Antiangiogenic versus cytotoxic therapeutic approaches to human pancreas cancer: An experimental study with a vascular endothelial growth factor receptor-2 tyrosine kinase inhibitor and gemcitabine

European Journal of Pharmacology

Volumn 498, Issue 1-3, 2004, Pages 9-18

  Bocci, Guido ^a   Danesi, Romano ^a   Marangoni, Gabriele ^b   Fioravanti, Anna ^a   Boggi, Ugo ^b   Esposito, Irene ^c   Fasciani, Alessandro ^d   Boschi, Elena ^b   Campani, Daniela ^c   Bevilacqua, Generoso ^c   Mosca, Franco ^b   Del Tacca, Mario ^a  

^a Division of Pharmacology and Chemotherapy   (Italy)

^b Transplants Adv Technol Med U

^c Transplants Adv Technol Med U

^d Unit of Gynaecology and Obstetrics   (Italy)

Author keywords

Angiogenesis; Endothelial cell; Gemcitabine; Pancreas cancer cell; SU5416; VEGF

Indexed keywords

GEMCITABINE; SEMAXANIB; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CANCER RECURRENCE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; DRUG MECHANISM; DRUG POTENTIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IC 50; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; CELL DIVISION; CELL LINE; CELL LINE, TUMOR; DEOXYCYTIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; ENDOTHELIAL CELLS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; MALE; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; PANCREATIC NEOPLASMS; PLACENTA; PREGNANCY; PROTEIN KINASE INHIBITORS; PYRROLES; TIME FACTORS; TISSUE CULTURE TECHNIQUES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 4444254354     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2004.07.062     Document Type: Article

References (48)

