Rho GTPases and the regulation of endothelial permeability

Vascular Pharmacology

Volumn 39, Issue 4-5, 2002, Pages 187-199

  Wojciak Stothard, Beata ^a,b   Ridley, Anne J ^a,b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Endothelial permeability; Lysophosphatidic acid; Rho GTPases; Tumour necrosis factor

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; BRADYKININ; GUANOSINE TRIPHOSPHATASE; HISTAMINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LYSOPHOSPHATIDIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SCATTER FACTOR; THROMBIN; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASOCONSTRICTOR AGENT; VASODILATOR AGENT;

CELL JUNCTION; CELL MEMBRANE PERMEABILITY; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXTRAVASATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECT; ENZYMOLOGY; METABOLISM; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; CELL MEMBRANE PERMEABILITY; ENDOTHELIUM, VASCULAR; RHO GTP-BINDING PROTEINS; VASOCONSTRICTOR AGENTS; VASODILATOR AGENTS;

EID: 0042344706     PISSN: 15371891     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1537-1891(03)00008-9     Document Type: Review

References (138)

1. Adamson P., Marshall C.J., Hall A., Tilbrook P.A. Post-translational modifications of p21rho proteins. J. Biol. Chem. 267:1992;20033-20038.
2. Adamson P., Etienne S., Couraud P.O., Calder V., Greenwood J. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J. Immunol. 162:1999;2964-2973.
3. Adamson R.H., Curry F.E., Adamson G., Liu B., Jiang Y., Aktories K., Barth H., Daigeler A., Golenhofen N., Ness W., Drenckahn D. Rho and Rho kinase modulation of barrier properties: cultured endothelial cells and intact microvessels of rats and mice. J. Physiol. 539:2002;295-308.
4. Aepfelbacher M., Essler M. Disturbance of endothelial barrier function by bacterial toxins and atherogenic mediators: a role for Rho/Rho kinase. Cell. Microbiol. 3:2001;649-658.
5. Aepfelbacher M., Zumbihl R., Ruckdeschel K., Jacobi C.A., Barz C., Heesemann J. The tranquilizing injection of Yersinia proteins: a pathogen’s strategy to resist host defense. Biol. Chem. 380:1999;795-802.
6. Aktories K., Hall A. Botulinum ADP-ribosyltransferase C3: a new tool to study low molecular weight GTP-binding proteins. Trends Pharmacol. Sci. 10:1989;415-418.
7. Aktories K., Schmidt G., Just I. Rho GTPases as targets of bacterial protein toxins. Biol. Chem. 381:2000;421-426.
8. Amano M., Chihara K., Nakamura N., Kaneko T., Matsuura Y., Kaibuchi K. The COOH terminus of Rho-kinase negatively regulates Rho-kinase activity. J. Biol. Chem. 45:1999;32418-32424.
9. Andor A., Trulzsch K., Essler M., Roggenkamp A., Wiedemann A., Heesemann J., Aepfelbacher M. YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell. Microbiol. 3:2001;301-310.
10. Andres D.A., Goldstein J.L., Ho Y.K., Brown M.S. Mutational analysis of alpha-subunit of protein farnesyltransferase. Evidence for a catalytic role. J. Biol. Chem. 268:1993;1383-1390.
11. Aoki H., Izumo S., Sadoshima J. Angiotensin II activates RhoA in cardiac myocytes: a critical role of RhoA in angiotensin II-induced premyofibril formation. Circ. Res. 82:1998;666-676.
12. Braga V. Cell-cell adhesion and signaling. Curr. Opin. Cell Biol. 14:2002;546.
13. Bretscher A., Edwards K., Fehon R.G. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell. Biol. 8:2002;586-599.
14. Buhl A.M., Johnson N.L., Dhanasekaran N., Johnson G.L. G alpha 12 and G alpha 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270:1995;24631-24634.
15. Cannon J.L., Labno C.M., Bosco G., Seth A., McGavin M.H., Siminovitch K.A., Rosen M.K., Burkhardt J.K. Wasp recruitment to the T cell, APC contact site occurs independently of Cdc42 activation. Immunity. 15:2001;249-259.
