Targeting vascular endothelial growth factor receptor-1 and -3 with cediranib (AZD2171): Effects on migration and invasion of gastrointestinal cancer cell lines

Molecular Cancer Therapeutics

Volumn 8, Issue 9, 2009, Pages 2546-2558

  Morelli, M Pia ^a,b   Brown, Amy M ^a   Pitts, Todd M ^a   Tentler, John J ^a   Ciardiello, Fortunato ^b   Ryan, Anderson ^c   Jürgensmeier, Juliane M ^c   Eckhardt, S Gail ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b SECOND UNIVERSITY OF NAPLES   (Italy)

^c ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CEDIRANIB; LIGAND; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ARTICLE; AUTOCRINE EFFECT; CANCER CELL CULTURE; CANCER INVASION; CARCINOMA CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; GASTROINTESTINAL CARCINOMA; GENE EXPRESSION; HUMAN; HUMAN CELL; LIVER CELL CARCINOMA; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SUPERNATANT;

ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GASTROINTESTINAL NEOPLASMS; GENE EXPRESSION PROFILING; HUMANS; NEOPLASM INVASIVENESS; QUINAZOLINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 70349495869     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0380     Document Type: Article

References (70)

1. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 2005;23:1011-1027 (Pubitemid 46202320)
2. Zetter BR. Angiogenesis and tumor metastasis. Ann Rev Med 1998;49:407-424
3. Wey JS, Stoeltzing O, Ellis LM. Vascular endothelial growth factor receptors: expression and function in solid tumors. Clin Adv Hematol Oncol 2004;2:37-45.
4. McMahon G. VEGF receptor signaling in tumor angiogenesis. Oncologist 2000;5 Suppl 1:3-10. (Pubitemid 30225450)
5. Ellis LM, Takahashi Y, Liu W, Shaheen RM. Vascular endothelial growth factor in human colon cancer: biology and therapeutic implications. The oncologist 2000;5 Suppl 1:11-15 (Pubitemid 30225451)
6. Linderholm B, Tavelin B, Grankvist K, Henriksson R. Vascular endothelial growth factor is of high prognostic value in node-negative breast carcinoma. J Clin Oncol 1998;16:3121-3128 (Pubitemid 28417435)
7. Linderholm B, Grankvist K, Wilking N, Johansson M, Tavelin B, Henriksson R.Correlation of vascular endothelial growth factor contentwith recurrences, survival, and first relapse site in primary node-positive breast carcinoma after adjuvant treatment. J Clin Oncol 2000;18:1423-1431 (Pubitemid 30205387)
8. Lee JC, Chow NH, Wang ST, Huang SM. Prognostic value of vascular endothelial growth factor expression in colorectal cancer patients. Eur J Cancer 2000;36:748-753 (Pubitemid 30179746)
9. Herbst RS, Onn A, Sandler A. Angiogenesis and lung cancer: prognostic and therapeutic implications. J Clin Oncol 2005;23:3243-3256 (Pubitemid 46211349)
10. O'Byrne KJ, Goddard J, Giatromanolaki A, Koukourakis MI. Vascular endothelial growth factor expression in non-small cell lung cancer. Methods Mol Med 2003;74:357-373
11. Li L, Wang L, Zhang W, et al. Correlation of serum VEGF levels with clinical stage, therapy efficacy, tumor metastasis and patient survival in ovarian cancer. Anticancer Res 2004;24:1973-1979 (Pubitemid 38954620)
12. Marion-Audibert AM, Barel C, Gouysse G, et al. Low microvessel density is an unfavorable histoprognostic factor in pancreatic endocrine tumors. Gastroenterology 2003;125:1094-1104 (Pubitemid 37193456)
13. Ugurel S, Rappl G, Tilgen W, Reinhold U. Increased serum concentration of angiogenic factors in malignant melanoma patients correlates with tumor progression and survival. J Clin Oncol 2001;19:577-583 (Pubitemid 32112873)
14. Schoell WM, Pieber D, Reich O, et al. Tumor angiogenesis as a prognostic factor in ovarian carcinoma: quantification of endothelial immunoreactivity by image analysis. Cancer 1997;80:2257-2262 (Pubitemid 28007396)