1. J.L. Abbruzzese Past and present treatment of pancreatic adenocarcinoma: chemotherapy as a standard treatment modality Semin. Oncol. 29 2002 2 8
2. A. Abdollahi, K.E. Lipson, A. Sckell, H. Zieher, F. Klenke, D. Poerschke, A. Roth, X. Han, M. Krix, M. Bischof, P. Hahnfeldt, H.J. Grone, J. Debus, L. Hlatky, and P.E. Huber Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects Cancer Res. 63 2003 8890 8898
3. C.H. Baker, C.C. Solorzano, and I.J. Fidler Blockade of vascular endothelial growth factor receptor and epidermal growth factor receptor signaling for therapy of metastatic human pancreatic cancer Cancer Res. 62 2002 1996 2003
4. J.D. Berlin, and M.L. Rothenberg Chemotherapeutic advances in pancreatic cancer Curr. Oncol. Rep. 5 2003 219 226
5. G. Bocci, A. Fasciani, R. Danesi, P. Viacava, A.R. Genazzani, and M. Del Tacca In-vitro evidence of autocrine secretion of vascular endothelial growth factor by endothelial cells from human placental blood vessels Mol. Hum. Reprod. 7 2001 771 777
6. B.J. Braakhuis, V.W. Ruiz van Haperen, E. Boven, G. Veerman, and G.J. Peters Schedule-dependent antitumor effect of gemcitabine in in vivo model system Semin. Oncol. 22 1995 42 46
7. L.F. Brown, B. Berse, R.W. Jackman, K. Tognazzi, E.J. Manseau, D.R. Senger, and H.F. Dvorak Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinomas of the gastrointestinal tract Cancer Res. 53 1993 4727 4735
8. C.J. Bruns, M. Shrader, M.T. Harbison, C. Portera, C.C. Solorzano, K.W. Jauch, D.J. Hicklin, R. Radinsky, and L.M. Ellis Effect of the vascular endothelial growth factor receptor-2 antibody DC101 plus gemcitabine on growth, metastasis and angiogenesis of human pancreatic cancer growing orthotopically in nude mice Int. J. Cancer 102 2002 101 108
9. P. Buchler, H.A. Reber, M.W. Buchler, H. Friess, and O.J. Hines VEGF-RII influences the prognosis of pancreatic cancer Ann. Surg. 236 2002 738 749
10. F. Bussolino, M.F. Di Renzo, M. Ziche, E. Bocchietto, M. Olivero, L. Naldini, G. Gaudino, L. Tamagnone, A. Coffer, and P.M. Comoglio Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth J. Cell Biol. 119 1992 629 641
11. T.C. Chou, Q.H. Tan, and F.M. Sirotnak Quantitation of the synergistic interaction of edatrexate and cisplatin in vitro Cancer Chemother. Pharmacol. 31 1993 259 264
12. M.J. Cross, J. Dixelius, T. Matsumoto, and L. Claesson-Welsh VEGF-receptor signal transduction Trends Biochem. Sci. 28 2003 488 494
13. S.E. DePrimo, L.M. Wong, D.B. Khatry, S.L. Nicholas, W.C. Manning, B.D. Smolich, A.M. O'Farrell, and J.M. Cherrington Expression profiling of blood samples from an SU5416 Phase III metastatic colorectal cancer clinical trial: a novel strategy for biomarker identification BMC Cancer 3 2003 3
14. R. Erber, A. Thurnher, A.D. Katsen, G. Groth, H. Kerger, H.P. Hammes, M.D. Menger, A. Ullrich, and P. Vajkoczy Combined inhibition of VEGF- and PDGF-signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms FASEB J. 18 2004 338 340
15. N. Ferrara, H.P. Gerber, and J. LeCouter The biology of VEGF and its receptors Nat. Med. 9 2003 669 676
16. W. Fiedler, R. Mesters, H. Tinnefeld, S. Loges, P. Staib, U. Duhrsen, M. Flasshove, O.G. Ottmann, W. Jung, F. Cavalli, R. Kuse, J. Thomalla, H. Serve, A.M. O'Farrell, M. Jacobs, N.M. Brega, P. Scigalla, D.K. Hossfeld, and W.E. Berdel A phase 2 clinical study of SU5416 in patients with refractory acute myeloid leukemia Blood 102 2003 2763 2767
17. T.A. Fong, L.K. Shawver, L. Sun, C. Tang, H. App, T.J. Powell, Y.H. Kim, R. Schreck, X. Wang, W. Risau, A. Ullrich, K.P. Hirth, and G. McMahon 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. 59 1999 99 106
18. K. Fujimoto, R. Hosotani, M. Wada, J.U. Lee, T. Koshiba, Y. Miyamoto, S. Tsuji, S. Nakajima, R. Doi, and M. Imamura Expression of two angiogenic factors, vascular endothelial growth factor and platelet-derived endothelial cell growth factor in human pancreatic cancer, and its relationship to angiogenesis Eur. J. Cancer 34 1998 1439 1447
