Vascular endothelial growth factor induces VE-cadherin tyrosine

Journal of Cell Science

Volumn 111, Issue 13, 1998, Pages 1853-1865

  Esser, Sybille ^a   Lampugnani, Maria Grazia ^b   Corada, Monica ^b   Dejana, Elisabetta ^b   Risau, Werner ^a  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Adherens junction; Cadherin; Catenin; Endothelial cell; Vascular endothelial growth factor

Indexed keywords

BETA CATENIN; CD31 ANTIGEN; PHOSPHOTYROSINE; PLAKOGLOBIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ARTICLE; AUTOPHOSPHORYLATION; CELL MIGRATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION;

ANTIGENS, CD; CADHERINS; CAPILLARY PERMEABILITY; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; HUMANS; INTERCELLULAR JUNCTIONS; LYMPHOKINES; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; TIGHT JUNCTIONS; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0031825437     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (86)

1. Abedi, H. and Zachary, I. (1997). Vascular endothelial growth factor stimulates tyrosine phosphorvlation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothclial cells. J. Biol. Chem. 272, 15442-15451.
2. Ausprunk, D. H. and Folkman, J. (1977). Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc. Res. 14, 53-65.
3. Ayalon, O., Sabanai, H., Lampugnani, M. G., Dejana, K. and Geiger, B. (1994). Spatial and temporal relationships between cadherins and PECAM-1 in cell-cell junctions of human endothelial cells. J. Cell Biol. 126, 247-258.
4. Balsamo, J., Leung, T., Krnst, H., Zanin, M. K., Hoffman, S. and Lilien, J. (1996). Regulated binding of PTPIB-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of beta-catenin. J. Cell Biol. 134, 801-813.
5. Barleon, B., Siemeister, G., Martinybaron, G., Weindel, K., Herzog, C. and Marme, D. (1997). Vascular endothelial growth factor up-regulates its receptor tms-like tyrosine kinase 1 (Flt-l) and a soluble variant of Flt-l in human vascular endothelial cells. Cancer Res. 57, 5421-5425.
6. Barth, A. I., Nathke, I. S. and Nelson, W. J. (1997). Cadherins, catemns and APC Protein-interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 9, 683-690.
7. Behrens, J., Vakaet, L., Friis, R., Winterhager, E., Van Roy, F., Marcel, M. M. and Birchmeier, W. (1993). Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/beta-catenin complex in cells transformed with a temperature-sensitive v-SRC gene. J. Cell Biol. 120, 757-766.
8. Bikfalvi, A., Sauzeau, C., Moukadiri, H., Maclouf, J., Busso, N., Bryckaert, M., Plouet, J. and Tobelem, G. (1991). Interaction of vasculotropin/vascular endothelial cell growth factor with human umbilical vein endothelial cells: binding, internalization. degradation, and biological effects. J. Cell Physiol. 149, 50-59.
9. Brady-Kalnay, S. M., Rimm, D. L. and Tonks, N. K. (1995). Receptor protein-tyrosine-phosphatase ptp-mu associates with cadherins and catenins in-vivo. J. Cell Biol. 130, 977-986.
10. Braga, V. M., Machesky, L. M., Hall, A. and Hotchin, N. A. (1997). The small GTPases Rho and Rac are required for the establishment of cadherin-dependent cell-cell contacts. J. Cell Biol. 137, 1421-1431
11. Breier, G., Albrecht, U., Sterrer, S. and Risau, W. (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation Development 114, 521-532
12. Breier, G., Clauss, M. and Risau, W. (1995). Coordinate expression of vascular endothclial growth factor receptor-1 (flt-1) and its ligand suggests a paracrine regulation of murine vascular development. Dev. Dynam. 204, 228-239.
13. Breier, G., Breviario, F., Caveda, L., Berthier, R., Schnürch, H., Gotsch, U., Vestweber, D., Risau, W. and Dejana, K. (1996). Molecular cloning and expression of murine vascular endothelial cadherin in early stage development of cardiovascular system. Blood 87, 630-641.
