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Vascular Endothelial Cadherin-mediated Cell-cell Adhesion Regulated by a Small GTPase, Rap1

  • Fukuhra, Shigetomo (Department of Structural Analysis, National Cardiovascular Center Research Institute) ;
  • Sakurai, Atsuko (Department of Structural Analysis, National Cardiovascular Center Research Institute) ;
  • Yamagishi, Akiko (Department of Structural Analysis, National Cardiovascular Center Research Institute) ;
  • Sako, Keisuke (Department of Structural Analysis, National Cardiovascular Center Research Institute) ;
  • Mochizuki, Naoki (Department of Structural Analysis, National Cardiovascular Center Research Institute)
  • Received : 2006.02.28
  • Published : 2006.03.31

Abstract

Vascular endothelial cadherin (VE-cadherin), which belongs to the classical cadherin family, is localized at adherens junctions exclusively in vascular endothelial cells. Biochemical and biomechanical cues regulate the VE-cadherin adhesive potential by triggering the intracellular signals. VE-cadherin-mediated cell adhesion is required for cell survival and endothelial cell deadhesion is required for vascular development. It is therefore crucial to understand how VE-cadherin-based cell adhesion is controlled. This review summarizes the inter-endothelial cell adhesions and introduces our recent advance in Rap1-regulated VE-cadherin adhesion. A further analysis of the VE-cadherin recycling system will aid the understanding of cell adhesion/deadhesion mechanisms mediated by VE-cadherin in response to extracellular stimuli during development and angiogenesis.

Keywords

References

  1. Adams, R. H. and Klein, R. (2000) Eph receptors and ephrin ligands. essential mediators of vascular development. Trends Cardiovasc. Med. 10, 183-188 https://doi.org/10.1016/S1050-1738(00)00046-3
  2. Akhtar, N. and Hotchin, N. A. (2001) RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol. Biol. Cell 12, 847-862 https://doi.org/10.1091/mbc.12.4.847
  3. Angst, B. D., Marcozzi, C. and Magee, A. I. (2001) The cadherin superfamily: diversity in form and function. J. Cell Sci. 114, 629-641
  4. Bazzoni, G. (2003) The JAM family of junctional adhesion molecules. Curr. Opin. Cell Biol. 15, 525-530 https://doi.org/10.1016/S0955-0674(03)00104-2
  5. Bos, J. L. (2003) Epac: a new cAMP target and new avenues in cAMP research. Nat. Rev. Mol. Cell Biol. 4, 733-738 https://doi.org/10.1038/nrm1197
  6. Bos, J. L., de Bruyn, K., Enserink, J., Kuiperij, B., Rangarajan, S., Rehmann, H., Riedl, J., de Rooij, J., van Mansfeld, F. and Zwartkruis, F. (2003) The role of Rap1 in integrin-mediated cell adhesion. Biochem. Soc. Trans. 31, 83-86 https://doi.org/10.1042/BST0310083
  7. Bos, J. L., de Rooij, J. and Reedquist, K. A. (2001) Rap1 signalling: adhering to new models. Nat. Rev. Mol. Cell Biol. 2, 369-377 https://doi.org/10.1038/35073073
  8. Broman, M. T., Kouklis, P., Gao, X., Ramchandran, R., Neamu, R. F., Minshall, R. D. and Malik, A. B. (2006) Cdc42 regulates adherens junction stability and endothelial permeability by inducing alpha-catenin interaction with the vascular endothelial cadherin complex. Circ. Res. 98, 73-80 https://doi.org/10.1161/01.RES.0000225256.68436.66
  9. Bryant, D. M. and Stow, J. L. (2004) The ins and outs of Ecadherin trafficking. Trends Cell Biol. 14, 427-434 https://doi.org/10.1016/j.tcb.2004.07.007
  10. Carmeliet, P., Lampugnani, M. G., Moons, L., Breviario, F., Compernolle, V., Bono, F., Balconi, G., Spagnuolo, R., Oostuyse, B., Dewerchin, M., Zanetti, A., Angellilo, A., Mattot, V., Nuyens, D., Lutgens, E., Clotman, F., de Ruiter, M. C., Gittenberger-de Groot, A., Poelmann, R., Lupu, F., Herbert, J. M., Collen, D. and Dejana, E. (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98, 147-157 https://doi.org/10.1016/S0092-8674(00)81010-7
