Endothelial junction regulation: A prerequisite for leukocytes crossing the vessel wall

Journal of Innate Immunity

Volumn 5, Issue 4, 2013, Pages 324-335

  Daniel, Anna E ^a   Van Buul, Jaap D ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Cell cell junctions; Diapedesis; Extravasation; Signaling; Transmigration; Vascular endothelial cadherin

Indexed keywords

GUANOSINE TRIPHOSPHATASE; METALLOPROTEINASE; PHOSPHATASE; PROTEIN TYROSINE KINASE;

ADAPTIVE IMMUNITY; BLOOD VESSEL WALL; CELL JUNCTION; ENDOTHELIUM; INFLAMMATION; LEUKOCYTE ADHERENCE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SHEAR STRESS; TIGHT JUNCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84879416297     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000348828     Document Type: Review

References (127)

1. Aird WC: Phenotypic heterogeneity of the endothelium. 1. Structure, function, and mechanisms. Circ Res 2007; 100: 158-173.
2. Wolburg H, Lippoldt A: Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul Pharmacol 2002; 38: 323-337.
3. Miyasaka M, Tanaka T: Lymphocyte trafficking across high endothelial venules: dogmas and enigmas. Nat Rev Immunol 2004; 4: 360-370.
4. Dejana E, Orsenigo F, Molendini C, Baluk P, McDonald DM: Organization and signaling of endothelial cell-to-cell junctions in various regions of the blood and lymphatic vascular trees. Cell Tissue Res 2009; 335: 17-25.
5. Nagy JA, Benjamin L, Zeng H, Dvorak AM, Dvorak HF: Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 2008; 11: 109-119.
6. Nemeth T, Mocsai A: The role of neutrophils in autoimmune diseases. Immunol Lett 2012; 143: 9-19.
7. Carman CV, Springer TA: Trans-cellular migration: cell-cell contacts get intimate. Curr Opin Cell Biol 2008; 20: 533-540.
8. Sage PT, Carman CV: Settings and mechanisms for trans-cellular diapedesis. Front Biosci 2009; 14: 5066-5083.
9. Wolburg H, Wolburg-Buchholz K, Engelhardt B: Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact. Acta Neuropathol 2005; 109: 181-190.
10. Feng D, Nagy JA, Pyne K, Dvorak HF, Dvorak AM: Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J Exp Med 1998; 187: 903-915.
11. Cho Y, De Bruyn PP: Internal structure of the postcapillary high-endothelial venules of rodent lymph nodes and Peyer's patches and the transendothelial lymphocyte passage. Am J Anat 1986; 177: 481-490.
12. Azzali G, Arcari ML, Caldara GF: The 'mode' of lymphocyte extravasation through HEV of Peyer's patches and its role in normal homing and inflammation. Microvasc Res 2008; 75: 227-237.
13. Schulte D, Kuppers V, Dartsch N, Broermann A, Li H, Zarbock A, Kamenyeva O, Kiefer F, Khandoga A, Massberg S, Vestweber D: Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 2011; 30: 4157-4170.
14. Lossinsky AS, Shivers RR: Structural pathways for macromolecular and cellular transport across the blood-brain barrier during inflammatory conditions. Review. Histol Histopathol 2004; 19: 535-564.
15. Raine CS, Cannella B, Duijvestijn AM, Cross AH: Homing to central nervous system vasculature by antigen-specific lymphocytes. 2. Lymphocyte/endothelial cell adhesion during the initial stages of autoimmune demyelination. Lab Invest 1990; 63: 476-489.
16. Lossinsky AS, Badmajew V, Robson JA, Moretz RC, Wisniewski HM: Sites of egress of inflammatory cells and horseradish peroxidase transport across the blood-brain barrier in a murine model of chronic relapsing experimental allergic encephalomyelitis. Acta Neuropathol 1989; 78: 359-371.
17. Lossinsky AS, Pluta R, Song MJ, Badmajew V, Moretz RC, Wisniewski HM: Mechanisms of inflammatory cell attachment in chronic relapsing experimental allergic encephalomyelitis: a scanning and high-voltage electron microscopic study of the injured mouse blood-brain barrier. Microvasc Res 1991; 41: 299-310.