16. Carbajal J.M., Schaeffer R.C. Jr. RhoA inactivation enhances endothelial barrier function. Am. J. Physiol. 277:1999;C955-C964.
17. Carson M.R., Shasby S.S., Shasby D.M. Histamine and inositol phosphate accumulation in endothelium: cAMP and a G protein. Am. J. Physiol. 257:1989;L259-L264.
18. Chen S., Apostolova M.D., Cherian M.G., Chakrabarti S. Interaction of endothelin-1 with vasoactive factors in mediating glucose-induced increased permeability in endothelial cells. Lab. Invest. 80:2000;1311-1321.
19. Chen Y., McCarron R.M., Azzam N., Bembry J., Reutzler C., Lenz F.A., Spatz M. Endothelin-1 and nitric oxide affect human cerebromicrovascular endothelial responses and signal transduction. Acta Neurochir., Suppl. 76:2000;131-135.
20. Chen J.M., Friedman F.K., Brandt-Rauf P.W., Pincus M.R., Chie L. 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. 21:2002;349-359.
21. Corada M., Mariotti M., Thurston G., Smith K., Kunkel R., Brockhaus M., Lampugnani M.G., Martin-Padura I., Stoppacciaro A., Ruco L., McDonald D.M., Ward P.A., Dejana E. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. U. S. A. 96:1999;9815-9820.
22. Cornelis G.R. The Yersinia Yop virulon, a bacterial system to subvert cells of the primary host defense. Folia Microbiol. 43:1998;253-261.
23. Danner R.L., Elin R.J., Hosseini J.M., Wesley R.A., Reilly J.M., Parillo J.E. Endotoxemia in human septic shock. Chest. 99:1991;169-175.
24. Davies S.P., Reddy H., Caivano M., Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:2000;95-105.
25. Dejana E., Lampugnani M.G., Martinez-Estrada O., Bazzoni G. The molecular organization of endothelial junctions and their functional role in vascular morphogenesis and permeability. Int. J. Dev. Biol. 44:2000;743-748.
26. Del Maschio A., Zanetti A., Corada M., Rival Y., Ruco L., Lampugnani M.G., Dejana E. Polymorphonuclear leukocyte adhesion triggers the disorganization of endothelial cell-to-cell adherens junctions. J. Cell Biol. 135:1996;497-510.
27. Dormond O., Bezzi M., Mariotti A., Ruegg C. Prostaglandin E2 promotes integrin aVb3-dependent endothelial cell adhesion, Rac-activation and spreading through cAMP/PKA signaling. J. Biol. Chem. 16:2002;16.
28. Draijer R., Atsma D.E., van der Laarse A., van Hinsbergh V.W. cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Regulation via different pathways in human aortic and umbilical vein endothelial cells. Circ. Res. 76:1995;199-208.
29. Drenckhahn D., Ness W. The endothelial contractile cytoskeleton. Born G.V.R., Schwartz C.J. Vascular Endothelium. Physiology, Pathology and Therapeutic Opportunities. 1997;1-27 Schattauer, Stuttgart, Germany.
30. Essler M., Hermann K., Amano M., Kaibuchi K., Heesemann J., Weber P.C., Aepfelbacher M. Pasteurella multocida toxin increases endothelial permeability via Rho kinase and myosin light chain phosphatase. J. Immunol. 161:1998;5640-5646.
31. Essler M., Retzer M., Bauer M., Heemskerk J.W., Aepfelbacher M., Siess W. 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. 274:1999;30361-30364.
32. Essler M., Staddon J.M., Weber P.C., Aepfelbacher M. Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of Rho/Rho kinase signaling. J. Immunol. 164:2000;6543-6549.
33. Etienne-Manneville S., Manneville J.B., Adamson P., Wilbourn B., Greenwood J., Couraud P.O. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J. Immunol. 165:2000;3375-3383.
