Cross talk between focal adhesion kinase and cadherins: Role in regulating endothelial barrier function

Microvascular Research

Volumn 83, Issue 1, 2012, Pages 3-11

  Quadri, Sadiqa K ^a  

^a Department of Medicine Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CADHERIN; CATENIN; FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATASE; PROTEIN TYROSINE KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; WNT PROTEIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL JUNCTION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CYTOSKELETON; EXTRACELLULAR MATRIX; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ACTIN CYTOSKELETON; ANIMALS; CADHERINS; CAPILLARY PERMEABILITY; CATENINS; ENDOTHELIAL CELLS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; FOCAL ADHESIONS; HUMANS; MONOMERIC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 82955207200     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2011.08.001     Document Type: Article

References (139)

1. Abercrombie M., Dunn G.A. Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy. Exp. Cell Res. 1975, 92:57-62.
2. Abercrombie M., et al. The locomotion of fibroblasts in culture. IV. Electron microscopy of the leading lamella. Exp. Cell Res. 1971, 67:359-367.
3. Aberle H., et al. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J. Cell Sci. 1994, 107(Pt 12):3655-3663.
4. Akhtar N., Hotchin N.A. RAC1 regulates adherens junctions through endocytosis of E-cadherin. Mol. Bio. Cell 2001, 4:847-862.
5. Al-Amoudi A., Frangakis A.S. Structural studies on desmosomes. Biochem. Soc. Trans. 2008, 36:181-187.
6. Anastasiadis P.Z., Reynolds A.B. The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 2000, 113(Pt 8):1319-1334.
7. Andl C.D., Rustgi A.K. No one-way street: cross-talk between e-cadherin and receptor tyrosine kinase (RTK) signaling: a mechanism to regulate RTK activity. Cancer Biol. Ther. 2005, 4:28-31.
8. Avizienyte E., et al. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat. Cell Biol. 2002, 4:632-638.
9. Barth A.I., et al. Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 1997, 9:683-690.
10. Behrens J., et al. 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. 1993, 120:757-766.
11. Bienz M., Clevers H. Linking colorectal cancer to Wnt signaling. Cell 2000, 103:311-320.
12. Birukov K.G., et al. Shear stress-mediated cytoskeletal remodeling and cortactin translocation in pulmonary endothelial cells. Am. J. Respir. Cell Mol. Biol. 2002, 26:453-464.
13. Boggon T.J., et al. C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 2002, 296:1308-1313.
14. Birukova A.A., et al. Paxillin-beta-catenin interactions are involved in Rac/Cdc42-mediated endothelial barrier-protective response to oxidized phospholipids. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L199-L211.
15. Braga V.M. Cell-cell adhesion and signalling. Curr. Opin. Cell Biol. 2002, 14:546-556.
16. Breier G., et al. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 1996, 87:630-641.
17. Broman M.T., et al. Cdc42 regulates adherens junction stability and endothelial permeability by inducing alpha-catenin interaction with the vascular endothelial cadherin complex. Circ. Res. 2006, 98:73-80.
18. Carbajal J.M., et al. ROCK mediates thrombin's endothelial barrier dysfunction. Am. J. Physiol. Cell Physiol. 2000, 279:C195-C204.
19. Chen S.Y., Chen H.C. Direct interaction of focal adhesion kinase (FAK) with Met is required for FAK to promote hepatocyte growth factor-induced cell invasion. Mol. Cell. Biol. 2006, 26:5155-5167.
20. Cheresh D.A., et al. Regulation of cell contraction and membrane ruffling by distinct signals in migratory cells. J. Cell Biol. 1999, 146:1107-1116.
21. Chishti A.H., et al. The FERM domain: a unique module involved in the linkage of cytoplasmic proteins to the membrane. Trends Biochem. Sci. 1998, 23:281-282.
22. Cines D.B., et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998, 91:3527-3561.
23. Conacci-Sorrell M., et al. The cadherin-catenin adhesion system in signaling and cancer. J. Clin. Invest. 2002, 109:987-991.