18. Nathan C: Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 2006; 6: 173-182.
19. Ley K, Laudanna C, Cybulsky MI, Nourshargh S: Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-689.
20. Burns AR, Walker DC, Brown ES, Thurmon LT, Bowden RA, Keese CR, Simon SI, Entman ML, Smith CW: Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J Immunol 1997; 159: 2893-2903.
21. Shulman Z, Cohen SJ, Roediger B, Kalchenko V, Jain R, Grabovsky V, Klein E, Shinder V, Stoler-Barak L, Feigelson SW, Meshel T, Nurmi SM, Goldstein I, Hartley O, Gahmberg CG, Etzioni A, Weninger W, Ben-Baruch A, Alon R: Transendothelial migration of lymphocytes mediated by intraendothelial vesicle stores rather than by extracellular chemokine depots. Nat Immunol 2012; 13: 67-76.
22. Luster AD, Alon R, von Andrian UH: Immune cell migration in inflammation: present and future therapeutic targets. Nat Immunol 2005; 6: 1182-1190.
23. Tarrant TK, Patel DD: Chemokines and leukocyte trafficking in rheumatoid arthritis. Pathophysiology 2006; 13: 1-14.
24. Mamdouh Z, Chen X, Pierini LM, Maxfield FR, Muller WA: Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 2003; 421: 748-753.
25. Mamdouh Z, Mikhailov A, Muller WA: Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J Exp Med 2009; 206: 2795-2808.
26. Schenkel AR, Chew TW, Muller WA: Platelet endothelial cell adhesion molecule deficiency or blockade significantly reduces leukocyte emigration in a majority of mouse strains. J Immunol 2004; 173: 6403-6408.
27. Lou O, Alcaide P, Luscinskas FW, Muller WA: CD99 is a key mediator of the transendothelial migration of neutrophils. J Immunol 2007; 178: 1136-1143.
28. Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA: CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 2002; 3: 143-150.
29. Morita K, Sasaki H, Furuse M, Tsukita S: Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J Cell Biol 1999; 147: 185-194.
30. Hirata K, Ishida T, Penta K, Rezaee M, Yang E, Wohlgemuth J, Quertermous T: Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J Biol Chem 2001; 276: 16223-16231.
31. Steed E, Balda MS, Matter K: Dynamics and functions of tight junctions. Trends Cell Biol 2010; 20: 142-149.
32. Wallez Y, Huber P: Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim Biophys Acta 2008; 1778: 794-809.
33. Hirase T, Staddon JM, Saitou M, Ando-Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL: Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 1997; 110: 1603-1613.
34. Kevil CG, Okayama N, Trocha SD, Kalogeris TJ, Coe LL, Specian RD, Davis CP, Alexander JS: Expression of Zonula occludens and adherens junctional proteins in human venous and arterial endothelial cells: role of occludin in endothelial solute barriers. Microcirculation 1998; 5: 197-210.
35. Greenwood J, Heasman SJ, Alvarez JI, Prat A, Lyck R, Engelhardt B: Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol Appl Neurobiol 2011; 37: 24-39.
36. Khandoga A, Huettinger S, Khandoga AG, Li H, Butz S, Jauch KW, Vestweber D, Krombach F: Leukocyte transmigration in inflamed liver: a role for endothelial cell-selective adhesion molecule. J Hepatol 2009; 50: 755-765.
37. Wegmann F, Petri B, Khandoga AG, Moser C, Khandoga A, Volkery S, Li H, Nasdala I, Brandau O, Fassler R, Butz S, Krombach F, Vestweber D: ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J Exp Med 2006; 203: 1671-1677.
38. Inoue M, Ishida T, Yasuda T, Toh R, Hara T, Cangara HM, Rikitake Y, Taira K, Sun L, Kundu RK, Quertermous T, Hirata K: Endothelial cell-selective adhesion molecule modulates atherosclerosis through plaque angiogenesis and monocyte-endothelial interaction. Microvasc Res 2010; 80: 179-187.
39. Kimura R, Ishida T, Kuriyama M, Hirata K, Hayashi Y: Interaction of endothelial cell-selective adhesion molecule and MAGI-1 promotes mature cell-cell adhesion via activation of RhoA. Genes Cells 2010; 15: 385-396.
40. Weber C, Fraemohs L, Dejana E: The role of junctional adhesion molecules in vascular inflammation. Nat Rev Immunol 2007; 7: 467-477.
41. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C: JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 2002; 3: 151-158.