19. F.J. Giles, M.A. Cooper, L. Silverman, J.E. Karp, J.E. Lancet, M. Zangari, P.J. Shami, K.D. Khan, A.L. Hannah, J.M. Cherrington, D.A. Thomas, G. Garcia-Manero, M. Albitar, H.M. Kantarjian, and A.T. Stopeck Phase II study of SU5416â€"a small-molecule, vascular endothelial growth factor tyrosine-kinase receptor inhibitorâ€"in patients with refractory myeloproliferative diseases Cancer 97 2003 1920 1928
20. J.F. Girmens, A. Erginay, P. Massin, P. Scigalla, A. Gaudric, and S. Richard Treatment of von Hippelâ€"Lindau retinal hemangioblastoma by the vascular endothelial growth factor receptor inhibitor SU5416 is more effective for associated macular edema than for hemangioblastomas Am. J. Ophthalmol. 136 2003 194 196
21. N. Ikeda, M. Adachi, T. Taki, C. Huang, H. Hashida, A. Takabayashi, M. Sho, Y. Nakajima, H. Kanehiro, M. Hisanaga, H. Nakano, and M. Miyake Prognostic significance of angiogenesis in human pancreatic cancer Br. J. Cancer 79 1999 1553 1563
22. J. Itakura, T. Ishiwata, H. Friess, H. Fujii, Y. Matsumoto, M.W. Buchler, and M. Korc Enhanced expression of vascular endothelial growth factor in human pancreatic cancer correlates with local disease progression Clin. Cancer Res. 3 1997 1309 1316
23. J. Itakura, T. Ishiwata, B. Shen, M. Kornmann, and M. Korc Concomitant over-expression of vascular endothelial growth factor and its receptors in pancreatic cancer Int. J. Cancer 85 2000 27 34
24. A.D. Jacobs Gemcitabine-based therapy in pancreas cancer: gemcitabine-docetaxel and other novel combinations Cancer 95 2002 923 927
25. R.S. Kerbel Human tumor xenografts as predictive preclinical models for anticancer drug activity in humans: better than commonly perceived†"but they can be improved Cancer Biol. Ther. 2 2003 S134 S139
26. R. Kerbel, and J. Folkman Clinical translation of angiogenesis inhibitors Nat. Rev., Cancer 2 2002 727 739
27. R.S. Kerbel, A. Viloria-Petit, G. Klement, and J. Rak 'Accidental' anti-angiogenic drugs. Anti-oncogene directed signal transduction inhibitors and conventional chemotherapeutic agents as examples Eur. J. Cancer 36 2000 1248 1257
28. J. Klem Current studies with PTK787, an oral inhibitor of vascular endothelial growth factor in colorectal cancer Clin. Colorectal Cancer 3 2003 147 149
29. R. Kuehn, P.I. Lelkes, C. Bloechle, A. Niendorf, and J.R. Izbicki Angiogenesis, angiogenic growth factors, and cell adhesion molecules are upregulated in chronic pancreatic diseases: angiogenesis in chronic pancreatitis and in pancreatic cancer Pancreas 18 1999 96 103
30. B.C. Kuenen, L. Rosen, E.F. Smit, M.R. Parson, M. Levi, R. Ruijter, H. Huisman, M.A. Kedde, P. Noordhuis, W.J. van der Vijgh, G.J. Peters, G.F. Cropp, P. Scigalla, K. Hoekman, H.M. Pinedo, and G. Giaccone Dose-finding and pharmacokinetic study of cisplatin, gemcitabine, and SU5416 in patients with solid tumors J. Clin. Oncol. 20 2002 1657 1667
31. B.C. Kuenen, J. Tabernero, J. Baselga, F. Cavalli, E. Pfanner, P.F. Conte, S. Seeber, S. Madhusudan, G. Deplanque, H. Huisman, P. Scigalla, K. Hoekman, and A.L. Harris Efficacy and toxicity of the angiogenesis inhibitor SU5416 as a single agent in patients with advanced renal cell carcinoma, melanoma, and soft tissue sarcoma Clin. Cancer Res. 9 2003 1648 1655
32. B.C. Kuenen, M. Levi, J.C. Meijers, V.W. van Hinsbergh, J. Berkhof, A.K. Kakkar, K. Hoekman, and H.M. Pinedo Potential role of platelets in endothelial damage observed during treatment with cisplatin, gemcitabine, and the angiogenesis inhibitor SU5416 J. Clin. Oncol. 21 2003 2192 2198
