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The Vascular Endothelial Growth Factor Family: Identification of a Fourth Molecular Species and Characterization of Alternative Splicing of RNA

Department of Molecular Biology, Genentech, Inc. South San Francisco, California 94080
Department of Cardiovascular Research, Genentech, Inc. South San Francisco, California 94080
Departments of Medicinal and Analytical Chemistry, Genentech, Inc. South San Francisco, California 94080

Address requests for reprints to: Dr. Keith A. Houck, Molecular Biology Department, Genentech, Inc., 460 Point San Bruno Boulevard, South San Francisco, California 94080.

Abstract

Vascular endothelial growth factor (VEGF) was recently identified as a secreted, direct-acting mitogen specific for vascular endothelial cells and capable of stimulating angiogenesis in vivo. Molecular cloning revealed multiple forms of VEGF, apparently arising from alternative splicing of its RNA transcript. We have examined various human cDNA libraries by the polymerase chain reaction technique and discovered a fourth molecular form, VEGF₂₀₆. This form contains a 41-amino acid insertion relative to the most abundant form, VEGF₁₆₅, and includes the highly basic 24-amino acid insertion found in VEGF₁₈₉. Southern blot analysis revealed that a single gene encoded these various forms, and nucleic acid sequence analysis of a portion of the VEGF gene revealed an intron/exon structure compatible with alternative splicing of RNA as a mechanism for their generation. Transient transfection of human embryonic kidney 293 cells showed that, like VEGF₁₈₉, VEGF₂₀₆ was predominately cell-associated and only very poorly secreted despite the presence of the signal peptide identical to that found in VEGF₁₂₁ and VEGF₁₆₅, both of which are efficiently exported from the cell. Vascular permeability activity was detected in the medium of 293 cells transfected with all four forms of VEGF; however, endothelial cell mitogenic activity was apparent only with VEGF₁₂₁ and VEGF₁₆₅. Thus, alternative splicing of VEGF RNA can produce four polypeptides with strikingly different secretion patterns, which suggests multiple physiological roles for this family of proteins.

Received for publication June 25, 1991. Revision received September 9, 1991. Accepted for publication September 26, 1991.

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				I. Pham, T. Uchida, C. Planes, L. B. Ware, R. Kaner, M. A. Matthay, and C. Clerici Hypoxia upregulates VEGF expression in alveolar epithelial cells in vitro and in vivo Am J Physiol Lung Cell Mol Physiol, November 1, 2002; 283(5): L1133 - L1142. [Abstract] [Full Text] [PDF]

				A. L. Niklaus, J. S. Babischkin, G. W. Aberdeen, G. J. Pepe, and E. D. Albrecht Expression of Vascular Endothelial Growth/Permeability Factor by Endometrial Glandular Epithelial and Stromal Cells in Baboons during the Menstrual Cycle and after Ovariectomy Endocrinology, October 1, 2002; 143(10): 4007 - 4017. [Abstract] [Full Text] [PDF]

				E. S. J. M. de Bont, V. Fidler, T. Meeuwsen, F. Scherpen, K. Hahlen, and W. A. Kamps Vascular Endothelial Growth Factor Secretion Is an Independent Prognostic Factor for Relapse-free Survival in Pediatric Acute Myeloid Leukemia Patients Clin. Cancer Res., September 1, 2002; 8(9): 2856 - 2861. [Abstract] [Full Text] [PDF]

				S. Koyama, E. Sato, M. Haniuda, H. Numanami, S. Nagai, and T. Izumi Decreased Level of Vascular Endothelial Growth Factor in Bronchoalveolar Lavage Fluid of Normal Smokers and Patients with Pulmonary Fibrosis Am. J. Respir. Crit. Care Med., August 1, 2002; 166(3): 382 - 385. [Abstract] [Full Text] [PDF]

				D. O. Bates, T.-G. Cui, J. M. Doughty, M. Winkler, M. Sugiono, J. D. Shields, D. Peat, D. Gillatt, and S. J. Harper VEGF165b, an Inhibitory Splice Variant of Vascular Endothelial Growth Factor, Is Down-Regulated in Renal Cell Carcinoma Cancer Res., July 15, 2002; 62(14): 4123 - 4131. [Abstract] [Full Text] [PDF]

				M. Stimpfl, D. Tong, B. Fasching, E. Schuster, A. Obermair, S. Leodolter, and R. Zeillinger Vascular Endothelial Growth Factor Splice Variants and Their Prognostic Value in Breast and Ovarian Cancer Clin. Cancer Res., July 1, 2002; 8(7): 2253 - 2259. [Abstract] [Full Text] [PDF]

				L. M. Veenendaal, H. Jin, S. Ran, L. Cheung, N. Navone, J. W. Marks, J. Waltenberger, P. Thorpe, and M. G. Rosenblum In vitro and in vivo studies of a VEGF121/rGelonin chimeric fusion toxin targeting the neovasculature of solid tumors PNAS, June 11, 2002; 99(12): 7866 - 7871. [Abstract] [Full Text] [PDF]

				S.-i. Yamagishi, Y. Inagaki, T. Okamoto, S. Amano, K. Koga, M. Takeuchi, and Z. Makita Advanced Glycation End Product-induced Apoptosis and Overexpression of Vascular Endothelial Growth Factor and Monocyte Chemoattractant Protein-1 in Human-cultured Mesangial Cells J. Biol. Chem., May 31, 2002; 277(23): 20309 - 20315. [Abstract] [Full Text] [PDF]