42. Chavakis T, Keiper T, Matz-Westphal R, Hersemeyer K, Sachs UJ, Nawroth PP, Preissner KT, Santoso S: The junctional adhesion molecule-C promotes neutrophil transendothelial migration in vitro and in vivo. J Biol Chem 2004; 279: 55602-55608.
43. Cunningham SA, Rodriguez JM, Arrate MP, Tran TM, Brock TA: JAM2 interacts with alpha4beta1. Facilitation by JAM3. J Biol Chem 2002; 277: 27589-27592.
44. Ostermann G, Fraemohs L, Baltus T, Schober A, Lietz M, Zernecke A, Liehn EA, Weber C: Involvement of JAM-A in mononuclear cell recruitment on inflamed or atherosclerotic endothelium: inhibition by soluble JAM-A. Arterioscler Thromb Vasc Biol 2005; 25: 729-735.
45. Bradfield PF, Scheiermann C, Nourshargh S, Ody C, Luscinskas FW, Rainger GE, Nash GB, Miljkovic-Licina M, Aurrand-Lions M, Imhof BA: JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood 2007; 110: 2545-2555.
46. Woodfin A, Voisin MB, Beyrau M, Colom B, Caille D, Diapouli FM, Nash GB, Chavakis T, Albelda SM, Rainger GE, Meda P, Imhof BA, Nourshargh S: The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat Immunol 2011; 12: 761-769.
47. Aurrand-Lions M, Johnson-Leger C, Wong C, Du PL, Imhof BA: Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 2001; 98: 3699-3707.
48. Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A, Houen G, Ruco LP, Dejana E: A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 1992; 118: 1511-1522.
49. Leach L, Clark P, Lampugnani MG, Arroyo AG, Dejana E, Firth JA: Immunoelectron characterisation of the inter-endothelial junctions of human term placenta. J Cell Sci 1993; 104: 1073-1081.
50. Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M, Lampugnani MG, Martin-Padura I, Stoppacciaro A, Ruco L, McDonald DM, Ward PA, Dejana E: Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA 1999; 96: 9815-9820.
51. Gotsch U, Borges E, Bosse R, Boggemeyer E, Simon M, Mossmann H, Vestweber D: VEcadherin antibody accelerates neutrophil recruitment in vivo. J Cell Sci 1997; 110: 583-588.
52. Dejana E, Orsenigo F, Lampugnani MG: The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 2008; 121: 2115-2122.
53. Kowalczyk AP, Reynolds AB: Protecting your tail: regulation of cadherin degradation by p120-catenin. Curr Opin Cell Biol 2004; 16: 522-527.
54. Herron CR, Lowery AM, Hollister PR, Reynolds AB, Vincent PA: p120 regulates endothelial permeability independently of its NH2 terminus and Rho binding. Am J Physiol Heart Circ Physiol 2011; 300:H36-H48.
55. Hinck L, Nathke IS, Papkoff J, Nelson WJ: Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J Cell Biol 1994; 125: 1327-1340.
56. 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: 903-915.
57. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ: Deconstructing the cadherin-catenin-Actin complex. Cell 2005; 123: 889-901.
58. Yonemura S: Cadherin-Actin interactions at adherens junctions. Curr Opin Cell Biol 2011; 23: 515-522.
59. Navaratna D, McGuire PG, Menicucci G, Das A: Proteolytic degradation of VE-cadherin alters the blood-retinal barrier in diabetes. Diabetes 2007; 56: 2380-2387.
60. Soeki T, Tamura Y, Shinohara H, Sakabe K, Onose Y, Fukuda N: Elevated concentration of soluble vascular endothelial cadherin is associated with coronary atherosclerosis. Circ J 2004; 68: 1-5.
61. Sidibe A, Mannic T, Arboleas M, Subileau M, Gulino-Debrac D, Bouillet L, Jan M, Vandhuick T, Le Loet X, Vittecoq O, Vilgrain I: Soluble VE-cadherin in rheumatoid arthritis patients correlates with disease activity: evidence for tumor necrosis factor alpha-induced VE-cadherin cleavage. Arthritis Rheum 2012; 64: 77-87.
62. Ichikawa Y, Ishikawa T, Momiyama N, Kamiyama M, Sakurada H, Matsuyama R, Hasegawa S, Chishima T, Hamaguchi Y, Fujii S, Saito S, Kubota K, Hasegawa S, Ike H, Oki S, Shimada H: Matrilysin (MMP-7) degrades VE-cadherin and accelerates accumulation of beta-catenin in the nucleus of human umbilical vein endothelial cells. Oncol Rep 2006; 15: 311-315.