  11. Caveda, L., Martin-Padura, I., Navarro, P., Breviario, F., Corada, M., Gulino, D., Lampugnani, M. G. and Dejana, E. (1996) Inhibition of cultured cell growth by vascular endothelial cadherin (cadherin-5/VE-cadherin). J. Clin. Invest 98, 886-893 https://doi.org/10.1172/JCI118870
  12. Chappuis-Flament, S., Wong, E., Hicks, L. D., Kay, C. M. and Gumbiner, B. M. (2001) Multiple cadherin extracellular repeats mediate homophilic binding and adhesion. J. Cell Biol. 154, 231-243 https://doi.org/10.1083/jcb.200103143
  13. Chen, X., Kojima, S., Borisy, G. G. and Green, K. J. (2003) p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol. 163, 547-557 https://doi.org/10.1083/jcb.200305137
  14. Cullere, X., Shaw, S. K., Andersson, L., Hirahashi, J., Luscinskas, F. W. and Mayadas, T. N. (2005) Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 105, 1950-1955 https://doi.org/10.1182/blood-2004-05-1987
  15. Davis, G. E. and Senger, D. R. (2005) Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 97, 1093- 1107 https://doi.org/10.1161/01.RES.0000191547.64391.e3
  16. Dejana, E. (2004) Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5, 261-270 https://doi.org/10.1038/nrm1357
  17. Dobrosotskaya, I., Guy, R. K. and James, G. L. (1997) MAGI-1, a membrane-associated guanylate kinase with a unique arrangement of protein-protein interaction domains. J. Biol. Chem. 272, 31589-31597 https://doi.org/10.1074/jbc.272.50.31589
  18. Dobrosotskaya, I. Y. (2001) Identification of mNET1 as a candidate ligand for the first PDZ domain of MAGI-1. Biochem. Biophys. Res. Commun. 283, 969-975 https://doi.org/10.1006/bbrc.2001.4880
  19. Dobrosotskaya, I. Y. and James, G. L. (2000) MAGI-1 interacts with beta-catenin and is associated with cell-cell adhesion structures. Biochem. Biophys. Res. Commun. 270, 903-909 https://doi.org/10.1006/bbrc.2000.2471
  20. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005) Alpha-catenin is a molecular switch that binds Ecadherin- beta-catenin and regulates actin-filament assembly. Cell 123, 903-915 https://doi.org/10.1016/j.cell.2005.09.021
  21. Esser, S., Lampugnani, M. G., Corada, M., Dejana, E. and Risau, W. (1998) Vascular endothelial growth factor induces VEcadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111, 1853-1865
  22. Farmer, P. J., Bernier, S. G., Lepage, A., Guillemette, G., Regoli, D. and Sirois, P. (2001) Permeability of endothelial monolayers to albumin is increased by bradykinin and inhibited by prostaglandins. Am. J. Physiol Lung Cell Mol. Physiol 280, 732-738 https://doi.org/10.1152/ajplung.2001.280.4.L732
  23. 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 https://doi.org/10.1038/376066a0
  24. Fukata, M. and Kaibuchi, K. (2001) Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2, 887-897 https://doi.org/10.1038/35103068
  25. Fukuhara, S., Sakurai, A., Sano, H., Yamagishi, A., Somekawa, S., Takakura, N., Saito, Y., Kangawa, K. and Mochizuki, N. (2005) Cyclic AMP potentiates vascular endothelial cadherinmediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol. Cell Biol. 25, 136-146 https://doi.org/10.1128/MCB.25.1.136-146.2005
  26. Fukuyama, T., Ogita, H., Kawakatsu, T., Fukuhara, T., Yamada, T., Sato, T., Shimizu, K., Nakamura, T., Matsuda, M. and Takai, Y. (2005) Involvement of the c-Src-Crk-C3G-Rap1 signaling in the nectin-induced activation of Cdc42 and formation of adherens junctions. J. Biol. Chem. 280, 815-825 https://doi.org/10.1074/jbc.M411099200
