Rho GTPases and the regulation of endothelial permeability

Vascular Pharmacology - Tập 39 Số 4-5 - Trang 187-199 - 2002
Beata Wójciak-Stothard1,2, Anne J. Ridley1,2
1Department of Biochemistry and Molecular Biology, University College London, Gower Street, London, UK
2Ludwig Institute for Cancer Research, Royal Free and University College School of Medicine Branch, 91 Riding House Street, London W1W 7BS, UK

Tóm tắt

Từ khóa


Tài liệu tham khảo

Adamson, 1992, Post-translational modifications of p21rho proteins, J. Biol. Chem., 267, 20033, 10.1016/S0021-9258(19)88661-1

Adamson, 1999, Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway, J. Immunol., 162, 2964, 10.4049/jimmunol.162.5.2964

Adamson, 2002, Rho and Rho kinase modulation of barrier properties: cultured endothelial cells and intact microvessels of rats and mice, J. Physiol., 539, 295, 10.1113/jphysiol.2001.013117

Aepfelbacher, 2001, Disturbance of endothelial barrier function by bacterial toxins and atherogenic mediators: a role for Rho/Rho kinase, Cell. Microbiol., 3, 649, 10.1046/j.1462-5822.2001.00145.x

Aepfelbacher, 1999, The tranquilizing injection of Yersinia proteins: a pathogen's strategy to resist host defense, Biol. Chem., 380, 795, 10.1515/BC.1999.099

Aktories, 1989, Botulinum ADP-ribosyltransferase C3: a new tool to study low molecular weight GTP-binding proteins, Trends Pharmacol. Sci., 10, 415, 10.1016/0165-6147(89)90191-0

Aktories, 2000, Rho GTPases as targets of bacterial protein toxins, Biol. Chem., 381, 421, 10.1515/BC.2000.054

Amano, 1999, The COOH terminus of Rho-kinase negatively regulates Rho-kinase activity, J. Biol. Chem., 45, 32418, 10.1074/jbc.274.45.32418

Andor, 2001, YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells, Cell. Microbiol., 3, 301, 10.1046/j.1462-5822.2001.00114.x

Andres, 1993, Mutational analysis of alpha-subunit of protein farnesyltransferase. Evidence for a catalytic role, J. Biol. Chem., 268, 1383, 10.1016/S0021-9258(18)54087-4

Aoki, 1998, Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation, Circ. Res., 82, 666, 10.1161/01.RES.82.6.666

Braga, 2002, Cell–cell adhesion and signaling, Curr. Opin. Cell Biol., 14, 546, 10.1016/S0955-0674(02)00373-3

Bretscher, 2002, ERM proteins and merlin: integrators at the cell cortex, Nat. Rev. Mol. Cell. Biol., 8, 586, 10.1038/nrm882

Buhl, 1995, G alpha 12 and G alpha 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly, J. Biol. Chem., 270, 24631, 10.1074/jbc.270.42.24631

Cannon, 2001, Wasp recruitment to the T cell, APC contact site occurs independently of Cdc42 activation, Immunity, 15, 249, 10.1016/S1074-7613(01)00178-9

Carbajal, 1999, RhoA inactivation enhances endothelial barrier function, Am. J. Physiol., 277, C955, 10.1152/ajpcell.1999.277.5.C955

Carson, 1989, Histamine and inositol phosphate accumulation in endothelium: cAMP and a G protein, Am. J. Physiol., 257, L259

Chen, 2000, Interaction of endothelin-1 with vasoactive factors in mediating glucose-induced increased permeability in endothelial cells, Lab. Invest., 80, 1311, 10.1038/labinvest.3780139

Chen, 2000, Endothelin-1 and nitric oxide affect human cerebromicrovascular endothelial responses and signal transduction, Acta Neurochir., Suppl., 76, 131

