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Vascular Permeability Factor/Vascular Endothelial Growth Factor: A Critical Cytokine in Tumor Angiogenesis and a Potential Target for Diagnosis and Therapy

From the Department of Pathology, Beth Israel Deaconess Medical Center, and Department of Pathology, Harvard Medical School, Boston, MA.

Address reprint requests to Harold F. Dvorak, MD, Department of Pathology, Beth Israel Deaconess Medical Center, 330 Brookline Ave, Boston, MA 02215; email: hdvorak{at}caregroup.harvard.edu

ABSTRACT: Vascular endothelial growth factor A (VEGF-A), the founding member of the vascular permeability factor (VPF)/VEGF family of proteins, is an important angiogenic cytokine with critical roles in tumor angiogenesis. This article reviews the literature with regard to VEGF-A’s multiple functions, the mechanisms by which it induces angiogenesis, and its current and projected roles in clinical oncology. VEGF-A is a multifunctional cytokine that is widely expressed by tumor cells and that acts through receptors (VEGFR-1, VEGFR-2, and neuropilin) that are expressed on vascular endothelium and on some other cells. It increases microvascular permeability, induces endothelial cell migration and division, reprograms gene expression, promotes endothelial cell survival, prevents senescence, and induces angiogenesis. Recently, VEGF-A has also been shown to induce lymphangiogenesis. Measurements of circulating levels of VEGF-A may have value in estimating prognosis, and VEGF-A and its receptors are potential targets for therapy. Recognized as the single most important angiogenic cytokine, VEGF-A has a central role in tumor biology and will likely have an important role in future approaches designed to evaluate patient prognosis. It may also become an important target for cancer therapy.

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				K. J. Till, D. G. Spiller, R. J. Harris, H. Chen, M. Zuzel, and J. C. Cawley CLL, but not normal, B cells are dependent on autocrine VEGF and {alpha}4{beta}1 integrin for chemokine-induced motility on and through endothelium Blood, June 15, 2005; 105(12): 4813 - 4819. [Abstract] [Full Text] [PDF]

				S. Lee, S. M. Jilani, G. V. Nikolova, D. Carpizo, and M. L. Iruela-Arispe Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors J. Cell Biol., May 23, 2005; 169(4): 681 - 691. [Abstract] [Full Text] [PDF]

				X. Jimenez, D. Lu, L. Brennan, K. Persaud, M. Liu, H. Miao, L. Witte, and Z. Zhu A recombinant, fully human, bispecific antibody neutralizes the biological activities mediated by both vascular endothelial growth factor receptors 2 and 3 Mol. Cancer Ther., March 1, 2005; 4(3): 427 - 434. [Abstract] [Full Text] [PDF]

				B. I. Rini VEGF-Targeted Therapy in Metastatic Renal Cell Carcinoma Oncologist, March 1, 2005; 10(3): 191 - 197. [Abstract] [Full Text] [PDF]

				B. I. Rini and E. J. Small Biology and Clinical Development of Vascular Endothelial Growth Factor-Targeted Therapy in Renal Cell Carcinoma J. Clin. Oncol., February 10, 2005; 23(5): 1028 - 1043. [Abstract] [Full Text] [PDF]

				D. J. Hicklin and L. M. Ellis Role of the Vascular Endothelial Growth Factor Pathway in Tumor Growth and Angiogenesis J. Clin. Oncol., February 10, 2005; 23(5): 1011 - 1027. [Abstract] [Full Text] [PDF]

				D. W. Davis, R. Takamori, C. P. Raut, H. Q. Xiong, R. S. Herbst, W. M. Stadler, J. V. Heymach, G. D. Demetri, A. Rashid, Y. Shen, et al. Pharmacodynamic Analysis of Target Inhibition and Endothelial Cell Death in Tumors Treated with the Vascular Endothelial Growth Factor Receptor Antagonists SU5416 or SU6668 Clin. Cancer Res., January 15, 2005; 11(2): 678 - 689. [Abstract] [Full Text] [PDF]

				R. K. Jain Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy Science, January 7, 2005; 307(5706): 58 - 62. [Abstract] [Full Text] [PDF]

				A. Hoeben, B. Landuyt, M. S. Highley, H. Wildiers, A. T. Van Oosterom, and E. A. De Bruijn Vascular Endothelial Growth Factor and Angiogenesis Pharmacol. Rev., December 1, 2004; 56(4): 549 - 580. [Abstract] [Full Text] [PDF]

				H. Kobayashi, K. Reijnders, S. English, A. T. Yordanov, D. E. Milenic, A. L. Sowers, D. Citrin, M. C. Krishna, T. A. Waldmann, J. B. Mitchell, et al. Application of a Macromolecular Contrast Agent for Detection of Alterations of Tumor Vessel Permeability Induced by Radiation Clin. Cancer Res., November 15, 2004; 10(22): 7712 - 7720. [Abstract] [Full Text] [PDF]

