Targeting vascular endothelial growth factor (VEGF) for anti-tumor therapy, by anti-VEGF neutralizing monoclonal antibodies or by VEGF receptor tyrosine-kinase inhibitors

Cancer and Metastasis Reviews

Volumn 18, Issue 4, 1999, Pages 473-481

  Schlaeppi, Jean Marc ^a   Wood, Jeanette M ^a  

^a NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Angiogenesis; Kinase inhibitor; Neutralizing antibody; VEGF; VEGFR

Indexed keywords

3 [(4,5 DIMETHYL 1H PYRROL 2 YL)METHYLENE] 1,3 DIHYDRO 2H INDOL 2 ONE; CANCER ANTIBODY; NEUTRALIZING ANTIBODY; PROTEIN TYROSINE KINASE INHIBITOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN ANTIBODY; VASCULOTROPIN RECEPTOR;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER TRANSPLANTATION; CARCINOMA; DRUG EFFICACY; HUMAN; NONHUMAN; PRIORITY JOURNAL; TUMOR VASCULARIZATION;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; ENDOTHELIAL GROWTH FACTORS; ENZYME INHIBITORS; HUMANS; LYMPHOKINES; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN-TYROSINE KINASES; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0033513497     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006358220123     Document Type: Article

References (71)

1. 1. Risau W: Mechanisms of angiogenesis. Nature 386: 671-674, 1997
2. 2. Folkman J: Angiogenesis in cancer, vascular, rheumatoid and other disease. Nature Med 1: 27-31, 1995
3. 3. Hanahan D, Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86: 353-364, 1996
4. 4. Weidner N: Tumoural vascularity as a prognostic factor in cancer patients: the evidence continues to grow. J Pathol 184: 119-122, 1998
5. 5. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF: Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219: 983-985, 1983
6. 6. Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246: 1306-1309, 1989
7. 7. Keck PJ, Hauser SD, Krivi G, Sanzo K, Warren T, Feder J, Connolly DT: Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246: 1309-1312, 1989
8. 8. Darland DC, D'Amore PA: Blood vessel maturation: vascular development comes of age. J Clin Invest 103: 157-158, 1999
9. 9. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG: Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 88: 9267-9271, 1991
10. 10. Olofsson B, Pajusola K, Kaipainen A, von-Euler G, Joukov V, Saksela O, Orpana A, Pettersson RF, Alitalo K, Eriksson U: Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc Natl Acad Sci USA 93: 2576-2581, 1996
11. 11. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K: A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15: 290-298, 1996
12. 12. Achen MG, Jeltsch M, Kukk E, Mäkinen T, Vitali A, Wilks AF, Alitalo K, Stacker SA: Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95: 548-553, 1998
13. 13. Meyer M, Clauss M, Lepple-Wienhues A, Waltenberger J, Augustin HG, Ziche M, Lanz C, Büttner M, Rziha HJ, Dehio C: A novel vascular endothelial growth factor encoded by Orf virus, VEGF-E, mediates angiogenesis via signalling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor tyrosine kinases. EMBO J 18: 363-374, 1999
14. 14. Tischer E, Mitchell R, Hartman T, Silva M, Gospodarowicz D, Fiddes JC, Abraham JA: The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J Biol Chem 266: 11947-11954, 1991
15. 145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J Biol Chem 272: 7151-7158, 1997
16. 16. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N: Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267: 26031-26037, 1992
17. 17. De Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT: The fins-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255: 989-991, 1992
18. 18. Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, Böhlen P: Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun 187: 1579-1586, 1992
19. 19. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z: Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13: 9-22, 1999