Chen, 2002, Comparison of the average structures, from molecular dynamics, of complexes of GTPase activating protein (GAP) with oncogenic and wild-type ras-p21: identification of potential effector domains, J. Protein Chem., 21, 349, 10.1023/A:1019994302273

Corada, 1999, Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo, Proc. Natl. Acad. Sci. U. S. A., 96, 9815, 10.1073/pnas.96.17.9815

Cornelis, 1998, The Yersinia Yop virulon, a bacterial system to subvert cells of the primary host defense, Folia Microbiol., 43, 253, 10.1007/BF02818610

Danner, 1991, Endotoxemia in human septic shock, Chest, 99, 169, 10.1378/chest.99.1.169

Davies, 2000, Specificity and mechanism of action of some commonly used protein kinase inhibitors, Biochem. J., 351, 95, 10.1042/0264-6021:3510095

Dejana, 2000, The molecular organization of endothelial junctions and their functional role in vascular morphogenesis and permeability, Int. J. Dev. Biol., 44, 743

Del Maschio, 1996, Polymorphonuclear leukocyte adhesion triggers the disorganization of endothelial cell-to-cell adherens junctions, J. Cell Biol., 135, 497, 10.1083/jcb.135.2.497

Dormond, 2002, Prostaglandin E2 promotes integrin aVb3-dependent endothelial cell adhesion, Rac-activation and spreading through cAMP/PKA signaling, J. Biol. Chem., 16, 16

Draijer, 1995, cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Regulation via different pathways in human aortic and umbilical vein endothelial cells, Circ. Res., 76, 199, 10.1161/01.RES.76.2.199

Drenckhahn, 1997, The endothelial contractile cytoskeleton, 1

Essler, 1998, Pasteurella multocida toxin increases endothelial permeability via Rho kinase and myosin light chain phosphatase, J. Immunol., 161, 5640, 10.4049/jimmunol.161.10.5640

Essler, 1999, Mildly oxidized low density lipoprotein induces contraction of human endothelial cells through activation of Rho/Rho kinase and inhibition of myosin light chain phosphatase, J. Biol. Chem., 274, 30361, 10.1074/jbc.274.43.30361

Essler, 2000, Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling, J. Immunol., 164, 6543, 10.4049/jimmunol.164.12.6543

Etienne-Manneville, 2000, ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines, J. Immunol., 165, 3375, 10.4049/jimmunol.165.6.3375

Eto, 2001, Thrombin suppresses endothelial nitric oxide synthase and upregulates endothelin-converting enzyme-1 expression by distinct pathways: role of Rho/ROCK and mitogen-activated protein kinase, Circ. Res., 89, 583, 10.1161/hh1901.097084

Feig, 1994, Signal transduction. The hunt for Ras targets, Nature, 370, 508, 10.1038/370508a0

Fleming, 1996, Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor, J. Biol. Chem., 271, 33067, 10.1074/jbc.271.51.33067

Garcia, 1998, Adherent neutrophils activate endothelial myosin light chain kinase: role in transendothelial migration, J. Appl. Physiol., 84, 1817, 10.1152/jappl.1998.84.5.1817

Garcia, 2001, Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement, J. Clin. Invest., 108, 689, 10.1172/JCI12450

Gewaltig, 2002, Vasoprotection by nitric oxide, mechanisms and therapeutic potential, Cardiovasc. Res., 55, 250, 10.1016/S0008-6363(02)00327-9

Ghabriel, 1999, Substance P-induced enhanced permeability of dura mater microvessels is accompanied by pronounced ultrastructural changes, but is not dependent on the density of endothelial cell anionic sites, Acta Neuropathol. (Berl.), 97, 297, 10.1007/s004010050988

Gingras, 2000, Tyrosine phosphorylation of the vascular endothelial-growth-factor receptor-2 (VEGFR-2) is modulated by Rho proteins, Biochem. J., 348, 273, 10.1042/0264-6021:3480273

Goeckeler, 1995, Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation, J. Cell. Biol., 130, 613, 10.1083/jcb.130.3.613

