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Review

Mechanotransduction at the basis of endothelial barrier function

Article: e24180 | Received 20 Dec 2012, Accepted 02 Mar 2013, Published online: 01 Apr 2013

References

  • Vollrath MA, Kwan KY, Corey DP. The micromachinery of mechanotransduction in hair cells. Annu Rev Neurosci 2007; 30:339 - 65; http://dx.doi.org/10.1146/annurev.neuro.29.051605.112917; PMID: 17428178
  • Hammerschmidt S, Kuhn H, Gessner C, Seyfarth HJ, Wirtz H. Stretch-induced alveolar type II cell apoptosis: role of endogenous bradykinin and PI3K-Akt signaling. Am J Respir Cell Mol Biol 2007; 37:699 - 705; http://dx.doi.org/10.1165/rcmb.2006-0429OC; PMID: 17630321
  • Affonce DA, Lutchen KR. New perspectives on the mechanical basis for airway hyperreactivity and airway hypersensitivity in asthma. J Appl Physiol 2006; 101:1710 - 9; http://dx.doi.org/10.1152/japplphysiol.00344.2006; PMID: 16902064
  • Heydemann A, McNally EM. Consequences of disrupting the dystrophin-sarcoglycan complex in cardiac and skeletal myopathy. Trends Cardiovasc Med 2007; 17:55 - 9; http://dx.doi.org/10.1016/j.tcm.2006.12.002; PMID: 17292047
  • Jaalouk DE, Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol 2009; 10:63 - 73; http://dx.doi.org/10.1038/nrm2597; PMID: 19197333
  • Lehoux S, Esposito B, Merval R, Tedgui A. Differential regulation of vascular focal adhesion kinase by steady stretch and pulsatility. Circulation 2005; 111:643 - 9; http://dx.doi.org/10.1161/01.CIR.0000154548.16191.2F; PMID: 15668343
  • Lehoux S, Castier Y, Tedgui A. Molecular mechanisms of the vascular responses to haemodynamic forces. J Intern Med 2006; 259:381 - 92; http://dx.doi.org/10.1111/j.1365-2796.2006.01624.x; PMID: 16594906
  • Zebda N, Dubrovskyi O, Birukov KG. Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc Res 2012; 83:71 - 81; http://dx.doi.org/10.1016/j.mvr.2011.06.007; PMID: 21741394
  • Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 2009; 6:16 - 26; http://dx.doi.org/10.1038/ncpcardio1397; PMID: 19029993
  • Davies PF. Overview: temporal and spatial relationships in shear stress-mediated endothelial signalling. J Vasc Res 1997; 34:208 - 11; http://dx.doi.org/10.1159/000159224; PMID: 9226302
  • Tzima E, del Pozo MA, Shattil SJ, Chien S, Schwartz MA. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J 2001; 20:4639 - 47; http://dx.doi.org/10.1093/emboj/20.17.4639; PMID: 11532928
  • DeMaio L, Chang YS, Gardner TW, Tarbell JM, Antonetti DA. Shear stress regulates occludin content and phosphorylation. Am J Physiol Heart Circ Physiol 2001; 281:H105 - 13; PMID: 11406474
  • Hahn C, Schwartz MA. Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009; 10:53 - 62; http://dx.doi.org/10.1038/nrm2596; PMID: 19197332
  • Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ Res 2006; 98:176 - 85; http://dx.doi.org/10.1161/01.RES.0000200162.94463.d7; PMID: 16456110
  • Tzima E, Del Pozo MA, Kiosses WB, Mohamed SA, Li S, Chien S, et al. Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J 2002; 21:6791 - 800; http://dx.doi.org/10.1093/emboj/cdf688; PMID: 12486000
  • Miao H, Hu YL, Shiu YT, Yuan S, Zhao Y, Kaunas R, et al. Effects of flow patterns on the localization and expression of VE-cadherin at vascular endothelial cell junctions: in vivo and in vitro investigations. J Vasc Res 2005; 42:77 - 89; http://dx.doi.org/10.1159/000083094; PMID: 15637443
  • Ting LH, Jahn JR, Jung JI, Shuman BR, Feghhi S, Han SJ, et al. Flow mechanotransduction regulates traction forces, intercellular forces and adherens junctions. Am J Physiol Heart Circ Physiol 2012; 302:H2220 - 9; http://dx.doi.org/10.1152/ajpheart.00975.2011; PMID: 22447948