34. Eto M., Barandier C., Rathgeb L., Kozai T., Joch H., Yang Z., Luscher T.F. 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. 89:2001;583-590.
35. Feig L.A., Schaffhausen B. Signal transduction. The hunt for Ras targets. Nature. 370:1994;508-509.
36. Fleming I.N., Elliott C.M., Exton J.H. Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor. J. Biol. Chem. 271:1996;33067-33073.
37. Garcia J.G., Verin A.D., Herenyiova M., English D. Adherent neutrophils activate endothelial myosin light chain kinase: role in transendothelial migration. J. Appl. Physiol. 84:1998;1817-1821.
38. Garcia J.G., Liu F., Verin A.D., Birukova A., Dechert M.A., Gerthoffer W.T., Bamberg J.R., English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108:2001;689-701.
39. Gewaltig M.T., Kojda G. Vasoprotection by nitric oxide, mechanisms and therapeutic potential. Cardiovasc. Res. 55:2002;250-260.
40. Ghabriel M.N., Lu M.X., Leigh C., Cheung W.C., Allt G. 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.). 97:1999;297-305.
41. Gingras D., Lamy S., Beliveau R. Tyrosine phosphorylation of the vascular endothelial-growth-factor receptor-2 (VEGFR-2) is modulated by Rho proteins. Biochem. J. 348(Pt 2):2000;273-280.
42. Goeckeler Z.M., Wysolmerski R.B. Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation. J. Cell. Biol. 130:1995;613-627.
43. Goeckeler Z.M., Masaracchia R.A., Zeng Q., Chew T.L., Gallagher P., Wysolmerski R.B. Phosphorylation of myosin light chain kinase by p21-activated kinase PAK2. J. Biol. Chem. 275:2000;18366-18374.
44. Gopalakrishnan S., Dunn K.W., Marrs J.A. Rac1, but not RhoA, signaling protects epithelial adherens junction assembly during ATP depletion. Am. J. Physiol., Cell Physiol. 283:2002;C261-C272.
45. Haddad E., Zugaza J.L., Louache F., Debili N., Crouin C., Schwarz K., Fischer A., Vainchenker W., Bertoglio J. The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis. Blood. 97:2001;33-38.
46. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
47. Hart M.J., Jiang X., Kozasa T., Roscoe W., Singer W.D., Gilman A.G., Sternweis P.C., Bollag G. Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by Galpha13. Science. 280:1998;2112-2114.
48. Hippenstiel S., Tannert-Otto S., Vollrath N., Krull M., Just I., Aktories K., von Eichel-Streiber C., Suttorp N. Glucosylation of small GTP-binding Rho proteins disrupts endothelial barrier function. Am. J. Physiol. 272:1997;L38-L43.
49. Hirao M., Sato N., Kondo T., Yonemura S., Monden M., Sasaki T., Takai Y., Tsukita S. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signaling pathway. J. Cell Biol. 135:1996;37-51.
50. Hirase T., Kawashima S., Wong E.Y., Ueyama T., Rikitake Y., Tsukita S., Yokoyama M., Staddon J.M. Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms. J. Biol. Chem. 276:2001;10423-10431.
51. Hirata A., Baluk P., Fujiwara T., McDonald D.M. Location of focal silver staining at endothelial gaps in inflamed venules examined by scanning electron microscopy. Am. J. Physiol. 269:1995;L403-L418.
52. Hordijk P.L., Anthony E., Mul F.P., Rientsma R., Oomen L.C., Roos D. Vascular-endothelial-cadherin modulates endothelial monolayer permeability. J. Cell. Sci. 112:1999;1915-1923.
53. Ikenoya M., Hidaka H., Hosoya T., Suzuki M., Yamamoto N., Sasaki Y. 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. 81:2002;9-16.
54. Ishizaki T., Uehata M., Tamechika I., Keel J., Nonomura K., Maekawa M., Narumiya S. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol. Pharmacol. 5:2000;976-983.
55. Just I., Selzer J., von Eichel-Streiber C., Aktories K. The low molecular mass GTP-binding protein Rho is affected by toxin A from Clostridium difficile. J. Clin. Invest. 95:1995;1026-1031.