Goeckeler, 2000, Phosphorylation of myosin light chain kinase by p21-activated kinase PAK2, J. Biol. Chem., 275, 18366, 10.1074/jbc.M001339200

Gopalakrishnan, 2002, Rac1, but not RhoA, signaling protects epithelial adherens junction assembly during ATP depletion, Am. J. Physiol., Cell Physiol., 283, C261, 10.1152/ajpcell.00604.2001

Haddad, 2001, The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis, Blood, 97, 33, 10.1182/blood.V97.1.33

Hall, 1998, Rho GTPases and the actin cytoskeleton, Science, 279, 509, 10.1126/science.279.5350.509

Hart, 1998, Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13, Science, 280, 2112, 10.1126/science.280.5372.2112

Hippenstiel, 1997, Glucosylation of small GTP-binding Rho proteins disrupts endothelial barrier function, Am. J. Physiol., 272, L38

Hirao, 1996, Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway, J. Cell Biol., 135, 37, 10.1083/jcb.135.1.37

Hirase, 2001, Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms, J. Biol. Chem., 276, 10423, 10.1074/jbc.M007136200

Hirata, 1995, Location of focal silver staining at endothelial gaps in inflamed venules examined by scanning electron microscopy, Am. J. Physiol., 269, L403

Hordijk, 1999, Vascular-endothelial-cadherin modulates endothelial monolayer permeability, J. Cell. Sci., 112, 1915, 10.1242/jcs.112.12.1915

Ikenoya, 2002, Inhibition of Rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor, J. Neurochem., 81, 9, 10.1046/j.1471-4159.2002.00801.x

Ishizaki, 2000, Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases, Mol. Pharmacol., 5, 976

Just, 1995, The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile, J. Clin. Invest., 95, 1026, 10.1172/JCI117747

Katso, 2001, Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer, Annu. Rev. Cell Dev. Biol., 17, 615, 10.1146/annurev.cellbio.17.1.615

Kawano, 1999, Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo, J. Cell Biol., 147, 1023, 10.1083/jcb.147.5.1023

Kolodney, 1992, Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study, J. Cell Biol., 117, 73, 10.1083/jcb.117.1.73

Kovacs, 2002, E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts, J. Biol. Chem., 277, 6708, 10.1074/jbc.M109640200

Kozasa, 1998, p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13, Science, 280, 2109, 10.1126/science.280.5372.2109

Kraynov, 2000, Localized Rac activation dynamics visualized in living cells, Science, 290, 333, 10.1126/science.290.5490.333

Kuroda, 1996, Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1, J. Biol. Chem., 271, 23363, 10.1074/jbc.271.38.23363

Lampugnani, 2002, VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of tiam, Mol. Biol. Cell, 13, 1175, 10.1091/mbc.01-07-0368

Lang, 1996, Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes, EMBO J., 15, 510, 10.1002/j.1460-2075.1996.tb00383.x

Langeler, 1991, Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP, Am. J. Physiol., 260, C1052, 10.1152/ajpcell.1991.260.5.C1052

Laufs, 2000, Neuroprotection mediated by changes in the endothelial actin cytoskeleton, J. Clin. Invest., 106, 15, 10.1172/JCI9639

Lee, 2000, Sphingosine 1-phosphate stimulates tyrosine phosphorylation of focal adhesion kinase and chemotactic motility of endothelial cells via the G(i) protein-linked phospholipase C pathway, Biochem. Biophys. Res. Commun., 268, 47, 10.1006/bbrc.2000.2087

Levin, 1995, Endothelins, N. Engl. J. Med., 333, 356, 10.1056/NEJM199508103330607

Lin, 1999, Specific contributions of the small GTPases Rho, Rac, and Cdc42 to Dbl transformation, J. Biol. Chem., 274, 23633, 10.1074/jbc.274.33.23633

Liu, 2002, Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta, FASEB J., 16, 950, 10.1096/fj.01-0870com