24. Corada M., et al. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9815-9820.
25. Cowan C.E., et al. Kruppel-like factor-4 transcriptionally regulates VE-cadherin expression and endothelial barrier function. Circ. Res. 2010, 107:959-966.
26. Cullere X., et al. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 2005, 105:1950-1955.
27. de Hoog C.L., et al. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell 2004, 117:649-662.
28. de Rooij J., et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
29. Dejana E., et al. Vascular endothelial (VE)-cadherin: only an intercellular glue?. Exp. Cell Res. 1999, 252:13-19.
30. Drees F., et al. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 2005, 123:903-915.
31. Ehringer W.D., et al. Quantitative image analysis of F-actin in endothelial cells. Microcirculation 1999, 6:291-303.
32. Eliceiri B.P., et al. Src-mediated coupling of focal adhesion kinase to integrin alpha(v)beta5 in vascular endothelial growth factor signaling. J. Cell Biol. 2002, 157:149-160.
33. Evans P.M., et al. KLF4 interacts with beta-catenin/TCF4 and blocks p300/CBP recruitment by beta-catenin. Mol. Cell. Biol. 2010, 30:372-381.
34. Fujita Y., et al. Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 2002, 4:222-231.
35. Fukata M., Kaibuchi K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2001, 2:887-897.
36. Fukata M., et al. Cdc42 and Rac1 regulate the interaction of IQGAP1 with beta-catenin. J. Biol. Chem. 1999, 274:26044-26050.
37. Gao X., et al. Reversibility of increased microvessel permeability in response to VE-cadherin disassembly. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L1218-L1225.
38. Garces C.A., et al. Vascular endothelial growth factor receptor-3 and focal adhesion kinase bind and suppress apoptosis in breast cancer cells. Cancer Res. 2006, 66:1446-1454.
39. Godzich M., et al. Activation of the stress protein response prevents the development of pulmonary edema by inhibiting VEGF cell signaling in a model of lung ischemia-reperfusion injury in rats. FASEB J. 2006, 20:1519-1521.
40. Gorovoy M., et al. RhoGDI-1 modulation of the activity of monomeric RhoGTPase RhoA regulates endothelial barrier function in mouse lungs. Circ. Res. 2007, 101:50-58.
41. Gottardi C.J., et al. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J. Cell Biol. 2001, 153:1049-1060.
42. Gumbiner B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 1996, 84:345-357.
43. Gumbiner B.M. Regulation of cadherin adhesive activity. J. Cell Biol. 2000, 148:399-404.
44. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
45. Halbleib J.M., Nelson W.J. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 2006, 20:3199-3214.
46. Hamaguchi M., et al. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO J. 1993, 12:307-314.
47. Harrison O.J., et al. Two-step adhesive binding by classical cadherins. Nat. Struct. Mol. Biol. 2010, 17:348-357.
48. Haussinger D., et al. Proteolytic E-cadherin activation followed by solution NMR and X-ray crystallography. EMBO J. 2004, 23:1699-1708.
49. Herwig M.C., et al. Endothelial VE-cadherin expression in human lungs. Pathol. Res. Pract. 2008, 204:725-730.
50. Hildebrand J.D., et al. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp 125FAK, to cellular focal adhesions. J. Cell Biol. 1993, 123:993-1005.
51. Hinck L., et al. Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J. Cell Biol. 1994, 125:1327-1340.
52. Hirokawa N., Heuser J.E. Quick-freeze, deep-etch visualization of the cytoskeleton beneath surface differentiations of intestinal epithelial cells. J. Cell Biol. 1981, 91:399-409.
53. Holinstat M., et al. Suppression of RhoA activity by focal adhesion kinase-induced activation of p190RhoGAP: role in regulation of endothelial permeability. J. Biol. Chem. 2006, 281:2296-2305.
