(Circulation. 1995;91:2793-2801.)
© 1995 American Heart Association, Inc.
Articles |
Local Delivery of Vascular Endothelial Growth Factor Accelerates Reendothelialization and Attenuates Intimal Hyperplasia in Balloon-Injured Rat Carotid Artery
From the Departments of Medicine (Cardiology) (T.A., C.B., C.P., M.K., S.R., S.B., N.F., J.M.I), Surgery (Cardiovascular) (J.F.S.), and Biomedical Research (T.A., C.B., C.P., M.K., S.R., S.B., N.F., J.M.I.), St Elizabeth's Medical Center, Tufts University School of Medicine, Boston, Mass; and the Department of Cardiovascular Research (S.B., N.F.), Genentech, Inc, South San Francisco, Calif.
Correspondence to Jeffrey M. Isner, MD, St Elizabeth's Medical Center, 736 Cambridge St, Boston, MA 02135.
Background Most strategies designed to reduce restenosis by the use of pharmacological or biological reagents involve direct inhibition of vascular smooth muscle cell (SMC) proliferation. Alternatively, SMC proliferation might be indirectly inhibited if reendothelialization could be specifically facilitated at sites of balloon-induced arterial injury. Accordingly, we investigated the hypothesis that application of an endothelial cell (EC)-specific mitogen to a freshly denuded intimal surface could accelerate reendothelialization and thereby attenuate intimal hyperplasia.
Methods and Results The left carotid artery of 31 Sprague-Dawley rats was subjected to balloon injury, after which 16 rats were treated with a 30-minute incubation with 100 µg of vascular endothelial growth factor (VEGF), an EC-specific mitogen. Control animals (n=15) received a 30-minute incubation with 0.9% saline. At 2 weeks after balloon injury, carotid artery reendothelialization was markedly superior in the VEGF-treated group compared with the control group (14.59±1.12 versus 7.96±0.51 mm2, P<.0005). The extent of reendothelialization measured at 4 weeks after balloon injury remained superior for arteries treated with VEGF (18.04±0.90 mm2) versus saline (13.42±0.84 mm2, P<.005). Neointimal thickening was correspondingly attenuated to a statistically significant degree in arteries treated with VEGF versus the control group at both the 2-week and 4-week time points. Immunostaining for proliferating cell nuclear antigen (PCNA) disclosed a threefold increase in PCNA-positive cells in the neointima of control arteries versus VEGF-treated arteries at 2 weeks after injury.
Conclusions Application of VEGF, an EC-specific growth regulatory molecule, may be effectively used in vivo to promote reendothelialization and thereby indirectly attenuate neointimal thickening due to SMC proliferation.
Key Words: growth factors • endothelium • neointima • stenosis
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J. Waltenberger, J. Lange, and A. Kranz Vascular Endothelial Growth Factor-A-Induced Chemotaxis of Monocytes Is Attenuated in Patients With Diabetes Mellitus : A Potential Predictor for the Individual Capacity to Develop Collaterals Circulation, July 11, 2000; 102(2): 185 - 190. [Abstract] [Full Text] [PDF]
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I. Zachary, A. Mathur, S. Yla-Herttuala, and J. Martin Vascular Protection : A Novel Nonangiogenic Cardiovascular Role for Vascular Endothelial Growth Factor Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1512 - 1520. [Abstract] [Full Text] [PDF]
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F. Vidal, J. Aragones, A. Alfranca, and M. O. de Landazuri Up-regulation of vascular endothelial growth factor receptor Flt-1 after endothelial denudation: role of transcription factor Egr-1 Blood, June 1, 2000; 95(11): 3387 - 3395. [Abstract] [Full Text] [PDF]
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S. Yasuda, T. Noguchi, M. Gohda, T. Arai, N. Tsutsui, T. Matsuda, and H. Nonogi Single Low-Dose Administration of Human Recombinant Hepatocyte Growth Factor Attenuates Intimal Hyperplasia in a Balloon-Injured Rabbit Iliac Artery Model Circulation, May 30, 2000; 101(21): 2546 - 2549. [Abstract] [Full Text] [PDF]
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H. J. Kwak, S. J. Lee, Y.-H. Lee, C. H. Ryu, K. N. Koh, H. Y. Choi, and G. Y. Koh Angiopoietin-1 Inhibits Irradiation- and Mannitol-Induced Apoptosis in Endothelial Cells Circulation, May 16, 2000; 101(19): 2317 - 2324. [Abstract] [Full Text] [PDF]
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D. Mukherjee, J. Wong, B. Griffin, S. G. Ellis, T. Porter, S. Sen, and J. D. Thomas Ten-fold augmentation of endothelial uptake of vascular endothelial growth factor with ultrasound after systemic administration J. Am. Coll. Cardiol., May 1, 2000; 35(6): 1678 - 1686. [Abstract] [Full Text] [PDF]
