Vascular Endothelial Growth Factor-Trap Decreases Tumor Burden, Inhibits Ascites, and Causes Dramatic Vascular Remodeling in an Ovarian Cancer Model

Clinical Cancer Research

Volumn 9, Issue 15, 2003, Pages 5721-5728

  Byrne, Annette T ^a,c   Ross, Leorah ^b   Holash, Joceyln ^b   Nakanishi, Mikiye ^a   Hu, Limin ^a   Hofmann, Judith I ^a   Yancopoulos, George D ^b   Jaffe, Robert B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b REGENERON PHARMACEUTICALS INC   (United States)

^c PHARMACYCLICS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; RETROVIRUS VECTOR; SOLUBLE DECOY RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN TRAP;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASCITES; BLOOD VESSEL; BLOOD VESSEL PERMEABILITY; CANCER MODEL; CARCINOMATOSIS; CELL GROWTH; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OVARY CANCER; PERITONEUM METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR AFFINITY; TUMOR VOLUME;

ANGIOGENESIS INHIBITORS; ANIMALS; ASCITES; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; OVARIAN NEOPLASMS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; TRANSPLANTATION, HETEROLOGOUS;

EID: 0345060442     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Folkman, J. Addressing tumor blood vessels. Nature Biotechnol., 15: 510, 1997.
2. Gospodarowicz, D., Abraham, J. A., and Schilling, J. Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo-stellate cells. Proc. Natl. Acad. Sci. USA, 86: 7311-7315, 1989.
3. Leung, D. W., Cachianes, G., Kuang, W. J., Goeddel, D. V., and Ferrara, N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science (Wash. DC), 246: 1306-1309, 1989.
4. Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J., and Connolly, D. T. Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science (Wash. DC), 246: 1309-1312, 1989.
5. Ferrara, N., and Henzel, W. J. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun., 161: 851-858, 1989.
6. Connolly, D. T., Olander, J. V., Heuvelman, D., Nelson, R., Monsell, R., Siegel, N., Haymore, B. L., Leimgruber, R., and Feder, J. Human vascular permeability factor. Isolation from U937 cells. J. Biol. Chem., 264: 20017-20024, 1989.
7. Senger, D. R., Perruzzi, C. A., Feder, J., and Dvorak, H. F. A highly conserved vascular permeability factor secreted by a variety of human and rodent tumor cell lines. Cancer Res., 46: 5629-5632, 1983.
8. Boocock, C. A., Charnock-Jones, D. S., Sharkey, A. M., McLaren, J., Barker, P. J., Wright, K. A., Twentyman, P. R., and Smith, S. K. Expression of vascular endothelial growth factor and its receptors flt and KDR in ovarian carcinoma. J. Natl. Cancer Inst. (Bethesda), 87: 506-516, 1995.
9. Olson, T. A., Mohanraj, D., Carson, L. F., and Ramakrishnan, S. Vascular permeability factor gene expression in normal and neoplastic human ovaries. Cancer Res., 54: 276-280, 1994.
10. Abu-Jawdeh, G. M., Faix, J. D., Niloff, J., Tognazzi, K., Manseau, E., Dvorak, H. F., and Brown, L. F. Strong expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in ovarian borderline and malignant neoplasms. Lab. Investig., 74: 1105-1115, 1996.
11. Paley, P. J., Staskus, K. A., Gebhard, K., Mohanraj, D., Twiggs, L. B., Carson, L. F., and Ramakrishnan, S. Vascular endothelial growth factor expression in early stage ovarian carcinoma. Cancer (Phila.), 80: 98-106, 1997.
12. Sowter, H. M., Corps, A. N., Evans, A. L., Clark, D. E., Charnock-Jones, D. S., and Smith, S. K. Expression and localization of the vascular endothelial growth factor family in ovarian epithelial tumors. Lab. Investig., 77: 607-614, 1997.
13. Barton, D. P., Cai, A., Wendt, K., Young, M., Gamero, A., and De Cesare, S. Angiogenic protein expression in advanced epithelial ovarian cancer. Clin. Cancer Res., 3: 1579-1586, 1997.
14. Orre, M., and Rogers, P. A., VEGF. VEGFR-1, VEGFR-2, microvessel density and endothelial cell proliferation in tumours of the ovary. Int. J. Cancer, 84: 101-108, 1999.
15. Dirix, L. Y., Vermeulen, P. B., Pawinski, A., Prove, A., Benoy, I., De Pooter, C., Martin, M., and Van Oosterom, A. T. Elevated levels of the angiogenic cytokines basic fibroblast growth factor and vascular endothelial growth factor in sera of cancer patients. Br. J. Cancer, 76: 238-243, 1997.