14. Breier, G. and Risau, W. (1996) The role of vascular cndoihelial growth factor in blood vessel formation. Trends Cell Biol. 6, 454-456.
15. Breviario, F., Caveda, L., Corada, M., Martin-Padura, I., Navarro, P., Golay, J., Introna, M., Gulino, D., Lampugnani, M. G. and Dcjana, E. (1995). Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin. Arterioscler. Thromb. Vasc. Biol. 15, 1229-1239.
16. Caplan, K. A. and Schwartz, C. J. (1973). Increased endothelial cell turnover in areas of in sivo Evans Blue uptake in the pig aorta. Atherosclerosis 17, 401-417.
17. Caveda, L., Martin-Padura, I., Navarro, P., Breviario, F., Corada, M., Gulino, D., Lampugnani, M. G. and Dejana, K. (1996). Inhibition of cultured cell growth by vascular endothelial cadhenn (eadherin-5/VE-cadherin). J. Clin. Invest. 98, 886-893.
18. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
19. Clauss, M., Weich, H., Breier, G., Knies, U., Rockl, W., Waltenberger. J. and Risau, W. (1996). The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J. Biol. Client. 271, 17629-17634.
20. Connolly, D. T., Olander, J. V., Heuvelman, D., Nelson, R., Monsell, R., Siegel, N., Haymore, B. L., Leimgruber, R. and Feder, J. (1989) Human vascular permeability factor. Isolation from U937 cells. J. Biol. Chem. 264, 20017-20024.
21. Cunningham, S. A., Waxham, M. N., Arrate, P. M. and Brock, T. A. (1995) Interaction of the Flt-1 tyrosine kinase receptor with the P85 subunit of phosphatidylinositol 3-kinase-mapping of a novel site involved in binding. J. Biol. Chem. 270, 20254-20257.
22. D'Angelo, G., Struman, I., Martial, J. and Weiner, R. I. (1995) Activation of mitogen-activated protein kinases by vascular cndoihelial growth factor and basic fibroblast growth factor in capillary endothelial cells is inhibited by the antiangiogenic factor 16-kDa N-tcrminal fragment of prolactin. Proc. Nat. Acad. Sci. USA 92, 6374-6378.
23. Daniel, J. M. and Reynolds, A. B. (1997). Tyrosine phosphorylation and cadherin/catenin function [Review]. BioEssays 19, 883-891.
24. 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.
25. Detmar, M., Yeo, K. T., Nagy, J. A., Van de Water, L., Brown, L. F., Berse, B., Elickcr, B. M., Ledbetter, S. and Dvorak, H. F. (1995). Keratinocyte-derived vascular permeability factor (vascular endothelial growth factor) is a potent mitogen for dermal microvascular endothelial cells. J. Invest. Dermatol. 105, 44-50.
26. Downing, J. R. and Reynolds, A. B. (1991) PDGF. CSF-I, and BGF induce tyrosine phosphorylation of p120, a pp60src transformation-associated substrate. Oncogene 6, 607-613.
27. Esser, S., Wolburg, K., Wolburg, H., Breier, G., Kurzchalia, T. and Risau, W. (1998). Vascular endothelial growth factor induces endothelial fenestrations in vitro. J. Cell Biol. 140, 947-959.
28. Ferrero, E., Villa, A., Ferrero, M. E., Toninelli, E., Bender, J. R., Pardi, R. and Zocchi, M. R. (1996). Tumor necrosis factor alpha-induced vascular leakage involves PHCAM1 phosphorylation. Cancer Res. 56, 3211-3215.
29. Fuchs, M., Muller, T., Lerch, M. M. and UIlrich, A. (1996). Association of human protein-tyrosine phosphatasc kappa with members of the armadillo family. J. Biol. Chem. 271, 16712-16719.
30. Gaits, F., Li, R. Y., Ragab, A., Ragab-Thomas, J. M. and Chap, H. (1995) Increase in receptor-like protein tyrosine phosphatase activity and expression level on density-dependent growth arrest of endothelial cells. Biochem. J. 311, 97-103.
