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Molecular Endocrinology Vol. 5, No. 12 1806-1814
doi:10.1210/mend-5-12-1806
Copyright © 1991 by the Endocrine Society.
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The Vascular Endothelial Growth Factor Family: Identification of a Fourth Molecular Species and Characterization of Alternative Splicing of RNA

Keith A. Houck, Napoleone Ferrara, Jane Winer, George Cachianes, Bing Li and David W. Leung

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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T. Lange, N. Guttmann-Raviv, L. Baruch, M. Machluf, and G. Neufeld
VEGF162, A New Heparin-binding Vascular Endothelial Growth Factor Splice Form That Is Expressed in Transformed Human Cells
J. Biol. Chem., May 2, 2003; 278(19): 17164 - 17169.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Y. Sonoda, M. Kanamori, D. F. Deen, S.-Y. Cheng, M. S. Berger, and R. O. Pieper
Overexpression of Vascular Endothelial Growth Factor Isoforms Drives Oxygenation and Growth but not Progression to Glioblastoma Multiforme in a Human Model of Gliomagenesis
Cancer Res., April 15, 2003; 63(8): 1962 - 1968.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
D.C Felmeden, A.D Blann, and G.Y.H Lip
Angiogenesis: basic pathophysiology and implications for disease
Eur. Heart J., April 1, 2003; 24(7): 586 - 603.
[Full Text] [PDF]


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Cancer Res.Home page
C. Benckert, S. Jonas, T. Cramer, Z. von Marschall, G. Schafer, M. Peters, K. Wagner, C. Radke, B. Wiedenmann, P. Neuhaus, et al.
Transforming Growth Factor {beta}1 Stimulates Vascular Endothelial Growth Factor Gene Transcription in Human Cholangiocellular Carcinoma Cells
Cancer Res., March 1, 2003; 63(5): 1083 - 1092.
[Abstract] [Full Text] [PDF]


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FASEB J.Home page
Y.-J. YIN, Z. SALAH, M. MAOZ, S. C. E. RAM, S. OCHAYON, G. NEUFELD, S. KATZAV, and R. BAR-SHAVIT
Oncogenic transformation induces tumor angiogenesis: a role for PAR1 activation
FASEB J, February 1, 2003; 17(2): 163 - 174.
[Abstract] [Full Text] [PDF]


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Mol Cancer ResHome page
K. D. Burroughs, J. Oh, J. C. Barrett, and R. P. DiAugustine
Phosphatidylinositol 3-Kinase and Mek1/2 Are Necessary for Insulin-Like Growth Factor-I-Induced Vascular Endothelial Growth Factor Synthesis in Prostate Epithelial Cells: A Role for Hypoxia-Inducible Factor-1?
Mol. Cancer Res., February 1, 2003; 1(4): 312 - 322.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
J. M. Hastings, D. R. Licence, G. J. Burton, D. S. Charnock-Jones, and S. K. Smith
Soluble Vascular Endothelial Growth Factor Receptor 1 Inhibits Edema and Epithelial Proliferation Induced by 17{beta}-Estradiol in the Mouse Uterus
Endocrinology, January 1, 2003; 144(1): 326 - 334.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
M. J. Mulligan-Kehoe, H. K. Kleinman, M. Drinane, R. J. Wagner, C. Wieland, and R. J. Powell
A Truncated Plasminogen Activator Inhibitor-1 Protein Blocks the Availability of Heparin-binding Vascular Endothelial Growth Factor A Isoforms
J. Biol. Chem., December 6, 2002; 277(50): 49077 - 49089.
[Abstract] [Full Text] [PDF]


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Eur Respir JHome page
S. Koyama, E. Sato, A. Tsukadaira, M. Haniuda, H. Numanami, M. Kurai, S. Nagai, and T. Izumi
Vascular endothelial growth factor mRNA and protein expression in airway epithelial cell lines in vitro
Eur. Respir. J., December 1, 2002; 20(6): 1449 - 1456.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
L. C. Rockwell, S. Pillai, C. E. Olson, and R. D. Koos
Inhibition of Vascular Endothelial Growth Factor/Vascular Permeability Factor Action Blocks Estrogen-Induced Uterine Edema and Implantation in Rodents
Biol Reprod, December 1, 2002; 67(6): 1804 - 1810.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
T. Shimizu, J.-Y. Jiang, H. Sasada, and E. Sato
Changes of Messenger RNA Expression of Angiogenic Factors and Related Receptors During Follicular Development in Gilts
Biol Reprod, December 1, 2002; 67(6): 1846 - 1852.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
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]


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EndocrinologyHome page
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]


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Clin. Cancer Res.Home page
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]


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Am. J. Respir. Crit. Care Med.Home page
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]


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Cancer Res.Home page
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]


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Clin. Cancer Res.Home page
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]


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Proc. Natl. Acad. Sci. USAHome page
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]


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J. Biol. Chem.Home page
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]


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Proc. Natl. Acad. Sci. USAHome page
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]


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Cancer Res.Home page
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]


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Am. J. Pathol.Home page
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]


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Mol. Endocrinol.Home page
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]


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J. Biol. Chem.Home page
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]


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J. Biol. Chem.Home page
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]


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J. Virol.Home page
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]


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Ann Rheum DisHome page
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]


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J. Biol. Chem.Home page
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]


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


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Eur Respir JHome page
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]


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Cancer Res.Home page
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]


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Am. J. Pathol.Home page
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]


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Am. J. Physiol. Cell Physiol.Home page
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]


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EndocrinologyHome page
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]


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Exp. Biol. Med.Home page
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]




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