A vascular endothelial growth factor receptor-2 kinase inhibitor potentiates the activity of the conventional chemotherapeutic agents paclitaxel and doxorubicin in tumor xenograft models

Molecular Pharmacology

Volumn 66, Issue 3, 2004, Pages 635-647

  Emanuel, Stuart ^a,f   Gruninger, Robert H ^a   Fuentes Pesquera, Angel ^a   Connolly, Peter J ^a   Seamon, Jennifer A ^a   Hazel, Susan ^c   Tominovich, Rose ^b   Hollister, Beth ^d   Napier, Cheryl ^d   D'Andrea, Michael R ^b   Reuman, Michael ^a   Bignan, Gilles ^a   Tuman, Robert ^b   Johnson, Dana ^b   Moffatt, David ^e   Batchelor, Mark ^e   Foley, Anne ^e   O'Connell, James ^e   Allen, Rodger ^e   Perry, Martin ^e   Jolliffe, Linda ^a   Middleton, Steven A ^a   more..

^a Cancer Therapeutics Research   (Australia)

^b Oncology Research   (United States)

^c INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^d Piedmont Research Center   (United States)

^e UCB PHARMA   (Belgium)

^f JOHNSON AND JOHNSON PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1 AMINO 1 METHYLETHYL)PHENYL] 2 [4 (2 MORPHOLIN 4 YLETHYL)PHENYLAMINO]PYRIMIDIN 5 CARBONITRILE; DOXORUBICIN; FIBROBLAST GROWTH FACTOR RECEPTOR; JNJ 17029259; METHYLCELLULOSE; MITOGEN ACTIVATED PROTEIN KINASE; PACLITAXEL; PLATELET DERIVED GROWTH FACTOR RECEPTOR; POLYSORBATE 80; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTERY; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CHORIOALLANTOIS; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; ENDOTHELIUM CELL; FEMALE; GROWTH INHIBITION; HISTOLOGY; HUMAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR GROWTH; TUMOR XENOGRAFT; VEIN;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL DIVISION; CELL MOVEMENT; DOXORUBICIN; DRUG THERAPY, COMBINATION; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; HUMANS; MICE; NEOPLASMS, EXPERIMENTAL; NITRILES; PACLITAXEL; PYRIMIDINES; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 4944227798     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: 10.1124/mol.104.000638     Document Type: Article

References (48)

