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Expression of Vascular Endothelial Growth Factor and Its Receptor, KDR, Correlates with Vascularity, Metastasis, and Proliferation of Human Colon Cancer¹

Departments of Cell Biology [Y. T., Y. K., C. D. B., L. M. E.], Surgical Oncology [Y. T., L. M. E.], and Pathology [K. R. C.], The University of Texas M. D. Anderson Cancer Center, Houston, Texas 77030

We studied the correlation between expression of vascular endothelial growth factor (VEGF), basic fibroblast growth factor (bFGF), and their receptors with vascularity, metastasis, and proliferative index of human colon cancers. Immunohistochemical analyses using antibodies against VEGF, bFGF, their receptors (KDR, flt-1, bek, and flg), factor VIII, and proliferating cell nuclear antigen were carried out on archival specimens of 52 human colon carcinomas and 10 adenomas. Vessels were quantitated by light microscopy (x200), and the intensity of staining for VEGF and bFGF was assessed on a scale of 0–3+. The presence or absence of immunostaining for KDR, flt-1, bek, and flg was evaluated in endothelial cells, and proliferation was determined by counting the number of proliferating cell nuclear antigen-positive cells per 500 tumor cells. Expression of VEGF and KDR was higher in metastatic than in nonmetastatic neoplasms and directly correlated with the extent of neovascularization and the degree of proliferation, whereas expression of bFGF, flt-1, bek, and flg did not differ among tumor types. Vessel counts were greater in metastatic tumors than in nonmetastatic tumors. These findings support the hypothesis that VEGF is an important angiogenic factor in primary and metastatic human colon cancer. VEGF expression and vessel counts may aid in predicting patients at risk for metastasis from colon cancer.

¹ This work was supported in part by American Cancer Society Cancer Development Award 94-21 (L. M. E.).

² To whom requests for reprints should be addressed, at The University of Texas M. D. Anderson Cancer Center, Texas Medical Center, Box 106, 1515 Holcombe Boulevard, Houston, TX 77030.

Received 6/ 5/95. Accepted 6/ 5/95.

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				A. Stopeck, M. Sheldon, M. Vahedian, G. Cropp, R. Gosalia, and A. Hannah Results of a Phase I Dose-escalating Study of the Antiangiogenic Agent, SU5416, in Patients with Advanced Malignancies Clin. Cancer Res., September 1, 2002; 8(9): 2798 - 2805. [Abstract] [Full Text] [PDF]

				S. Kinuya, A. Kawashima, K. Yokoyama, K. Koshida, S. Konishi, N. Watanabe, N. Shuke, H. Bunko, T. Michigishi, and N. Tonami Cooperative Effect of Radioimmunotherapy and Antiangiogenic Therapy with Thalidomide in Human Cancer Xenografts J. Nucl. Med., August 1, 2002; 43(8): 1084 - 1089. [Abstract] [Full Text] [PDF]

				B. Restucci, S. Papparella, P. Maiolino, and G. De Vico Expression of Vascular Endothelial Growth Factor in Canine Mammary Tumors Veterinary Pathology, July 1, 2002; 39(4): 488 - 493. [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]

				A. N. Witmer, J. Dai, H. A. Weich, G. F.J.M. Vrensen, and R. O. Schlingemann Expression of Vascular Endothelial Growth Factor Receptors 1, 2, and 3 in Quiescent Endothelia J. Histochem. Cytochem., June 1, 2002; 50(6): 767 - 778. [Abstract] [Full Text] [PDF]

				M. Lucchi, A. Mussi, G. Fontanini, P. Faviana, A. Ribechini, and C. A. Angeletti Small cell lung carcinoma (SCLC): the angiogenic phenomenon Eur. J. Cardiothorac. Surg., June 1, 2002; 21(6): 1105 - 1110. [Abstract] [Full Text] [PDF]

				C.S. Brock and S.M. Lee Anti-angiogenic strategies and vascular targeting in the treatment of lung cancer Eur. Respir. J., March 1, 2002; 19(3): 557 - 570. [Abstract] [Full Text] [PDF]

				A. Yuan, C.-J. Yu, K.-T. Luh, S.-H. Kuo, Y.-C. Lee, and P.-C. Yang Aberrant p53 Expression Correlates With Expression of Vascular Endothelial Growth Factor mRNA and Interleukin-8 mRNA and Neoangiogenesis in Non-Small-Cell Lung Cancer J. Clin. Oncol., February 15, 2002; 20(4): 900 - 910. [Abstract] [Full Text] [PDF]

				T. Maeno, T. Tanaka, Y. Sando, T. Suga, Y. Maeno, J. Nakagawa, T. Hosono, M. Sato, H. Akiyama, S. Kishi, et al. Stimulation of Vascular Endothelial Growth Factor Gene Transcription by all trans Retinoic Acid through Sp1 and Sp3 Sites in Human Bronchioloalveolar Carcinoma Cells Am. J. Respir. Cell Mol. Biol., February 1, 2002; 26(2): 246 - 253. [Abstract] [Full Text] [PDF]

				R. Koomagi, F. Zintl, A. Sauerbrey, and M. Volm Vascular Endothelial Growth Factor in Newly Diagnosed and Recurrent Childhood Acute Lymphoblastic Leukemia as Measured by Real-Time Quantitative Polymerase Chain Reaction Clin. Cancer Res., November 1, 2001; 7(11): 3381 - 3384. [Abstract] [Full Text] [PDF]

