In vivo adenoviral vector-mediated gene transfer into balloon-injured rat carotid arteries

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Circulation Research. 1993;73:797-807

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In vivo adenoviral vector-mediated gene transfer into balloon-injured rat carotid arteries

SW Lee, BC Trapnell, JJ Rade, R Virmani and DA Dichek
Molecular Hematology Branch, National Heart, Lung, and Blood Institute, Bethesda, Md. 20892.

We studied the ability of adenoviral vectors to achieve gene transfer into injured arteries. A recombinant adenoviral vector expressing a nuclear-targeted beta-galactosidase gene was constructed and infused into balloon-injured rat carotid arteries. Three days after gene transfer, recombinant gene expression was assessed quantitatively by (1) measuring beta-galactosidase antigen and activity in tissue extracts and (2) histochemical staining and counting of cells expressing beta-galactosidase. Exposure of injured carotid arteries to increasing concentrations of the vector (10(8) to 10(10) plaque-forming units per milliliter) resulted in a dose-responsive increase in beta- galactosidase expression, with peak expression of approximately 43 mU or 25 ng beta-galactosidase per vessel. Microscopic examination of histochemically stained arteries demonstrated gene transfer limited to the vascular media; transduced cells were identified immunohistochemically as smooth muscle cells. Counting of both histochemically stained and total nuclei in the media revealed that approximately 30% of the cells in the media of the injured vessels were transduced. Calculations based on both counting cells and on the level of beta-galactosidase expression in tissue extracts suggested the presence of 5000 to 10,000 transduced cells per 10 mm of vessel. Arteries infused with either vehicle only, a control adenoviral vector, or liposomes combined with the vector plasmid contained little or no evidence of beta-galactosidase expression. High levels of in vivo beta- galactosidase expression persisted for at least 7 days after gene transfer but declined significantly by day 14. We conclude that adenoviral vector-mediated gene transfer into the injured rat carotid artery results in efficient gene transfer into the vascular media, with levels of recombinant protein production significantly higher than any previously reported in arterial gene transfer studies. Adenoviral vectors appear to be particularly useful agents for in vivo arterial gene transfer.

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				K.-W. Park, H.-M. Yang, S.-W. Youn, H.-J. Yang, I.-H. Chae, B.-H. Oh, M.-M. Lee, Y.-B. Park, Y.-S. Choi, H.-S. Kim, et al. Constitutively Active Glycogen Synthase Kinase-3{beta} Gene Transfer Sustains Apoptosis, Inhibits Proliferation of Vascular Smooth Muscle Cells, and Reduces Neointima Formation After Balloon Injury in Rats Arterioscler Thromb Vasc Biol, August 1, 2003; 23(8): 1364 - 1369. [Abstract] [Full Text] [PDF]

				S. Fleury, E. Simeoni, C. Zuppinger, N. Deglon, L. K. von Segesser, L. Kappenberger, and G. Vassalli Multiply Attenuated, Self-Inactivating Lentiviral Vectors Efficiently Deliver and Express Genes for Extended Periods of Time in Adult Rat Cardiomyocytes In Vivo Circulation, May 13, 2003; 107(18): 2375 - 2382. [Abstract] [Full Text] [PDF]

				M. Falkenberg, C. Tom, M. B. DeYoung, S. Wen, R. Linnemann, and D. A. Dichek Increased expression of urokinase during atherosclerotic lesion development causes arterial constriction and lumen loss, and accelerates lesion growth PNAS, August 6, 2002; 99(16): 10665 - 10670. [Abstract] [Full Text] [PDF]

				V. Mittoux, S. Ouary, C. Monville, F. Lisovoski, T. Poyot, F. Conde, C. Escartin, R. Robichon, E. Brouillet, M. Peschanski, et al. Corticostriatopallidal Neuroprotection by Adenovirus-Mediated Ciliary Neurotrophic Factor Gene Transfer in a Rat Model of Progressive Striatal Degeneration J. Neurosci., June 1, 2002; 22(11): 4478 - 4486. [Abstract] [Full Text] [PDF]

