Identification of a peptide blocking vascular endothelial growth factor (VEGF)-mediated angiogenesis

EMBO Journal

Volumn 19, Issue 7, 2000, Pages 1525-1533

  Binétruy Tournaire, Roselyne ^a   Demangel, Caroline ^b   Malavaud, Bernard ^c,d   Vassy, Roger ^a   Rouyre, Sylvie ^b   Kraemer, Michel ^a   Plouët, Jean ^d   Derbin, Claude ^a   Perret, Gérard ^a   Mazié, Jean Claude ^b  

^a UNIVERSITÉ PARIS 13   (France)

^b INSTITUT PASTEUR   (France)

^c CHU RANGUEIL   (France)

^d INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Angiogenesis; Antagonist peptides; KDR; Phage display; Vascular endothelial cell growth factor

Indexed keywords

MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CORNEA; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; RABBIT; TUMOR VASCULARIZATION; VASCULAR ENDOTHELIUM;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0343294352     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.7.1525     Document Type: Article

References (58)

1. Albini, A. et al. (1996) The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR on endothelial cells. Nature Med., 2, 1371-1375.
2. Albo, D., Granick, M.S., Jhala, N., Atkinson, B. and Solomon, M.P. (1994) The relationship of angiogenesis biological activity in human squamous cell carcinomas of the head and neck. Ann. Plastic Surg., 32, 588-594.
3. Ausprunk, D.H. and Folkman, J. (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during angiogenesis. Microvasc. Res., 14, 53-65.
4. Boehm, T., Folkman, J., Browder, T. and O'Reilly, M.S. (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature, 390, 404-407.
5. Bouck, N., Stellmach, V. and Hsu, S.C. (1996) How tumors become angiogenic. Adv. Cancer Res., 69, 135-174.
6. Cheng, S.Y., Huang, H.J.S., Nagane, M., Ji, X.D., Wang, D., Shih, C.C.Y., Arap, W., Huang, C.M. and Cavenee, W.K. (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.
7. Cliff, W.J. (1963) Observations on healing tissues: a combined light and electron microscopic investigation. Philos. Trans. R. Soc., 246, 305-325.
8. Cortese, R. et al. (1996) Selection of biologically active peptides by phage display of random peptides libraries. Curr. Opin. Biotechnol., 7, 616-621.
9. Cwirla, S.E., Peters, E.A., Barrett, R.W. and Dower, W.J. (1990) Peptides of phage: a vast library of peptides for identifying ligands. Proc. Natl Acad. Sci. USA, 87, 6378-6382.
10. Detmar, M., Brown, L.F., Claffey, K.P., Yeo, K.T., Kocher, O., Jackman, R.W., Berse, B. and Dvorak, H.F. (1994) Overexpression of vascular permeability factor/vascular endothelial growth factor and its receptor in psoriasis. J. Exp. Med., 180, 1141-1146.
11. De Vries, C., Escobedo, J.A., Ueno, H., Houck, K., Ferrara, N. and Williams, L.T. (1992) The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science, 255, 989-991.
12. Esko, J.D. (1991) Genetic analysis of proteoglycan structure, function and metabolism. Curr. Opin. Cell Biol., 3, 805-816.
13. Favard, C., Moukadiri, H., Dorey, C., Praloran, V. and Plouët, J. (1991) Purification and biological properties of vasculotropin, a new angiogenic cytokine. Biol. Cell, 73, 1-6.
14. Felici, F., Luzzago, A., Monaci, P., Nicosia, A., Sollazo, M. and Traboni, C. (1995) Peptide and protein display on the surface of filamentous bacteriophage. In Raafat El-Gewely, M. (ed.), Biotechnology Annual Review. Elsevier, Amsterdam, The Netherlands, pp. 149-183.
15. Ferrara, N. (1993) Vascular endothelial growth factor. Trends Cardiovasc. Med., 3, 244-250.
16. Ferrara, N. (1999) Molecular and biological properties of vascular endothelial growth factor. J. Mol. Med., 77, 527-543.
17. Ferrara, N. and Davis-Smyth, T. (1997) The biology of vascular endothelial growth factor. Endocr. Rev., 18, 4-25.