33. E.L. Lund, M.W. Olsen, K.E. Lipson, G. McMahon, A.R. Howlett, and P.E. Kristjansen Improved effect of an antiangiogenic tyrosine kinase inhibitor (SU5416) by combinations with fractionated radiotherapy or low molecular weight heparin Neoplasia 5 2003 155 160
34. S. McKenna, and M. Eatock The medical management of pancreatic cancer: a review Oncologist 8 2003 149 160
35. B. Meister, F. Grunebach, F. Bautz, W. Brugger, F.M. Fink, L. Kanz, and R. Mohle Expression of vascular endothelial growth factor (VEGF) and its receptors in human neuroblastoma Eur. J. Cancer 35 1999 445 449
36. D.B. Mendel, A.D. Laird, B.D. Smolich, R.A. Blake, C. Liang, A.L. Hannah, R.M. Shaheen, L.M. Ellis, S. Weitman, L.K. Shawver, and J.M. Cherrington Development of SU5416, a selective small molecule inhibitor of VEGF receptor tyrosine kinase activity, as an anti-angiogenesis agent Anticancer Drug Des. 15 2000 29 41
37. J.A. Nagy, L.F. Brown, D.R. Senger, N. Lanir, W.L. Van de, A.M. Dvorak, and H.F. Dvorak Pathogenesis of tumor stroma generation: a critical role for leaky blood vessels and fibrin deposition Biochim. Biophys. Acta 948 1989 305 326
38. J.A. Nagy, E.S. Morgan, K.T. Herzberg, E.J. Manseau, A.M. Dvorak, and H.F. Dvorak Pathogenesis of ascites tumor growth: angiogenesis, vascular remodeling, and stroma formation in the peritoneal lining Cancer Res. 55 1995 376 385
39. S.S.W. Ng, M.S. Tsao, S. Chow, and D.W. Hedley Inhibition of phosphatidylinositide 3-kinase enhances gemcitabine-induced apoptosis in human pancreatic cancer cells Cancer Res. 60 2000 5451 5455
40. M. Niedergethmann, R. Hildenbrand, B. Wostbrock, M. Hartel, J.W. Sturm, A. Richter, and S. Post High expression of vascular endothelial growth factor predicts early recurrence and poor prognosis after curative resection for ductal adenocarcinoma of the pancreas Pancreas 25 2002 122 129
41. M. Prewett, J. Huber, Y. Li, A. Santiago, W. O'Connor, K. King, J. Overholser, A. Hooper, B. Pytowski, L. Witte, P. Bohlen, and D.J. Hicklin Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis and growth of several mouse and human tumors Cancer Res. 59 1999 5209 5218
42. H. Qu, J.A. Nagy, D.R. Senger, H.F. Dvorak, and A.M. Dvorak Ultrastructural localization of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) to the abluminal plasma membrane and vesiculovacuolar organelles of tumor microvascular endothelium J. Histochem. Cytochem. 43 1995 381 389
43. G. Schuch, O. Kisker, A. Atala, and S. Soker Pancreatic tumor growth is regulated by the balance between positive and negative modulators of angiogenesis Angiogenesis 5 2002 181 190
44. R.M. Shaheen, D.W. Davis, W. Liu, B.K. Zebrowski, M.R. Wilson, C.D. Bucana, D.J. McConkey, G. McMahon, and L.M. Ellis Antiangiogenic therapy targeting the tyrosine kinase receptor for vascular endothelial growth factor receptor inhibits the growth of colon cancer liver metastasis and induces tumor and endothelial cell apoptosis Cancer Res. 59 1999 5412 5416
45. C.C. Solorzano, C.H. Baker, C.J. Bruns, J.J. Killion, L.M. Ellis, J. Wood, and I.J. Fidler Inhibition of growth and metastasis of human pancreatic cancer growing in nude mice by PTK 787/ZK222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases Cancer Biother. Radiopharm. 16 2001 359 370
46. T. Trinh, A. Abdollahi, R. Krempien, L. Hlatky, K.E. Lipson, and P.E. Huber SU5416 and SU6668 decrease angiogenic effects of radiation-induced factor productions by tumor cells and amplify the direct anti-endothelial action of radiation in vitro Int. J. Radiat. Oncol. Biol. Phys. 57 2003 S319
47. Z.Q. Wang, J.S. Li, G.M. Lu, X.H. Zhang, Z.Q. Chen, and K. Meng Correlation of CT enhancement, tumor angiogenesis and pathologic grading of pancreatic carcinoma World J. Gastroenterol. 9 2003 2100 2104
48. A.A. Yunis, G.K. Arimura, and D.J. Russin Human pancreatic carcinoma (MIA PaCa-2) in continuous culture: sensitivity to asparaginase Int. J. Cancer 19 1977 218 235