				E. Cavusoglu, I. Chen, J. Rappaport, and J. D. Marmur Inhibition of Tissue Factor Gene Induction and Activity Using a Hairpin Ribozyme Circulation, May 14, 2002; 105(19): 2282 - 2287. [Abstract] [Full Text] [PDF]

				D. A. Tulis, W. Durante, X. Liu, A. J. Evans, K. J. Peyton, and A. I. Schafer Adenovirus-Mediated Heme Oxygenase-1 Gene Delivery Inhibits Injury-Induced Vascular Neointima Formation Circulation, November 27, 2001; 104(22): 2710 - 2715. [Abstract] [Full Text] [PDF]

				M. B. DeYoung, C. Tom, and D. A. Dichek Plasminogen Activator Inhibitor Type 1 Increases Neointima Formation in Balloon-Injured Rat Carotid Arteries Circulation, October 16, 2001; 104(16): 1972 - 1971. [Abstract] [Full Text] [PDF]

				H. Ooboshi, S. Ibayashi, J. Takada, H. Yao, T. Kitazono, and M. Fujishima Adenovirus-Mediated Gene Transfer to Ischemic Brain : Ischemic Flow Threshold for Transgene Expression Stroke, April 1, 2001; 32(4): 1043 - 1047. [Abstract] [Full Text] [PDF]

				P. Sinnaeve, J.-D. Chiche, Z. Nong, O. Varenne, N. Van Pelt, H. Gillijns, D. Collen, K. D. Bloch, and S. Janssens Soluble Guanylate Cyclase {{alpha}}1 and {beta}1 Gene Transfer Increases NO Responsiveness and Reduces Neointima Formation After Balloon Injury in Rats via Antiproliferative and Antimigratory Effects Circ. Res., January 19, 2001; 88(1): 103 - 109. [Abstract] [Full Text] [PDF]

				S. L. Meyerson, C. L. Skelly, M. A. Curi, and L. B. Schwartz Gene Therapy for Cardiovascular Disease Seminars in Cardiothoracic and Vascular Anesthesia, November 1, 2000; 4(4): 289 - 300. [Abstract] [PDF]

				H. Ishii, M. Yoshida, A. Rosenzweig, M. A. Gimbrone Jr, Y. Yasukochi, and F. Numano Adenoviral transduction of human E-selectin into isolated, perfused, rat aortic segments: an ex vivo model for studying leukocyte-endothelial interactions J. Leukoc. Biol., November 1, 2000; 68(5): 687 - 692. [Abstract] [Full Text]

				S. Wen, D. B. Schneider, R. M. Driscoll, G. Vassalli, A. B. Sassani, and D. A. Dichek Second-Generation Adenoviral Vectors Do Not Prevent Rapid Loss of Transgene Expression and Vector DNA From the Arterial Wall Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1452 - 1458. [Abstract] [Full Text] [PDF]

				R. Agah, K. S. S. Prasad, R. Linnemann, M. T. Firpo, T. Quertermous, and D. A. Dichek Cardiovascular Overexpression of Transforming Growth Factor-{beta}1 Causes Abnormal Yolk Sac Vasculogenesis and Early Embryonic Death Circ. Res., May 26, 2000; 86(10): 1024 - 1030. [Abstract] [Full Text] [PDF]

				D. B. Schneider, G. Vassalli, S. Wen, R. M. Driscoll, A. B. Sassani, M. B. DeYoung, R. Linnemann, R. Virmani, and D. A. Dichek Expression of Fas Ligand in Arteries of Hypercholesterolemic Rabbits Accelerates Atherosclerotic Lesion Formation Arterioscler Thromb Vasc Biol, February 1, 2000; 20(2): 298 - 308. [Abstract] [Full Text] [PDF]

				N. Faraday, J. J. Rade, D. C. Johns, G. Khetawat, S. J. Noga, J. F. DiPersio, Y. Jin, J. L. Nichol, J. S. Haug, and P. F. Bray Ex Vivo Cultured Megakaryocytes Express Functional Glycoprotein IIb-IIIa Receptors and Are Capable of Adenovirus-Mediated Transgene Expression Blood, December 15, 1999; 94(12): 4084 - 4092. [Abstract] [Full Text] [PDF]