  27. Gale, N. W., Thurston, G., Hackett, S. F., Renard, R., Wang, Q., McClain, J., Martin, C., Witte, C., Witte, M. H., Jackson, D., Suri, C., Campochiaro, P. A., Wiegand, S. J. and Yancopoulos, G. D. (2002) Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell 3, 411-423 https://doi.org/10.1016/S1534-5807(02)00217-4
  28. Gale, N. W. and Yancopoulos, G. D. (1999) Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. Genes Dev. 13, 1055-1066 https://doi.org/10.1101/gad.13.9.1055
  29. Grazia, L. M., Zanetti, A., Corada, M., Takahashi, T., Balconi, G., Breviario, F., Orsenigo, F., Cattelino, A., Kemler, R., Daniel, T. O. and Dejana, E. (2003b) Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, betacatenin, and the phosphatase DEP-1/CD148. J. Cell Biol. 161, 793-804 https://doi.org/10.1083/jcb.200209019
  30. Grazia, L. M., Zanetti, A., Corada, M., Takahashi, T., Balconi, G., Breviario, F., Orsenigo, F., Cattelino, A., Kemler, R., Daniel, T. O. and Dejana, E. (2003a) Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, betacatenin, and the phosphatase DEP-1/CD148. J. Cell Biol. 161, 793-804 https://doi.org/10.1083/jcb.200209019
  31. Gumbiner, B., Lowenkopf, T. and Apatira, D. (1991) Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88, 3460-3464 https://doi.org/10.1073/pnas.88.8.3460
  32. Gumbiner, B. M. (2000) Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-404 https://doi.org/10.1083/jcb.148.3.399
  33. Herren, B., Levkau, B., Raines, E. W. and Ross, R. (1998) Cleavage of beta-catenin and plakoglobin and shedding of VEcadherin during endothelial apoptosis: evidence for a role for caspases and metalloproteinases. Mol. Biol. Cell 9, 1589-1601 https://doi.org/10.1091/mbc.9.6.1589
  34. Hippenstiel, S., Witzenrath, M., Schmeck, B., Hocke, A., Krisp, M., Krull, M., Seybold, J., Seeger, W., Rascher, W., Schutte, H. and Suttorp, N. (2002) Adrenomedullin reduces endothelial hyperpermeability. Circ. Res. 91, 618-625 https://doi.org/10.1161/01.RES.0000036603.61868.F9
  35. Hogan, C., Serpente, N., Cogram, P., Hosking, C. R., Bialucha, C. U., Feller, S. M., Braga, V. M., Birchmeier, W. and Fujita, Y. (2004) Rap1 regulates the formation of E-cadherin-based cellcell contacts. Mol. Cell Biol. 24, 6690-6700 https://doi.org/10.1128/MCB.24.15.6690-6700.2004
  36. Hudry-Clergeon, H., Stengel, D., Ninio, E. and Vilgrain, I. (2005) Platelet-activating factor increases VE-cadherin tyrosine phosphorylation in mouse endothelial cells and its association with the PtdIns3'-kinase. FASEB J. 19, 512-520 https://doi.org/10.1096/fj.04-2202com
  37. Jackson, D. E., Ward, C. M., Wang, R. and Newman, P. J. (1997) The protein-tyrosine phosphatase SHP-2 binds platelet/ endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1- and integrinmediated cellular signaling. J. Biol. Chem. 272, 6986-6993 https://doi.org/10.1074/jbc.272.11.6986
  38. Kawajiri, A., Itoh, N., Fukata, M., Nakagawa, M., Yamaga, M., Iwamatsu, A. and Kaibuchi, K. (2000) Identification of a novel beta-catenin-interacting protein. Biochem. Biophys. Res. Commun. 273, 712-717 https://doi.org/10.1006/bbrc.2000.3002
  39. Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J. and Connolly, D. T. (1989) Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246, 1309-1312 https://doi.org/10.1126/science.2479987
  40. Kim, D. Y., Ingano, L. A. and Kovacs, D. M. (2002) Nectin- 1alpha, an immunoglobulin-like receptor involved in the formation of synapses, is a substrate for presenilin/gammasecretase- like cleavage. J. Biol. Chem. 277, 49976-49981 https://doi.org/10.1074/jbc.M210179200