15. Yuan A, Yu CJ, Kuo SH, et al. 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 2001;19:432-441 (Pubitemid 32112856)
16. Galizia G, Lieto E, Ferraraccio F, et al. Determination of molecular marker expression can predict clinical outcome in colon carcinomas. Clin Cancer Res 2004;10:3490-3499
17. Galizia G, Lieto E, Ferraraccio F, et al. Prognostic significance of epidermal growth factor receptor expression in colon cancer patients undergoing curative surgery. Ann Surg Oncol 2006;13:823-835 (Pubitemid 43727367)
18. De Vita F, Orditura M, Lieto E, et al. Elevated perioperative serum vascular endothelial growth factor levels in patients with colon carcinoma. Cancer 2004;100:270-278 (Pubitemid 38063634)
19. Lurje G, Zhang W, Schultheis AM, et al. Polymorphisms in VEGF and IL-8 predict tumor recurrence in stage III colon cancer. Ann Oncol 2008;19:1734-1741
20. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004;350:2335-2342 (Pubitemid 38702844)
21. Heymach JV, Johnson BE, Prager D, et al. Randomized, placebo-controlled phase II study of vandetanib plus docetaxel in previously treated non small-cell lung cancer. J Clin Oncol 2007;25:4270-4277 (Pubitemid 47548567)
22. Wedge SR, Ogilvie DJ, Dukes M, et al. ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis, and tumor growth following oral administration. Cancer Res 2002;62:4645-4655 (Pubitemid 34898591)
23. Troiani T, Lockerbie O, Morrow M, Ciardiello F, Eckhardt SG. Sequence-dependent inhibition of human colon cancer cell growth and of prosurvival pathways by oxaliplatin in combination with ZD6474 (Zactima), an inhibitor of VEGFR and EGFR tyrosine kinases. Mol Cancer Ther 2006;5:1883-1894.
24. Troiani T, Serkova NJ, Gustafson DL, et al. Investigation of two dosing schedules of vandetanib (ZD6474), an inhibitor of vascular endothelial growth factor receptor and epidermal growth factor receptor signaling, in combination with irinotecan in a human colon cancer xenograft model. Clin Cancer Res 2007;13:6450-6458 (Pubitemid 350075035)
25. Tuccillo C, Romano M, Troiani T, et al. Antitumor activity of ZD6474, a vascular endothelial growth factor-2 and epidermal growth factor receptor small molecule tyrosine kinase inhibitor, in combination with SC-236, a cyclooxygenase-2 inhibitor. Clin Cancer Res 2005;11:1268-1276 (Pubitemid 40175780)
26. Miller KD, Trigo JM, Wheeler C, et al. A multicenter phase II trial of ZD6474, a vascular endothelial growth factor receptor-2 and epidermal growth factor receptor tyrosine kinase inhibitor, in patients with previously treated metastatic breast cancer. Clin Cancer Res 2005;11:3369-3376 (Pubitemid 40627889)
27. Abou-Alfa GK, Schwartz L, Ricci S, et al. Phase II study of sorafenib in patients with advanced hepatocellular carcinoma. J Clin Oncol 2006;24:4293-4300 (Pubitemid 46630787)
28. Escudier B, Eisen T, Stadler WM, et al. Sorafenib in advanced clearcell renal-cell carcinoma. N Engl J Med 2007;356:125-134 (Pubitemid 46089673)
29. Gridelli C, Maione P, Del Gaizo F, et al. Sorafenib and sunitinib in the treatment of advanced non-small cell lung cancer. Oncologist 2007;12:191-200. (Pubitemid 46271621)
30. Wilhelm SM, Carter C, Tang L, et al. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 2004;64:7099-7109 (Pubitemid 39331023)
31. Wedge SR, Kendrew J, Hennequin LF, et al. AZD2171: a highly potent, orally bioavailable, vascular endothelial growth factor receptor-2 tyrosine kinase inhibitor for the treatment of cancer. Cancer Res 2005;65:4389-4400 (Pubitemid 40775678)
