Vascular endothelial growth factor (VEGF)-C synergizes with basic fibroblast growth factor and VEGF in the induction of angiogenesis in vitro and alters endothelial cell extracellular proteolytic activity

Journal of Cellular Physiology

Volumn 177, Issue 3, 1998, Pages 439-452

  Pepper, Michael S ^a   Mandriota, Stefano J ^a   Jeltsch, Michael ^b   Kumar, Vijay ^b   Alitalo, Kari ^b  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 ANTIPLASMIN; BASIC FIBROBLAST GROWTH FACTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HORMONE ACTION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATTLE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; DRUG SYNERGISM; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; LYMPHOKINES; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDE HYDROLASES; PLASMINOGEN ACTIVATOR INHIBITOR 1; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CELL SURFACE; URINARY PLASMINOGEN ACTIVATOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; VASCULAR ENDOTHELIAL GROWTH FACTORS;

ANIMALIA; BOVINAE;

EID: 0031784561     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199812)177:3<439::AID-JCP7>3.0.CO;2-2     Document Type: Article

References (60)

1. Achen, M.G., Jeltsch, M., Kukk, E., Mäkinen, T., Vitali, A., Wilks, A.F., Alitalo, K., and Stacker, S.A. (1998) 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. U.S.A., 95:548-553.
2. Asahara, T., Bauters, C., Zheng, L.P., Takeshita, S., Bunting, S., Ferrara, N., Symes, J.F., and Isner, J.M. (1995) Synergistic effect of vascular endothelial growth factor and basic fibroblast growth factor on angiogenesis in vivo. Circulation, 92(Suppl II):II365-II371.
3. Christofori, G. (1997) The role of fibroblast growth factors in tumour progression and angiogenesis. In: Tumour Angiogenesis. R. Bicknell, C.E. Lewis, and N. Ferrara, eds. Oxford University Press, Cambridge, pp. 201-237.
4. 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.
5. Ferrara, N., and Davis-Smyth, T. (1997) The biology of vascular endothelial growth factor. Endocr. Rev., 18:4-25.
6. Finnerty, H., Kelleher, K., Morris, G.E., Bean, K., Merberg, D.M., Kriz, R., Morris, J.C., Sookdeo, H., Turner, K.J., and Wood, C.R. (1993) Molecular cloning of murine FLT and FLT4. Oncogene, 8:2293-2298.
7. Fisher, R., Waller, E.K., Grossi, G., Thompson, D., Tizard, R., and Schleuning, W.D. (1985) Isolation and characterization of the human tissue-type plasminogen activator structural gene including its 5′ flanking region. J. Biol. Chem., 260:11223-11230.
8. Flaumenhaft, R., and Rifkin, D.B. (1992) The extracellular regulation of growth factor action. Mol. Biol. Cell., 3:1057-1065.
9. Folkman, J. (1995) Clinical applications of research on angiogenesis. N. Engl. J. Med., 333:1757-1763.
10. Fong, G.H., Rossant, J., Gertsenstein, M., and Breitman, M.L. (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature, 376:66-70.
11. Furie, M.B., Cramer, E.B., Naprstek, B.L., and Silverstein, S.C. (1984) Cultured endothelial cell monolayers that restrict the transendothelial passage of macromolecules and electrical current. J. Cell. Biol., 98:1033-1041.
12. 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.
13. Goto, F., Goto, K., Weindel, K., and Folkman, J. (1993) Synergistic effects of vascular endothelial growth factor and basic fibroblast growth factor on the proliferation and cord formation of bovine capillary endothelial cells within collagen gels. Lab. Invest., 69:508-517.
14. Hu, D.E., and Fan, T.P.D. (1995) Suppression of VEGF-induced angiogenesis by the protein tyrosine kinase inhibitor, lavendustin A. Br. J. Pharmacol., 114:262-268.
15. Jeltsch, M., Kaipainen, A., Joukov Meng, X., Lakso, M., Rauvala, H., Swartz, M., Fukumura, D., Jain, R.K., and Alitalo, K. (1997) Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science, 276:1423-1425.
16. 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., 15:290-298.