63. Donners MM, Wolfs IM, Olieslagers S, Mohammadi-Motahhari Z, Tchaikovski V, Heeneman S, van Buul JD, Caolo V, Molin DG, Post MJ, Waltenberger J: A disintegrin and metalloprotease 10 is a novel mediator of vascular endothelial growth factor-induced endothelial cell function in angiogenesis and is associated with atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30: 2188-2195.
64. Schulz B, Pruessmeyer J, Maretzky T, Ludwig A, Blobel CP, Saftig P, Reiss K: ADAM10 regulates endothelial permeability and T-cell transmigration by proteolysis of vascular endothelial cadherin. Circ Res 2008; 102: 1192-1201.
65. Sun C, Wu MH, Lee ES, Yuan SY: A disintegrin and metalloproteinase 15 contributes to atherosclerosis by mediating endothelial barrier dysfunction via Src family kinase activity. Arterioscler Thromb Vasc Biol 2012; 32: 2444-2451.
66. Sun C, Wu MH, Guo M, Day ML, Lee ES, Yuan SY: ADAM15 regulates endothelial permeability and neutrophil migration via Src/ERK1/2 signalling. Cardiovasc Res 2010; 87: 348-355.
67. Koenen RR, Pruessmeyer J, Soehnlein O, Fraemohs L, Zernecke A, Schwarz N, Reiss K, Sarabi A, Lindbom L, Hackeng TM, Weber C, Ludwig A: Regulated release and functional modulation of junctional adhesion molecule A by disintegrin metalloproteinases. Blood 2009; 113: 4799-4809.
68. Dreymueller D, Pruessmeyer J, Groth E, Ludwig A: The role of ADAM-mediated shedding in vascular biology. Eur J Cell Biol 2012; 91: 472-485.
69. Vestweber D, Winderlich M, Cagna G, Nottebaum AF: Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol 2009; 19: 8-15.
70. Timmerman I, Hordijk PL, van Buul JD: Phosphorylation at endothelial cell-cell junctions: implications for VE-cadherin function. Cell Health Cytoskeleton 2010; 2: 23-31.
71. 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: 31906-31912.
72. Alcaide P, Newton G, Auerbach S, Sehrawat S, Mayadas TN, Golan DE, Yacono P, Vincent P, Kowalczyk A, Luscinskas FW: p120-catenin regulates leukocyte transmigration through an effect on VE-cadherin phosphorylation. Blood 2008; 112: 2770-2779.
73. Alcaide P, Martinelli R, Newton G, Williams MR, Adams A, Vincent PA, Luscinskas FW: p120-catenin prevents neutrophil transmigration independently of RhoA inhibition by impairing Src dependent VE-cadherin phosphorylation. Am J Physiol Cell Physiol 2012; 303:C385-C395.
74. Hudry-Clergeon H, Stengel D, Ninio E, Vilgrain I: Platelet-Activating factor increases VE-cadherin tyrosine phosphorylation in mouse endothelial cells and its association with the PtdIns3 ?-kinase. FASEB J 2005; 19: 512-520.
75. Bazzoni G, Dejana E: Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 2004; 84: 869-901.
76. Angelini DJ, Hyun SW, Grigoryev DN, Garg P, Gong P, Singh IS, Passaniti A, Hasday JD, Goldblum SE: TNF-Alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am J Physiol Lung Cell Mol Physiol 2006; 291:L1232-L1245.
77. 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: 4053-4063.
78. van Buul JD, Anthony EC, Fernandez-Borja M, Burridge K, Hordijk PL: Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin-based cell-cell adhesion by regulating beta-catenin tyrosine phosphorylation. J Biol Chem 2005; 280: 21129-21136.
79. Turowski P, Martinelli R, Crawford R, Wateridge D, Papageorgiou AP, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E, Greenwood J: Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 2008; 121: 29-37.
80. Gavard J, Gutkind JS: VEGF controls endothelial-cell permeability by promoting the beta-Arrestin-dependent endocytosis of VEcadherin. Nat Cell Biol 2006; 8: 1223-1234.