				D. K. Das, R. M. Engelman, N. Maulik, J. A. Rousou, J. E. Flack III, and D. W. Deaton Molecular targets of gene therapy Ann. Thorac. Surg., November 1, 1999; 68(5): 1929 - 1933. [Abstract] [Full Text] [PDF]

				G. Vassalli, R. Agah, R. Qiao, C. Aguilar, and D. A. Dichek A Mouse Model of Arterial Gene Transfer : Antigen-Specific Immunity Is a Minor Determinant of the Early Loss of Adenovirus-Mediated Transgene Expression Circ. Res., October 29, 1999; 85 (9): e25 - e32. [Abstract] [Full Text] [PDF]

				J. Raymond, A. C. Desfaits, D. Roy, and J. P. Muizelaar Fibrinogen and Vascular Smooth Muscle Cell Grafts Promote Healing of Experimental Aneurysms Treated by Embolization � Editorial Comment Stroke, August 1, 1999; 30(8): 1657 - 1664. [Abstract] [Full Text] [PDF]

				J. Guy, X. Qi, N. Muzyczka, and W. W. Hauswirth Reporter Expression Persists 1 Year After Adeno-Associated Virus-Mediated Gene Transfer to the Optic Nerve Arch Ophthalmol, July 1, 1999; 117(7): 929 - 937. [Abstract] [Full Text] [PDF]

				J. L. Aschner, N. Kovacs, J. V. Perciaccante, J. P. Figueroa, N. Thrikawala, G. S. Robins, and D. W. Busija Endothelial nitric oxide synthase gene transfer enhances dilation of newborn piglet pulmonary arteries Am J Physiol Heart Circ Physiol, July 1, 1999; 277(1): H371 - H379. [Abstract] [Full Text] [PDF]

				J Yap, T O'Brien, C Pellegrini, D.A Barber, H.D Tazelaar, S.R Severson, V.M Miller, and C.G.A McGregor Distribution and function of recombinant endothelial nitric oxide synthase in transplanted hearts Cardiovasc Res, June 1, 1999; 42(3): 720 - 727. [Abstract] [Full Text] [PDF]

				J. M. Waugh, M. Kattash, J. Li, E. Yuksel, M. D. Kuo, M. Lussier, A. B. Weinfeld, R. Saxena, E. D. Rabinovsky, S. Thung, et al. Gene therapy to promote thromboresistance: Local overexpression of tissue plasminogen activator to prevent arterial thrombosis in an in vivo rabbit model PNAS, February 2, 1999; 96(3): 1065 - 1070. [Abstract] [Full Text] [PDF]

				J. M. Waugh, E. Yuksel, J. Li, M. D. Kuo, M. Kattash, R. Saxena, R. Geske, S. N. Thung, S. M. Shenaq, and S. L. C. Woo Local Overexpression of Thrombomodulin for In Vivo Prevention of Arterial Thrombosis in a Rabbit Model Circ. Res., January 22, 1999; 84(1): 84 - 92. [Abstract] [Full Text] [PDF]

				S. Fang, R. V. Sharma, and R. C. Bhalla Enhanced Recovery of Injury-Caused Downregulation of Paxillin Protein by eNOS Gene Expression in Rat Carotid Artery : Mechanism of NO Inhibition of Intimal Hyperplasia? Arterioscler Thromb Vasc Biol, January 1, 1999; 19(1): 147 - 152. [Abstract] [Full Text] [PDF]

				D. D. Lund, F. M. Faraci, H. Ooboshi, B. L. Davidson, D. D. Heistad, and C. D. Kontos Adenovirus-Mediated Gene Transfer Is Augmented in Basilar and Carotid Arteries of Heritable Hyperlipidemic Rabbits � Editorial Comment Stroke, January 1, 1999; 30(1): 120 - 125. [Abstract] [Full Text] [PDF]

				K. Toyoda, H. Ooboshi, Y. Chu, A. Fasbender, B. L. Davidson, M. J. Welsh, D. D. Heistad, and G. K. Steinberg Cationic Polymer and Lipids Enhance Adenovirus-Mediated Gene Transfer to Rabbit Carotid Artery � Editorial Comment Stroke, October 1, 1998; 29(10): 2181 - 2188. [Abstract] [Full Text] [PDF]