16. Yamamoto, S., Konishi, I., Mandai, M., Kuroda, H., Komatsu, T., Nanbu, K., Sakahara, H., and Mori T. Expression of vascular endothelial growth factor (VEGF) in epithelial ovarian neoplasms: correlation with clinicopathology and patient survival, and analysis of serum VEGF levels. Br. J. Cancer, 76: 1221-1227, 1997.
17. Tempfer, C., Obermair, A., Hefler, L., Haeusler, G., Gitsch, G., and Kainz, C. Vascular endothelial growth factor serum concentrations in ovarian cancer. Obstet. Gynecol., 92: 360-363, 1998.
18. Kraft, A., Weindel, K., Ochs, A., Marth, C., Zmija, J., Schumacher, P., Unger, C., Marme, D., and Gastl, G. Vascular endothelial growth factor in the sera and effusions of patients with malignant and nonmalignant disease. Cancer (Phila.), 85: 178-187, 1999.
19. Gadducci, A., Ferdeghini, M., Fanucchi, A., Annicchiarico, C., Ciampi, B., Prontera, C., and Genazzani, A. R. Serum preoperative vascular endothelial growth factor (VEGF) in epithelial ovarian cancer: relationship with prognostic variables and clinical outcome. Anticancer Res., 19: 1401-1405, 1999.
20. Oehler, M. K., and Caffier, H. Diagnostic value of serum VEGF in women with ovarian tumors. Anticancer Res., 19: 2519-2522, 1999.
21. Obermair, A., Hefler, L., Nather, A., Preyer, O., and Kaider, A. Correlation of the serum concentration of vascular endothelial growth factor (VEGF) and hemoglobin levels in patients with epithelial ovarian cancer. Ann. Oncol., 10: 998, 1999.
22. Oehler, M. K., and Caffier, H. Prognostic relevance of serum vascular endothelial growth factor in ovarian cancer. Anticancer Res., 20: 5109-5112, 2000.
23. Nagy, J. A., Masse, E. M., Herzberg, K. T., Meyers, M. S., Yeo, K. T., Yeo, T. K., Sioussat, T. M., and Dvorak, H. F. Pathogenesis of ascites tumor growth: vascular permeability factor, vascular hyperpermeability, and ascites fluid accumulation. Cancer Res., 55: 360-368, 1995.
24. Yoneda, J., Kuniyasu, H., Crispens, M. A., Price, J. E., Bucana, C. D., and Fidler, I. J. Expression of angiogenesis-related genes and progression of human ovarian carcinomas in nude mice. J. Natl. Cancer Inst. (Bethesda), 90: 447-454, 1998.
25. Garzetti, G. G., Ciavattini, A., Lucarini, G., Pugnaloni, A., De Nictolis, M., Amati, S., Romanini, C., and Biagini, G. Vascular endothelial growth factor expression as a prognostic index in serous ovarian cystoadenocarcinomas: relationship with MIBI immunostaining. Gynecol. Oncol., 73: 396-401, 1999.
26. Zebrowski, B. K., Liu, W., Ramirez, K., Akagi, Y., Mills, G. B., and Ellis, L. M. Markedly elevated levels of vascular endothelial growth factor in malignant ascites. Ann. Surg. Oncol., 6: 373-378, 1999.
27. Ke-Lin, Qu-Hong, Nagy, J. A., Eckelhoefer, I. A., Masse, E. M., Dvorak, A. M., and Dvorak, H. F. Vascular targeting of solid and ascites tumours with antibodies to vascular endothelial growth factor. Eur. J. Cancer, 32A: 2467-2473, 1996.
28. Mesiano, S., Ferrara, N., and Jaffe, R. B. Role of vascular endothelial growth factor in ovarian cancer: inhibition of ascites formation by immunoneutralization. Am. J. Pathol., 153: 1249-1256, 1998.
29. Yukita, A., Asano, M., Okamoto, T., Mizutani, S., and Suzuki, H. Suppression of ascites formation and re-accumulation associated with human ovarian cancer by an anti-VPF monoclonal antibody in vivo. Anticancer Res., 20: 155-160, 2000.
30. Mu, J., Abe, Y., Tsutsui, T., Yamamoto, N., Tai, X. G., Niwa, O., Tsujimura, T., Sato, B., Terano, H., Fujiwara, H., and Hamaoka, T. Inhibition of growth and metastasis of ovarian carcinoma by administering a drug capable of interfering with vascular endothelial growth factor activity. Jpn. J. Cancer Res., 87: 963-971, 1996.
31. Xu, L., Yoneda, J., Herrera, C., Wood, J., Killion, J. J., Fidler, I. J. Inhibition of malignant ascites and growth of human ovarian carcinoma by oral administration of a potent inhibitor of the vascular endothelial growth factor receptor tyrosine kinases. Int. J. Oncol., 16: 445-454, 2000.
