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[Cancer Research 53, 4727-4735, October 1, 1993]
© 1993 American Association for Cancer Research
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Expression of Vascular Permeability Factor (Vascular Endothelial Growth Factor) and Its Receptors in Adenocarcinomas of the Gastrointestinal Tract1

Lawrence F. Brown2, Brygida Berse, Robert W. Jackman, Kathi Tognazzi, Eleanor J. Manseau, Donald R. Senger and Harold F. Dvorak

Department of Pathology, Beth Israel Hospital, and Department of Pathology, Harvard Medical School, Boston, Massachusetts 02215

2 To whom requests for reprints should be addressed, at Department of Pathology, Beth Israel Hospital, 330 Brookline Ave., Boston, MA 02215.

Vascular permeability factor (VPF) is one of the most potent known inducers of microvascular hyperpermeability; in addition, it is a selective endothelial cell growth factor, hence its alternate name, vascular endothelial growth factor. VPF exerts its actions on the microvasculature by interacting with specific endothelial cell receptors. VPF is expressed by many transplantable animal tumors, by tumor cell lines in culture, and by certain normal cells in situ. The purpose of the present investigation was to determine whether and with what consistency VPF and its endothelial cell receptors are expressed in primary autochthonous human tumors of gastrointestinal tract origin, as determined by in situ hybridization and immunohistochemistry. Twenty-one primary adenocarcinomas (17 colon, 2 stomach, 1 small bowel, and 1 pancreas) were studied. The malignant epithelial cells expressed VPF mRNA strongly, in contrast to normal epithelium, hyperplastic polyps, and adenomas, which expressed little or no VPF mRNA. VPF expression was further increased in tumor cells immediately adjacent to zones of tumor necrosis; in such areas, occasional stromal cells also expressed VPF mRNA. In the ten colon carcinomas studied, tumor cells stained for VPF protein by immunohistochemistry. The endothelial cells of nearby stromal blood vessels also stained for VPF by immunohistochemistry and in addition expressed mRNAs encoding the VPF receptors flt~l and kdr as determined by in situ hybridization. Endothelial cells away from the tumor did not stain for VPF and no definite mRNA expression for flt-1 or kdr was detected by in situ hybridization. The ganglion cells of the myenteric plexus of normal bowel expressed VPF mRNA and protein. These data indicate that primary autochthonous human tumors of gastrointestinal origin regularly express both VPF mRNA and VPF protein and that adjacent stromal vessels express mRNAs for both known VPF receptors. VPF is likely to contribute to tumor growth by promoting angiogenesis and stroma formation, both directly, through its action as an endothelial cell growth factor, and indirectly, by increasing vascular permeability, thereby leading to plasma protein extravasation, fibrin deposition, and the eventual replacement of the resulting matrix with vascularized stroma.

1 This work was supported by USPHS Research Grants CA-50453 and CA-58845 (to H. F. D.), and by CA-43967 (to D. R. S.) awarded by the National Cancer Institute, Department of Health and Human Services, and under terms of a contract from the National Foundation for Cancer Research, and by grants from the BIH Pathology Foundation, Inc.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 5/ 5/93. Accepted 7/19/93.




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Y. D. Jung, K. Nakano, W. Liu, G. E. Gallick, and L. M. Ellis
Extracellular Signal-regulated Kinase Activation Is Required for Up-Regulation of Vascular Endothelial Growth Factor by Serum Starvation in Human Colon Carcinoma Cells
Cancer Res., October 1, 1999; 59(19): 4804 - 4807.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Prewett, J. Huber, Y. Li, A. Santiago, W. O'Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, et al.
Antivascular Endothelial Growth Factor Receptor (Fetal Liver Kinase 1) Monoclonal Antibody Inhibits Tumor Angiogenesis and Growth of Several Mouse and Human Tumors
Cancer Res., October 1, 1999; 59(20): 5209 - 5218.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Yoshiji, S. Kuriyama, D. K. Ways, J. Yoshii, Y. Miyamoto, M. Kawata, Y. Ikenaka, H. Tsujinoue, T. Nakatani, M. Shibuya, et al.
Protein Kinase C Lies on the Signaling Pathway for Vascular Endothelial Growth Factor-mediated Tumor Development and Angiogenesis
Cancer Res., September 1, 1999; 59(17): 4413 - 4418.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L. F. Brown, A. J. Guidi, S. J. Schnitt, L. Van De Water, M. L. Iruela-Arispe, T.-K. Yeo, K. Tognazzi, and H. F. Dvorak
Vascular Stroma Formation in Carcinoma in Situ, Invasive Carcinoma, and Metastatic Carcinoma of the Breast
Clin. Cancer Res., May 1, 1999; 5(5): 1041 - 1056.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
M. D. Balbay, C. A. Pettaway, H. Kuniyasu, K. Inoue, E. Ramirez, E. Li, I. J. Fidler, and C. P. N. Dinney
Highly Metastatic Human Prostate Cancer Growing within the Prostate of Athymic Mice Overexpresses Vascular Endothelial Growth Factor
Clin. Cancer Res., April 1, 1999; 5(4): 783 - 789.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
W. T. Bellamy, L. Richter, Y. Frutiger, and T. M. Grogan
Expression of Vascular Endothelial Growth Factor and Its Receptors in Hematopoietic Malignancies
Cancer Res., February 1, 1999; 59(3): 728 - 733.
[Abstract] [Full Text] [PDF]