54. Hsia D.A., et al. Differential regulation of cell motility and invasion by FAK. J. Cell Biol. 2003, 160:753-767.
55. Huber A.H., Weis W.I. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 2001, 105:391-402.
56. Hulsken J., et al. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J. Cell Biol. 1994, 127:2061-2069.
57. Ireton R.C., et al. A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 2002, 159:465-476.
58. Ishiyama N., et al. Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell-cell adhesion. Cell 2010, 141:117-128.
59. Izzard C.S., Lochner L.R. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell Sci. 1976, 21:129-159.
60. Izzard C.S., Lochner L.R. Formation of cell-to-substrate contacts during fibroblast motility: an interference-reflexion study. J. Cell Sci. 1980, 42:81-116.
61. Jamora C., Fuchs E. Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 2002, 4:E101-E108.
62. Kitagawa M., et al. Mutation analysis of cadherin-4 reveals amino acid residues of EC1 important for the structure and function. Biochem. Biophys. Res. Commun. 2000, 271:358-363.
63. Kooistra M.R., et al. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 2005, 579:4966-4972.
64. Kouklis P., et al. Cdc42 regulates the restoration of endothelial barrier function. Circ. Res. 2004, 94:159-166.
65. Kovacs E.M., et al. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 2002, 277:6708-6718.
66. Kuroda S., et al. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science 1998, 281:832-835.
67. Lahlou H., et al. Mammary epithelial-specific disruption of the focal adhesion kinase blocks mammary tumor progression. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20302-20307.
68. Lampugnani M.G., et al. 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. 1995, 129:203-217.
69. Lampugnani M.G., et al. VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol. Biol. Cell 2002, 13:1175-1189.
70. Liaw C.W., et al. Identification and cloning of two species of cadherins in bovine endothelial cells. EMBO J. 1990, 9:2701-2708.
71. Lim S.T., et al. FERM control of FAK function: implications for cancer therapy. Cell Cycle 2008, 7:2306-2314.
72. Liu H., et al. Involvement of p120 carboxy-terminal domain in cadherin trafficking. Cell Struct. Funct. 2007, 32:127-137.
73. Lobo M., Zachary I. Nuclear localization and apoptotic regulation of an amino-terminal domain focal adhesion kinase fragment in endothelial cells. Biochem. Biophys. Res. Commun. 2000, 276:1068-1074.
74. Luo M., Guan J.L. Focal adhesion kinase: a prominent determinant in breast cancer initiation, progression and metastasis. Cancer Lett. 2010, 289:127-139.
75. May C., et al. Identification of a transiently exposed VE-cadherin epitope that allows for specific targeting of an antibody to the tumor neovasculature. Blood 2005, 105:4337-4344.
76. Mazaki Y., et al. An ADP-ribosylation factor GTPase-activating protein Git2-short/KIAA0148 is involved in subcellular localization of paxillin and actin cytoskeletal organization. Mol. Biol. Cell 2001, 12:645-662.
77. McLachlan R.W., et al. E-cadherin adhesion activates c-Src signaling at cell-cell contacts. Mol. Biol. Cell 2007, 18:3214-3223.
78. McLean G.W., et al. Specific deletion of focal adhesion kinase suppresses tumor formation and blocks malignant progression. Genes Dev. 2004, 18:2998-3003.
79. Mehta D., et al. Modulatory role of focal adhesion kinase in regulating human pulmonary arterial endothelial barrier function. J. Physiol. 2002, 539:779-789.
80. Miyaguchi K. Ultrastructure of the zonula adherens revealed by rapid-freeze deep-etching. J. Struct. Biol. 2000, 132:169-178.
81. Morin P.J., et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275:1787-1790.
82. Nagar B., et al. Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 1996, 380:360-364.
83. Nishimura T., Takeichi M. Remodeling of the adherens junctions during morphogenesis. Curr. Top. Dev. Biol. 2009, 89:33-54.