18. Ferrara, N. and Henzel, W.J. (1989) Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem. Biophys. Res. Commun., 161, 851-858.
19. Folkman, J. (1995a) Angiogenesis in cancer, vascular, rheumatoid and other diseases. Nature Med., 1, 27-30.
20. Folkman, J. (1995b) Clinical applications of research on angiogenesis. N. Engl. J. Med., 333, 1757-1763.
21. Gita-Goren, H., Soker, S., Vlodavsky, I. and Neufeld, G. (1992) The binding of vascular endothelial growth factor to its receptor is dependent on cell surface-associated heparin-like molecules. J. Biol. Chem., 267, 6093-6098.
22. Gita-Goren, H., Halaban, R. and Neufeld, G. (1993) Human melanoma cells but not normal melanocytes express vascular endothelial growth factor receptors. Biochem. Biophys. Res. Commun., 190, 702-709.
23. Goodson, R.J., Doyle, M.V., Kaufman, S.E. and Rosenberg, S. (1994) High-affinity urokinase receptor antagonists identified with bacteriophage peptide display. Proc. Natl Acad. Sci. USA, 91, 7129-7133.
24. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
25. Hoess, R.H. (1993) Phage display of peptide and protein domains. Curr. Opin. Struct. Biol., 3, 572-579.
26. Houck, K., Ferrara, N., Winer, J., Cachianes, G., Li, B. and Leung, D.W (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol., 5, 1806-1814.
27. Houck, K., Leung, D.W., Rowland, A.M., Winer, J. and Ferrara, N. (1992) Dual regulation of vascular endothelial growth factor biovailability by genetic and proteolytic mechanisms. J. Biol. Chem., 267, 26031-26036.
28. Kerbel, R.S. (1991) Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents. Bioassays, 13, 31-36.
29. Kim, K.J., Li, B., Winer, J., Armanini, M., Gillett, N., Philips, H.S. and Ferrara, N. (1993) Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumor growth in vivo. Nature, 362, 841-844.
30. Klagsbrun, M. and D'Amore, P.A. (1996) Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev., 7, 259-270.
31. Koivunen, E., Gay, D.A. and Ruoslahti, E. (1993) Selection of peptides binding to the α5β1 integrin from phage display library. J. Biol. Chem., 268, 20205-20210.
32. Leung, D.L., Cachianes, G., Kuang, W.J., Goeddel, D.V. and Ferrara, N. (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science, 246, 1306-1309.
33. Matthews, W., Jordan, C.T., Gavin, M., Jenkins, N.A., Copeland, N.G. and Lemischka, I.R. (1991) A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hematopoietic cells and exhibiting close genetic linkage to c-kit. Proc. Natl Acad. Sci. USA, 88, 9026-9030.
34. Millauer, B., Wizigmann-Voos, S., Schnürch, H., Martinez, R., Moller, N.P.H., 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.
35. Muller, Y.A., Christinger, H.W., Bruce, A.K. and De Vos, A.M. (1997a) The crystal structure of vascular endothelial growth factor (VEGF) refined to 1.93 Å resolution: multiple copy flexibility and receptor binding. Stucture, 5, 1325-1338.
36. Muller, Y.A., Li, S., Christinger, H.W., Wells, J.A., Cunningham, B.C. and De Vos, A.M. (1997b) Vascular endothelial growth factor: crystal structure and functional mapping of the kinase domain receptor binding site. Proc. Natl Acad. Sci. USA, 94, 7192-7197.
37. Myoken, Y., Kayada, Y., Okamoto, T., Kan, M., Sato, G.H. and Sato, J.D. (1991) Vascular endothelial cell growth factor (VEGF) produced by A-431 human epidermoid carcinoma cells and identification of VEGF membrane binding sites. Proc. Natl Acad. Sci. USA, 88, 5819-5823.
38. O'Neil, K.T., Hoess, R.H., Jackson, S.A., Ramachandran, N.S., Mousa, S.A. and Degrado, W.F. (1992) Identification of novel peptide antagonists for gpIIB/IIIa from a conformationally constrained phage peptide library. Proteins, 14, 509-515.