31. Gebbink, M. F., Zondag, G. C., Koningstein, G. M., Feiken, E., Wubbolts, R. W. and Moolenaar, W. H. (1995). Cell surface expression of receptor protein tyrosine phosphatase RPTP mu is regulated by cell-cell contact. J. Cell Biol. 131, 251-260
32. Guo, D., Jia, Q., Song, H. Y., Warren, R. S. and Donner, D. B. (1995) Vascular endothelial cell growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains. Association with endothelial cell proliferation. J. Biol. Chem. 270, 6729-6733.
33. Hamaguchi, M., Matsuyoshi, N., Ohnishi, Y., Gotoh, B., Takeichi, M. and Nagai, Y. (1993). P60(v-src) causes tyrosine phosphorylation and inaciivation of the n-cadherin catenin cell-adhesion system. EMBO J. 12, 307-314.
34. Hoschuetzky, H., Aberie, H. and Kemier, R. (1994). Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127, 1375-1380.
35. Ikeda, E., Achen, M. G., Breier, G. and Risau, W. (1995). Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J. Biol. Chem. 270, 19761-19766.
36. Itoh, M., Nagafuchi, A., Moroi, S. and Tsukita, S. (1997). Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J. Cell Biol. 138, 181-192.
37. Jaffe, E. A., Nachman, R. L., Becker, C. G. and Minick, C. R. (1973) Culture of human endothelial cells derived from umbilical veins Identification by morphologic and immunologie criteria. J. Clin. Invest. 52, 2745-2756.
38. Jarrell, B., Levine, E., Shapiro, S., Williams, S., Carabasi, R. A., Mueller, S. and Thornton, S. (1984). Human adult endolhelial cell growth in culture. J. Vasc. Surgery 1, 757-764.
39. Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J. and Connolly, D. T. (1989). Vascular perrneabilily factor, an endothelial cell mitogen related to PDGF. Science 246, 1309-1312.
40. Kendall, R. L., Wang, G., DiSalvo, J. and Thomas, K. A. (1994). Specificity of vascular endothelial cell growth factor receptor ligand binding domains. Biochem. Biophys. Kes. Commun. 201, 326-330.
41. Kinch, M. S., Clark, G. J., Der, C. J. and Burridge, K. (1995). Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia. J. Cell Biol. 130, 461-471.
42. Kost, T. A., Theodorakis, N. and Hughes, S. H. (1983). The nucleotide sequence of the chick cytoplasmic beta-actin gene. Nuct. Acids Res. 11, 8287-8301.
43. Kremer, C., Breier, G., Risau, W. and Plate, K. H. (1997). Up-regulation of flk-1/vascular endothelial growth factor receptor 2 by its ligand in a cerebral slice culture system. Cancer Res. 57, 3852-3859.
44. Kypta, R. M., Su, H. and Reichardt, L. F. (1996). Association between a transmembrane protein lyrosine phosphatase and the cadherin-catenin complex. J. Cell Biol. 134, 1519-1529.
45. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bactenophage T4. Nature 227, 680-685.
46. Lampugnani, M. G., Resnati, M., Raiteri, M., Pigott, R., Pisacane, A., Houen, G., Ruco, L. P. and Dejana, E. (1992). A novel endothelial-speeific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118, 1511-1522.
47. Lampugnani, M. G., Corada, M., Caveda, L., Breviario, F., Ayalon, O., Geiger, B. and Dejana, E. (1995). The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catcnin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129, 203-217.
48. Lampugnani, M. G., Corada, M., Andriopoulou, P., Ksser, S., Risau, W. and Dejana, E. (1997). Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J. Cell Sci. 110, 2065-2077.
49. Lampugnani, M. G. and Dejana, E. (1997). Interendothelial junctions -structure, signalling and functional roles. Curr. Opin. Cell Biol. 9, 674-682.
50. Levick, J. R. and Smaje, L. H. (1987). An analysis of the permeability of a fenestra. Micmvasc. Res. 33, 233-256.
51. Lu, T. T., Yan, L. G. and Yladri, J. A. (1996). Integrin engagement mediates tyrosine dephosphorylation on platelet-endolhelial cell adhesion molecule I. Proc. Nat. Acad. Sci. USA 93, 11808-11813.
