Vascular endothelial growth factor (VEGF) receptor-2 signaling mediates VEGF-CΔNΔC- and VEGF-A-induced angiogenesis in vitro

Experimental Cell Research

Volumn 285, Issue 2, 2003, Pages 286-298

  Tille, Jean Christophe ^a   Wang, Xueyan ^b   Lipson, Kenneth E ^b   McMahon, Gerald ^b   Ferrara, Napoleone ^c   Zhu, Zhenping ^d   Hicklin, Daniel J ^d   Sleeman, Jonathan P ^e   Eriksson, Ulf ^f   Alitalo, Kari ^g   Pepper, Michael S ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b SUGEN INC   (United States)

^c GENENTECH INC   (United States)

^d ELI LILLY AND COMPANY   (United States)

^e KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^f LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^g UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Angiogenesis; Endothelium; Lymphangiogenesis; Plasminogen activator; VEGF A; VEGF C; VEGFR 2

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PLASMINOGEN ACTIVATOR INHIBITOR 1; SEMAXANIB; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A; VASCULOTROPIN ANTIBODY; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL INVASION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WILD TYPE;

BOVINAE;

EID: 0345269272     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00053-3     Document Type: Article

References (55)

1. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6:2000;389-395.
2. Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am. J. Physiol. Cell Physiol. 280:2001;C1358-C1366.
3. Jussila L., Alitalo K. Vascular growth factors and lymphangiogenesis. Physiol. Rev. 82:2002;673-700.
4. Jeltsch M., Kaipainen A., Joukov V., Meng X., Lakso M., Rauvala H., Swartz M., Fukumura D., Jain R.K., Alitalo K. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 276:1997;1423-1425.
5. Mandriota S.J., Jussila L., Jeltsch M., Compagni A., Baetens D., Prevo R., Banerji S., Huarte J., Montesano R., Jackson D.G., Orci L., Alitalo K., Christofori G., Pepper M.S. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J. 20:2001;672-682.
6. Dumont D.J., Jussila L., Taipale J., Lymboussaki A., Mustonen T., Pajusola K., Breitman M., Alitalo K. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science. 282:1998;946-949.
7. Valtola R., Salven P., Heikkila P., Taipale J., Joensuu H., Rehn M., Pihlajaniemi T., Weich H., deWaal R., Alitalo K. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am. J. Pathol. 154:1999;1381-1390.
8. Kubo H., Fujiwara T., Jussila L., Hashi H., Ogawa M., Shimizu K., Awane M., Sakai Y., Takabayashi A., Alitalo K., Yamaoka Y., Nishikawa S.I. Involvement of vascular endothelial growth factor receptor-3 in maintenance of integrity of endothelial cell lining during tumor angiogenesis. Blood. 96:2000;546-553.
9. Witzenbichler B., Asahara T., Murohara T., Silver M., Spyridopoulos I., Magner M., Principe N., Kearney M., Hu J.S., Isner J.M. Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am. J. Pathol. 153:1998;381-394.
10. Cao Y., Linden P., Farnebo J., Cao R., Eriksson A., Kumar V., Qi J.H., Claesson-Welsh L., Alitalo K. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc. Natl. Acad. Sci. USA. 95:1998;14389-14394.
11. Joukov V., Sorsa T., Kumar V., Jeltsch M., Claesson-Welsh L., Cao Y., Saksela O., Kalkkinen N., Alitalo K. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 16:1997;3898-3911.
12. Pepper M.S., Mandriota S.J., Jeltsch M., Kumar V., Alitalo K. 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. J. Cell Physiol. 177:1998;439-452.
13. Mandriota S.J., Menoud P.A., Pepper M.S. Transforming growth factor beta 1 down-regulates vascular endothelial growth factor receptor 2/flk-1 expression in vascular endothelial cells. J. Biol. Chem. 271:1996;11500-11505.
14. Pepper M.S., Mandriota S.J. Regulation of vascular endothelial growth factor receptor-2 (Flk-1) expression in vascular endothelial cells. Exp. Cell Res. 241:1998;414-425.
15. Pepper M.S., Ferrara N., Orci L., Montesano R. Potent synergism between vascular endothelial growth factor and basic fibroblast growth factor in the induction of angiogenesis in vitro. Biochem. Biophys. Res. Commun. 189:1992;824-831.
16. Pepper M.S., Ferrara N., Orci L., Montesano R. Leukemia inhibitory factor (LIF) inhibits angiogenesis in vitro. J. Cell Sci. 108:(Pt 1):1995;73-83.