32. Hu, L., Zaloudek, C., Mills, G. B., Gray, J., and Jaffe, R. B. In vivo and in vitro ovarian carcinoma growth inhibition by a phosphatidylinositol 3-kinase inhibitor (LY294002). Clin. Cancer Res., 6: 880-886, 2000.
33. Hu, L., Hofmann, J., Lu, Y., Mills, G. B., and Jaffe, R. B. Inhibition of phosphatidylinositol 3′-kinase increases efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Cancer Res., 62: 1087-1092, 2002.
34. Holash, J., Davis, S., Papadopoulos, N., Croll, S. D., Ho, L., Russell, M., Boland, P., Leidich, R., Hylton, D., Burova, E., Ioffe, E., Huang, T., Radziejewski, C., Bailey, K., Fandl, J. P., Daly, T., Wiegand, S. J., Yancopoulos, G. D., and Rudge, J. S. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc. Natl. Acad. Sci. USA, 99: 11393-11398, 2002.
35. Kim, E. S., Serur, A., Huang, J., Manley, C. A., McCrudden, K. W., Frischer, J. S., Soffer, S. Z., Ring, L., New, T., Zabisky, S., Rudge, J. S., Holash, J., Yancopoulos, G. D., Kandel, J. J., and Yamashiro, D. J. Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc. Natl. Acad. Sci. USA, 99: 11399-11404, 2002.
36. Rommel, C., Clarke, B. A., Zimmermann, S., Nunez, L., Rossman, R., Reid, K., Moelling, K., Yancopoulos, G. D., and Glass, D. J. Differentiation stage-specific inhibition of the Raf-MEK-ERK pathway by Akt. Science (Wash. DC), 286: 1738-1741, 1999.
37. Grignani, F., Kinsella, T., Mencarelli, A., Valtieri, M., Riganelli, D., Grignani, F., Lanfrancone, L., Peschle, C., Nolan, G. P., and Pelicci, P. G. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res., 58: 14-19, 1998.
38. Thurston, G., Rudge, J. S., Ioffe, E., Zhou, H., Ross, L., Croll, S. D., Glazer, N., Holash, J., McDonald, D. M., and Yancopoulos, G. D. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med., 460-463, 2000.
39. Nakanishi, Y., Kodama, J., Yoshinouchi, M., Tokumo, K., Kamimura, S., Okuda, H., and Kudo, T. The expression of vascular endothelial growth factor and transforming growth factor-β associates with angiogenesis in epithelial ovarian cancer. Int. J. Gynecol. Pathol., 16: 256-262, 1997.
40. Fujimoto, J., Sakaguchi, H., Hirose, R., Ichigo, S., and Tamaya, T. Biologic implications of the expression of vascular endothelial growth factor subtypes in ovarian carcinoma. Cancer (Phila.), 83: 2528-2533, 1998.
41. Sioussat, T. M., Dvorak, H. F., Brock, T. A., and Senger, D. R. Inhibition of vascular permeability factor (vascular endothelial growth factor) with antipeptide antibodies. Arch. Biochem. Biophys., 301: 15-20, 1993.
42. Akutagawa, N., Nishikawa, A., Iwasaki, M., Fujimoto, T., Teramoto, M., Kitajima, Y., Endo, T., Shibuya, M., and Kudo, R. Expression of vascular endothelial growth factor and E-cadherin in human ovarian cancer: association with ascites fluid accumulation and peritoneal dissemination in mouse ascites model. Jpn. J. Cancer Res., 93: 644-651, 2002.
43. Sykes J. A. Pharmacologically active substances in malignant ascites fluid. Br. J. Pharmacol., 40: 595P+, 1970.
44. Greenbaum, L. M., Grebow, P., Johnston, M., Prakash, A., and Semente, G. Pepstatin, an inhibitor of leukokinin formation and ascitic fluid accumulation. Cancer Res., 35: 706-710, 1975.
45. Ettinghausen, S. E., Puri, R. K., and Rosenberg, S. A. Increased vascular permeability in organs mediated by the systemic administration of lymphokine-activated killer cells and recombinant interleukin-2 in mice. J. Natl. Cancer Inst. (Bethesda), 80: 177-188, 1988.
46. Ohmura, E., Tsushima, T., Kamiya, Y., Okada, M., Onoda, N., Shizume, K., and Demura, H. Epidermal growth factor and transforming growth factor α induce ascitic fluid in mice. Cancer Res., 50: 4915-4917, 1990.
47. Hasumi, Y., Mizukami, H., Urabe, M., Kohno, T., Takeuchi, K., Kume, A., Momoeda, M., Yoshikawa, H., Tsuruo, T., Shibuya, M., Taketani, Y., and Ozawa, K. Soluble FLT-1 expression suppresses carcinomatous ascites in nude mice bearing ovarian cancer. Cancer Res., 62: 2019-2023, 2002.
48. Hu, L., Hofmann, J., Zaloudek, C., Ferrara, N., Hamilton T., and Jaffe R. B. VEGF immunoneutralization plus paclitaxel markedly reduces tumor burden and ascites in athymic mouse model of ovarian cancer. Am. J. Pathol., 161: 1917-1924, 2002.