84. Noren N.K., et al. Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 2003, 278:13615-13618.
85. Noren N.K., et al. Cadherin engagement regulates Rho family GTPases. J. Biol. Chem. 2001, 276:33305-33308.
86. Nose A., et al. Localization of specificity determining sites in cadherin cell adhesion molecules. Cell 1990, 61:147-155.
87. Ofori-Acquah S.F., et al. Heterogeneity of barrier function in the lung reflects diversity in endothelial cell junctions. Microvasc. Res. 2008, 75:391-402.
88. Orsulic S., et al. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J. Cell Sci. 1999, 112(Pt 8):1237-1245.
89. Palacios F., et al. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol. Cell. Biol. 2005, 25:389-402.
90. Papkoff J. Regulation of complexed and free catenin pools by distinct mechanisms. Differential effects of Wnt-1 and v-Src. J. Biol. Chem. 1997, 272:4536-4543.
91. Parisini E., et al. The crystal structure of human E-cadherin domains 1 and 2, and comparison with other cadherins in the context of adhesion mechanism. J. Mol. Biol. 2007, 373:401-411.
92. Parker J.C., et al. Hydraulic conductance of pulmonary microvascular and macrovascular endothelial cell monolayers. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 291:L30-L37.
93. Parthasarathi K.a.Q.,.S.K. Cadherin and connexin in pulmonary endothelial function. The Pulmonary Endothelium Function in Health and Disease 2009, John Wiley & Sons, Ltd., Chichester, UK. N. Rounds (Ed.).
94. Pece S., Gutkind J.S. Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J. Biol. Chem. 2000, 275:41227-41233.
95. Pece S., Gutkind J.S. E-cadherin and Hakai: signalling, remodeling or destruction?. Nat. Cell Biol. 2002, 4:E72-E74.
96. Pertz O., et al. A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J. 1999, 18:1738-1747.
97. Pokutta S., Weis W.I. Structure of the dimerization and beta-catenin-binding region of alpha-catenin. Mol. Cell 2000, 5:533-543.
98. Posy S., et al. Sequence and structural determinants of strand swapping in cadherin domains: do all cadherins bind through the same adhesive interface?. J. Mol. Biol. 2008, 378:954-968.
99. Quadri S.K., et al. Endothelial barrier strengthening by activation of focal adhesion kinase. J. Biol. Chem. 2003, 278:13342-13349.
100. Quadri S.K., Bhattacharya J. Resealing of endothelial junctions by focal adhesion kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 292:L334-L342.
101. Rabiet M.J., et al. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 1996, 16:488-496.
102. Reynolds A.B., Carnahan R.H. Regulation of cadherin stability and turnover by p120ctn: implications in disease and cancer. Semin. Cell Dev. Biol. 2004, 15:657-663.
103. Safdar Z., et al. Hyperosmolarity enhances the lung capillary barrier. J. Clin. Invest. 2003, 112:1541-1549.
104. Salomon D., et al. Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci. 1992, 102(Pt 1):7-17.
105. Sander E.E., et al. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 1998, 143:1385-1398.
106. Schaller M.D., et al. Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp 125FAK. Mol. Cell. Biol. 1993, 13:785-791.
107. Schilling W.P., et al. Depletion of the inositol 1,4,5-trisphosphate-sensitive intracellular Ca2+ store in vascular endothelial cells activates the agonist-sensitive Ca(2+)-influx pathway. Biochem. J. 1992, 284(Pt 2):521-530.
108. Serrels B., et al. A complex between FAK, RACK1, and PDE4D5 controls spreading initiation and cancer cell polarity. Curr. Biol. 2010, 20:1086-1092.
109. Serrels B., et al. Focal adhesion kinase controls actin assembly via a FERM-mediated interaction with the Arp2/3 complex. Nat. Cell Biol. 2007, 9:1046-1056.