81. Orsenigo F, Giampietro C, Ferrari A, Corada M, Galaup A, Sigismund S, Ristagno G, Maddaluno L, Young KG, Franco D, Kurtcuoglu V, Poulikakos D, Baluk P, McDonald D, Grazia LM, Dejana E: Phosphorylation of VEcadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 2012; 3: 1208.
82. Broermann A, Winderlich M, Block H, Frye M, Rossaint J, Zarbock A, Cagna G, Linnepe R, Schulte D, Nottebaum AF, Vestweber D: Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. J Exp Med 2011; 208: 2393-2401.
83. Nottebaum AF, Cagna G, Winderlich M, Gamp AC, Linnepe R, Polaschegg C, Filippova K, Lyck R, Engelhardt B, Kamenyeva O, Bixel MG, Butz S, Vestweber D: VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VEcadherin by leukocytes and by VEGF. J Exp Med 2008; 205: 2929-2945.
84. Hatanaka K, Lanahan AA, Murakami M, Simons M: Fibroblast growth factor signaling potentiates VE-cadherin stability at adherens junctions by regulating SHP2. PLoS One 2012; 7:e37600.
85. Timmerman I, Hoogenboezem M, Bennett AM, Geerts D, Hordijk PL, van Buul JD: The tyrosine phosphatase SHP2 regulates recovery of endothelial adherens junctions through control of beta-catenin phosphorylation. Mol Biol Cell 2012; 23: 4212-4225.
86. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, De-Lisser H, Schwartz MA: A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 2005; 437: 426-431.
87. Tzima E: Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ Res 2006; 98: 176-185.
88. McEver RP, Zhu C: Rolling cell adhesion. Annu Rev Cell Dev Biol 2010; 26: 363-396.
89. Lawrence MB, Kansas GS, Kunkel EJ, Ley K: Threshold levels of fluid shear promote leukocyte adhesion through selectins (CD62L,P,E). J Cell Biol 1997; 136: 717-727.
90. Cinamon G, Shinder V, Alon R: Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat Immunol 2001; 2: 515-522.
91. Hahn C, Schwartz MA: Mechanotransduction in vascular physiology and atherogenesis. Nat Rev Mol Cell Biol 2009; 10: 53-62.
92. Malek AM, Alper SL, Izumo S: Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999; 282: 2035-2042.
93. Rabodzey A, Yao Y, Luscinskas FW, Shaw SK, Dewey CF Jr: Early response of endothelial cells to flow is mediated by VE-cadherin. Cell Commun Adhes 2007; 14: 195-209.
94. Miao H, Hu YL, Shiu YT, Yuan S, Zhao Y, Kaunas R, Wang Y, Jin G, Usami S, Chien S: 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.
95. Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, Rehmann H, de Rooij J: Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 2012; 196: 641-652.
96. Beckers CM, van Hinsbergh VW, van Nieuw Amerongen GP: Driving Rho GTPase activity in endothelial cells regulates barrier integrity. Thromb Haemost 2010; 103: 40-55.
97. Jaffe AB, Hall A: Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005; 21: 247-269.
98. Menke A, Giehl K: Regulation of adherens junctions by Rho GTPases and p120-catenin. Arch Biochem Biophys 2012; 524: 48-55.
99. Yamada S, Nelson WJ: Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 2007; 178: 517-527.
100. Ratheesh A, Gomez GA, Priya R, Verma S, Kovacs EM, Jiang K, Brown NH, Akhmanova A, Stehbens SJ, Yap AS: Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 2012; 14: 818-828.
101. Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB: p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006; 127: 1027-1039.
102. Deem TL, Abdala-Valencia H, Cook-Mills JM: VCAM-1 activation of endothelial cell protein tyrosine phosphatase 1B. J Immunol 2007; 178: 3865-3873.
103. Cook-Mills JM, Johnson JD, Deem TL, Ochi A, Wang L, Zheng Y: Calcium mobilization and Rac1 activation are required for VCAM-1 (vascular cell adhesion molecule-1) stimulation of NADPH oxidase activity. Biochem J 2004; 378: 539-547.
104. Cain RJ, Vanhaesebroeck B, Ridley AJ: The PI3K p110alpha isoform regulates endothelial adherens junctions via Pyk2 and Rac1. J Cell Biol 2010; 188: 863-876.
105. Monaghan-Benson E, Burridge K: The regulation of vascular endothelial growth factorinduced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 2009; 284: 25602-25611.