  • Colgan OC, Ferguson G, Collins NT, Murphy RP, Meade G, Cahill PA, et al. Regulation of bovine brain microvascular endothelial tight junction assembly and barrier function by laminar shear stress. Am J Physiol Heart Circ Physiol 2007; 292:H3190 - 7; http://dx.doi.org/10.1152/ajpheart.01177.2006; PMID: 17308001
  • Phelps JE, DePaola N. Spatial variations in endothelial barrier function in disturbed flows in vitro. Am J Physiol Heart Circ Physiol 2000; 278:H469 - 76; PMID: 10666077
  • Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A 2010; 107:9944 - 9; http://dx.doi.org/10.1073/pnas.0914547107; PMID: 20463286
  • Zaidel-Bar R, Geiger B. The switchable integrin adhesome. J Cell Sci 2010; 123:1385 - 8; http://dx.doi.org/10.1242/jcs.066183; PMID: 20410370
  • Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, et al. Nanoscale architecture of integrin-based cell adhesions. Nature 2010; 468:580 - 4; http://dx.doi.org/10.1038/nature09621; PMID: 21107430
  • Michaelson JE, Huang H. Cell-cell junctional proteins in cardiovascular mechanotransduction. Ann Biomed Eng 2012; 40:568 - 77; http://dx.doi.org/10.1007/s10439-011-0439-6; PMID: 22016325
  • Aijaz S, Balda MS, Matter K. Tight junctions: molecular architecture and function. Int Rev Cytol 2006; 248:261 - 98; http://dx.doi.org/10.1016/S0074-7696(06)48005-0; PMID: 16487793
  • Luissint AC, Artus C, Glacial F, Ganeshamoorthy K, Couraud PO. Tight junctions at the blood brain barrier: physiological architecture and disease-associated dysregulation. Fluids Barriers CNS 2012; 9:23; http://dx.doi.org/10.1186/2045-8118-9-23; PMID: 23140302
  • McCue S, Noria S, Langille BL. Shear-induced reorganization of endothelial cell cytoskeleton and adhesion complexes. Trends Cardiovasc Med 2004; 14:143 - 51; http://dx.doi.org/10.1016/j.tcm.2004.02.003; PMID: 15177265
  • de Beco S, Gueudry C, Amblard F, Coscoy S. Endocytosis is required for Ecadherin redistribution at mature adherens junctions. Proc Natl Acad Sci USA 2009; 106:70107015; http://dx.doi.org/10.1073/pnas.0811253106
  • Conklin BS, Zhong DS, Zhao W, Lin PH, Chen C. Shear stress regulates occludin and VEGF expression in porcine arterial endothelial cells. J Surg Res 2002; 102:13 - 21; http://dx.doi.org/10.1006/jsre.2001.6295; PMID: 11792146
  • Collins NT, Cummins PM, Colgan OC, Ferguson G, Birney YA, Murphy RP, et al. Cyclic strain-mediated regulation of vascular endothelial occludin and ZO-1: influence on intercellular tight junction assembly and function. Arterioscler Thromb Vasc Biol 2006; 26:62 - 8; http://dx.doi.org/10.1161/01.ATV.0000194097.92824.b3; PMID: 16269664
  • Tarbell JM. Shear stress and the endothelial transport barrier. Cardiovasc Res 2010; 87:320 - 30; http://dx.doi.org/10.1093/cvr/cvq146; PMID: 20543206
  • Nishimura T, Takeichi M. Remodeling of the adherens junctions during morphogenesis. Curr Top Dev Biol 2009; 89:33 - 54; http://dx.doi.org/10.1016/S0070-2153(09)89002-9; PMID: 19737641
  • Maruthamuthu V, Aratyn-Schaus Y, Gardel ML. Conserved F-actin dynamics and force transmission at cell adhesions. Curr Opin Cell Biol 2010; 22:583 - 8; http://dx.doi.org/10.1016/j.ceb.2010.07.010; PMID: 20728328
  • Chu YS, Thomas WA, Eder O, Pincet F, Perez E, Thiery JP, et al. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J Cell Biol 2004; 167:1183 - 94; http://dx.doi.org/10.1083/jcb.200403043; PMID: 15596540
  • Chu YS, Eder O, Thomas WA, Simcha I, Pincet F, Ben-Ze’ev A, et al. Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains. J Biol Chem 2006; 281:2901 - 10; http://dx.doi.org/10.1074/jbc.M506185200; PMID: 16253998
  • le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 2010; 189:1107 - 15; http://dx.doi.org/10.1083/jcb.201001149; PMID: 20584916
  • Maruthamuthu V, Sabass B, Schwarz US, Gardel ML. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. Proc Natl Acad Sci U S A 2011; 108:4708 - 13; http://dx.doi.org/10.1073/pnas.1011123108; PMID: 21383129
