sod gene. Arterioscler Thromb Vasc Biol 1999; 19(9): 2171-8.
90. Ferrara N, Bunting S. Vascular endothelial growth factor, a specific regulator of angiogenesis. Curr Opin Nephrol Hypertens 1996; 5: 35-44.
91. Murohara T, Horowitz JR, Silver M et al. Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation 1998; 97: 99-107.
92. Pedram A, Razandi M, Levin ER. Extracellular signal-regulated protein kinase/Jun kinase cross-talk underlies vascular endothelial cell growth factor-induced endothelial cell proliferation. J Biol Chem 1998; 273: 26722-28.
93. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1995; 1: 1024-28.
94. Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem 1998; 273: 13313-16.
95. Wheeler-Jones C, Abu-Ghazaleh R, Cospedal R, Houliston RA, Martin J, Zachary I. Vascular endothelial growth factor stimulates prostacyclin production and activation of cytosolic phospholipase A2 in endothelial cells via p42/p44 mitogen-activated protein kinase. FEBS Lett 1997; 420: 28-32.
96. Asahara T, Bauters C, Pastore C et al. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimai hyperplasia in balloon-injured rat carotid artery. Circulation 1995; 91: 2793-801.
97. Burke PA, Lehmann-Bruinsma K, Powell JS. Vascular endothelial growth factor causes endothelial proliferation after vascular injury. Biochem Biophys Res Commun 1995; 207: 348-54.
98. Cao Y, Linden P. Farnebo J et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 1998; 95: 14 389-94.
99. Tsurumi Y, Kearney M. Chen DF et al. Treatment of acute limb ischemia by intramuscular injection of vascular endothelial growth factor gene. Circulation 1997; 96: 382-88.
100. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 1995; 108: 2369-79.
101. Nicosia RF. What is the role of vascular endothelial growth factor-related molecules in tumor angiogenesis? Am J Pathol 1998; 153: 11-16.
102. Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev 1997; 18: 4-25.
103. Giordano FJ, Ping P, McKirnan MD et al. Intracoronary gene transfer of fibroblast growth factor-5 increases blood flow and contractile function in an ischemic region of the heart. Nat Med 1996; 2: 534-39.
104. Ueno H, Li JJ, Masuda S, Qi Z, Yamamoto H, Takeshita A. Adenovirus-mediated expression of the secreted form of basic fibroblast growth factor (FGF-2) induces cellular proliferation and angiogenesis in vivo. Arterioscler Thromb Vasc Biol 1997; 17: 2453-60.
105. Tabata H, Silver M, Isner JM. Arterial gene transfer of acidic fibroblast growth factor for therapeutic angiogenesis in vivo: critical role of secretion signal in use of naked DNA [published erratum appears in Cardiovasc Res 1998; 38: 272]. Cardiovasc Res 1997; 35: 470-79.
106. Nabel EG, Yang ZY, Plautz G et al. Recombinant fibroblast growth factor-1 promotes intimal hyperplasia and angiogenesis in arteries in vivo. Nature 1993; 362: 844-46.
107. Schumacher B, Pecher P, von Specht BU, Stegmann T. Induction of neoangiogenesis in ischemic myocardium by human growth factors: first clinical results of a new treatment of coronary heart disease. Circulation 1998; 97: 645-50.
108. Davis S, Aldrich TH, Jones PF et al. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 1996; 87: 1161-69.
109. Suri C, Jones PF, Patan S et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996; 87: 1171-80.
110. Maisonpierre PC, Suri C, Jones PF et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 1997; 277: 55-60.
111. Van Belle E, Witzenbichler B, Chen D et al. Potentiated angiogenic effect of scatter factor/hepatocyte growth factor via induction of vascular endothelial growth factor: the case for paracrine amplification of angiogenesis. Circulation 1998; 97: 381-90.
112. Lovich MA, Edelman ER. Mechanisms of transmural heparin transport in the rat abdominal aorta after local vascular delivery. Circ Res 1995; 77: 1143-50.