				M. Ancelin, H. Buteau-Lozano, G. Meduri, M. Osborne-Pellegrin, S. Sordello, J. Plouet, and M. Perrot-Applanat A dynamic shift of VEGF isoforms with a transient and selective progesterone-induced expression of VEGF189 regulates angiogenesis and vascular permeability in human uterus PNAS, April 30, 2002; 99(9): 6023 - 6028. [Abstract] [Full Text] [PDF]

				L. D. Ke, Y.-X. Shi, and W. K. A. Yung VEGF121, VEGF165 Overexpression Enhances Tumorigenicity in U251 MG but not in NG-1 Glioma Cells Cancer Res., March 1, 2002; 62(6): 1854 - 1861. [Abstract] [Full Text] [PDF]

				M. C. A. Duyndam, M. C. G. W. Hilhorst, H. M. M. Schluper, H. M. W. Verheul, P. J. van Diest, G. Kraal, H. M. Pinedo, and E. Boven Vascular Endothelial Growth Factor-165 Overexpression Stimulates Angiogenesis and Induces Cyst Formation and Macrophage Infiltration in Human Ovarian Cancer Xenografts Am. J. Pathol., February 1, 2002; 160(2): 537 - 548. [Abstract] [Full Text] [PDF]

				I. Huez, S. Bornes, D. Bresson, L. Creancier, and H. Prats New Vascular Endothelial Growth Factor Isoform Generated by Internal Ribosome Entry Site-Driven CUG Translation Initiation Mol. Endocrinol., December 1, 2001; 15(12): 2197 - 2210. [Abstract] [Full Text] [PDF]

				C. Treins, S. Giorgetti-Peraldi, J. Murdaca, and E. Van Obberghen Regulation of Vascular Endothelial Growth Factor Expression by Advanced Glycation End Products J. Biol. Chem., November 16, 2001; 276(47): 43836 - 43841. [Abstract] [Full Text] [PDF]

				M. E. Baldwin, S. Roufail, M. M. Halford, K. Alitalo, S. A. Stacker, and M. G. Achen Multiple Forms of Mouse Vascular Endothelial Growth Factor-D Are Generated by RNA Splicing and Proteolysis J. Biol. Chem., November 16, 2001; 276(47): 44307 - 44314. [Abstract] [Full Text] [PDF]

				C. Liu, Y. Okruzhnov, H. Li, and J. Nicholas Human Herpesvirus 8 (HHV-8)-Encoded Cytokines Induce Expression of and Autocrine Signaling by Vascular Endothelial Growth Factor (VEGF) in HHV-8-Infected Primary-Effusion Lymphoma Cell Lines and Mediate VEGF-Independent Antiapoptotic Effects J. Virol., November 15, 2001; 75(22): 10933 - 10940. [Abstract] [Full Text] [PDF]

				D Pfander, D Kortje, R Zimmermann, G Weseloh, T Kirsch, M Gesslein, T Cramer, and B Swoboda Vascular endothelial growth factor in articular cartilage of healthy and osteoarthritic human knee joints Ann Rheum Dis, November 1, 2001; 60(11): 1070 - 1073. [Abstract] [Full Text] [PDF]

				K.-Y. Kim, S.-Y. Jeong, J. Won, P.-D. Ryu, and M.-J. Nam Induction of Angiogenesis by Expression of Soluble Type II Transforming Growth Factor-beta Receptor in Mouse Hepatoma J. Biol. Chem., October 12, 2001; 276(42): 38781 - 38786. [Abstract] [Full Text] [PDF]

				R. K. Bruick and S. L. McKnight Building better vasculature Genes & Dev., October 1, 2001; 15(19): 2497 - 2502. [Full Text] [PDF]

				B. Maitre, S. Boussat, D. Jean, M. Gouge, L. Brochard, B. Housset, S. Adnot, and C. Delclaux Vascular endothelial growth factor synthesis in the acute phase of experimental and clinical lung injury Eur. Respir. J., July 1, 2001; 18(1): 100 - 106. [Abstract] [Full Text] [PDF]

				J. A. Foekens, H. A. Peters, N. Grebenchtchikov, M. P. Look, M. E. Meijer-van Gelder, A. Geurts-Moespot, T. H. van der Kwast, C. G. J. Sweep, and J. G. M. Klijn High Tumor Levels of Vascular Endothelial Growth Factor Predict Poor Response to Systemic Therapy in Advanced Breast Cancer Cancer Res., July 1, 2001; 61(14): 5407 - 5414. [Abstract] [Full Text] [PDF]

				O. Straume and L. A. Akslen Expresson of Vascular Endothelial Growth Factor, Its Receptors (FLT-1, KDR) and TSP-1 Related to Microvessel Density and Patient Outcome in Vertical Growth Phase Melanomas Am. J. Pathol., July 1, 2001; 159(1): 223 - 235. [Abstract] [Full Text] [PDF]

				N. Ferrara Role of vascular endothelial growth factor in regulation of physiological angiogenesis Am J Physiol Cell Physiol, June 1, 2001; 280(6): C1358 - C1366. [Abstract] [Full Text] [PDF]

				V. A. Hildebrandt, J. S. Babischkin, R. D. Koos, G. J. Pepe, and E. D. Albrecht Developmental Regulation of Vascular Endothelial Growth/Permeability Factor Messenger Ribonucleic Acid Levels in and Vascularization of the Villous Placenta During Baboon Pregnancy Endocrinology, May 1, 2001; 142(5): 2050 - 2057. [Abstract] [Full Text]

				X. Long, K. A. Burke, R. M. Bigsby, and K. P. Nephew Effects of the Xenoestrogen Bisphenol A on Expression of Vascular Endothelial Growth Factor (VEGF) in the Rat Experimental Biology and Medicine, May 1, 2001; 226(5): 477 - 482. [Abstract] [Full Text]