  • Ganz A, Lambert M, Saez A, Silberzan P, Buguin A, Mège RM, et al. Traction forces exerted through N-cadherin contacts. Biol Cell 2006; 98:721 - 30; http://dx.doi.org/10.1042/BC20060039; PMID: 16895521
  • Yonemura S. A mechanism of mechanotransduction at the cell-cell interface: emergence of α-catenin as the center of a force-balancing mechanism for morphogenesis in multicellular organisms. Bioessays 2011; 33:732 - 6; http://dx.doi.org/10.1002/bies.201100064; PMID: 21826690
  • del Rio A, Perez-Jimenez R, Liu R, Roca-Cusachs P, Fernandez JM, Sheetz MP. Stretching single talin rod molecules activates vinculin binding. Science 2009; 323:638 - 41; http://dx.doi.org/10.1126/science.1162912; PMID: 19179532
  • Lee SE, Kamm RD, Mofrad MR. Force-induced activation of talin and its possible role in focal adhesion mechanotransduction. J Biomech 2007; 40:2096 - 106; http://dx.doi.org/10.1016/j.jbiomech.2007.04.006; PMID: 17544431
  • Hu K, Ji L, Applegate KT, Danuser G, Waterman-Storer CM. Differential transmission of actin motion within focal adhesions. Science 2007; 315:111 - 5; http://dx.doi.org/10.1126/science.1135085; PMID: 17204653
  • Humphries JD, Wang P, Streuli C, Geiger B, Humphries MJ, Ballestrem C. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J Cell Biol 2007; 179:1043 - 57; http://dx.doi.org/10.1083/jcb.200703036; PMID: 18056416
  • Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, et al. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A 2010; 107:9944 - 9; http://dx.doi.org/10.1073/pnas.0914547107; PMID: 20463286
  • Brevier J, Montero D, Svitkina T, Riveline D. The asymmetric self-assembly mechanism of adherens junctions: a cellular push-pull unit. Phys Biol 2008; 5:016005; http://dx.doi.org/10.1088/1478-3975/5/1/016005; PMID: 18379019
  • Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 2004; 5:261 - 70; http://dx.doi.org/10.1038/nrm1357; PMID: 15071551
  • Dejana E, Bazzoni G, Lampugnani MG. Vascular endothelial (VE)-cadherin: only an intercellular glue?. Exp Cell Res 1999; 252:13 - 9; http://dx.doi.org/10.1006/excr.1999.4601; PMID: 10502395
  • Hordijk PL, Anthony E, Mul FP, Rientsma R, Oomen LC, Roos D. Vascular-endothelial-cadherin modulates endothelial monolayer permeability. [In Process Citation] J Cell Sci 1999; 112:1915 - 23; PMID: 10341210
  • Gulino D, Delachanal E, Concord E, Genoux Y, Morand B, Valiron MO, et al. Alteration of endothelial cell monolayer integrity triggers resynthesis of vascular endothelium cadherin. J Biol Chem 1998; 273:29786 - 93; http://dx.doi.org/10.1074/jbc.273.45.29786; PMID: 9792693
  • Hirano S, Kimoto N, Shimoyama Y, Hirohashi S, Takeichi M. Identification of a neural alpha-catenin as a key regulator of cadherin function and multicellular organization. Cell 1992; 70:293 - 301; http://dx.doi.org/10.1016/0092-8674(92)90103-J; PMID: 1638632
  • Drees F, Pokutta S, Yamada S, Nelson WJ, Weis WI. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 2005; 123:903 - 15; http://dx.doi.org/10.1016/j.cell.2005.09.021; PMID: 16325583
  • Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell 2005; 123:889 - 901; http://dx.doi.org/10.1016/j.cell.2005.09.020; PMID: 16325582
  • Schulte D, Küppers V, Dartsch N, Broermann A, Li H, Zarbock A, et al. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 2011; 30:4157 - 70; http://dx.doi.org/10.1038/emboj.2011.304; PMID: 21857650
  • Maiden SL, Hardin J. The secret life of α-catenin: moonlighting in morphogenesis. J Cell Biol 2011; 195:543 - 52; http://dx.doi.org/10.1083/jcb.201103106; PMID: 22084304
  • Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 2010; 12:533 - 42; http://dx.doi.org/10.1038/ncb2055; PMID: 20453849
