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(Circulation. 1998;98:2108-2116.)
© 1998 American Heart Association, Inc.


Clinical Investigation and Reports

Vascular Endothelial Growth Factor (VEGF) Expression in Human Coronary Atherosclerotic Lesions

Possible Pathophysiological Significance of VEGF in Progression of Atherosclerosis

Mayumi Inoue, MD; Hiroshi Itoh, MD, PhD; Makiko Ueda, MD, PhD; Takahiko Naruko, MD, PhD; Akiko Kojima, PhD; Ryushi Komatsu, MD; Kentaro Doi, MD; Yoshihiro Ogawa, MD, PhD; Naohisa Tamura, MD, PhD; Kazuhiko Takaya, MD; Toshio Igaki, MD; Jun Yamashita, MD; Tae-Hwa Chun, MD; Ken Masatsugu, MD; Anton E. Becker, MD, PhD; ; Kazuwa Nakao, MD, PhD

From the Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine (M.I., H.I., K.D., Y.O., N.T., K.T., T.I., J.Y., T.-H.C., K.M., K.N.); Department of Pathology, Osaka City University Medical School (M.U., R.K.); Department of Cardiology, Osaka City General Hospital (T.N.); and Department of Anatomy, Osaka City University Medical School (A.K.), Japan; and the Department of Cardiovascular Pathology, Academic Medical Center, University of Amsterdam, The Netherlands (A.E.B.)

Correspondence to Hiroshi Itoh, MD, PhD, Department of Medicine and Clinical Science, Kyoto University Graduate School of Medicine, 54 Shogoin Kawahara-cho, Sakyo-ku, Kyoto 606-8507, Japan. E-mail hiito{at}kuhp.kyoto-u.ac.jp

Background—Vascular endothelial growth factor (VEGF) is an important angiogenic factor reported to induce migration and proliferation of endothelial cells, enhance vascular permeability, and modulate thrombogenicity. VEGF expression in cultured cells (smooth muscle cells, macrophages, endothelial cells) is controlled by growth factors and cytokines. Hence, the question arises of whether VEGF could play a role in atherogenesis.

Methods and Results—Frozen sections from 38 coronary artery segments were studied. The specimens were characterized as normal with diffuse intimal thickening, early atherosclerosis with hypercellularity, and advanced atherosclerosis (atheromatous plaques, fibrous plaques, and totally occlusive lesions). VEGF expression as well as the expression of 2 VEGF receptors, flt-1 and Flk-1, were studied with immunohistochemical techniques in these samples at the different stages of human coronary atherosclerosis progression. The expression of VEGF mRNA was also studied with reverse transcription–polymerase chain reaction. Normal arterial segments showed no substantial VEGF expression. Hypercellular and atheromatous lesions showed distinct VEGF positivity of activated endothelial cells, macrophages, and partially differentiated smooth muscle cells. VEGF positivity was also detected in endothelial cells of intraplaque microvessels within advanced lesions. In totally occlusive lesions with extensive neovascularization, intense immunostaining for VEGF was observed in accumulated macrophages and endothelial cells of the microvessels. Furthermore, VEGF mRNA expression was detected in atherosclerotic coronary segments but not in normal coronary segments. The immunostainings for flt-1 and Flk-1 were detected in aggregating macrophages in atherosclerotic lesions and also in endothelial cells of the microvessels in totally occlusive lesions.

Conclusions—These results demonstrate distinct expression of VEGF and its receptors (flt-1 and Flk-1) in atherosclerotic lesions in human coronary arteries. Considering the multipotent actions of VEGF documented experimentally in vivo and in vitro, our findings suggest that VEGF may have some role in the progression of human coronary atherosclerosis, as well as in recanalization processes in obstructive coronary diseases.


Key Words: angiogenesis • atherosclerosis • coronary disease • immunohistochemistry • pathology




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J. Am. Coll. Cardiol., December 1, 2001; 38(7): 2137 - 2138.
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Cardiovasc ResHome page
J. Herrmann, L. O Lerman, M. Rodriguez-Porcel, D. R Holmes Jr., D. M Richardson, E. L Ritman, and A. Lerman
Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia
Cardiovasc Res, September 1, 2001; 51(4): 762 - 766.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
J. M. Isner, P. R. Vale, J. F. Symes, and D. W. Losordo
Assessment of Risks Associated With Cardiovascular Gene Therapy in Human Subjects
Circ. Res., August 31, 2001; 89(5): 389 - 400.
[Abstract] [Full Text] [PDF]