56. Katso R., Okkenhaug K., Ahmadi K., White S., Timms J., Waterfield M.D. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 17:2001;615-675.
57. Kawano Y., Fukata Y., Oshiro N., Amano M., Nakamura T., Ito M., Matsumura F., Inagaki M., Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147:1999;1023-1038.
58. Kolodney M.S., Wysolmerski R.B. Isometric contraction by fibroblasts and endothelial cells in tissue culture: a quantitative study. J. Cell Biol. 117:1992;73-82.
59. Kovacs E.M., Ali R.G., McCormack A.J., Yap A.S. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J. Biol. Chem. 277:2002;6708-6718.
60. Kozasa T., Jiang X., Hart M.J., Sternweis P.M., Singer W.D., Gilman A.G., Bollag G., Sternweis P.C. p115 RhoGEF, a GTPase activating protein for Galpha12 and Galpha13. Science. 280:1998;2109-2111.
61. Kraynov V.S., Chamberlain C., Bokoch G.M., Schwartz M.A., Slabaugh S., Hahn K.M. Localized Rac activation dynamics visualized in living cells. Science. 290:2000;333-337.
62. Kuroda S., Fukata M., Kobayashi K., Nakafuku M., Nomura N., Iwamatsu A., Kaibuchi K. Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J. Biol. Chem. 271:1996;23363-23367.
63. Lampugnani M.G., Zanetti A., Breviario F., Balconi G., Orsenigo F., Corada M., Spagnuolo R., Betson M., Braga V., Dejana E. VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of tiam. Mol. Biol. Cell. 13:2002;1175-1189.
64. Lang P., Gesbert F., Delespine-Carmagnat M., Stancou R., Pouchelet M., Bertoglio J. Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J. 15:1996;510-519.
65. Langeler E.G., van Hinsbergh V.W. Norepinephrine and iloprost improve barrier function of human endothelial cell monolayers: role of cAMP. Am. J. Physiol. 260:1991;C1052-C1059.
66. Laufs U., Endres M., Stagliano N., Amin-Hanjani S., Chui D.S., Yang S.X., Simoncini T., Yamada M., Rabkin E., Allen P.G., Huang P.L., Bohm M., Schoen F.J., Moskowitz M.A., Liao J.K. Neuroprotection mediated by changes in the endothelial actin cytoskeleton. J. Clin. Invest. 106:2000;15-24.
67. Lee O.H., Lee D.J., Kim Y.M., Kim Y.S., Kwon H.J., Kim K.W., Kwon Y.G. 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. 268:2000;47-53.
68. Levin E.R. Endothelins. N. Engl. J. Med. 333:1995;356-363.
69. Lin R., Cerione R.A., Manor D. Specific contributions of the small GTPases Rho, Rac, and Cdc42 to Dbl transformation. J. Biol. Chem. 274:1999;23633-23641.
70. Liu F., Schaphorst K.L., Verin A.D., Jacobs K., Birukova A., Day R.M., Bogatcheva N., Bottaro D.P., Garcia J.G. Hepatocyte growth factor enhances endothelial cell barrier function and cortical cytoskeletal rearrangement: potential role of glycogen synthase kinase-3beta. FASEB J. 16:2002;950-962.
71. Lum H., Malik A.B. Regulation of vascular endothelial barrier function. Am. J. Physiol. 267:1994;L223-L241.
72. Lynch J.J., Ferro T.J., Blumenstock F.A., Brockenauer A.M., Malik A.B. Increased endothelial albumin permeability mediated by protein kinase C activation. J. Clin. Invest. 85:1990;1991-1998.
73. Mehta D., Rahman A., Malik A.B. Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 276:2001;22614-22620.
74. Miao L., Dai Y., Zhang J. Mechanism of RhoA/Rho kinase activation in endothelin-1-induced contraction in rabbit basilar artery. Am. J. Physiol, Heart Circ. Physiol. 283:2002;H983-H989.