20. 20. Ferrara N, Davis-Smyth T: The biology of vascular endothelial growth factor. Endocrine Rev 18: 4-25, 1997
21. 21. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A: Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439, 1996
22. 22. Paley PJ, Staskus KA, Gebhard K, Mohanraj D, Twiggs LB, Carson LF, Ramakrishnan S: Vascular endothelial growth factor expression in early stage ovarian carcinoma. Cancer 80: 98-106, 1997
23. 23. Maeda K, Chung Y-S, Ogawa Y, Takatsuka S, Kang S-M, Ogawa M, Sawada T, Sowa M: Prognostic value of vascular endothelial growth factor expression in gastric carcinoma. Cancer 77: 858-863, 1996
24. 24. Volm M, Koomägi R, Mattern J: Prognostic value of vascular endothelial growth factor and its receptor Flt-1 in squamous cell lung cancer. Int J Cancer 74: 64-68, 1997
25. 25. Gasparini G, Toi M, Gion M, Verderio P, Dittadi R, Hanatani M, Matsubara I, Vinante O, Bonoldi E, Boracchi P, Gatti C, Suzuki H, Tominaga T: Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. J Natl Cancer Inst 89: 139-147, 1997
26. 26. Eppenberger U, Kueng W, Schlaeppi J-M, Roesel JL, Benz C, Mueller H, Matter A, Zuber M, Luescher K, Litschgi M, Schmitt M, Foekens JA, Eppenberger-Castori S: Markers of tumor angiogenesis and proteolysis independently define high-and low-risk subsets of node-negative breast cancer patients. J Clin Oncol 16: 3129-3136, 1998
27. 27. 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 16: 3121-3128, 1998
28. 28. Yeo KT, Wang HH, Nagy JA, Sioussat TM, Ledbetter SR, Hoogewerf AJ, Zhou Y, Masse EM, Senger DR, Dvorak HF, Yeo TK: Vascular permeability factor (vascular endothelial growth factor) in guinea pig and human tumor and inflammatory effusions. Cancer Res 53: 2912-2918, 1993
29. 29. Freeman MR, Schneck FX, Gagnon ML, Corless C, Soker S, Niknejad K, Peoples GE, Klagsbrun M: Peripheral blood T lymphocytes and lymphocytes infiltrating human cancers express vascular endothelial growth factor: a potential role of T cells in angiogenesis. Cancer Res 55: 4140-4145, 1995
30. 30. Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK, Seed B: Tumor induction of VEGF promoter activity in stromal cells. Cell 94: 715-725, 1998
31. 31. Shweiki D, Itin A, Soffer D, Keshet E: Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843-845, 1992
32. 32. Okada F, Rak JW, St. Croix B, Lieubeau B, Kaya M, Roncari L, Shirasawa S, Sasazuki T, Kerbel RS: Impact of oncogenes in tumor angiogenesis: mutant K-ras upregulation of vascular endothelial growth factor/vascular permeability factor is necessary, but not sufficient for tumorigenicity of human colorectal carcinoma cells. Proc Natl Acad Sci USA 95: 3609-3614, 1998
33. 33. Rak J, Filmus J, Finkenzeller G, Grugel S, Marmé D, Kerbel RS: Oncogenes as inducers of tumor angiogenesis. Cancer Metastasis Rev 14: 263-277, 1995
34. 34. Kim KJ, Li B, Winer J, Armanini M, Gillett N, Phillips HS, Ferrara N: Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362: 841-844, 1993
35. 35. Millauer B, Shawver LK, Plate KH, Risau W, Ullrich A: Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 367: 576-578, 1994
36. 36. Cheng SY, Su Huang HJ, Nagane M, Ji XD, Wang D, Shih CCY, Arap W, Huang CM, Cavenee WK: Suppression of glioblastoma angiogenicity and tumorigenicity by inhibition of endogenous expression of vascular endothelial growth factor. Proc Natl Acad Sci USA 93: 8502-8507, 1996
37. 37. Witte L, Hicklin DJ, Zhu Z, Pytowski B, Kotanides H, Rockwell P, Böhlen P: Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev 17: 155-161, 1998
38. 38. Goldman CK, Kendall RL, Cabrera G, Soroceanu L, Heike Y, Gillespie GY, Siegal GP, Mao X, Bett AJ, Huckle WR, Thomas KA, Curiel DT: Paracrine expression of a native soluble vascular endothelial growth factor receptor inhibits tumor growth, metastasis, and mortality rate. Proc Natl Acad Sci USA 95: 8795-8800, 1998