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CirculationHome page
S. E. Epstein, R. Kornowski, S. Fuchs, and H. F. Dvorak
Angiogenesis Therapy : Amidst the Hype, the Neglected Potential for Serious Side Effects
Circulation, July 3, 2001; 104(1): 115 - 119.
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Arterioscler. Thromb. Vasc. Bio.Home page
M. Kuzuya, M. A. Ramos, S. Kanda, T. Koike, T. Asai, K. Maeda, K. Shitara, M. Shibuya, and A. Iguchi
VEGF Protects Against Oxidized LDL Toxicity to Endothelial Cells by an Intracellular Glutathione-Dependent Mechanism Through the KDR Receptor
Arterioscler Thromb Vasc Biol, May 1, 2001; 21(5): 765 - 770.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
M. Inoue, H. Itoh, T. Tanaka, T.-H. Chun, K. Doi, Y. Fukunaga, N. Sawada, J. Yamshita, K. Masatsugu, T. Saito, et al.
Oxidized LDL Regulates Vascular Endothelial Growth Factor Expression in Human Macrophages and Endothelial Cells Through Activation of Peroxisome Proliferator-Activated Receptor-{{gamma}}
Arterioscler Thromb Vasc Biol, April 1, 2001; 21(4): 560 - 566.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
S. E. Epstein, S. Fuchs, Y. F. Zhou, R. Baffour, and R. Kornowski
Therapeutic interventions for enhancing collateral development by administration of growth factors: basic principles, early results and potential hazards
Cardiovasc Res, February 16, 2001; 49(3): 532 - 542.
[Abstract] [Full Text] [PDF]


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CirculationHome page
M. F. Brizzi, L. Formato, P. Dentelli, A. Rosso, M. Pavan, G. Garbarino, M. Pegoraro, G. Camussi, and L. Pegoraro
Interleukin-3 Stimulates Migration and Proliferation of Vascular Smooth Muscle Cells : A Potential Role in Atherogenesis
Circulation, January 30, 2001; 103(4): 549 - 554.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Heart Circ. Physiol.Home page
P. Bausero, M.-H. Ben-Mahdi, J.-P. Mazucatelli, C. Bloy, and M. Perrot-Applanat
Vascular endothelial growth factor is modulated in vascular muscle cells by estradiol, tamoxifen, and hypoxia
Am J Physiol Heart Circ Physiol, November 1, 2000; 279(5): H2033 - H2042.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
G. Dahlfors and H. J. Arnqvist
Vascular Endothelial Growth Factor and Transforming Growth Factor-{beta}1 Regulate the Expression of Insulin-Like Growth Factor-Binding Protein-3, -4, and -5 in Large Vessel Endothelial Cells
Endocrinology, June 1, 2000; 141(6): 2062 - 2067.
[Abstract] [Full Text] [PDF]


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Pharmacol. Rev.Home page
A. W. Griffioen and G. Molema
Angiogenesis: Potentials for Pharmacologic Intervention in the Treatment of Cancer, Cardiovascular Diseases, and Chronic Inflammation
Pharmacol. Rev., June 1, 2000; 52(2): 237 - 268.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
V. Ollivier, J. Chabbat, J. M. Herbert, J. Hakim, and D. de Prost
Vascular Endothelial Growth Factor Production by Fibroblasts in Response to Factor VIIa Binding to Tissue Factor Involves Thrombin and Factor Xa
Arterioscler Thromb Vasc Biol, May 1, 2000; 20(5): 1374 - 1381.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
C. Dong and P. J. Goldschmidt-Clermont
Bone Sialoprotein and the Paradox of Angiogenesis Versus Atherosclerosis
Circ. Res., April 28, 2000; 86(8): 827 - 828.
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LupusHome page
B J Hunt
The endothelium in atherogenesis
Lupus, March 1, 2000; 9(3): 189 - 193.
[Abstract] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
N. Akuzawa, M. Kurabayashi, Y. Ohyama, M. Arai, and R. Nagai
Zinc Finger Transcription Factor Egr-1 Activates Flt-1 Gene Expression in THP-1 Cells on Induction for Macrophage Differentiation
Arterioscler Thromb Vasc Biol, February 1, 2000; 20(2): 377 - 384.
[Abstract] [Full Text] [PDF]


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CirculationHome page
R. Kornowski, S. Fuchs, M. B. Leon, and S. E. Epstein
Delivery Strategies to Achieve Therapeutic Myocardial Angiogenesis
Circulation, February 1, 2000; 101(4): 454 - 458.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
P. Sinnaeve, O. Varenne, D. Collen, and S. Janssens
Gene therapy in the cardiovascular system: an update
Cardiovasc Res, December 1, 1999; 44(3): 498 - 506.
[Abstract] [Full Text] [PDF]


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CirculationHome page
I. Moussa and J. W. Moses
Angiogenesis for Treatment of Ischemic Heart Disease: Should We Worry About Progression of Atherosclerosis?
Circulation, November 30, 1999; 100 (22): e109 - e109.
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SEMIN CARDIOTHORAC VASC ANESTHHome page
C. E. Chambers, S. T Riebel, and M. Kozak
Interventional Cardiology: Advances in Percutaneous Techniques for the Treatment of Cardiac Disease
Seminars in Cardiothoracic and Vascular Anesthesia, July 1, 1999; 3(2): 109 - 125.
[Abstract] [PDF]


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BMJHome page
T. D Henry
Science, medicine, and the future: Therapeutic angiogenesis
BMJ, June 5, 1999; 318(7197): 1536 - 1539.
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Am. J. Physiol. Heart Circ. Physiol.Home page
C. K. Sen, S. Khanna, M. Venojarvi, P. Trikha, E. C. Ellison, T. K. Hunt, and S. Roy
Copper-induced vascular endothelial growth factor expression and wound healing
Am J Physiol Heart Circ Physiol, May 1, 2002; 282(5): H1821 - H1827.
[Abstract] [Full Text] [PDF]