17. Joukov, V., Sorsa, T., Kumar, V., Claesson-Welsh, L., Cao, Y., Saksela, O., Kalkkinen, N., and Alitalo, K. (1997) Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J., 16:3898-3911.
18. Kaipainen, A., Korhonen, J., Mustonen, T., van Hinsbergh, V.W.M., Fang, G.H., Dumont, D., Breitman, M., and Alitalo, K. (1995) Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl. Acad. Sci. U.S.A., 92:3566-3570.
19. Kandel, J., Bossy-Wetzel, E., Radvanyl, F., Klagsbrun, M., Folkman, J., and Hanahan, D. (1991) Neovascularization is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell, 66:1095-1104.
20. Klagsbrun, M., and D'Amore, P.A. (1991) Regulators of angiogenesis. Annu. Rev. Physiol., 53:217-239.
21. Krätzschmar, J., Haendler, B., Kojima, S., Rifkin, D.B., and Schleuning, W.D. (1993) Bovine urokinase-type plasminogen activator and its receptor: Cloning and induction by retinoic acid. Gene, 125:177-183.
22. 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, 122:3829-3827.
23. 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. U.S.A., 93:1988-1992.
24. Leek, R.D., Harris, A.L., and Lewis, C.E. (1994) Cytokine networks in solid human tumors: Regulation of angiogenesis. J. Leukoc. Biol., 56:423-435.
25. Mandriota, S.J., Seghezzi, G., Vassalli, J.D., Ferrara, N., Wasi, S., Mazzieri, R., Mignatti, P., and Pepper, M.S. (1995) Vascular endothelial growth factor increases urokinase receptor expression in vascular endothelial cells. J. Biol. Chem., 270:9709-9716.
26. Mandriota, S.J., Menoud, P.A., and Pepper, M.S. (1996) Transforming growth factor-1 downregulates vascular endothelial growth factor receptor-2/flk-1 expression in vascular endothelial cells. J. Biol. Chem., 271:11500-11505.
27. Mandriota, S.J., and Pepper, M.S. (1997) Vascular endothelial growth factor-induced in vitro angiogenesis and plasminogen activator expression are dependent on endogenous basic fibroblast growth factor. J. Cell. Sci., 110:2293-2302.
28. 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.
29. Millauer, B., Shawver, L.K., Plate, K.H., Risau, W., and Ullrich, A. (1994) Glioblastoma growth inhibited in vivo by a dominant negative Flk-1 mutant. Nature, 367:576-579.
30. Millauer, B., Longhi, M.P., Plate, K.H., Shawver, L.K., Risau, W., Ullrich, A., and Strawn, L.M. (1996) Dominant negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo. Cancer Res., 56:1615-1620.
31. Min, H.Y., Doyle, L.V., Vitt, C.R., Zandonella, L., Stratton-Thomas, J.R., Shuman, M.A., and Rosenberg, S. (1996) Urokinase receptor antagonists inhibit angiogenesis and primary tumor growth in syngeneic mice. Cancer Res., 56:2428-2433.
32. Montesano, R., and Orci, L. (1985) Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell, 42:469-477.
33. Montesano, R., Vassalli, J.D., Baird, A., Guillemin, R., and Orci, L. (1986) Basic fibroblast growth factor induces angiogenesis in vitro. Proc. Natl. Acad. Sci. U.S.A., 83:7297-7301.
34. Mustonen, T., and Alitalo, K. (1995) Endothelial receptor tyrosine kinases involved in angiogenesis. J. Cell. Biol., 129:895-898.
35. Nathan, C., and Sporn, M. (1991) Cytokines in context. J. Cell. Biol., 113:981-986.
36. Olofsson, B., Korpelainen, E., Pepper, M.S., Mandriota, S.J., Aase, K., Kumar, V., Gunji, Y., Jeltsch, M., Shibuya, M., Alitalo, K., and Eriksson, U. (1998) VEGF-B binds to VEGFR-1 and regulates plasminogen activator activity in endothelial cells. Proc. Natl. Acad. Sci. USA (in press).
37. Paavonen, K., Horelli-Kuitunen, N., Chilov, D., Kukk, E., Pennanen, S., Kallioniemi, O.P., Pajusola, K., Olofsson, B., Eriksson, U., Joukov, V., Palotie, A., and Alitalo, K. (1996) Novel human vascular endothelial growth factor genes VEGF-B and VEGF-C localize to chromosomes 11q13 and 4q34, respectively. Circulation, 93:1079-1082.
38. Pepper, M.S. (1997) Manipulating angiogenesis: From basic science to the bedside. Arterioscler. Thromb. Vasc. Biol., 17:605-619.
39. Pepper, M.S., and Montesano, R. (1991) Proteolytic balance and capillary morphogenesis. Cell Differ. Dev., 32:319-328.