39. 39. Fong TAT, Shawver LK, Sun L, Tang C, App H, Powell TJ, Kim YH, Schreck R, Wang X, Risau W, Ullrich A, Hirth KP, McMahon G: 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: 99-106, 1999
40. 40. Wood JM, Bold G, Buchdunger E, Ferrari S, Cozens R, Frei J, Stover D, Hofmann F, Mestan J, Towbin H, Schnell C, Mett H, O'Reilly T, Persohn E, Wood-Cook K, Rösel J, Siemeister G, Menrad A, Schirner M, Thierauch KH, Schneider MR, Tolzke F, Martiny-Baron G, Drevs J, Marmé D: PTK787/ZK 222584, a novel and potent inhibitor of VEGF receptor tyrosine kinases, impairs VEGF-induced responses and tumor growth after oral administration. Cancer Res (Provisionally accepted)
41. 121). Hybridoma 14: 475-480, 1995
42. 42. Asano M, Yukita A, Matsumoto T, Hanatani M, Suzuki H: An anti-human VEGF monoclonal antibody, MV833, that exhibits potent anti-tumor activity in vivo. Hybridoma 17: 185-190, 1998
43. 43. Schlaeppi JM, Siemeister G, Weindel K, Schnell C, Wood J: Characterization of a new potent, in vivo neutralizing monoclonal antibody to human vascular endothelial growth factor. J Cancer Res Clin Oncol 125: 336-342, 1999
44. 44. Schlaeppi J-M, Eppenberger U, Martiny-Baron G, Küng W: Chemiluminescence immunoassay for vascular endothelial growth factor (vascular permeability factor) in tumor-tissue homogenates. Clin Chem 42: 1777-1784, 1996
45. 45. Kondo S, Asano M, Suzuki H: Significance of vascular endothelial growth factor/vascular permeability factor for solid tumor growth and its inhibition by the antibody. Biochim Biophys Res Commun 194: 1234-1241, 1993
46. 46. Luo JC, Toyoda M, Shibuya M: Differential inhibition of fluid accumulation and tumor growth in two mouse ascites tumors by an antivascular endothelial growth factor/permeability factor neutralizing antibody. Cancer Res 58: 2594-2600, 1998
47. 47. Olson TA, Mohanraj D, Ramakrishnan S: In vivo neutralization of vascular endothelial growth factor (VEGF)/vascular permeability factor (VPF) inhibits ovarian carcinoma-associated ascites formation and tumor growth. Int J Onc 8: 505-511, 1996
48. 121. Cancer Res 55: 5296-5301, 1995
49. 49. Asano M, Yukita A, Suzuki H: Wide spectrum of antitumor activity of a neutralizing monoclonal antibody to human vascular endothelial growth factor. Jpn J Cancer Res 90: 93-100, 1999
50. 50. Bernsen HJJA, Rijken PFJW, Peters JPW, Bakker H, van der Kogel AJ: Delayed vascular changes after antiangiogenic therapy with antivascular endothelial growth factor antibodies in human glioma xenografts in nude mice. Neurosurgery 43: 570-575, 1998
51. 51. Borgström P, Hillan KJ, Sriramarao P, Ferrara N: Complete inhibition of angiogenesis and growth of microtumors by anti-vascular endothelial growth factor neutralizing antibody: novel concepts of angiostatic therapy from intravital videomicroscopy. Cancer Res 56: 4032-4039, 1996
52. 52. Borgström P, Bourdon MA, Hillan KJ, Sriramarao P, Ferrara N: Neutralizing anti-vascular endothelial growth factor antibody completely inhibits angiogenesis and growth of human prostate carcinoma micro tumors in vivo. Prostate 35: 1-10, 1998
53. 53. Melnyk O, Shuman MA, Kim KJ: Vascular endothelial growth factor promotes tumor dissemination by a mechanism distinct from its effect on primary tumor growth. Cancer Res 56: 921-924, 1996
54. 54. Melnyk O, Zimmerman M, Kim KJ, Shuman M: Neutralizing anti-vascular endothelial growth factor antibody inhibits further growth of established prostate cancer and metastases in a pre-clinical model. J Urol 161: 960-963, 1999
55. 55. Mesiano S, Ferrara N, Jaffe RB: Role of vascular endothelial growth factor in ovarian cancer. Inhibiton of Ascites formation by immunoneutralization. Am J Pathol 153: 1249-1256, 1998
56. 56. Warren RS, Yuan H, Matli MR, Gillet NA, Ferrara N: Regulation by vascular endothelial growth factor of human colon cancer tumorigenesis in a mouse model of experimental liver metastasis. J Clin Invest 95: 1789-1797, 1995