52. Matsuyoshi, N., Hamaguchi, M., Taniguchi, S., Nagafuchi, A., Tsukita, S. and Takeichi, M. (1992). Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic tibroblasts. J. Cell Biol. 118, 703-714.
53. Nabeshima, K., Asada, V., Inoue, T., Kataoka, H., Shimao, V., Sumiyoshi, A. and Koono, M. (1997). Modulation of E-cadherin expression in TPA-induced cell motility: well-differentiated human adenocarcinoma cells move as coherent sheets associated with phosphorylation of E-cadherin-calenin complex. Lab. Invest. 76, 139-151.
54. Navarro, P., Caveda, L., Breviario, F., Mandoteanu, I., Lampugnani, M. G. and Dejana, E. (1995). Caienin-dependent and -independent functions of vascular endothelial cadherin. J. Biol. Chem. 270, 30965-30972.
55. Omura, T., Miyazawa, K., Ostman, A. and Heldin, C. H. (1997). Identification of a 190-kDa vascular endothelial growth factor 165 cell surface binding protein on a human glioma cell line. J. Biol. Chem. 272, 23317-23322.
56. Osawa, M., Masuda, M., Harada, N., Lopes, R. B. and Fujiwara, K. (1997). Tyrosine phosphorylalion of platelet endothclial cell adhesion molecule-1 (PECAM-1. CD31) in mechanically stimulated ascular endothelial cells. Eur. J Cell Biol. 72, 229-237.
57. Fallen, C. J. and Tong, P. H. (1991). Elevation of membrane tyrosine phosphatase activity in density-dependent growth-arrested fibroblasts. Proc. Nat. Acad. Sci. USA 88, 6996-7000.
58. Papkoff, J. (1997). Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-l and v-Src. J. Biol. Chem. 272, 4536-4543.
59. Park, J. K., Chen, H. H., Winer, J., Houck, K. A. and Ferrara, N. (1994). Placenta growth factor. Potentiation of vascular endothelial growth factor bioactivity, in vitro and in vivo, and high affinity binding to Flt-1 but not to Flk-1/KDR J. Biol. Chem. 269, 25646-25654.
60. Plate, K. H., Breier, G., Weich, H. A. and Risau, W. (1992) Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359, 845-848.
61. Plouet, J. and Moukadiri, H. (1990). Characterization of the receptor to vasculotropin on bovine adrenal cortex-derived capillary endothelial cells. J. Biol. Chem. 265. 22071-22074.
62. Poltorak, Z., Cohen, T., Sivan, R., Kandelis, Y., Spira, G., Vlodavsky, I., Keshet, K. and Neufeld, G. (1997). VLGF145, a secreted vascular endothelial growth factor isoform that binds to extracellular matrix. J. Biol. Chem. 272, 7151-7158.
63. Kabiet, M. J., Plantier, J. L., Rival, Y., Genoux, Y., Lampugnani, M. G. and Dejana, E. (1996). Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 16, 488-496.
64. Reynolds, A. B., Daniel, J., McCrea, P. D., Wheelock, M. J., Wu, J. and Zhang, X. (1994). Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell. Biol. 14, 8333-8342.
65. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
66. Roberts, W. G. and Palade, G. E. (1995). Increased microvascular permeability and endothclial feneslralion induced by vascular endothelial growth factor. J. Cell Sci. 108, 2369-2379.
67. Roberts, W. G. and Palade, G. E. (1997). Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res. 57, 765-772.
68. Seetharam, L., Gotoh, N., Maru, Y., Neufeld, G., Yamaguchi, S. and Shibuya, M. (1995). A unique signal transduction from FLT tyrosine kinase. a receptor for vascular endothelial growth factor VLGF. Oncogene 10, 135-147.
69. Senger, D. R., Galli, S. J., Dvorak, A. M., Perruzzi, C. A., Harvey, V. S. and Dvorak, H. F. (1983). Tumor cells secrete a vascular permeability factor that promotes accumulation of ascitcs fluid. Science 219, 983-985.