40. Pepper, M.S., and Mandriota, S.J. (1998) Regulation of vascular endothelial growth factor receptor-2 (Flk-1) expression in vascular endothelial cells. Exp. Cell Res., 241:414-425.
41. Pepper, M.S., Belin, D., Montesano, R., Orci, L., and Vassalli, J.D. (1990) Transforming growth factor beta-1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J. Cell. Biol., 111:743-755.
42. Pepper, M.S., Ferrara, N., Orci, L., and Montesano, R. (1991) Vascular endothelial growth factor (VEGF) induces plasminogen activators and plasminogen activator inhibitor-1 in microvascular endothelial cells. Biochem. Biophys. Res. Commun., 181:902-906.
43. Pepper, M.S., Ferrara, N., Orci, L., and Montesano, R. (1992a) Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem. Biophys. Res. Commun., 189:824-831.
44. Pepper, M.S., Montesano, R., El Aoumari, A., Gros, D., Orci, L., and Meda, P. (1992b) Coupling and connexin 43 expression in microvascular and large vessel endothelial cells. Am. J. Physiol., 262:C1246-C1257.
45. Pepper, M.S., Sappino, A.P., Stöcklin, R., Montesano, R., Orci, L., and Vassalli, J.D. (1993a) Upregulation of urokinase receptor expression on migrating endothelial cells. J. Cell. Biol., 122:673-684.
46. Pepper, M.S., Vassalli, J.D., Orci, L., and Montesano, R. (1993b) Biphasic effect of transforming growth factor-beta 1 on in vitro angiogenesis. Exp. Cell Res., 204:356-363.
47. Pepper, M.S., Wasi, S., Ferrara, N., Orci, L., and Montesano, R. (1994) In vitro angiogenic and proteolytic properties of bovine lymphatic endothelial cells. Exp. Cell Res., 210:298-305.
48. Pepper, M.S., Ferrara, N., Orci, L., and Montesano, R. (1995a) Leukemia inhibitory factor (LIF) is a potent inhibitor of in vitro angiogenesis. J. Cell. Sci., 108:73-83.
49. Pepper, M.S., Soriano, J.V., Menoud, P.A., Sappino, A.P., Orci, L., and Montesano, R. (1995b) Modulation of hepatocyte growth factor and c-met expression in the rat mammary gland during pregnancy, lactation and involution. Exp. Cell Res., 219:204-210.
50. Pepper, M.S., Mandriota, S.J., Vassalli, J.D., Orci, L., and Montesano, R. (1996a) Angiogenesis regulating cytokines: Activities and interactions. Attempts to understand metastasis formation. Curr. Top. Microbiol. Immunol., 213:31-67.
51. Pepper, M.S., Montesano, R., Mandriota, S.J., Orci, L., and Vassalli, J.D. (1996b) Angiogenesis: A paradigm for balanced extracellular proteolysis during cell migration and morphogenesis. Enzyme Protein, 49:138-162.
52. Quinn, T.P., Peters, K.G., De Vries, C., Ferrara, N., and Williams, L.T. (1993) Fetal liver kinase-1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc. Natl. Acad. Sci. U.S.A., 90:7533-7537.
53. Sage, E.H. (1997) Pieces of eight: Bioactive fragments of extracellular proteins as regulators of angiogenesis. Trends Cell Biol,. 7:182-186.
54. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. U.S.A., 74:5463-5467.
55. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., and Schuh, A.C. (1995) Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature, 376:62-66.
56. Soff, G.A., Sanderowitz, J., Gately, S., Verrusio, E., Weiss, I., Brem, S., and Kwaan, H.C. (1995) Expression of plasminogen activator inhibitor type 1 by human prostate carcinoma cells inhibits primary tumor growth, tumor-associated angiogenesis, and metastasis to lung and liver in an athymic mouse model. J. Clin. Invest., 96:2593-2600.
57. Sporn, M.B., and Roberts, A.B. (1988) Peptide growth factors are multifunctional. Nature, 332:217-219.
58. Tessier, D.C., Thomas, D.Y., Khouri, H.E., Laliberte, F., and Vernet, T. (1991) Enhanced secretion from insect cells of a foreign protein fused to the honeybee melittin signal peptide. Gene, 98:177-183.
59. Thomas, K.A. (1996) Vascular endothelial growth factor, a potent and selective angiogenic agent. J. Biol. Chem., 271:603-606.
60. Vassalli, J.D., Dayer, J.M., Wohlwend, A., and Belin, D. (1984) Concomitant secretion of prourokinase and of a plasminogen activator-specific inhibitor by cultured human monocytes-macrophages. J. Exp. Med., 159:1653-1668.