106. van Wetering S, van den Berk N, van Buul JD, Mul FP, Lommerse I, Mous R, ten Klooster JP, Zwaginga JJ, Hordijk PL: VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leukocyte transmigration. Am J Physiol Cell Physiol 2003; 285:C343-C352.
107. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ: Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 2001; 114: 1343-1355.
108. Warfel JM, D'Agnillo F: Anthrax lethal toxin-mediated disruption of endothelial VEcadherin is attenuated by inhibition of the Rho-Associated kinase pathway. Toxins (Basel) 2011; 3: 1278-1293.
109. Wojciak-Stothard B, Tsang LY, Haworth SG: Rac and Rho play opposing roles in the regulation of hypoxia/reoxygenation-induced permeability changes in pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 2005; 288:L749-L760.
110. Etienne S, Adamson P, Greenwood J, Strosberg AD, Cazaubon S, Couraud PO: ICAM-signaling pathways associated with Rho activation in microvascular brain endothelial cells. J Immunol 1998; 161: 5755-5761.
111. Adamson P, Etienne S, Couraud PO, Calder V, Greenwood J: Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a Rho-dependent pathway. J Immunol 1999; 162: 2964-2973.
112. Wojciak-Stothard B, Williams L, Ridley AJ: Monocyte adhesion and spreading on human endothelial cells is dependent on Rhoregulated receptor clustering. J Cell Biol 1999; 145: 1293-1307.
113. Etienne-Manneville S, Manneville JB, Adamson P, Wilbourn B, Greenwood J, Couraud PO: ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J Immunol 2000; 165: 3375-3383.
114. Thompson PW, Randi AM, Ridley AJ: Intercellular adhesion molecule (ICAM)-1, but not ICAM-2, activates RhoA and stimulates c-fos and RhoA transcription in endothelial cells. J Immunol 2002; 169: 1007-1013.
115. van Buul JD, Allingham MJ, Samson T, Meller J, Boulter E, Garcia-Mata R, Burridge K: RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol 2007; 178: 1279-1293.
116. Pannekoek WJ, van Dijk JJ, Chan OY, Huveneers S, Linnemann JR, Spanjaard E, Brouwer PM, van der Meer AJ, Zwartkruis FJ, Rehmann H, de Rooij J, Bos JL: Epac1 and PDZ-GEF cooperate in Rap1 mediated endothelial junction control. Cell Signal 2011; 23: 2056-2064.
117. Noda K, Zhang J, Fukuhara S, Kunimoto S, Yoshimura M, Mochizuki N: Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through alpha-And beta-catenins in cyclic AMP-Epac-Rap1 signal-Activated endothelial cells. Mol Biol Cell 2010; 21: 584-596.
118. Kooistra MR, Corada M, Dejana E, Bos JL: Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett 2005; 579: 4966-4972.
119. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N: Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol 2005; 25: 136-146.
120. Cullere X, Shaw SK, Andersson L, Hirahashi J, Luscinskas FW, Mayadas TN: Regulation of vascular endothelial barrier function by Epac, a cAMP-Activated exchange factor for Rap GTPase. Blood 2005; 105: 1950-1955.
121. Birukova AA, Zagranichnaya T, Alekseeva E, Bokoch GM, Birukov KG: Epac/Rap and PKA are novel mechanisms of ANP-induced Rac-mediated pulmonary endothelial barrier protection. J Cell Physiol 2008; 215: 715-724.
122. Pannekoek WJ, Kooistra MR, Zwartkruis FJ, Bos JL: Cell-cell junction formation: the role of Rap1 and Rap1 guanine nucleotide exchange factors. Biochim Biophys Acta 2009; 1788: 790-796.
123. Orlova VV, Economopoulou M, Lupu F, Santoso S, Chavakis T: Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherinmediated cell-cell contacts. J Exp Med 2006; 203: 2703-2714.
124. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E: Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142: 117-127.
125. Mandell KJ, Babbin BA, Nusrat A, Parkos CA: Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on beta1 integrins and Rap1 activity. J Biol Chem 2005; 280: 11665-11674.
126. Wittchen ES, Worthylake RA, Kelly P, Casey PJ, Quilliam LA, Burridge K: Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J Biol Chem 2005; 280: 11675-11682.
127. van Buul JD, Voermans C, van den Berg V, Anthony EC, Mul FP, van Wetering S, van der Schoot CE, Hordijk PL: Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol 2002; 168: 588-596.