  • Pokutta S, Drees F, Takai Y, Nelson WJ, Weis WI. Biochemical and structural definition of the l-afadin- and actin-binding sites of alpha-catenin. J Biol Chem 2002; 277:18868 - 74; http://dx.doi.org/10.1074/jbc.M201463200; PMID: 11907041
  • Nieset JE, Redfield AR, Jin F, Knudsen KA, Johnson KR, Wheelock MJ. Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin. J Cell Sci 1997; 110:1013 - 22; PMID: 9152027
  • Kobielak A, Pasolli HA, Fuchs E. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 2004; 6:21 - 30; http://dx.doi.org/10.1038/ncb1075; PMID: 14647292
  • Abe K, Takeichi M. EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt. Proc Natl Acad Sci U S A 2008; 105:13 - 9; http://dx.doi.org/10.1073/pnas.0710504105; PMID: 18093941
  • Itoh M, Nagafuchi A, Moroi S, Tsukita S. Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments. J Cell Biol 1997; 138:181 - 92; http://dx.doi.org/10.1083/jcb.138.1.181; PMID: 9214391
  • Aberle H, Butz S, Stappert J, Weissig H, Kemler R, Hoschuetzky H. Assembly of the cadherin-catenin complex in vitro with recombinant proteins. J Cell Sci 1994; 107:3655 - 63; PMID: 7706414
  • Pokutta S, Weis WI. Structure of the dimerization and beta-catenin-binding region of alpha-catenin. Mol Cell 2000; 5:533 - 43; http://dx.doi.org/10.1016/S1097-2765(00)80447-5; PMID: 10882138
  • Nagafuchi A, Ishihara S, Tsukita S. The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-alpha catenin fusion molecules. J Cell Biol 1994; 127:235 - 45; http://dx.doi.org/10.1083/jcb.127.1.235; PMID: 7929566
  • Shewan AM, Maddugoda M, Kraemer A, Stehbens SJ, Verma S, Kovacs EM, et al. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol Biol Cell 2005; 16:4531 - 42; http://dx.doi.org/10.1091/mbc.E05-04-0330; PMID: 16030252
  • Smutny M, Yap AS. Neighborly relations: cadherins and mechanotransduction. J Cell Biol 2010; 189:1075 - 7; http://dx.doi.org/10.1083/jcb.201005151; PMID: 20584914
  • Zheng Q, Zhao Y. The diverse biofunctions of LIM domain proteins: determined by subcellular localization and protein-protein interaction. Biol Cell 2007; 99:489 - 502; http://dx.doi.org/10.1042/BC20060126; PMID: 17696879
  • Maul RS, Song Y, Amann KJ, Gerbin SC, Pollard TD, Chang DD. EPLIN regulates actin dynamics by cross-linking and stabilizing filaments. J Cell Biol 2003; 160:399 - 407; http://dx.doi.org/10.1083/jcb.200212057; PMID: 12566430
  • Jiang WG, Martin TA, Lewis-Russell JM, Douglas-Jones A, Ye L, Mansel RE. Eplin-alpha expression in human breast cancer, the impact on cellular migration and clinical outcome. Mol Cancer 2008; 7:71; http://dx.doi.org/10.1186/1476-4598-7-71; PMID: 18796137
  • Han MY, Kosako H, Watanabe T, Hattori S. Extracellular signal-regulated kinase/mitogen-activated protein kinase regulates actin organization and cell motility by phosphorylating the actin cross-linking protein EPLIN. Mol Cell Biol 2007; 27:8190 - 204; http://dx.doi.org/10.1128/MCB.00661-07; PMID: 17875928
  • Chircop M, Oakes V, Graham ME, Ma MP, Smith CM, Robinson PJ, et al. The actin-binding and bundling protein, EPLIN, is required for cytokinesis. Cell Cycle 2009; 8:757 - 64; http://dx.doi.org/10.4161/cc.8.5.7878; PMID: 19221476
  • Zhang S, Wang X, Iqbal S, Wang Y, Osunkoya AO, Chen Z, et al. Epidermal growth factor promotes protein degradation of epithelial protein lost in neoplasm (EPLIN), a putative metastasis suppressor, during epithelial-mesenchymal transition. J Biol Chem 2012; PMID: 23188829
  • Chervin-Pétinot A, Courçon M, Almagro S, Nicolas A, Grichine A, Grunwald D, et al. Epithelial protein lost in neoplasm (EPLIN) interacts with α-catenin and actin filaments in endothelial cells and stabilizes vascular capillary network in vitro. J Biol Chem 2012; 287:7556 - 72; http://dx.doi.org/10.1074/jbc.M111.328682; PMID: 22194609
  • Taguchi K, Ishiuchi T, Takeichi M. Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J Cell Biol 2011; 194:643 - 56; http://dx.doi.org/10.1083/jcb.201104124; PMID: 21844208