  41. Kooistra, M. R., Corada, M., Dejana, E. and Bos, J. L. (2005) Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 579, 4966-4972 https://doi.org/10.1016/j.febslet.2005.07.080
  42. Kotelevets, L., van Hengel, J., Bruyneel, E., Mareel, M., van Roy, F. and Chastre, E. (2005) Implication of the MAGI-1b/PTEN signalosome in stabilization of adherens junctions and suppression of invasiveness. FASEB J. 19, 115-117 https://doi.org/10.1096/fj.04-1942fje
  43. Kouklis, P., Konstantoulaki, M. and Malik, A. B. (2003) VEcadherin- induced Cdc42 signaling regulates formation of membrane protrusions in endothelial cells. J. Biol. Chem. 278, 16230-16236 https://doi.org/10.1074/jbc.M212591200
  44. Kovacs, E. M., Ali, R. G., McCormack, A. J. and Yap, A. S. (2002) E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277, 6708-6718 https://doi.org/10.1074/jbc.M109640200
  45. Lambeng, N., Wallez, Y., Rampon, C., Cand, F., Christe, G., Gulino-Debrac, D., Vilgrain, I. and Huber, P. (2005) Vascular endothelial-cadherin tyrosine phosphorylation in angiogenic and quiescent adult tissues. Circ. Res. 96, 384-391 https://doi.org/10.1161/01.RES.0000156652.99586.9f
  46. 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-catenin, and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129, 203-217 https://doi.org/10.1083/jcb.129.1.203
  47. Langeler, E. G. and van Hinsbergh, V. W. (1991) Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. Am. J. Physiol. 260, 1052-1059 https://doi.org/10.1152/ajpcell.1991.260.5.C1052
  48. Laura, R. P., Ross, S., Koeppen, H. and Lasky, L. A. (2002) MAGI-1: a widely expressed, alternatively spliced tight junction protein. Exp. Cell Res. 275, 155-170 https://doi.org/10.1006/excr.2002.5475
  49. Luo, Y. and Radice, G. L. (2005) N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis. J. Cell Biol. 169, 29-34 https://doi.org/10.1083/jcb.200411127
  50. Mary, S., Charrasse, S., Meriane, M., Comunale, F., Travo, P., Blangy, A. and Gauthier-Rouviere, C. (2002) Biogenesis of Ncadherin- dependent cell-cell contacts in living fibroblasts is a microtubule-dependent kinesin-driven mechanism. Mol. Biol. Cell 13, 285-301 https://doi.org/10.1091/mbc.01-07-0337
  51. Masuda, M., Osawa, M., Shigematsu, H., Harada, N. and Fujiwara, K. (1997) Platelet endothelial cell adhesion molecule- 1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett. 408, 331-336 https://doi.org/10.1016/S0014-5793(97)00457-2
  52. Mino, A., Ohtsuka, T., Inoue, E. and Takai, Y. (2000) Membraneassociated guanylate kinase with inverted orientation (MAGI)- 1/brain angiogenesis inhibitor 1-associated protein (BAP1) as a scaffolding molecule for Rap small G protein GDP/GTP exchange protein at tight junctions. Genes Cells 5, 1009-1016 https://doi.org/10.1046/j.1365-2443.2000.00385.x
  53. Mochizuki, N., Yamashita, S., Kurokawa, K., Ohba, Y., Nagai, T., Miyawaki, A. and Matsuda, M. (2001) Spatio-temporal images of growth-factor-induced activation of Ras and Rap1. Nature 411, 1065-1068 https://doi.org/10.1038/35082594
  54. Nagashima, K., Endo, A., Ogita, H., Kawana, A., Yamagishi, A., Kitabatake, A., Matsuda, M. and Mochizuki, N. (2002) Adaptor protein Crk is required for Ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol. Biol. Cell 13, 4231-4242 https://doi.org/10.1091/mbc.E02-04-0181
  55. Nakajima, M., Yuasa, S., Ueno, M., Takakura, N., Koseki, H. and Shirasawa, T. (2003) Abnormal blood vessel development in mice lacking presenilin-1. Mech. Dev. 120, 657-667 https://doi.org/10.1016/S0925-4773(03)00064-9
  56. Navarro, P., Ruco, L. and Dejana, E. (1998) Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J. Cell Biol. 140, 1475-1484 https://doi.org/10.1083/jcb.140.6.1475