17. Keyt B.A., Nguyen H.V., Berleau L.T., Duarte C.M., Park J., Chen H., Ferrara N. 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. 271:1996;5638-5646.
18. Gerber H.P., McMurtrey A., Kowalski J., Yan M., Keyt B.A., Dixit V., Ferrara N. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 273:1998;30336-30343.
19. 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. 15:1996;290-298.
20. Kirkin V., Mazitschek R., Krishnan J., Steffen A., Waltenberger J., Pepper M.S., Giannis A., Sleeman J.P. Characterization of indolinones which preferentially inhibit VEGF-C- and VEGF-D-induced activation of VEGFR-3 rather than VEGFR-2. Eur. J. Biochem. 268:2001;5530-5540.
21. Joukov V., Kumar V., Sorsa T., Arighi E., Weich H., Saksela O., Alitalo K. A recombinant mutant vascular endothelial growth factor-C that has lost vascular endothelial growth factor receptor-2 binding, activation, and vascular permeability activities. J. Biol. Chem. 273:1998;6599-6602.
22. Olofsson B., Pajusola K., Kaipainen A., von Euler G., Joukov V., Saksela O., Orpana A., Pettersson R.F., Alitalo K., Eriksson U. Vascular endothelial growth factor B, a novel growth factor for endothelial cells. Proc. Natl. Acad. Sci. USA. 93:1996;2576-2581.
23. Olofsson B., Korpelainen E., Pepper M.S., Mandriota S.J., Aase K., Kumar V., Gunji Y., Jeltsch M.M., Shibuya M., Alitalo K., Eriksson U. Vascular endothelial growth factor B (VEGF-B) binds to VEGF receptor-1 and regulates plasminogen activator activity in endothelial cells. Proc. Natl. Acad. Sci. USA. 95:1998;11709-11714.
24. Rockwell P., Neufeld G., Glassman A., Caron D., Goldstein N.I. In vitro neutralization of vascular endothelial growth factor activation of Flk-1 by a monoclonal antibody. Mol. Cell. Differ. 3:1995;91-109.
25. Zhu Z., Lu D., Kotanides H., Santiago A., Jimenez X., Simcox T., Hicklin D.J., Bohlen P., Witte L. Inhibition of vascular endothelial growth factor induced mitogenesis of human endothelial cells by a chimeric anti-kinase insert domain-containing receptor antibody. Cancer Lett. 136:1999;203-213.
26. Witte L., Hicklin D.J., Zhu Z., Pytowski B., Kotanides H., Rockwell P., Bohlen P. Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev. 17:1998;155-161.
27. Goldstein N.I., Prewett M., Zuklys K., Rockwell P., Mendelsohn J. Biological efficacy of a chimeric antibody to the epidermal growth factor receptor in a human tumor xenograft model. Clin. Cancer Res. 1:1995;1311-1318.
28. Fong T.A., Shawver L.K., Sun L., Tang C., App H., Powell T.J., Kim Y.H., Schreck R., Wang X., Risau W., Ullrich A., Hirth K.P., 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. 59:1999;99-106.
29. Furie M.B., Cramer E.B., Naprstek B.L., Silverstein S.C. Cultured endothelial cell monolayers that restrict the transendothelial passage of macromolecules and electrical current. J. Cell Biol. 98:1989;1033-1041.
30. Pepper M.S., Montesano R., el Aoumari A., Gros D., Orci L., Meda P. Coupling and connexin 43 expression in microvascular and large vessel endothelial cells. Am. J. Physiol. 262:1992;C1246-C1257.
31. Montesano R., Orci L. Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell. 42:1985;469-477.
32. Shibuya M. Structure and dual function of vascular endothelial growth factor receptor-1 (Flt-1). Int. J. Biochem. Cell Biol. 33:2001;409-420.
33. Pepper M.S., Montesano R., Mandriota S.J., Orci L., Vassalli J.D. Angiogenesis a paradigm for balanced extracellular proteolysis during cell migration and morphogenesis . Enzyme Protein. 49:1996;138-162.
34. Yee K.W., O'Farrell A.M., Smolich B.D., Cherrington J.M., McMahon G., Wait C.L., McGreevey L.S., Griffith D.J., Heinrich M.C. SU5416 and SU5614 inhibit kinase activity of wild-type and mutant FLT3 receptor tyrosine kinase. Blood. 100:2002;2941-2949.
35. Gille H., Kowalski J., Li B., LeCouter J., Moffat B., Zioncheck T.F., Pelletier N., Ferrara N. Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J. Biol. Chem. 276:2001;3222-3230.
36. Yang S., Toy K., Ingle G., Zlot C., Williams P.M., Fuh G., Li B., De Vos A., Gerritsen M.E. Vascular endothelial growth factor-induced genes in human umbilical vein vein endothelial cells relative roles of KDR and Flt-1 receptors . Arterioscler. Thromb. Vasc. Bio. 22:2002;1797-1803.