75. Michel C.C., Curry F.E. Microvascular permeability. Physiol. Rev. 79:1999;703-761.
76. Minnear F.L., Sandeep P., Bell D., Gainor J.P., Morton C.A. Platelet lipid(s) bound to albumin increases endothelial electrical resistance: mimicked by LPA. Am. J. Physiol., Lung Cell. Mol. Physiol. 281:2001;L1334-L1337.
77. Mitani K., Kubo S. Adenovirus as an integrating vector. Curr. Gene Ther. 2:2002;135-144.
78. Moy A.B., Van Engelenhoven J., Bodmer J., Kamath J., Keese C., Giaever I., Shasby S., Shasby D.M. Histamine and thrombin modulate endothelial focal adhesion through centripetal and centrifugal forces. J. Clin. Invest. 97:1996;1020-1027.
79. Nakasone T., Hanashiro K., Nakamura M., Sunakawa H., Kosugi T. Mast cell-derived VEGF enhances the passage of IgE FE-3 through the rat aortic endothelial cell monolayer. Int. Arch. Allergy Immunol. 129:2002;76-85.
80. Nobes C.D., Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23:1995;456-459.
81. Noren N.K., Niessen C.M., Gumbiner B.M., Burridge K. Cadherin engagement regulates Rho family GTPases. J. Biol. Chem. 276:2001;33305-33308.
82. Panetti T.S. Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim. Biophys. Acta. 1582:2002;190-196.
83. Park H.J., Kong D., Iruela-Arispe L., Begley U., Tang D., Galper J.B. 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA. Circ. Res. 91:2002;143-150.
84. Petrache I., Verin A.D., Crow M.T., Birukova A., Liu F., Garcia J.G. Differential effect of MLC kinase in TNF-alpha-induced endothelial cell apoptosis and barrier dysfunction. Am. J. Physiol., Lung Cell. Mol. Physiol. 280:2001;L1168-L1178.
85. Rabiet M.J., Plantier J.L., Rival Y., Genoux Y., Lampugnani M.G., Dejana E. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler. Thromb. Vasc. Biol. 16:1996;488-496.
86. Ren X.D., Schwartz M.A. Determination of GTP loading on Rho. Methods Enzymol. 325:2000;264-272.
87. Ridley A.J. Rho. Hall A. GTPases. Hames B.D., Glover D.M. Frontiers in Molecular Biology. 2000;89-119 Oxford Univ. Press, Oxford, UK.
88. Ridley A.J. Rho family proteins: coordinating cell responses. Trends Cell Biol. 11:2001;471-477.
89. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:1992;389-399.
90. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
91. Rottner K., Hall A., Small J.V. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr. Biol. 17:1999;640-648.
92. Sah V.P., Seasholtz T.M., Sagi S.A., Brown J.H. The role of Rho in G protein-coupled receptor signal transduction. Annu. Rev. Pharmacol. Toxicol. 40:2000;459-489.
93. Sahai E., Ishizaki T., Narumiya S., Treisman R. Transformation mediated by RhoA requires activity of ROCK kinases. Curr. Biol. 9:1999;136-145.
94. Sahai E., Olson M.F., Marshall C.J. Cross-talk between Ras and Rho signaling pathways in transformation favours proliferation and increased motility. EMBO J. 20:2001;755-766.
95. Saito H., Minamiya Y., Kitamura M., Saito S., Enomoto K., Terada K., Ogawa J. Endothelial myosin light chain kinase regulates neutrophil migration across human umbilical vein endothelial cell monolayer. J. Immunol. 161:1998;1533-1540.
96. Sander E.E., ten Klooster J.P., van Delft S., van der Kammen R.A., Collard J.G. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J. Cell Biol. 147:1999;1009-1022.
97. 2+ sensitization of contraction in vascular smooth muscle. J. Biol. Chem. 275:2000;21722-21729.
98. Schneeberger E.E., Lynch R.D. Structure, function, and regulation of cellular tight junctions. Am. J. Physiol. 262:1992;L647-L661.