Lum, 1994, Regulation of vascular endothelial barrier function, Am. J. Physiol., 267, L223

Lynch, 1990, Increased endothelial albumin permeability mediated by protein kinase C activation, J. Clin. Invest., 85, 1991, 10.1172/JCI114663

Mehta, 2001, Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function, J. Biol. Chem., 276, 22614, 10.1074/jbc.M101927200

Miao, 2002, Mechanism of RhoA/Rho kinase activation in endothelin-1-induced contraction in rabbit basilar artery, Am. J. Physiol, Heart Circ. Physiol., 283, H983, 10.1152/ajpheart.00141.2002

Michel, 1999, Microvascular permeability, Physiol. Rev., 79, 703, 10.1152/physrev.1999.79.3.703

Minnear, 2001, Platelet lipid(s) bound to albumin increases endothelial electrical resistance: mimicked by LPA, Am. J. Physiol., Lung Cell. Mol. Physiol., 281, L1334, 10.1152/ajplung.2001.281.6.L1337

Mitani, 2002, Adenovirus as an integrating vector, Curr. Gene Ther., 2, 135, 10.2174/1566523024605591

Moy, 1996, Histamine and thrombin modulate endothelial focal adhesion through centripetal and centrifugal forces, J. Clin. Invest., 97, 1020, 10.1172/JCI118493

Nakasone, 2002, Mast cell-derived VEGF enhances the passage of IgE FE-3 through the rat aortic endothelial cell monolayer, Int. Arch. Allergy Immunol., 129, 76, 10.1159/000065176

Nobes, 1995, Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility, Biochem. Soc. Trans., 23, 456, 10.1042/bst0230456

Noren, 2001, Cadherin engagement regulates Rho family GTPases, J. Biol. Chem., 276, 33305, 10.1074/jbc.C100306200

Panetti, 2002, Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells, Biochim. Biophys. Acta, 1582, 190, 10.1016/S1388-1981(02)00155-5

Park, 2002, 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA, Circ. Res., 91, 143, 10.1161/01.RES.0000028149.15986.4C

Petrache, 2001, Differential effect of MLC kinase in TNF-alpha-induced endothelial cell apoptosis and barrier dysfunction, Am. J. Physiol., Lung Cell. Mol. Physiol., 280, L1168, 10.1152/ajplung.2001.280.6.L1168

Rabiet, 1996, Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization, Arterioscler. Thromb. Vasc. Biol., 16, 488, 10.1161/01.ATV.16.3.488

Ren, 2000, Determination of GTP loading on Rho, Methods Enzymol., 325, 264, 10.1016/S0076-6879(00)25448-7

Ridley, 2000, Rho, 89

Ridley, 2001, Rho family proteins: coordinating cell responses, Trends Cell Biol., 11, 471, 10.1016/S0962-8924(01)02153-5

Ridley, 1992, The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors, Cell, 70, 389, 10.1016/0092-8674(92)90163-7

Ridley, 1992, The small GTP-binding protein rac regulates growth factor-induced membrane ruffling, Cell, 70, 401, 10.1016/0092-8674(92)90164-8

Rottner, 1999, Interplay between Rac and Rho in the control of substrate contact dynamics, Curr. Biol., 17, 640, 10.1016/S0960-9822(99)80286-3

Sah, 2000, The role of Rho in G protein-coupled receptor signal transduction, Annu. Rev. Pharmacol. Toxicol., 40, 459, 10.1146/annurev.pharmtox.40.1.459

Sahai, 1999, Transformation mediated by RhoA requires activity of ROCK kinases, Curr. Biol., 9, 136, 10.1016/S0960-9822(99)80067-0

Sahai, 2001, Cross-talk between Ras and Rho signaling pathways in transformation favours proliferation and increased motility, EMBO J., 20, 755, 10.1093/emboj/20.4.755

Saito, 1998, Endothelial myosin light chain kinase regulates neutrophil migration across human umbilical vein endothelial cell monolayer, J. Immunol., 161, 1533, 10.4049/jimmunol.161.3.1533