32. Chow LQ, Eckhardt SG. Sunitinib: from rational design to clinical efficacy. J Clin Oncol 2007;25:884-896
33. Saltz LB, Rosen LS, Marshall JL, et al. Phase II trial of sunitinib in patients with metastatic colorectal cancer after failure of standard therapy. J Clin Oncol 2007;25:4793-4799 (Pubitemid 350086483)
34. Socinski MA, Novello S, Brahmer JR, et al. Multicenter, phase II trial of sunitinib in previously treated, advanced non-small-cell lung cancer. J Clin Oncol 2008;26:650-656 (Pubitemid 351264362)
35. Fan F, Wey JS, McCarty MF, et al. Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene 2005;24:2647-2653 (Pubitemid 40593092)
36. Lesslie DP, Summy JM, Parikh NU, et al. Vascular endothelial growth factor receptor-1 mediates migration of human colorectal carcinoma cells by activation of Src family kinases. Br J Cancer 2006;94:1710-1717 (Pubitemid 43924937)
37. Longatto Filho A, Martins A, Costa SM, Schmitt FC. VEGFR-3 expression in breast cancer tissue is not restricted to lymphatic vessels. Pathol Res Practice 2005;201:93-99 (Pubitemid 40443822)
38. Su JL, Yang PC, Shih JY, et al. The VEGF-C/Flt-4 axis promotes invasion and metastasis of cancer cells. Cancer Cell 2006;9:209-223 (Pubitemid 43357947)
39. Papazisis KT, Geromichalos GD, Dimitriadis KA, Kortsaris AH. Optimization of the sulforhodamine B colorimetric assay. J Immunol Methods 1997;208:151-158
40. Robinson CJ, Stringer SE. The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J Cell Sci 2001;114:853-865 (Pubitemid 32273121)
41. Arinaga M, Noguchi T, Takeno S, Chujo M, Miura T, Uchida Y. Clinical significance of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in patients with nonsmall cell lung carcinoma. Cancer 2003;97:457-464 (Pubitemid 36133813)
42. Bianco R, Rosa R, Damiano V, et al. Vascular endothelial growth factor receptor-1 contributes to resistance to anti-epidermal growth factor receptor drugs in human cancer cells. Clin Cancer Res 2008;14:5069-5080
43. Bando H, Weich HA, Horiguchi S, Funata N, Ogawa T, Toi M. The association between vascular endothelial growth factor-C, its corresponding receptor, VEGFR-3, and prognosis in primary breast cancer: a study with 193 cases. Oncol Rep 2006;15:653-659
44. Bando H, Brokelmann M, Toi M, et al. Immunodetection and quantification of vascular endothelial growth factor receptor-3 in human malignant tumor tissues. Int J Cancer 2004;111:184-191 (Pubitemid 38924694)
45. Lee TH, Seng S, Sekine M, et al. Vascular endothelial growth factor mediates intracrine survival in human breast carcinoma cells through internally expressed VEGFR1/FLT1. PLoS Med 2007;4:e186. (Pubitemid 46998627)
46. Wu Y, Zhong Z, Huber J, et al. Anti-vascular endothelial growth factor receptor-1 antagonist antibody as a therapeutic agent for cancer. Clin Cancer Res 2006;12:6573-6584 (Pubitemid 44799733)
47. Garces CA, Kurenova EV, Golubovskaya VM, Cance WG. Vascular endothelial growth factor receptor-3 and focal adhesion kinase bind and suppress apoptosis in breast cancer cells. Cancer Res 2006;66:1446-1454
48. Liu XE, Sun XD, Wu JM. Expression and significance of VEGF-C and FLT-4 in gastric cancer. World J Gastroenterol 2004;10:352-355 (Pubitemid 38208085)
49. Gray MJ, Van Buren G, Dallas NA, et al. Therapeutic targeting of neuropilin-2 on colorectal carcinoma cells implanted in the murine liver. J Natl Cancer Inst 2008;100:109-120
50. Juttner S, Wissmann C, Jons T, et al. Vascular endothelial growth factor-D and its receptor VEGFR-3: two novel independent prognostic markers in gastric adenocarcinoma. J Clin Oncol 2006;24:228-240 (Pubitemid 46622052)