1. Arbiser JL, Moses MA, Fernandez CA, Ghiso N, Cao Y, Klauber N, Frank D, Brownlee M, Flynn E, Parangi S, et al. (1997) Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc Natl Acad Sci USA 94:861-866.
2. Barleon B, Sozzani S, Zhou D, Weich HA, Mantovani A, and Marme D (1996) Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 87:3336-3343.
3. Benjamin LE and Keshet E (1997) Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc Natl Acad Sci USA 94:8761-8766.
4. Bergers G and Hanahan D (2002) Combining antiangiogenic agents with metronomic chemotherapy enhances efficacy against late-stage pancreatic islet carcinomas in mice. Cold Spring Harb Symp Quant Biol 67:293-300.
5. Boehm T, Folkman J, Browder T, and O'Reilly MS (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature (Lond) 390:404-407.
6. Bruns CJ, Solorzano CC, Harbison MT, Ozawa S, Tsan R, Fan D, Abbruzzese J, Traxler P, Buchdunger E, Radinsky R, et al. (2000) Blockade of the epidermal growth factor receptor signaling by a novel tyrosine kinase inhibitor leads to apoptosis of endothelial cells and therapy of human pancreatic carcinoma. Cancer Res 60:2926-2935.
7. Cheng S-Y, Huang H-JS, Nagane M, Ji X-D, Wang D, Shih CC-Y, Arap W, Huang C-M, and Cavenee WK (1996) Suppression of glioblastoma angiogenicity and tumorigenicity by inhibition of endogenous expression of vascular endothelial growth factor. Proc Natl Acad Sci USA 93:8502-8507.
8. Ciardiello F, Bianco R, Damiano V, De Lorenzo S, Pepe S, De Placido S, Fan Z, Mendelsohn J, Bianco AR, and Tortora G (1999) Antitumor activity of sequential treatment with topotecan and anti-epidermal growth factor receptor monoclonal antibody C225. Clin Cancer Res 5:909-916.
9. Ciardiello F, Caputo R, Damiano V, Caputo R, Troiani T, Vitagliano D, Carlomagno F, Veneziani BM, Fontanini G, Bianco AR, et al. (2003) Antitumor effects of ZD6474, a small molecule vascular endothelial growth factor receptor tyrosine kinase inhibitor, with additional activity against epidermal growth factor receptor tyrosine kinase. Clin Cancer Res 9:1546-1556.
10. Compagni A, Wilgenbus P, Impagnatiello M-A, Cotton M, and Christofori G (2000) Fibroblast growth factors are required for efficient tumor angiogenesis. Cancer Res 60:7163-7169.
11. Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77:527-543.
12. Folkman J (1972) Anti-angiogenesis: new concept for therapy of solid tumors. Ann Surg 175:409-416.
13. Folkman J (1995) Clinical implications of research on angiogenesis. N Engl J Med 333:1757-1763.
14. Fong TAT, Shawver LK, Tang C, App H, Powell TJ, Kim YH, Schreck R, Wang X, Risau W, Ullrich A, et al. (1999) SU5416 is a potent and selective inhibitor of the vascular endothelial growth factor receptor (Flk-/KDR) that inhibits tyrosine kinase catalysis, tumor vascularization and growth of multiple tumor types. Cancer Res 59:99-106.
15. Grosskreutz CL, Anand-Apte B, Duplaa C, Quinn TP, Terman B, Zetter B, and D'Amore PA (1999) Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 58:128-136.
16. Hazel S (2003) A novel early chorioallantoic membrane assay demonstrates quantitative and qualitative changes caused by antiangiogenic substances. J Lab Clin Med 141:217-228.
17. Hiratsuka S, Maru Y, Okada A, Seiki M, Noda T, and Shibuya M (2001) Involvement of Flt-1 tyrosine kinase (vascular endothelial growth factor receptor-1) in pathological angiogenesis. Cancer Res 61:1207-1213.
18. Kabbinavar F, Hurwitz HI, Fehrenbacher L, Meropol NJ, Novotny WF, Lieberman G, Griffing S, and Bergsland E (2003) Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21:60-65.
19. Ke LD, Fueyo J, Chen X, Steck PA, Shi Y-X, Im A-A, and Yung WKA (1998) A novel approach to glioma gene therapy: down-regulation of the vascular endothelial growth factor in glioma cells using ribozymes. Int J Oncol 12:1391-1396.
20. Kim H-K, Kim J-W, Zilberstein A, Margolis B, Kim J-G, Schlessinger J, and Rhee S-G (1991) PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell 65:435-441.
21. Kim KJ, Bing L, Winer J, Armanini M, Gillett N, Philips HS, and Ferrera N (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature (Lond) 362:841-844.
22. Kroll J and Waltenberger J (1997) The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J Biol Chem 272:32521-32527.
23. Liu B, Earl HM, Baban D, Shoaibi M, Fabra A, Kerr DJ, and Seymour LW (1995) Melanoma cell lines express VEGF receptor KDR and respond to exogenously added VEGF. Biochem Biophys Res Commun 217:721-727.
24. Manley PW, Furet P, Bold G, Bruggen J, Mestan J, Meyer T, Schnell CR, and Wood J (2002) Anthranilic acid amides: a novel class of antiangiogenic VEGF receptor kinase inhibitors. J Med Chem 45:5687-5693.