37. Murphy J.F., Fitzgerald D.J. Vascular endothelial growth factor induces cyclooxygenase-dependent proliferation of endothelial cells via the VEGF-2 receptor. FASEB J. 15:2001;1667-1669.
38. Shen B.Q., Lee D.Y., Cortopassi K.M., Damico L.A., Zioncheck T.F. Vascular endothelial growth factor KDR receptor signaling potentiates tumor necrosis factor-induced tissue factor expression in endothelial cells. J. Biol. Chem. 276:2001;5281-5286.
39. Shen B.Q., Lee D.Y., Zioncheck T.F. Vascular endothelial growth factor governs endothelial nitric-oxide synthase expression via a KDR/Flk-1 receptor and a protein kinase C signaling pathway. J. Biol. Chem. 274:1999;33057-33063.
40. Bematchez P.N., Soker S., Sirois M.G. Vascular endothelial growth factor effect on endothelial cell proliferation, migration, and platelet-activating factor synthesis is Flk-1-dependent. J. Biol. Chem. 274:1999;31047-31054.
41. Suarez S., Ballmer-Hofer K. VEGF transiently disrupts gap junctional communication in endothelial cells. J. Cell Sci. 114:2001;1229-1235.
42. 2+ mobilization in human umbilical vein endothelial cells. Am. J. Physiol. 276:1999;C176-C181.
43. Veikkola T., Jussila L., Makinen T., Karpanen T., Jeltsch M., Petrova T., Kubo H., Thurston G., McDonald D.M., Achen M.G., Stacker S.A., Alitalo K. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20:2001;1223-1231.
44. Enholm B., Karpanen T., Jeltsch M., Kubo H., Stenback F., Prevo R., Jackson D.G., Yla-Herttuala S., Alitalo K. Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ. Res. 88:2001;623-629.
45. Karkkainen M.J., Makinen T., Alitalo K. Lymphatic endothelium a new frontier of metastasis research . Nat. Cell Biol. 4:2002;E2-E5.
46. Koolwijk P., Peters E., van der Vecht B., Hornig C., Weich H.A., Alitalo K., Hicklin D.J., Wu Y., Witte L., van Hinsbergh V.W. Involvement of VEGFR-2 (kdr/flk-1) but not VEGFR-1 (flt-1) in VEGF-A and VEGF-C-induced tube formation by human microvascular endothelial cells in fibrin matrices in vitro. Angiogenesis. 4:2001;53-60.
47. Hamada K., Oike Y., Takakura N., Ito Y., Jussila L., Dumont D.J., Alitalo K., Suda T. VEGF-C signaling pathways through VEGFR-2 and VEGFR-3 in vasculoangiogenesis and hematopoiesis. Blood. 96:2000;3793-3800.
48. Kadambi A., Carreira C.M., Yun C.O., Padera T.P., Dolmans D.E., Carmeliet P., Fukumura D., Jain R.K. Vascular endothelial growth factor (VEGF)-C differentially affects tumor vascular function and leukocyte recruitment role of VEGF-receptor 2 and host VEGF-A . Cancer Res. 61:2001;2404-2408.
49. Pepper M.S. Role of the matrix metalloproteinase and plasminogen activator-plasmin systems in angiogenesis. Arterioscler. Thromb. Vasc. Biol. 21:2001;1104-1117.
50. Dubor F., Dosne A.M., Chedid L.A. Effect of polymyxin B and colimycin on induction of plasminogen antiactivator by lipopolysaccharide in human endothelial cell culture. Infect. Immun. 52:1986;725-729.
51. Yang S., Xin X., Zlot C., Ingle G., Fuh G., Li B., Moffat B., de Vos A.M., Gerritsen M.E. Vascular endothelial cell growth factor-driven endothelial tube formation is mediated by vascular endothelial cell growth factor receptor-2, a kinase insert domain-containing receptor. Arterioscler. Thromb. Vasc. Biol. 21:2001;1934-1940.
52. Bernatchez P.N., Rollin S., Soker S., Sirois M.G. Relative effects of VEGF-A and VEGF-C on endothelial cell proliferation, migration and PAF synthesis role of neuropilin-1 . J. Cell Biochem. 85:2002;629-639.
53. Makinen T., Olofsson B., Karpanen T., Hellman U., Soker S., Klagsbrun M., Eriksson U., Alitalo K. Differential binding of vascular endothelial growth factor B splice and proteolytic isoforms to neuropilin-1. J. Biol. Chem. 274:1999;21217-21222.
54. Karkkainen M.J., Saaristo A., Jussila L., Karila K.A., Lawrence E.C., Pajusola K., Bueler H., Eichmann A., Kauppinen R., Kettunen M.I., Yla-Herttuala S., Finegold D.N., Ferrell R.E., Alitalo K. A model for gene therapy of human hereditary lymphedema. Proc. Natl. Acad. Sci. USA. 98:2001;12677-12682.
55. Neufeld G., Cohen T., Shraga N., Lange T., Kessler O., Herzog Y. The neuropilins multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis . Trends Cardiovasc. Med. 12:2002;13-19.