				G. Bocci, S. Man, S. K. Green, G. Francia, J. M. L. Ebos, J. M. du Manoir, A. Weinerman, U. Emmenegger, L. Ma, P. Thorpe, et al. Increased Plasma Vascular Endothelial Growth Factor (VEGF) as a Surrogate Marker for Optimal Therapeutic Dosing of VEGF Receptor-2 Monoclonal Antibodies Cancer Res., September 15, 2004; 64(18): 6616 - 6625. [Abstract] [Full Text] [PDF]

				W Hilbe, S Dirnhofer, F Oberwasserlechner, T Schmid, E Gunsilius, G Hilbe, E Woll, and C M Kahler CD133 positive endothelial progenitor cells contribute to the tumour vasculature in non-small cell lung cancer J. Clin. Pathol., September 1, 2004; 57(9): 965 - 969. [Abstract] [Full Text] [PDF]

				J. M. Davison, V. Homuth, A. Jeyabalan, K. P. Conrad, S. A. Karumanchi, S. Quaggin, R. Dechend, and F. C. Luft New Aspects in the Pathophysiology of Preeclampsia J. Am. Soc. Nephrol., September 1, 2004; 15(9): 2440 - 2448. [Abstract] [Full Text] [PDF]

				N. Ferrara Vascular Endothelial Growth Factor: Basic Science and Clinical Progress Endocr. Rev., August 1, 2004; 25(4): 581 - 611. [Abstract] [Full Text] [PDF]

				S. S. Yoon, N. H. Segal, A. B. Olshen, M. F. Brennan, and S. Singer Circulating angiogenic factor levels correlate with extent of disease and risk of recurrence in patients with soft tissue sarcoma Ann. Onc., August 1, 2004; 15(8): 1261 - 1266. [Abstract] [Full Text] [PDF]

				D. W. Davis, K. Inoue, C. P. N. Dinney, D. J. Hicklin, J. L. Abbruzzese, and D. J. McConkey Regional Effects of an Antivascular Endothelial Growth Factor Receptor Monoclonal Antibody on Receptor Phosphorylation and Apoptosis in Human 253J B-V Bladder Cancer Xenografts Cancer Res., July 1, 2004; 64(13): 4601 - 4610. [Abstract] [Full Text] [PDF]

				D. Chakroborty, C. Sarkar, R. B. Mitra, S. Banerjee, P. S. Dasgupta, and S. Basu Depleted Dopamine in Gastric Cancer Tissues: Dopamine Treatment Retards Growth of Gastric Cancer by Inhibiting Angiogenesis Clin. Cancer Res., July 1, 2004; 10(13): 4349 - 4356. [Abstract] [Full Text] [PDF]

				H. Rossiter, C. Barresi, J. Pammer, M. Rendl, J. Haigh, E. F. Wagner, and E. Tschachler Loss of Vascular Endothelial Growth Factor A Activity in Murine Epidermal Keratinocytes Delays Wound Healing and Inhibits Tumor Formation Cancer Res., May 15, 2004; 64(10): 3508 - 3516. [Abstract] [Full Text] [PDF]

				J. Sun, M. A. Blaskovich, R. K. Jain, F. Delarue, D. Paris, S. Brem, M. Wotoczek-Obadia, Q. Lin, D. Coppola, K. Choi, et al. Blocking Angiogenesis and Tumorigenesis with GFA-116, a Synthetic Molecule that Inhibits Binding of Vascular Endothelial Growth Factor to its Receptor Cancer Res., May 15, 2004; 64(10): 3586 - 3592. [Abstract] [Full Text] [PDF]

				A M Jubb, T Q Pham, A M Hanby, G D Frantz, F V Peale, T D Wu, H W Koeppen, and K J Hillan Expression of vascular endothelial growth factor, hypoxia inducible factor 1{alpha}, and carbonic anhydrase IX in human tumours J. Clin. Pathol., May 1, 2004; 57(5): 504 - 512. [Abstract] [Full Text] [PDF]

				B. I. Rini, S. Halabi, J. Taylor, E. J. Small, and R. L. Schilsky Cancer and Leukemia Group B 90206: A Randomized Phase III Trial of Interferon-{alpha} or Interferon-{alpha} Plus Anti-Vascular Endothelial Growth Factor Antibody (Bevacizumab) in Metastatic Renal Cell Carcinoma Clin. Cancer Res., April 15, 2004; 10(8): 2584 - 2586. [Abstract] [Full Text] [PDF]

				G. Hopfl, O. Ogunshola, and M. Gassmann HIFs and tumors--causes and consequences Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2004; 286(4): R608 - R623. [Abstract] [Full Text] [PDF]