Proteolytic processing regulates receptor specificity and activity of VEGF-C

EMBO Journal

Volumn 16, Issue 13, 1997, Pages 3898-3911

  Joukov, Vladimir ^a   Sorsa, Tarja ^a   Kumar, Vijay ^a   Jeltsch, Michael ^a   Claesson Welsh, Lena ^c   Cao, Yihai ^d   Saksela, Olli ^b   Kalkkinen, Nisse ^a   Alitalo, Kari ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Angiogenesis; Growth factor; Proteolytic processing; VEGF; VEGF C

Indexed keywords

GROWTH FACTOR RECEPTOR; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DISULFIDE BOND; FAMILY; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; YEAST;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; COS CELLS; DIMERIZATION; DISULFIDES; ENDOPEPTIDASES; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; HUMANS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RABBITS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 0031011529     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.13.3898     Document Type: Article

References (54)

1. Andersson, M., Östman, A., Bäckström, G., Hellman, U., George-Nascimento, C., Westermark, B. and Heldin, C.-H. (1992) Assignment of interchain disulfide bonds in platelet-derived growth factor (PDGF) and evidence for agonist activity of monomeric PDGF. J. Biol. Chem., 267, 11260-11266.
2. Apella, E., Weber, I.T. and Blasi, F. (1988) Structure and function of epidermal growth factor-like regions in proteins. FEBS Lett., 231, 1-4.
3. Aprelikova, O. et al. (1992) FLT4, a novel class III receptor tyrosine kinase in chromosome 5q33-qter. Cancer Res., 52, 746-748.
4. 5 integrin, and interferes with HeLa cell spreading. Mol. Cell. Biol., 15, 711-722.
5. Cao, Y. et al. (1996) Heterodimers of placenta growth factor/vascular endothelial growth factor. Endothelial activity, tumor cell expression, and high affinity binding to Flk-1/KDR. J. Biol. Chem., 271, 3154-3162.
6. Carmeliet, P. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature, 380, 435-439.
7. Clauss, M., Weich, H., Breiter, G., Knies, U., Röckl, W., Waltenberger, J. and Risau, W. (1996) The vascular endothelial growth factor receptor Fit-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J. Biol. Chem., 271, 17629-17634.
8. 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.
9. DiSalvo, J., Bayne, M.L., Conn, G., Kwok, P.W., Trivedi, P.G., Soderman, D.D., Palisi, T.M., Sullivan, K.A. and Thomas, K.A. (1995) Purification and characterization of a naturally occurring vascular endothelial growth factor-placenta growth factor heterodimer. J. Biol. Chem., 270, 7717-7723.
10. Dubois, C.M., Laprise, M.-H., Blanchette, F., Gentry, L.E. and Leduc, R. (1995) Processing of transforming growth factor β1 precursor by human furin convertase. J. Biol. Chem., 270, 10618-10624.
11. Dvorak, H.F., Brown, L.F., Detmar, M. and Dvorak, A.M. (1995) Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol., 146, 1029-1039.
12. Ferrara, N. (1997) The biology of vascular endothelial growth factor. Endocrine Rev., 18, 4-25.
13. Ferrara, N., Carvermoore, K., Chen, H., Dowd, M., Lu, L., Oshea, K.S., Powellbraxton, L., Hillan, K.J. and Moore, M.W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature, 380, 439-442.
14. Folkman, J., Haudenschild, C.C. and Zetter, B.R. (1979) Long-term culture of capillary endothelial cells. Proc. Natl Acad. Sci. USA, 76, 5217-5221.
15. Galland, F., Karamysheva, A., Pebusque, M.-J., Borg, J.-P., Rottapel, R., Dubreuil, P., Rosnet, O. and Birnbaum, D. (1993) The FLT4 gene encodes a transmembrane tyrosine kinase related to the vascular endothelial growth factor receptor. Oncogene, 8, 1233-1240.
16. Grimmond, S. et al. (1996) Cloning and characterization of a novel human gene related to vascular endothelial growth factor. Genome Res., 6, 124-131.
17. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
18. Harlow, E. and Lane, D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. Heldin, C.H., Ostman, A. and Westermark, B. (1993) Structure of platelet-derived growth factor: implications for functional properties. Growth Factors, 8, 245-252.
20. Houck, K., Leung, D., Rowland, A., Winer, J. and Ferrara, N. (1992) Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J. Biol. Chem., 267, 26031-26037.
21. Jeltsch, M. et al. (1997) Hyperplasia lymphatic vessels in VEGF-C transgenic mice. Science, 276, 1423-1425.
22. Joukov, V., Pajusola, K., Kaipainen, A., Chilov, D., Lahtinen, I., Kukk, E., Saksela, O., Kalkkinen, N. and Alitalo, K. (1996) 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., 5, 290-298.
23. Kaipainen, A., Korhonen, J., Mustonen, T., van Hinsberg, V., Fang, G.-H., Dumont, D., Breitman, M. and Alitalo, K. (1995) Expression of the FLT4 receptor tyrosine kinase becomes restricted to endothelium of lymphatic vessels and some high endothelial venules during development. Proc. Natl Acad. Sci. USA, 92, 3566-3570.
24. Kenney, W.C., Haniu, M., Herman, A.C., Arakawa, T., Costigan, V.J., Lary, J., Yphantis, D.A. and Thomason, A.R. (1994) Formation of mitogenically active PDGF-B dimer does not require interchain disulfide bonds. J. Biol. Chem., 269, 12351-12359.
25. Keyt, B.A., Berleau, L.T., Nguyen, H.V., Chen, H., Heinsohn, H., Vandlen, R. and Ferrara, N. (1996a) The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J. Biol. Chem., 271, 7788-7795.
26. Keyt, B.A., Nguyen, H.V., Berleau, L.T., Duarte, C.M., Park, J., Chen, H. and Ferrara, N. (1996b) Identification of vascular endothelial growth factor determinants for binding KDR and FLT-1 receptors. Generation of receptor-selective VEGF variants by site-directed mutagenesis. J. Biol. Chem., 271, 5638-5646.
27. Klagsbrun, M. and D'Amore, P. (1996) Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev., 7, 259-270.
28. Kukk, E., Lymboussaki, A., Taira, S., Kaipainen, A., Jeltsch, M., Joukov, V. and Alitalo, K. (1996) VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development, 122, 3829-3837.
29. La Rochelle, W.J., May-Siroff, M., Robbins, K.C. and Aaronson, S.A. (1991) A novel mechanism regulating growth factor association with the cell surface: identification of PDGF retention domain. Genes Dev., 5, 1191-1199.
30. Lee, J., Gray, A., Yuan, J., Luoh, S.M., Avraham, H. and Wood, W.I. (1996) Vascular endothelial growth factor-related protein - a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc. Natl Acad. Sci. USA, 93, 1988-1992.
31. Maglione, D., Guerriero, V., Viglietto, G., Delli-Bovi, P. and Persico, M.G. (1991) Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc. Natl Acad. Sci. USA, 88, 9267-9271.
32. Miles, A.A. and Miles, E.M. (1952) Vascular reactions to histamine, histamine-inhibitor, and leukotaxine in the skin of guinea pigs. J. Physiol., 118, 228-257.
33. Miyazono, K., Ten Dijke, P., Ichijo, H. and Heldin, C.-H. (1994) Receptors for transforming growth factor-beta. Adv. Immunol., 55, 181-220.
34. Mustonen, T. and Alitalo, K. (1995) Endothelial receptor tyrosine kinases involved in vasculogenesis and angiogenesis. J. Cell Biol., 129, 895-898.
35. Naka, D., Ishii, T., Yoshiyama, Y., Miyazawa, K., Hara, H., Hishida, T. and Kitamura, N. (1992) Activation of hepatocyte growth factor by proteolytic conversion of a single chain form to a heterodimer. J. Biol. Chem., 267, 20114-20119.
36. Oefner, C., Arcy, A.D., Winkler, F.K., Eggimann, B. and Hosang, M. (1992) Crystal structure of human platelet-derived growth factor BB. EMBO J., 11, 3921-3926.
37. Olofsson, B. et al. (1996a) Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc. Natl Acad. Sci. USA, 93, 2576-2581.