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E. R. Schwarz, M. T. Speakman, M. Patterson, S. S. Hale, J. M. Isner, L. H. Kedes, and R. A. Kloner Evaluation of the effects of intramyocardial injection of DNA expressing vascular endothelial growth factor (VEGF) in a myocardial infarction model in the rat--angiogenesis and angioma formation J. Am. Coll. Cardiol., April 1, 2000; 35(5): 1323 - 1330. [Abstract] [Full Text] [PDF]
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K. G. Lehmann, J. J. Popma, J. A. Werner, A. J. Lansky, and R. L. Wilensky Vascular remodeling and the local delivery of cytochalasin B after coronary angioplasty in humans J. Am. Coll. Cardiol., March 1, 2000; 35(3): 583 - 591. [Abstract] [Full Text] [PDF]
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D. Chen, K. Walsh, and J. Wang Regulation of cdk2 Activity in Endothelial Cells That Are Inhibited From Growth by Cell Contact Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 629 - 635. [Abstract] [Full Text] [PDF]
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J. Dulak, A. Jozkowicz, A. Dembinska-Kiec, I. Guevara, A. Zdzienicka, D. Zmudzinska-Grochot, I. Florek, A. Wojtowicz, A. Szuba, and J. P. Cooke Nitric Oxide Induces the Synthesis of Vascular Endothelial Growth Factor by Rat Vascular Smooth Muscle Cells Arterioscler Thromb Vasc Biol, March 1, 2000; 20(3): 659 - 666. [Abstract] [Full Text] [PDF]
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 J. Dulak, A. Jozkowicz, A. Ratajska, A. Szuba, J. P Cooke, and A. Dembinska-Kiec Vascular endothelial growth factor is efficiently synthesized in spite of low transfection efficiency of pSG5VEGF plasmids in vascular smooth muscle cells Vascular Medicine, February 1, 2000; 5(1): 33 - 40. [Abstract] [PDF]
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M. O Hiltunen, M. P Turunen, M. Laitinen, and S. Yla-Herttuala Insights into the molecular pathogenesis of atherosclerosis and therapeutic strategies using gene transfer Vascular Medicine, February 1, 2000; 5(1): 41 - 48. [Abstract] [PDF]
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M. F. Flanagan, T. Aoyagi, L. W. Arnold, C. Maute, A. M. Fujii, J. Currier, D. Bergau, H. B. Warren, and K. Rakusan Effects of Chronic Heparin Administration on Coronary Vascular Adaptation to Hypertension and Ventricular Hypertrophy in Sheep Circulation, August 31, 1999; 100(9): 981 - 987. [Abstract] [Full Text] [PDF]
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D. Chen, T. Asahara, K. Krasinski, B. Witzenbichler, J. Yang, M. Magner, M. Kearney, W. A. Frazier, J. M. Isner, and V. Andres Antibody Blockade of Thrombospondin Accelerates Reendothelialization and Reduces Neointima Formation in Balloon-Injured Rat Carotid Artery Circulation, August 24, 1999; 100(8): 849 - 854. [Abstract] [Full Text] [PDF]
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N. Kronemann, A. Bouloumie, S. Bassus, C. M. Kirchmaier, R. Busse, and V. B. Schini-Kerth Aggregating Human Platelets Stimulate Expression of Vascular Endothelial Growth Factor in Cultured Vascular Smooth Muscle Cells Through a Synergistic Effect of Transforming Growth Factor-{beta}1 and Platelet-Derived Growth FactorAB Circulation, August 24, 1999; 100(8): 855 - 860. [Abstract] [Full Text] [PDF]
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J. Y. Jeremy, D. Rowe, A. M. Emsley, and A. C. Newby Nitric oxide and the proliferation of vascular smooth muscle cells Cardiovasc Res, August 15, 1999; 43(3): 580 - 594. [Full Text] [PDF]
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I. Six, E. Van Belle, R. Bordet, D. Corseaux, J. Callebert, B. Dupuis, C. Bauters, and M. E. Bertrand L-Arginine and L-NAME have no effects on the reendothelialization process after arterial balloon injury Cardiovasc Res, August 15, 1999; 43(3): 731 - 738. [Abstract] [Full Text] [PDF]
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M. Harada, Y. Toki, Y. Numaguchi, H. Osanai, T. Ito, K. Okumura, and T. Hayakawa Prostacyclin synthase gene transfer inhibits neointimal formation in rat balloon-injured arteries without bleeding complications Cardiovasc Res, August 1, 1999; 43(2): 481 - 491. [Abstract] [Full Text] [PDF]
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J. M. Isner Cancer and Atherosclerosis : The Broad Mandate of Angiogenesis Circulation, April 6, 1999; 99(13): 1653 - 1655. [Full Text] [PDF]
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 A. Basile-Borgia, J. H Abel, and H. Mahloogi Molecular advances in cardiac and cardiovascular disease Perfusion, March 1, 1999; 14(2): 89 - 99. [Abstract] [PDF]