Sander, 1999, Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior, J. Cell Biol., 147, 1009, 10.1083/jcb.147.5.1009

Sauzeau, 2000, Cyclic GMP-dependent protein kinase signaling pathway inhibits RhoA-induced Ca2+ sensitization of contraction in vascular smooth muscle, J. Biol. Chem., 275, 21722, 10.1074/jbc.M000753200

Schneeberger, 1992, Structure, function, and regulation of cellular tight junctions, Am. J. Physiol., 262, L647

Schraufstatter, 2002, Complement c3a and c5a induce different signal transduction cascades in endothelial cells, J. Immunol., 169, 2102, 10.4049/jimmunol.169.4.2102

Shaw, 1998, RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts, Mol. Biol. Cell, 9, 403, 10.1091/mbc.9.2.403

Simonson, 1993, Endothelins: multifunctional renal peptides, Physiol. Rev., 73, 375, 10.1152/physrev.1993.73.2.375

Soga, 2001, Rho family GTPases regulate VEGF-stimulated endothelial cell motility, Exp. Cell Res., 269, 73, 10.1006/excr.2001.5295

Sokol, 2001, The effect of IQGAP1 on Xenopus embryonic ectoderm requires Cdc42, J. Biol. Chem., 276, 48425, 10.1074/jbc.M107975200

Spyridopoulos, 2002, Divergence of angiogenic and vascular permeability signaling by VEGF, inhibition of protein kinase C suppresses VEGF-induced angiogenesis, but promotes VEGF-induced, NO-dependent vascular permeability, Arterioscler. Thromb. Vasc. Biol., 22, 901, 10.1161/01.ATV.0000020006.89055.11

Stasek, 1992, The role of protein kinase C in alpha-thrombin-mediated endothelial cell activation, Semin. Thromb. Hemost., 18, 117, 10.1055/s-2007-1002416

Suttorp, 1993, Role of phosphodiesterases in the regulation of endothelial permeability in vitro, J. Clin. Invest., 91, 1421, 10.1172/JCI116346

Takahashi, 1997, Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein, J. Biol. Chem., 272, 23371, 10.1074/jbc.272.37.23371

Takemoto, 2002, Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase, Circulation, 106, 57, 10.1161/01.CIR.0000020682.73694.AB

Taylor, 1999, Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho, J. Cell Sci., 112, 231, 10.1242/jcs.112.2.231

Thompson, 2002, Intercellular adhesion molecule (ICAM)-1, but not ICAM-2, activates RhoA and stimulates c-fos and rhoA transcription in endothelial cells, J. Immunol., 169, 1007, 10.4049/jimmunol.169.2.1007

Tinsley, 1999, Activated neutrophils induce hyperpermeability and phosphorylation of adherens junction proteins in coronary venular endothelial cells, J. Biol. Chem., 274, 24930, 10.1074/jbc.274.35.24930

Tokuyama, 2002, Effects of Y-27632, a Rho/Rho kinase inhibitor, on leukotriene D(4)- and histamine-induced airflow obstruction and airway microvascular leakage in guinea pigs in vivo, Pharmacology, 64, 189, 10.1159/000056170

Tseng, 2002, Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study, Mol. Pharmacol., 62, 864, 10.1124/mol.62.4.864

Tsuji, 2002, ROCK and mDia1 antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts, J. Cell Biol., 157, 819, 10.1083/jcb.200112107

Uehata, 1997, Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension, Nature, 389, 990, 10.1038/40187

Vallota, 1973, Formation of C3a and C5a anaphylatoxins in whole human serum after inhibition of the anaphylatoxin inactivator, J. Exp. Med., 137, 1109, 10.1084/jem.137.5.1109