110. Shan W.S., et al. The adhesive binding site of cadherins revisited. Biophys. Chem. 1999, 82:157-163.
111. Shapiro L., et al. Structural basis of cell-cell adhesion by cadherins. Nature 1995, 374:327-337.
112. Shikata Y., et al. S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J. Appl. Physiol. 2003, 94:1193-1203.
113. Sieg D.J., et al. FAK integrates growth-factor and integrin signals to promote cell migration. Nat. Cell Biol. 2000, 2:249-256.
114. Singleton P.A., et al. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, and alpha-actinin. FASEB J. 2005, 19:1646-1656.
115. Sovova V., et al. Transactivation of E-cadherin is not involved in the activity of EGF receptor in colorectal carcinoma cells. Int. J. Oncol. 2004, 25:1459-1464.
116. Stewart A., et al. The focal adhesion kinase amino-terminal domain localises to nuclei and intercellular junctions in HEK 293 and MDCK cells independently of tyrosine 397 and the carboxy-terminal domain. Biochem. Biophys. Res. Commun. 2002, 299:62-73.
117. Stockinger A., et al. E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J. Cell Biol. 2001, 154:1185-1196.
118. Sun X., et al. Enhanced interaction between focal adhesion and adherens junction proteins: involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement. Microvasc. Res. 2009, 77:304-313.
119. Sunita Bhattacharya, Sadiqa Quadri, Jahar Bhattacharya Endothelial-matrix interactions in the lung. Perspectives on Lung Endothelial Barrier Function 2005, Vol. 35:237-250. Elsevier B.V.
120. Takahashi K., Suzuki K. Density-dependent inhibition of growth involves prevention of EGF receptor activation by E-cadherin-mediated cell-cell adhesion. Exp. Cell Res. 1996, 226:214-222.
121. Takemoto H., et al. Localization of IQGAP1 is inversely correlated with intercellular adhesion mediated by e-cadherin in gastric cancers. Int. J. Cancer 2001, 91:783-788.
122. Tamura K., et al. Structure-function analysis of cell adhesion by neural (N-) cadherin. Neuron 1998, 20:1153-1163.
123. Taylor J.M., et al. Selective expression of an endogenous inhibitor of FAK regulates proliferation and migration of vascular smooth muscle cells. Mol. Cell. Biol. 2001, 21:1565-1572.
124. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell Biol. 2000, 2:E231-E236.
125. Turner C.E., Brown M.C. Cell motility: ARNOand ARF6 at the cutting edge. Curr. Biol. 2001, 11:R875-R877.
126. Uehata M., et al. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 1997, 389:990-994.
127. van Nimwegen M.J., van de Water B. Focal adhesion kinase: a potential target in cancer therapy. Biochem. Pharmacol. 2007, 73:597-609.
128. Volk T., Kox W.J. Endothelium function in sepsis. Inflamm. Res. 2000, 49:185-198.
129. Winder S.J. Structural insights into actin-binding, branching and bundling proteins. Curr. Opin. Cell Biol. 2003, 15:14-22.
130. Wu X., et al. Focal adhesion kinase regulation of N-WASP subcellular localization and function. J. Biol. Chem. 2004, 279:9565-9576.
131. Xiao K., et al. p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol. Biol. Cell 2005, 16:5141-5151.
132. Yamada S., Nelson W.J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 2007, 178:517-527.
133. Yamada S., et al. Deconstructing the cadherin-catenin-actin complex. Cell 2005, 123:889-901.
134. Yano H., et al. Roles played by a subset of integrin signaling molecules in cadherin-based cell-cell adhesion. J. Cell Biol. 2004, 166:283-295.
135. Yap A.S., Kovacs E.M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 2003, 160:11-16.
136. Zachary I. VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 2003, 31:1171-1177.
137. Zantek N.D., et al. E-cadherin regulates the function of the EphA2 receptor tyrosine kinase. Cell Growth Differ. 1999, 10:629-638.
138. Zhao J., Guan J.L. Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 2009, 28:35-49.
139. Zigmond S. Formin' adherens junctions. Nat. Cell Biol. 2004, 6:12-14.