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 Toxicol PatholHome page
A. M. Ryan, D. B. Eppler, K. E. Hagler, R. H. Bruner, P. J. Thomford, R. L. Hall, G. M. Shopp, and C. A. O'Neill
Preclinical Safety Evaluation of rhuMAbVEGF, an Antiangiogenic Humanized Monoclonal Antibody
Toxicol Pathol, January 1, 1999; 27(1): 78 - 86.
[Abstract] [PDF]

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 Cancer Res.Home page
T. A. T. Fong, L. K. Shawver, L. Sun, C. Tang, H. App, T. J. Powell, Y. H. Kim, R. Schreck, X. Wang, W. Risau, et al.
SU5416 Is a Potent and Selective Inhibitor of the Vascular Endothelial Growth Factor Receptor (Flk-1/KDR) That Inhibits Tyrosine Kinase Catalysis, Tumor Vascularization, and Growth of Multiple Tumor Types
Cancer Res., January 1, 1999; 59(1): 99 - 106.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
S. Mesiano, N. Ferrara, and R. B. Jaffe
Role of Vascular Endothelial Growth Factor in Ovarian Cancer : Inhibition of Ascites Formation by Immunoneutralization
Am. J. Pathol., October 1, 1998; 153(4): 1249 - 1256.
[Abstract] [Full Text] [PDF]

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 JCBHome page
G. Seghezzi, S. Patel, C. J. Ren, A. Gualandris, G. Pintucci, E. S. Robbins, R. L. Shapiro, A. C. Galloway, D. B. Rifkin, and P. Mignatti
Fibroblast Growth Factor-2 (FGF-2) Induces Vascular Endothelial Growth Factor (VEGF) Expression in the Endothelial Cells of Forming Capillaries: An Autocrine Mechanism Contributing to Angiogenesis
J. Cell Biol., June 29, 1998; 141(7): 1659 - 1673.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Cell Mol. Bio.Home page
H. Christou, A. Yoshida, V. Arthur, T. Morita, and S. Kourembanas
Increased Vascular Endothelial Growth Factor Production in the Lungs of Rats with Hypoxia-induced Pulmonary Hypertension
Am. J. Respir. Cell Mol. Biol., June 1, 1998; 18(6): 768 - 776.
[Abstract] [Full Text]

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 J. Histochem. Cytochem.Home page
L. F. Brown, A. J. Guidi, K. Tognazzi, and H. F. Dvorak
Vascular Permeability Factor/Vascular Endothelial Growth Factor and Vascular Stroma Formation in Neoplasia: Insights from In Situ Hybridization Studies
J. Histochem. Cytochem., May 1, 1998; 46(5): 569 - 576.
[Abstract] [Full Text]

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 Mol. Biol. CellHome page
K. P. Claffey, S.-C. Shih, A. Mullen, S. Dziennis, J. L. Cusick, K. R. Abrams, S. W. Lee, and M. Detmar
Identification of a Human VPF/VEGF 3' Untranslated Region Mediating Hypoxia-induced mRNA Stability
Mol. Biol. Cell, February 1, 1998; 9(2): 469 - 481.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
L. M. Ellis, C. A. Staley, W. Liu, R. Y. D. Fleming, N. U. Parikh, C. D. Bucana, and G. E. Gallick
Down-regulation of Vascular Endothelial Growth Factor in a Human Colon Carcinoma Cell Line Transfected with an Antisense Expression Vector Specific for c-src
J. Biol. Chem., January 9, 1998; 273(2): 1052 - 1057.
[Abstract] [Full Text] [PDF]

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 BloodHome page
P. Salven, L. Teerenhovi, and H. Joensuu
A High Pretreatment Serum Vascular Endothelial Growth Factor Concentration Is Associated With Poor Outcome in Non-Hodgkin's Lymphoma
Blood, October 15, 1997; 90(8): 3167 - 3172.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. S. Wang, M. Miura, H. Demura, and K. Sato
Anabolic Effects of 1,25-Dihydroxyvitamin D3 on Osteoblasts Are Enhanced by Vascular Endothelial Growth Factor Produced by Osteoblasts and by Growth Factors Produced by Endothelial Cells
Endocrinology, July 1, 1997; 138(7): 2953 - 2962.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
N. Ferrara and T. Davis-Smyth
The Biology of Vascular Endothelial Growth Factor
Endocr. Rev., February 1, 1997; 18(1): 4 - 25.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
R. S. Warren, H. Yuan, M. R. Matli, N. Ferrara, and D. B. Donner
Induction of Vascular Endothelial Growth Factor by Insulin-like Growth Factor 1in Colorectal Carcinoma
J. Biol. Chem., November 15, 1996; 271(46): 29483 - 29488.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. Song, S. Ramaswamy, S. Ramachandran, L. C. Flowers, I. R. Horowitz, J. A. Rock, and S. Parthasarathy
Angiogenic role for glycodelin in tumorigenesis
PNAS, July 31, 2001; 98(16): 9265 - 9270.
[Abstract] [Full Text] [PDF]


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