				Y. Hamma-Kourbali, R. Vassy, A. Starzec, V. Le Meuth-Metzinger, O. Oudar, R. Bagheri-Yarmand, G. Perret, and M. Crepin Vascular Endothelial Growth Factor 165 (VEGF165) Activities Are Inhibited by Carboxymethyl Benzylamide Dextran That Competes for Heparin Binding to VEGF165 and VEGF165{middle dot}KDR Complexes J. Biol. Chem., October 19, 2001; 276(43): 39748 - 39754. [Abstract] [Full Text] [PDF]

				C. C. Solorzano, Y. D. Jung, C. D. Bucana, D. J. McConkey, G. E. Gallick, G. McMahon, and L. M. Ellis In Vivo Intracellular Signaling as a Marker of Antiangiogenic Activity Cancer Res., October 1, 2001; 61(19): 7048 - 7051. [Abstract] [Full Text] [PDF]

				F. Bentzien, I. Struman, J.-F. Martini, J. Martial, and R. Weiner Expression of the Antiangiogenic Factor 16K hPRL in Human HCT116 Colon Cancer Cells Inhibits Tumor Growth in Rag1-/- Mice Cancer Res., October 1, 2001; 61(19): 7356 - 7362. [Abstract] [Full Text] [PDF]

				X. Zhang, J. P. Gaspard, and D. C. Chung Regulation of Vascular Endothelial Growth Factor by the Wnt and K-ras Pathways in Colonic Neoplasia Cancer Res., August 1, 2001; 61(16): 6050 - 6054. [Abstract] [Full Text] [PDF]

				T. Etoh, H. Inoue, S. Tanaka, G. F. Barnard, S. Kitano, and M. Mori Angiopoietin-2 Is Related to Tumor Angiogenesis in Gastric Carcinoma: Possible in Vivo Regulation via Induction of Proteases Cancer Res., March 1, 2001; 61(5): 2145 - 2153. [Abstract] [Full Text]

				M.-D. Tabone, J. Landman-Parker, B. Arcil, M.-C. Coudert, I. Gerota, M. Benbunan, G. Leverger, and C. Dosquet Are Basic Fibroblast Growth Factor and Vascular Endothelial Growth Factor Prognostic Indicators in Pediatric Patientswith Malignant Solid Tumors? Clin. Cancer Res., March 1, 2001; 7(3): 538 - 543. [Abstract] [Full Text]

				M. Yang, E. Baranov, X.-M. Li, J. W. Wang, P. Jiang, L. Li, A. R. Moossa, S. Penman, and R. M. Hoffman Whole-body and intravital optical imaging of angiogenesis in orthotopically implanted tumors PNAS, February 27, 2001; 98(5): 2616 - 2621. [Abstract] [Full Text] [PDF]

				K. D. Miller, C. J. Sweeney, and G. W. Sledge Jr Redefining the Target: Chemotherapeutics as Antiangiogenics J. Clin. Oncol., February 15, 2001; 19(4): 1195 - 1206. [Abstract] [Full Text] [PDF]

				H. Ishikawa, A. P. Heaney, R. Yu, G. A. Horwitz, and S. Melmed Human Pituitary Tumor-Transforming Gene Induces Angiogenesis J. Clin. Endocrinol. Metab., February 1, 2001; 86(2): 867 - 874. [Abstract] [Full Text]

				R. M. Shaheen, W. W. Tseng, D. W. Davis, W. Liu, N. Reinmuth, R. Vellagas, A. A. Wieczorek, Y. Ogura, D. J. McConkey, K. E. Drazan, et al. Tyrosine Kinase Inhibition of Multiple Angiogenic Growth Factor Receptors Improves Survival in Mice Bearing Colon Cancer Liver Metastases by Inhibition of Endothelial Cell Survival Mechanisms Cancer Res., February 1, 2001; 61(4): 1464 - 1468. [Abstract] [Full Text]

				A. Yuan, C.-J. Yu, S.-H. Kuo, W.-J. Chen, F.-Y. Lin, K.-T. Luh, P.-C. Yang, and Y.-C. Lee Vascular Endothelial Growth Factor 189 mRNA Isoform Expression Specifically Correlates With Tumor Angiogenesis, Patient Survival, and Postoperative Relapse in Non-Small-Cell Lung Cancer J. Clin. Oncol., January 15, 2001; 19(2): 432 - 441. [Abstract] [Full Text] [PDF]

				Z von Marschall, T Cramer, M Hocker, G Finkenzeller, B Wiedenmann, and S Rosewicz Dual mechanism of vascular endothelial growth factor upregulation by hypoxia in human hepatocellular carcinoma Gut, January 1, 2001; 48(1): 87 - 96. [Abstract] [Full Text] [PDF]

				P. P. Claudio, P. Stiegler, C. M. Howard, C. Bellan, C. Minimo, G. M. Tosi, J. Rak, A. Kovatich, Paola De Fazio, P. Micheli, et al. RB2/p130 Gene-enhanced Expression Down-Regulates Vascular Endothelial Growth Factor Expression and Inhibits Angiogenesis in Vivo Cancer Res., January 1, 2001; 61(2): 462 - 468. [Abstract] [Full Text]

				E A Baker, F G Bergin, and D J Leaper Plasminogen activator system, vascular endothelial growth factor, and colorectal cancer progression Mol. Pathol., December 1, 2000; 53(6): 307 - 312. [Abstract] [Full Text]

				G. Zeng, L. Gao, S. Birklé, and R. K. Yu Suppression of Ganglioside GD3 Expression in a Rat F-11 Tumor Cell Line Reduces Tumor Growth, Angiogenesis, and Vascular Endothelial Growth Factor Production Cancer Res., December 1, 2000; 60(23): 6670 - 6676. [Abstract] [Full Text]