57. 57. Kanai T, Konno H, Tanaka T, Baba M, Matsumoto K, Nakamura S, Yukita A, Asano M, Suzuki H, Baba S: Anti-tumor and anti-metastatic effects of human-vascular-endothelial-growth-factor-neutralizing antibody on human colon and gastric carcinoma xenotransplanted orthotopically into nude mice. Int J Cancer 77: 933-936, 1998
58. 58. Yuan F, Chen Y, Dellian M, Safabakhsh N, Ferrara N, Jain RK: Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc Natl Acad Sci USA 93: 14765-14770, 1996
59. 59. Nagy JA, Masse EM, Herzberg KT, Meyers MS, Yeo KT, Yeo TK, Sioussat TM, Dvorak HF: Pathogenesis of ascites tumor growth: vascular permeability factor, vascular hyper-permeability, and ascites fluid accumulation. Cancer Res 55: 360-368, 1995
60. 60. Rak J, Filmus J, Kerbel RS: Reciprocal paracrine interactions between tumour cells and endothelial cells: the 'angiogenesis progression' hypothesis. Eur J Cancer 32A: 2438-2450, 1996
61. 61. Kim KJ, Li B, Houck K, Winer J, Ferrara N: The vascular endothelial growth factor proteins: identification of biologically relevant regions by neutralizing monoclonal antibodies. Growth Fact 7: 53-64, 1992
62. 62. Presta LG, Chen H, O'Connor SJ, Chisholm V, Meng YG, Krummen L, Winkler M, Ferrara N: Humanization of an anti-vascular endothelial growth factor monoclonal antibody for the therapy of solid tumors and other disorders. Cancer Res 57: 4593-4599, 1997
63. 63. Muller YA, Chen Y, Christinger HW, Li B, Cunningham BC, Lowman HB, De Vos AM: VEGF and the Fab fragment of a humanized neutralizing antibody: crystal structure of the complex at 2.4 Å resolution and mutational analysis of the interface. Structure 6: 1153-1167, 1998
64. 64. Muller YA, Li B, Christinger HW, Wells JA, Cunningham BC, De Vos AM: Vascular endothelial growth factor: crystal structure and functional mapping of the kinase domain receptor binding site. Proc Natl Acad Sci USA 94: 7192-7197, 1997
65. 65. Wiesmann C, Fuh G, Christinger HW, Eigenbrot C, Wells JA, De Vos AM: Crystal structure at 1.7 Å resolution of VEGF in complex with domain 2 of the Flt-1 receptor. Cell 91: 695-704, 1997
66. 66. Sun L, Tran N, Tang F, App H, Hirth P, McMahon G and Tang C: Synthesis and biological evaluation of 3-substituted indolin-2-ones: a novel class of tyrosine kinase inhibitors that exhibit selectivity towards particular receptor tyrosine kinases. J Med Chem 41: 2588-2603, 1998
67. 67. Xu L, Yoneda J, Herrera C, Wood J, Killion J, Fidler I: Inhibition of malignant ascites and growth of human ovarian carcinoma by oral administration of a potent inhibitor of VEGF receptor tyrosine kinases. Int J Oncol (Submitted)
68. 68. Yano S, Herbst R, Shinohara H, Knighton B, Bucana C, Killion J, Wood J, Fidler I: Treatment for malignant pleural effusion of human lung adenocarcinoma by inhibition of vascular endothelial growth factor receptor tyrosine kinase phosphorylation. Clin Cancer Res (In press)
69. 69. Ryan AM, Bates-Eppler D, Hagler KE, Bruner RH, Thomford PJ, Hall RL, Shopp GM, O'Neil CA: Preclinical safety evaluation of rhuMAbVEGF an antiangiogenic humanized monoclonal antibody. Toxicol Pathol 27: 78-86, 1999
70. 70. Margolin K, Gordon MS, Talpaz M, Fyfe G, Novotny W, Adelman D, Breed J: Phase Ib trial of intravenous (i.v.) recombinant humanized monoclonal antibody (MAb) to vascular endothelial growth factor (rhuMAbVEGF) in combination with chemotherapy (ChRx) in patients (pts) with advanced cancer (CA): pharmacologic and longterm safety data. Abstract, Americ Soc Clin Oncol 1678, 1999
71. 71. Salven P, Lymboussaki A, Heikkilä P, Jääskela-Saari H, Enholm B, Aase K, von Euler G, Eriksson U, Alitalo K, Joensuu H: Vascular endothelial growth factors VEGF-B and VEGF-C are expressed in human tumors. Am J Pathol 153: 103-107, 1998