39. Ortéga, N., Jonca, F., Vincent, S., Favard, C., Malavaud, B., Ruchoux, M.-M. and Plouët, J. (1997) Systemic activation of the vascular endothelial growth factor receptor flk-1 selectively triggers angiogenic endothelial cells. Am. J. Pathol., 151, 1215-1224.
40. Peters, K.G., De Vries, C. and Williams, L.T. (1993) Vascular endothelial growth factor receptor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc. Natl Acad. Sci. USA, 90, 8915-8919.
41. Pierce, E.A., Avery, R.L., Foley, E.D., Aiello, L.P. and Smith, L.R.H. (1995) Vascular endothelial growth factor/vascular permeability factor expression in a mouse model of retinal neovascularization. Proc. Natl Acad. Sci. USA, 92, 905-909.
42. Plouët, J., Schilling, J. and Gospodarowicz, D. (1989) Isolation and characterization of newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J., 8, 3801-3806.
43. Plouët, J., Moro, F., Bertagnolli, S., Coldeboeuf, N., Mazarguil, H., Clamens, S. and Bayard, F. (1997) Extracellular cleavage of the vascular endothelial growth factor 189-amino acid form by urokinase is required for its mitogenic effect. J. Biol. Chem., 272, 13390-13396.
44. Scatchard, G. (1986) The attraction of proteins for small molecules and ions. Ann. NY Acad. Sci., 261, 4660-4662.
45. Schoefi, G.I. (1963) Studies on inflammation. III. Growing capillaries: their structure and permeability. Virchows Arch. Pathol. Anat., 337, 97-141.
46. Smith, G.P. (1985) Filamentous fusion phage: novel expression vectors that display cloned antigens on the virion surface. Science, 228, 1315-1317.
47. Soker, S., Takashima, S., Miao, H.Q., Neufeld, G. and Klagsbrun, M. (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell, 92, 735-745.
48. Terman, B.I., Carrion, M.E., Kovacs, E., Rasmussen, B.A., Eddy, R.L. and Shows, T.B. (1991) Identification of a new endothelial growth factor receptor tyrosine kinase. Oncogene, 6, 1677-1683.
49. Terman, B.I., Dougher-Vermazen, M., Carrion, M., Dimitrov, D., Armellino, D., Gospodarowicz, D. and Bohlen, P. (1992) Identification of the KDR tyrosine kinase as a receptor for vascular endothelial growth factor. Biochem. Biophys. Res. Commun., 187, 1579-1586.
50. Terman, B.I. et al. (1994) VEGF receptor subtypes KDR and FLT1 show different sensitivities to heparin and placenta growth factor. Growth Factors, 11, 187-195.
51. Tisher, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., Fiddes, J.C. and Abraham, J.A. (1991) The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem., 266, 11947-11954.
52. Thorpe, P.E and Burrows, F.J. (1995) Antibody-directed targeting of the vasculature of solid tumors. Breast Cancer Res. Treat., 36, 237-251.
53. Waltenberger, J., Claesson-Welsh, L., Siegbahn, M. and Heldin, C.H. (1994) Different signal transduction properties of KDR and FLT-1, two receptors for vascular endothelial growth factor. J. Biol. Chem., 269, 26988-26995.
54. Watters, J.M., Telleman, P. and Junghans, R.P. (1997) An optimized method for cell-based phage displayed panning. Immunotechnology, 3, 21-29.
55. Weidner, N., Semple, J.P., Welch, W.R. and Folkman, J. (1991) Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N. Engl. J. Med., 324, 1-8.
56. Wizigmann-Voos, S., Breier, G., Risau, W. and Plate, K.H. (1995) Up-regulation of vascular endothelial growth factor and its receptor in von Hippel-Lindau disease-associated and sporadic hemangioblastomas. Cancer Res., 55, 1358-1364.
57. Yayon, A., Aviezer, D., Safran, M., Gross, J.L., Heldman, Y., Cabilly, S., Givol, D. and Katchalski-Katzir, E. (1993) Isolation of peptides that inhibit binding of basic fibroblast growth factor to its receptor from a random phage-epitope library. Proc. Natl Acad. Sci. USA, 90, 10643-10647.
58. Young, R.C. (1989) Drug resistance: the clinical problem. Cancer Treat. Res., 48, 1-12.