  57. Nelson, C. M. and Chen, C. S. (2003) VE-cadherin simultaneously stimulates and inhibits cell proliferation by altering cytoskeletal structure and tension. J. Cell Sci. 116, 3571-3581 https://doi.org/10.1242/jcs.00680
  58. Newman, P. J. and Newman, D. K. (2003) Signal transduction pathways mediated by PECAM-1: new roles for an old molecule in platelet and vascular cell biology. Arterioscler. Thromb. Vasc. Biol. 23, 953-964 https://doi.org/10.1161/01.ATV.0000071347.69358.D9
  59. Nwariaku, F. E., Liu, Z., Zhu, X., Nahari, D., Ingle, C., Wu, R. F., Gu, Y., Sarosi, G. and Terada, L. S. (2004) NADPH oxidase mediates vascular endothelial cadherin phosphorylation and endothelial dysfunction. Blood 104, 3214-3220 https://doi.org/10.1182/blood-2004-05-1868
  60. Osawa, M., Masuda, M., Kusano, K. and Fujiwara, K. (2002) Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J. Cell Biol. 158, 773-785 https://doi.org/10.1083/jcb.200205049
  61. Paterson, A. D., Parton, R. G., Ferguson, C., Stow, J. L. and Yap, A. S. (2003) Characterization of E-cadherin endocytosis in isolated MCF-7 and chinese hamster ovary cells: the initial fate of unbound E-cadherin. J. Biol. Chem. 278, 21050-21057 https://doi.org/10.1074/jbc.M300082200
  62. Pece, S. and Gutkind, J. S. (2002) E-cadherin and Hakai: signalling, remodeling or destruction? Nat. Cell Biol. 4, 72-74 https://doi.org/10.1038/ncb0402-e72
  63. Peifer, M. and Yap, A. S. (2003) Traffic control: p120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells. J. Cell Biol. 163, 437-440 https://doi.org/10.1083/jcb.200310090
  64. Periz, G. and Fortini, M. E. (2004) Functional reconstitution of gamma-secretase through coordinated expression of presenilin, nicastrin, Aph-1, and Pen-2. J. Neurosci. Res. 77, 309-322 https://doi.org/10.1002/jnr.20203
  65. Potter, M. D., Barbero, S. and Cheresh, D. A. (2005) Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state. J. Biol. Chem. 280, 31906-31912 https://doi.org/10.1074/jbc.M505568200
  66. Price, L. S., Hajdo-Milasinovic, A., Zhao, J., Zwartkruis, F. J., Collard, J. G. and Bos, J. L. (2004) Rap1 regulates E-cadherinmediated cell-cell adhesion. J. Biol. Chem. 279, 35127-35132 https://doi.org/10.1074/jbc.M404917200
  67. Rahimi, N. and Kazlauskas, A. (1999) A role for cadherin-5 in regulation of vascular endothelial growth factor receptor 2 activity in endothelial cells. Mol. Biol. Cell 10, 3401-3407 https://doi.org/10.1091/mbc.10.10.3401
  68. Reymond, N., Imbert, A. M., Devilard, E., Fabre, S., Chabannon, C., Xerri, L., Farnarier, C., Cantoni, C., Bottino, C., Moretta, A., Dubreuil, P. and Lopez, M. (2004) DNAM-1 and PVR regulate monocyte migration through endothelial junctions. J. Exp. Med. 199, 1331-1341 https://doi.org/10.1084/jem.20032206
  69. Sakisaka, T. and Takai, Y. (2004) Biology and pathology of nectins and nectin-like molecules. Curr. Opin. Cell Biol. 16, 513-521 https://doi.org/10.1016/j.ceb.2004.07.007
  70. Sakurai, A., Fukuhara, S., Yamagishi, A., Sako, K., Kamioka, Y., Masuda, M., Nakaoka, Y. and Mochizuki, N. (2006) MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol. Biol. Cell 17, 966-976 https://doi.org/10.1091/mbc.E05-07-0647
  71. Salomon, D., Ayalon, O., Patel-King, R., Hynes, R. O. and Geiger, B. (1992) Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci. 102, 7-17
  72. 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 https://doi.org/10.1038/376062a0
  73. Shay-Salit, A., Shushy, M., Wolfovitz, E., Yahav, H., Breviario, F., Dejana, E. and Resnick, N. (2002) VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl. Acad. Sci. USA 99, 9462-9467 https://doi.org/10.1073/pnas.142224299