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M. Camera, P. L. A. Giesen, J. Fallon, B. M. Aufiero, M. Taubman, E. Tremoli, and Y. Nemerson Cooperation Between VEGF and TNF-{alpha} Is Necessary for Exposure of Active Tissue Factor on the Surface of Human Endothelial Cells Arterioscler Thromb Vasc Biol, March 1, 1999; 19(3): 531 - 537. [Abstract] [Full Text] [PDF]
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Y. Numaguchi, K. Naruse, M. Harada, H. Osanai, S. Mokuno, K. Murase, H. Matsui, Y. Toki, T. Ito, K. Okumura, et al. Prostacyclin Synthase Gene Transfer Accelerates Reendothelialization and Inhibits Neointimal Formation in Rat Carotid Arteries After Balloon Injury Arterioscler Thromb Vasc Biol, March 1, 1999; 19(3): 727 - 733. [Abstract] [Full Text] [PDF]
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A. Bouloumie, V. B. Schini-Kerth, and R. Busse Vascular endothelial growth factor up-regulates nitric oxide synthase expression in endothelial cells Cardiovasc Res, March 1, 1999; 41(3): 773 - 780. [Abstract] [Full Text] [PDF]
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Y. Furukawa, A. Matsumori, N. Ohashi, T. Shioi, K. Ono, A. Harada, K. Matsushima, and S. Sasayama Anti–Monocyte Chemoattractant Protein-1/Monocyte Chemotactic and Activating Factor Antibody Inhibits Neointimal Hyperplasia in Injured Rat Carotid Arteries Circ. Res., February 19, 1999; 84(3): 306 - 314. [Abstract] [Full Text] [PDF]
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I. J. Kullo, R. D. Simari, and R. S. Schwartz Vascular Gene Transfer : From Bench to Bedside Arterioscler Thromb Vasc Biol, February 1, 1999; 19(2): 196 - 207. [Full Text] [PDF]
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 C. PUPILLI, L. LASAGNI, P. ROMAGNANI, F. BELLINI, M. MANNELLI, N. MISCIGLIA, C. MAVILIA, U. VELLEI, D. VILLARI, and M. SERIO Angiotensin II Stimulates the Synthesis and Secretion of Vascular Permeability Factor/Vascular Endothelial Growth Factor in Human Mesangial Cells J. Am. Soc. Nephrol., February 1, 1999; 10(2): 245 - 255. [Abstract] [Full Text]
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 G. Neufeld, T. Cohen, S. Gengrinovitch, and Z. Poltorak Vascular endothelial growth factor (VEGF) and its receptors FASEB J, January 1, 1999; 13(1): 9 - 22. [Abstract] [Full Text]
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I. Spyridopoulos, N. Principe, K. L. Krasinski, S.-h. Xu, M. Kearney, M. Magner, J. M. Isner, and D. W. Losordo Restoration of E2F Expression Rescues Vascular Endothelial Cells From Tumor Necrosis Factor-{alpha}–Induced Apoptosis Circulation, December 22, 1998; 98(25): 2883 - 2890. [Abstract] [Full Text] [PDF]
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C. Partovian, S. Adnot, S. Eddahibi, E. Teiger, M. Levame, P. Dreyfus, B. Raffestin, and C. Frelin Heart and lung VEGF mRNA expression in rats with monocrotaline- or hypoxia-induced pulmonary hypertension Am J Physiol Heart Circ Physiol, December 1, 1998; 275(6): H1948 - H1956. [Abstract] [Full Text] [PDF]
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F. Gonzalez-Fernandez, A. Lopez-Farre, J. A. Rodriguez-Feo, J. Farre, J. Guerra, J. Fortes, I. Millas, M. Garcia-Duran, L. Rico, P. Mata, et al. Expression of Inducible Nitric Oxide Synthase After Endothelial Denudation of the Rat Carotid Artery : Role of Platelets Circ. Res., November 30, 1998; 83(11): 1080 - 1087. [Abstract] [Full Text] [PDF]
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H. Wang and J. A. Keiser Vascular Endothelial Growth Factor Upregulates the Expression of Matrix Metalloproteinases in Vascular Smooth Muscle Cells : Role of flt-1 Circ. Res., October 19, 1998; 83(8): 832 - 840. [Abstract] [Full Text] [PDF]
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O. Varenne, S. Pislaru, H. Gillijns, N. Van Pelt, R. D. Gerard, P. Zoldhelyi, F. Van de Werf, D. Collen, and S. P. Janssens Local Adenovirus-Mediated Transfer of Human Endothelial Nitric Oxide Synthase Reduces Luminal Narrowing After Coronary Angioplasty in Pigs Circulation, September 1, 1998; 98(9): 919 - 926. [Abstract] [Full Text] [PDF]
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A. Matsuura, W. Yamochi, K.-i. Hirata, S. Kawashima, and M. Yokoyama Stimulatory Interaction Between Vascular Endothelial Growth Factor and Endothelin-1 on Each Gene Expression Hypertension, July 1, 1998; 32(1): 89 - 95. [Abstract] [Full Text] [PDF]
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M. Oberhoff, S. Novak, C. Herdeg, A. Baumbach, A. Kranzhofer, A. Bohnet, B. Horch, H. Hanke, K. K. Haase, and K. R. Karsch Local and systemic delivery of low molecular weight heparin stimulates the reendothelialization after balloon angioplasty Cardiovasc Res, June 1, 1998; 38(3): 751 - 762. [Abstract] [Full Text] [PDF]
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