Van Aelst, 1997, Rho GTPases and signaling networks, Genes Dev., 11, 2295, 10.1101/gad.11.18.2295

van Buul, 2002, Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin, J. Immunol., 168, 588, 10.4049/jimmunol.168.2.588

van Hinsbergh, 2002, Intracellular signalling involved in modulating human endothelial barrier function, J. Anat., 200, 549, 10.1046/j.1469-7580.2002.00060.x

van Leeuwen, 1999, Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading, Nat. Cell Biol., 1, 242, 10.1038/12068

van Nieuw Amerongen, 2001, Cytoskeletal effects of rho-like small guanine nucleotide-binding proteins in the vascular system, Arterioscler. Thromb. Vasc. Biol., 21, 300, 10.1161/01.ATV.21.3.300

van Nieuw Amerongen, 1998, Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA, Circ. Res., 83, 1115, 10.1161/01.RES.83.11.1115

van Nieuw Amerongen, 2000, Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases, Circ. Res., 87, 335, 10.1161/01.RES.87.4.335

van Nieuw Amerongen, 2000, Simvastatin improves disturbed endothelial barrier function, Circulation, 102, 2803, 10.1161/01.CIR.102.23.2803

van Nieuw Amerongen, 2000, Role of RhoA and Rho kinase in lysophosphatidic acid-induced endothelial barrier dysfunction, Arterioscler. Thromb. Vasc. Biol., 20, E127, 10.1161/01.ATV.20.12.e127

van Wetering, 2002, Reactive oxygen species mediate Rac-induced loss of cell–cell adhesion in primary human endothelial cells, J. Cell Sci., 115, 1837, 10.1242/jcs.115.9.1837

Vastrik, 1999, Sema3A-induced growth-cone collapse is mediated by rac1 amino acids 17–32, Curr. Biol., 18, 991, 10.1016/S0960-9822(99)80447-3

Von Pawel-Rammingen, 2000, GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure, Mol. Microbiol., 36, 737, 10.1046/j.1365-2958.2000.01898.x

Vouret-Craviari, 1998, Regulation of the actin cytoskeleton by thrombin in human endothelial cells: role of Rho proteins in endothelial barrier function, Mol. Biol. Cell, 9, 2639, 10.1091/mbc.9.9.2639

Vouret-Craviari, 1999, Effects of cytotoxic necrotizing factor 1 and lethal toxin on actin cytoskeleton and VE-cadherin localization in human endothelial cell monolayers, Infect. Immun., 67, 3002, 10.1128/IAI.67.6.3002-3008.1999

Vouret-Craviari, 2002, Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells, J. Cell. Sci., 115, 2475, 10.1242/jcs.115.12.2475

Wang, 2001, Mechanisms of sodium fluoride-induced endothelial cell barrier dysfunction: role of MLC phosphorylation, Am. J. Physiol., Lung Cell. Mol. Physiol., 281, L1472, 10.1152/ajplung.2001.281.6.L1472

Wojciak-Stothard, 1998, Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell–cell junctions by Rho, Rac, and Cdc42 in human endothelial cells, J. Cell. Physiol., 176, 150, 10.1002/(SICI)1097-4652(199807)176:1<150::AID-JCP17>3.0.CO;2-B

Wojciak-Stothard, 1999, Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering, J. Cell Biol., 145, 1293, 10.1083/jcb.145.6.1293

Wojciak-Stothard, 2001, Rho and Rac but not Cdc42 regulate endothelial cell permeability, J. Cell. Sci., 114, 1343, 10.1242/jcs.114.7.1343

Zhao, 2002, Substance P-stimulated interleukin-8 expression in human colonic epithelial cells involves Rho family small GTPases, Biochem. J., 368, 665, 10.1042/bj20020950

Zondag, 2000, Oncogenic Ras downregulates Rac activity which leads to increased Rho activity and epithelial-mesenchymal transition, J. Cell Biol., 149, 775, 10.1083/jcb.149.4.775

Zumbihl, 1999, The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA, J. Biol. Chem., 274, 29289, 10.1074/jbc.274.41.29289