  74. Shoji, H., Tsuchida, K., Kishi, H., Yamakawa, N., Matsuzaki, T., Liu, Z., Nakamura, T. and Sugino, H. (2000) Identification and characterization of a PDZ protein that interacts with activin type II receptors. J. Biol. Chem. 275, 5485-5492 https://doi.org/10.1074/jbc.275.8.5485
  75. Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., Sato, T. N. and Yancopoulos, G. D. (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180 https://doi.org/10.1016/S0092-8674(00)81813-9
  76. Takai, Y. and Nakanishi, H. (2003) Nectin and afadin: novel organizers of intercellular junctions. J. Cell Sci. 116, 17-27 https://doi.org/10.1242/jcs.00167
  77. Telo', P., Breviario, F., Huber, P., Panzeri, C. and Dejana, E. (1998) Identification of a novel cadherin (vascular endothelial cadherin-2) located at intercellular junctions in endothelial cells. J. Biol. Chem. 273, 17565-17572 https://doi.org/10.1074/jbc.273.28.17565
  78. Tsukita, S., Furuse, M. and Itoh, M. (2001) Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2, 285-293 https://doi.org/10.1038/35067088
  79. Ukropec, J. A., Hollinger, M. K., Salva, S. M. and Woolkalis, M. J. (2000) SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin. J. Biol. Chem. 275, 5983-5986 https://doi.org/10.1074/jbc.275.8.5983
  80. Vincent, P. A., Xiao, K., Buckley, K. M. and Kowalczyk, A. P. (2004) VE-cadherin: adhesion at arm's length. Am. J. Physiol Cell Physiol 286, 987-997 https://doi.org/10.1152/ajpcell.00522.2003
  81. Wegmann, F., Ebnet, K., Du, P. L., Vestweber, D. and Butz, S. (2004) Endothelial adhesion molecule ESAM binds directly to the multidomain adaptor MAGI-1 and recruits it to cell contacts. Exp. Cell Res. 300, 121-133 https://doi.org/10.1016/j.yexcr.2004.07.010
  82. Weis, S., Shintani, S., Weber, A., Kirchmair, R., Wood, M., Cravens, A., McSharry, H., Iwakura, A., Yoon, Y. S., Himes, N., Burstein, D., Doukas, J., Soll, R., Losordo, D. and Cheresh, D. (2004) Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J. Clin. Invest 113, 885-894 https://doi.org/10.1172/JCI200420702
  83. Wheelock, M. J. and Johnson, K. R. (2003) Cadherin-mediated cellular signaling. Curr. Opin. Cell Biol. 15, 509-514 https://doi.org/10.1016/S0955-0674(03)00101-7
  84. Wittchen, E. S., Worthylake, R. A., Kelly, P., Casey, P. J., Quilliam, L. A. and Burridge, K. (2005) Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J. Biol. Chem. 280, 11675-11682 https://doi.org/10.1074/jbc.M412595200
  85. 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 https://doi.org/10.1083/jcb.136.2.399
  86. Xiao, K., Garner, J., Buckley, K. M., Vincent, P. A., Chiasson, C. M., Dejana, E., Faundez, V. and Kowalczyk, A. P. (2005) p120-Catenin regulates clathrin-dependent endocytosis of VEcadherin. Mol. Biol. Cell 16, 5141-5151 https://doi.org/10.1091/mbc.E05-05-0440
  87. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901 https://doi.org/10.1016/j.cell.2005.09.020
  88. Yancopoulos, G. D., Davis, S., Gale, N. W., Rudge, J. S., Wiegand, S. J. and Holash, J. (2000) Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 https://doi.org/10.1038/35025215
  89. Zanetti, A., Lampugnani, M. G., Balconi, G., Breviario, F., Corada, M., Lanfrancone, L. and Dejana, E. (2002) Vascular endothelial growth factor induces SHC association with vascular endothelial cadherin: a potential feedback mechanism to control vascular endothelial growth factor receptor-2 signaling. Arterioscler. Thromb. Vasc. Biol. 22, 617-622 https://doi.org/10.1161/01.ATV.0000012268.84961.AD

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