38. Olofsson, B., Pajusola, K., von Euler, G., Chilov, D., Alitalo, K. and Eriksson, U. (1996b) Genomic organization of the mouse and human genes for vascular endothelial growth factor B (VEGF-B) and characterization of a second splice isoform. J. Biol. Chem., 271, 19310-19317.
39. Orlandini, M., Marconcini, L., Ferruzzi, R. and Oliviero, S. (1996) Identification of a c-fos induced gene that is related to the platelet-derived growth factor/vascular endothelial growth factor family. Proc. Natl Acad. Sci. USA, 93, 11675-11680.
40. Östman, A., Rall, L., Hammacher, A., Wormstead, M.A., Coit, D., Valenzuela, P., Betsholtz, C., Westermark, B. and Heldin, C.-H. (1988) Synthesis and assembly of a functionally active recombinant platelet-derived growth factor AB heterodimer. J. Biol. Chem., 263, 16202-16208.
41. Östman, A., Thyberg, J., Westermark, B. and Heldin, C.-H. (1992) PDGF-AA and PDGF-BB biosynthesis: proprotein processing in the Golgi complex and lysosomal degradation of PDGF-BB retained intracellularly. J. Cell Biol., 118, 509-519.
42. Pajusola, K., Aprelikova, O., Korhonen, J., Kaipainen, A., Pertovaara, L., Alitalo, R. and Alitalo, K. (1992) FLT4 receptor tyrosine kinase contains seven immunoglobulin-like loops and is expressed in multiple human tissues and cell lines. Cancer Res., 52, 5738-5743.
43. Pajusola, K., Aprelikova, O., Armstrong, E., Morris, S. and Alitalo, K. (1993) Two human FLT4 receptor tyrosine kinase isoforms with distinct carboxy terminal tails are produced by alternative processing of primary transcripts. Oncogene, 8, 2931-2937.
44. Pajusola, K., Aprelikova, O., Pelicci, G., Weich, H., Claesson-Welsh, L. and Alitalo, K. (1994) Signalling properties of FLT4, a proteolytically processed receptor tyrosine kinase related to two VEGF receptors. Oncogene, 9, 3545-3555.
45. Park, J.E., Chen, H.H., Winer, J., Houck, K.A. and Ferrara, N. (1994) Placenta growth factor. J. Biol. Chem., 269, 25646-25654.
46. Pertovaara, L., Kaipainen, A., Mustonen, T., Orpana, A., Ferrara, N., Saksela, O. and Alitalo, K. (1994) Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells. J. Biol. Chem., 269, 6271-6274.
47. Pötgens, A.J.G., Lubsen, N.H., van Altena, M.C., Vermeulen, R., Bakker, A., Schoenmakers, J.G.G., Ruiter, D.J. and de Waal, R.M.W. (1994) Covalent dimerization of vascular permeability factor/vascular endothelial growth factor is essential for its biological activity. J. Biol. Chem., 269, 32879-32885.
48. Shalaby, F., Rossant, J., Yamaguchi, T. P., Gertsenstein, M., Wu, X.-F., Breitman, M. and Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature, 376, 62-66.
49. Shibuya, M. (1995) Role of VEGF-FLT receptor system in normal and tumor angiogenesis Adv. Cancer Res., 67, 281-316.
50. Taipale, J. and Keski-Oja, J. (1997) Growth factors in the extracellular matrix. FASEB J., 11, 51-59.
51. Terman, B.C., Dougher-Vermazen, M., Carrion, M.E., Dimitrov, D., Armellino, D.C., Gospodarowicz, D. and Böhlen, P. (1992) Identification of the KDR tyrosine kinase as a receptor for vascular endothelial growth factor. Biochem. Biophys. Res. Commun., 187, 1579-1586.
52. Udaka, K., Takeuchi, Y. and Movat, H.Z. (1970) Simple method for quantitation of enhanced vascular permeability. Proc. Soc. Exp. Biol. Med., 133, 1384-1387.
53. Vigna, E., Naldini, L., Tamagnone, L., Longati, P., Bardelli, A., Maina, F., Ponzetto, C. and Comoglio, P.M. (1994) Hepatocyte growth factor and its receptor, the tyrosine kinase encoded by the c-MET proto-oncogene. Cell. Mol. Biol., 40, 597-604.
54. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M. and Heldin, C.-H. (1994) Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J. Biol. Chem., 269, 26988-26995.