113. Lovich MA, Brown L, Edelman ER. Drug clearance and arterial uptake after local perivascular delivery to the rat carotid artery. J Am Coll Cardiol 1997; 29: 1645-50.
114. Huth F, Kojimahara M, Franken T, Rhedin P, Rosenbauer KA. Aortic alterations in rabbits following sheathing with silastic and polyethylene tubes. Curr Top Pathol 1975; 60: 1-32.
115. Booth RF, Martin JF, Honey AC, Hassall DG, Beesley JE, Moncada S. Rapid development of atherosclerotic lesions in the rabbit carotid artery induced by perivascular manipulation. Atherosclerosis 1989; 76: 257-68.
116. Kozarsky KF, McKinley DR, Austin LL, Raper SE, Stratford-Perricaudet LD. Wilson JM. In vivo correction of low density lipoprotein receptor deficiency in the Watanabe heritable hyperlipidemic rabbit with recombinant adenoviruses. J Biol Chem 1994; 269: 13695-702.
117. Pakkanen TM, Laitinen M, Hippelainen M et al. Enhanced plasma cholesterol lowering effect of retrovirus-mediated LDL receptor gene transfer to WHHL rabbit liver after improved surgical technique and stimulation of hepatocyte proliferation by combined partial liver resection and thymidine kinase ganciclovir treatment. Gene Ther 1999; 6: 34-41.
118. Grossman M, Rader DJ, Muller DW et al. A pilot study of ex vivo gene therapy for homozygous familial hypercholesterolaemia. Nat Med 1995; 1: 1148-54.
119. Benoit P, Emmanuel F, Caillaud JM et al. Somatic gene transfer of human ApoA-I inhibits atherosclerosis progression in mouse models [see comments]. Circulation 1999; 99: 105-10.
120. Zsigmond E, Kobayashi K, Tzung KW, Li L, Fuke Y, Chan L. Adenovirus-mediated gene transfer of human lipoprotein lipase ameliorates the hyperlipidemias associated with apolipoprotein E and LDL receptor deficiencies in mice. Hum Gene Ther 1997; 8: 1921-33.
121. Tai IT, Sun AM. Microencapsulation of recombinant cells: a new delivery system for gene therapy. FASEB J 1993; 7: 1061-69.
122. Hughes M, Vassilakos A, Andrews DW, Hortelano G, Belmont JW, Chang PL. Delivery of a secretable adenosine deaminase through microcapsules-a novel approach to somatic gene therapy. Hum Gene Ther 1994; 5: 1445-55.
123. Lynch CM, Clowes MM, Osborne WR, Clowes AW, Miller AD. Long-term expression of human adenosine deaminase in vascular smooth muscle cells of rats: a model for gene therapy. Proc Natl Acad Sci USA 1992; 89: 1138-42.
124. Dichek DA, Neville RF, Zwiebel JA, Freeman SM, Leon MB, Anderson WF. Seeding of intravascuiar stents with genetically engineered endothelial cells. Circulation 1989; 80: 1347-53.
125. Rossi FM, Blau HM. Recent advances in inducible gene expression systems. Curr Opin Biotechnol 1998; 9: 451-56.
126. Ylä-Herttuala S, Martin JF. Cardiovascular gene therapy. Lancet 2000; 355: 213-22.
127. Losordo DW, Vale PR, Symes JF et al. Gene therapy for myocardial angiogenesis - initial clinical results with direct myocardial injection of phVEGF(165) as sole therapy for myocardial ischemia. Circulation 1998; 98: 2800-804.
128. 121 cDNA to individuals with clinically significant severe coronary artery disease. Circulation 1999; 100: 468-74.
129. Laham RJ, Selke FW, Edelman ER et al. Local perivascular delivery of basic fibroblast growth factor in patients undergoing coronary bypass surgery: results of a phase I randomized, double-blind, placebo-controlled trial. Circulation 1999; 100: 1865-71.