51. Mimori K, Fukagawa T, Kosaka Y, et al. Hematogenous metastasis in gastric cancer requires isolated tumor cells and expression of vascular endothelial growth factor receptor-1. Clin Cancer Res 2008;14:2609-2616
52. Gockel I, Moehler M, Frerichs K, et al. Co-expression of receptor tyrosine kinases in esophageal adenocarcinoma and squamous cell cancer. Oncol Rep 2008;20:845-850
53. Moehler M, Frings C, Mueller A, et al. VEGF-D expression correlates with colorectal cancer aggressiveness and is downregulated by cetuximab. World J Gastroenterol 2008;14:4156-4167
54. Kodama M, Kitadai Y, Tanaka M, et al. Vascular endothelial growth factor c stimulates progression of human gastric cancer via both autocrine and paracrine mechanisms. Clin Cancer Res 2008;14:7205-7214
55. Laakkonen P, Waltari M, Holopainen T, et al. Vascular endothelial growth factor receptor 3 is involved in tumor angiogenesis and growth. Cancer Res 2007;67:593-599 (Pubitemid 46192197)
56. Padera TP, Kuo AH, Hoshida T, et al. Differential response of primary tumor versus lymphatic metastasis to VEGFR-2 and VEGFR-3 kinase inhibitors cediranib and vandetanib. Mol Cancer Ther 2008;7:2272-2279
57. Petrova TV, Bono P, Holnthoner W, et al. VEGFR-3 expression is restricted to blood and lymphatic vessels in solid tumors. Cancer Cell 2008;13:554-556 (Pubitemid 351763905)
58. Heckman CA, Holopainen T, Wirzenius M, et al. The tyrosine kinase inhibitor cediranib blocks ligand-induced vascular endothelial growth factor receptor-3 activity and lymphangiogenesis. Cancer Res 2008;68:4754-4762
59. Smith NR, James NH, Oakley I, et al. Acute pharmacodynamic and antivascular effects of the vascular endothelial growth factor signaling inhibitor AZD2171 in Calu-6 human lung tumor xenografts. Mol Cancer Ther 2007;6:2198-2208 (Pubitemid 47294748)
60. Yang AD, Camp ER, Fan F, et al. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res 2006;66:46-51. (Pubitemid 43166007)
61. Li J, Hong M, Pan T. Clinical significance of VEGF-C and VEGFR-3 expression in non-small cell lung cancer. Journal of Huazhong University of Science and Technology Medical sciences = Hua zhong ke ji da xue xue bao Yi xue Ying De wen ban = Huazhong keji daxue xuebao 2006;26:587-590
62. Takizawa H, Kondo K, Fujino H, et al. The balance of VEGF-C and VEGFR-3 mRNA is a predictor of lymph node metastasis in non-small cell lung cancer. Br J Cancer 2006;95:75-79 (Pubitemid 43980557)
63. Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 2002;1:219-227 (Pubitemid 41039145)
64. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocrine Rev 2004;25:581-611. (Pubitemid 39099316)
65. Yu L, Wu X, Cheng Z, et al. Interaction between bevacizumab and murine VEGF-A: a reassessment. Invest Ophthalmol Visual Sci 2008;49:522-527
66. Wey JS, Fan F, Gray MJ, et al. Vascular endothelial growth factor receptor-1 promotes migration and invasion in pancreatic carcinoma cell lines. Cancer 2005;104:427-438 (Pubitemid 40993273)
67. Abdelrahim M, Baker CH, Abbruzzese JL, et al. Regulation of vascular endothelial growth factor receptor-1 expression by specificity proteins 1, 3, and 4 in pancreatic cancer cells. Cancer Res 2007;67:3286-3294
68. Chen CN, Chang CC, Su TE, et al. Identification of calreticulin as a prognosis marker and angiogenic regulator in human gastric cancer. Anna Surg Oncol 2008;16:524-533
69. Han H, Silverman JF, Santucci TS, et al. Vascular endothelial growth factor expression in stage I non-small cell lung cancer correlates with neoangiogenesis and a poor prognosis. Ann Surg Oncol 2001;8:72-79 (Pubitemid 32126827)
70. Liao X, Siu MK, Au CW, et al. Aberrant activation of hedgehog signaling pathway in ovarian cancers: effect on prognosis, cell invasion and differentiation. Carcinogenesis 2008;30:131-140