  • Ziegler WH, Liddington RC, Critchley DR. The structure and regulation of vinculin. Trends Cell Biol 2006; 16:453 - 60; http://dx.doi.org/10.1016/j.tcb.2006.07.004; PMID: 16893648
  • Bois PR, O’Hara BP, Nietlispach D, Kirkpatrick J, Izard T. The vinculin binding sites of talin and alpha-actinin are sufficient to activate vinculin. J Biol Chem 2006; 281:7228 - 36; http://dx.doi.org/10.1074/jbc.M510397200; PMID: 16407299
  • Choi HJ, Pokutta S, Cadwell GW, Bobkov AA, Bankston LA, Liddington RC, et al. αE-catenin is an autoinhibited molecule that coactivates vinculin. Proc Natl Acad Sci U S A 2012; 109:8576 - 81; http://dx.doi.org/10.1073/pnas.1203906109; PMID: 22586082
  • Peng X, Maiers JL, Choudhury D, Craig SW, DeMali KA. α-Catenin uses a novel mechanism to activate vinculin. J Biol Chem 2012; 287:7728 - 37; http://dx.doi.org/10.1074/jbc.M111.297481; PMID: 22235119
  • Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, et al. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 2012; 196:641 - 52; http://dx.doi.org/10.1083/jcb.201108120; PMID: 22391038
  • Tang VW, Brieher WM. α-Actinin-4/FSGS1 is required for Arp2/3-dependent actin assembly at the adherens junction. J Cell Biol 2012; 196:115 - 30; http://dx.doi.org/10.1083/jcb.201103116; PMID: 22232703
  • Sun X, Shikata Y, Wang L, Ohmori K, Watanabe N, Wada J, 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 - 13; http://dx.doi.org/10.1016/j.mvr.2008.12.004; PMID: 19323978
  • Olson MF. Contraction reaction: mechanical regulation of Rho GTPase. Trends Cell Biol 2004; 14:111 - 4; http://dx.doi.org/10.1016/j.tcb.2004.01.005; PMID: 15055199
  • Wójciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 2001; 114:1343 - 55; PMID: 11257000
  • Carbajal JM, Schaeffer RC Jr.. RhoA inactivation enhances endothelial barrier function. Am J Physiol 1999; 277:C955 - 64; PMID: 10564088
  • Vouret-Craviari V, Boquet P, Pouysségur J, Van Obberghen-Schilling E. Regulation of the actin cytoskeleton by thrombin in human endothelial cells: role of Rho proteins in endothelial barrier function. Mol Biol Cell 1998; 9:2639 - 53; PMID: 9725917
  • Tan H, Biechler S, Junor L, Yost MJ, Dean D, Li J, et al. Fluid flow forces and rhoA regulate fibrous development of the atrioventricular valves. Dev Biol 2012; PMID: 23261934
  • Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 2007; 9:121 - 67; http://dx.doi.org/10.1146/annurev.bioeng.9.060906.151959; PMID: 17373886
  • Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, et al. A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005; 437:426 - 31; http://dx.doi.org/10.1038/nature03952; PMID: 16163360
  • Orsenigo F, Giampietro C, Ferrari A, Corada M, Galaup A, Sigismund S, et al. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 2012; 3:1208; http://dx.doi.org/10.1038/ncomms2199; PMID: 23169049
  • Kroll MH, Hellums JD, McIntire LV, Schafer AI, Moake JL. Platelets and shear stress. Blood 1996; 88:1525 - 41; PMID: 8781407
  • Turowski P, Martinelli R, Crawford R, Wateridge D, Papageorgiou AP, Lampugnani MG, et al. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 2008; 121:29 - 37; http://dx.doi.org/10.1242/jcs.022681; PMID: 18096689
  • Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 2007; 179:4053 - 64; PMID: 17785844
  • Adam AP, Sharenko AL, Pumiglia K, Vincent PA. Src-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 2010; 285:7045 - 55; http://dx.doi.org/10.1074/jbc.M109.079277; PMID: 20048167
  • Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem 2005; 280:31906 - 12; http://dx.doi.org/10.1074/jbc.M505568200; PMID: 16027153
  • Harris TJ, Tepass U. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 2010; 11:502 - 14; http://dx.doi.org/10.1038/nrm2927; PMID: 20571587