70. Shibamoto, S., Hayakawa, M., Takeuchi, K., Hori, T., Oku, N., Miyazawa, K., Kitamura, N., Takcichi, M. and Ito, F. (1994). Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1, 295-305.
71. Shibata, T., Gotoh, M., Ochiai, A. and Hirohashi, S. (1994) Association of plakoglobin with APC, a tumor suppressor gene product, and its regulation by tyrosine phosphorylation. Biochem. Biophys. Res. Commun. 203, 519-522.
72. Staddon, J. M., Herrenknecht, K., Smalcs, C. and Rubin, L. L. (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J. Cell Sci. 108, 609-619.
73. Takahashi, T. and Shibuya, M. (1997). The 230 kDa mature form of KDR/Flk-1 (VEGF receptor-2) activates the PLC-gamma pathway and partially induces mitotic signals in NIH3T3 fibroblasts. Oncogene 14, 2079-2089.
74. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H. and Takai, Y. (1997) Regulation of cell-cell adhesion by rac and rho small G proteins in MDCJ cells. J. Cell Biol. 139, 1047-1059.
75. Takeda, H., Nagafuchi, A., Yonemura, S., Tsukita, S., Behrens, J., Birchmeier, W. and Tsukita, S. (1995). V-src kinase shifts the cadhennhased cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J. Cell Biol. 131, 1839-1847.
76. Terman, B. I., Carrion, M. E., Kovacs, E., Rasmussen, B. A., Eddy, R. L. and Shows, T. B. (1991). Identification ot a new endothelial cell growth factor receptor tyrosine kinase. Oncogene 6, 1677-1683.
77. Tokman, M. G., Porter, R. A. and Williams, C. L. (1997). Regulation of cadherin-mediaied adhesion by the small GTP-binding protein Rho in small cell lung carcinoma cells. Cancer Res. 57, 1785-1793.
78. Tsukita, S., Oishi, K., Akiyama, T., Vamanashi, Y., Yamamoto, T. and Tsukita, S. (1991). Specific proto-oncogenic tyrosine kmases of src family are enriched in cell-to-cell adherens junctions where the level of tyrosine phosphorylation is elevated. J. Cell Biol. 113, 867-879.
79. Vaisman, N., Gospodarowicz, D. and Necufeld, G. (1990). Characterization of the receptors for vascular endothelial growth factor. J. Biol. Chem. 265, 19461-19466.
80. Vittet, D., Prandini, M. H., Berthitr, R., Schweitzer, A., Martin-Sisteron, H., Uzan, G. and Dejana, E. (1996). Embryonic stem cells differentiate in vitro to endothelial cells through successive maturation steps. Blood 88. 3424-3431.
81. Volberg, T., Geiger, B., Dror, R. and Zick, Y. (1991). Modulation of intercellular adherens-type junctions and tyrosine phosphorylation of their components in RSV-transformed cultured chick lens cells. Cell Regul. 2, 105-120.
82. Volberg, T., Zick, Y., Dror, R., Sabanay, I., Gilon, C., Levitzki, A. and Geiger, B. (1992). The effect of tyrosinc-spccilic proiein phosphorylation on the assembly of adherens-type junctions. EMBO J. 11, 1733-1742.
83. Waltenberger, J., Claesson-Welsh, L., Siegbahn, A., Shibuya, M. and Heldin, C. H. (1994). Different signal transaction properties of KDR and Ftl1, two receptors for vascular endothelial growth factor. J. Biol. Chem. 269, 26988-26995.
84. Wong, V. and Gumbiner, B. M. (1997). A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol. 136, 399-409.
85. Xu, Y., Guo, D. F., Oavidson, M., Inagami, T. and Carpenter, G. (1997). Interaction of the adaptor protein She and the adhesion molecule cadherin. J. Biol. Chem. 272, 13463-13466.
86. Yap, A. S., Brieher, W. M., Pruschy, M. and Gumbiner, B. M. (1997). Lateral clustering of the adhesive ectodomam: a fundamental determinant of cadherin function. Curr Biol. 7, 308-315.