25. Meyer RD, Latz C, and Rahimi N (2003) Recruitment and activation of phospholipase Cγ1 by vascular endothelial growth factor receptor-2 are required for tubulogenesis and differentiation of endothelial cells. J Biol Chem 278:16347-16355.
26. Millauer B, Longhi MP, Plate KH, Shawver LK, Risau W, Ullrich A, and Strawn LM (1996) Dominant-negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo. Cancer Res 56:1615-1620.
27. Millauer B, Shawver LK, Plate KH, Risau W, and Ullrich A (1994) Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1. Nature (Lond) 367:576-579.
28. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller NP, Risau W, and Ullrich A (1993) High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72:835-846.
29. Morioka H, Weissbach L, Vogel T, Nielsen GP, Faircloth GT, Shao L, and Hornicek FJ (2003) Antiangiogenesis treatment combined with chemotherapy produces chondrosarcoma necrosis. Clin Cancer Res 9:1211-1217.
30. Mustonen T and Alitalo K (1995) Endothelial receptor tyrosine kinases involved in angiogenesis. J Cell Biol 129:895-898.
31. Nicosia RF and Antonetti A (1990) Growth of microvessels in serum free matrix culture of rat aorta. Lab Investig 63:115-122.
32. Nissanov J, Tuman RW, Gruver LM, and Fortunato JM (1995) Automatic vessel segmentation and quantitation of the rat aortic ring assay of angiogenesis. Lab Investig 73:734-739.
33. Okada F, Rak J, St. Croix B, Lieubeau B, Kaya M, Roncari L, Shirasawa S, Sasazuki T, and Kerbel RS (1998) Impact of oncogenes in tumor angiogenesis: mutant K-ras up-regulation of vascular endothelial growth factor/vascular permeability factor is necessary, but not sufficient for tumorigenicity of human colorectal cells. Proc Natl Acad Sci USA 95:3609-3614.
34. Ravindranath N, Wion D, Brachet P, and Djakiew D (2001) Epidermal growth factor modulates the expression of vascular endothelial growth factor in the human prostate. J Androl 22:432-443.
35. Rhee S-G (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281-312.
36. Rousseau S, Houle F, Landry J, and Huot J (1997) p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15:2169-2177.
37. Schmitt O, Schubert C, Feyerabend T, Hellwig-Burgel T, Weiss C, and Kuhnel W (2002) Preferential topography of protein regulating vascularization and apoptosis in a MX1 xenotransplant after treatment with hypoxia, hyperthermia, ifosamide and irradiation. Am J Clin Oncol 25:325-336.
38. Sheehan DC and Hrapchak BB (1980) Theory and Practice of Histotechnology, 2nd ed, pp 143-144, Battelle Press, Columbus.
39. Siemeister G, Schirner M, Reusch P, Barleon B, Marme D, and Martiny-Baron G (1998) An antagonistic vascular endothelial growth factor (VEGF) variant inhibits VEGF-stimulated receptor autophosphorylation and proliferation of human endothelial cells. Proc Natl Acad Sci USA 95:4625-4629.
40. Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, and Ellis L (1995) Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis and proliferation of human colon cancer. Cancer Res 55:3964-3968.
41. Takahashi T, Ueno H, and Shibuya M (1999) VEGF activates protein kinase C-dependent, but ras-independent raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18:2221-2230.
42. Viloria-Petit A, Crombet T, Jothy S, Hicklin D, Bohlen P, Schlaeppi JM, Rak J, and Kerbel RS (2001) Acquired resistance to the antitumor effect of epidermal growth factor receptor-blocking antibodies in vivo: a role for altered tumor angiogenesis. Cancer Res 61:5090-5101.
43. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, and Heldin CH (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269:26988-26995.
44. Wedge SR, Ogilvie DJ, Dukes M, Kendrew J, Chester R, Jackson JA, Boffey SJ, Valentine PJ, Curwen JO, Musgrove HL, et al. (2002) ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis and tumor growth following oral administration. Cancer Res 62:4645-4655.
45. White JD, Hewett PW, Kosuge D, McCulloch T, Enholm E, Carmichael J, and Murray JC (2002) Vascular endothelial growth factor-D expression is an independent prognostic marker for survival in colorectal carcinoma. Cancer Res 62:1669-1675.
46. Witte L, Hicklin DJ, Zhu Z, Pytowski B, Kotanides H, Rockwell P, and Bohlen P (1998) Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev 17:155-161.
47. Wood JM, Bold G, Buchdunger E, Cozens R, Ferrari S, Frei J, Hofmann F, Mestan J, Mett H, O'Reilly T, et al. (2000) PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration. Cancer Res 60:2178-2189.
48. Yang JC, Haworth L, Sherry RM, Hwu P, Schwartzentruber DJ, Topalian SL, Steinberg SM, Chen HX, and Rosenberg SA (2003) A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N Engl J Med 349:427-434.