99. Schraufstatter I.U., Trieu K., Sikora L., Sriramarao P., DiScipio R. Complement c3a and c5a induce different signal transduction cascades in endothelial cells. J. Immunol. 169:2002;2102-2110.
100. Shaw R.J., Henry M., Solomon F., Jacks T. RhoA-dependent phosphorylation and relocalization of ERM proteins into apical membrane/actin protrusions in fibroblasts. Mol. Biol. Cell. 9:1998;403-419.
101. Simonson M.S. Endothelins: multifunctional renal peptides. Physiol. Rev. 73:1993;375-411.
102. Soga N., Namba N., McAllister S., Cornelius L., Teitelbaum S.L., Dowdy S.F., Kawamura J., Hruska K.A. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp. Cell Res. 269:2001;73-87.
103. Sokol S.Y., Li Z., Sacks D.B. The effect of IQGAP1 on Xenopus embryonic ectoderm requires Cdc42. J. Biol. Chem. 276:2001;48425-48430.
104. Spyridopoulos I., Luedemann C., Chen D., Kearney M., Murohara T., Principe N., Isner J.M., Losordo D.W. 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. 22:2002;901-906.
105. Stasek J.E. Jr., Garcia J.G. The role of protein kinase C in alpha-thrombin-mediated endothelial cell activation. Semin. Thromb. Hemost. 18:1992;117-125.
106. Suttorp N., Weber U., Welsch T., Schudt C. Role of phosphodiesterases in the regulation of endothelial permeability in vitro. J. Clin. Invest. 91:1993;1421-1428.
107. Takahashi K., Sasaki T., Mammoto A., Takaishi K., Kameyama T., Tsukita S., Takai Y. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J. Biol. Chem. 272:1997;23371-23375.
108. Takemoto M., Sun J., Hiroki J., Shimokawa H., Liao J.K. Rho-kinase mediates hypoxia-induced downregulation of endothelial nitric oxide synthase. Circulation. 106:2002;57-62.
109. Taylor J.M., Macklem M.M., Parsons J.T. Cytoskeletal changes induced by GRAF, the GTPase regulator associated with focal adhesion kinase, are mediated by Rho. J. Cell Sci. 112:1999;231-242.
110. Thompson P.W., Randi A.M., Ridley A.J. Intercellular adhesion molecule (ICAM)-1, but not ICAM-2, activates RhoA and stimulates c-fos and rhoA transcription in endothelial cells. J. Immunol. 169:2002;1007-1013.
111. Tinsley J.H., Wu M.H., Ma W., Taulman A.C., Yuan S.Y. Activated neutrophils induce hyperpermeability and phosphorylation of adherens junction proteins in coronary venular endothelial cells. J. Biol. Chem. 274:1999;24930-24934.
112. Tokuyama K., Nishimura H., Iizuka K., Kato M., Arakawa H., Saga R., Mochizuki H., Morikawa A. 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. 64:2002;189-195.
113. Tseng Y.L., Liu J.J., Hong R.L. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol. Pharmacol. 62:2002;864-872.
114. Tsuji T., Ishizaki T., Okamoto M., Higashida C., Kimura K., Furuiashiki T., Arakawa Y., Birge R.B., Nakamoto T., Hirai H., Narumiya S. ROCK and mDia1 antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts. J. Cell Biol. 157:2002;819-830.
115. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 389:1997;990-994.
116. Vallota E.H., Muller-Eberhard H.J. Formation of C3a and C5a anaphylatoxins in whole human serum after inhibition of the anaphylatoxin inactivator. J. Exp. Med. 137:1973;1109-1123.
117. Van Aelst L., D’Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev. 11:1997;2295-2322.
118. van Buul J.D., Voermans C., van den Berg V., Anthony E.C., Mul F.P., van Wetering S., van der Schoot C.E., Hordijk P.L. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J. Immunol. 168:2002;588-596.
119. van Hinsbergh V.W., van Amerongen G.P. Intracellular signalling involved in modulating human endothelial barrier function. J. Anat. 200:2002;549-560.
120. van Leeuwen F.N., van Delft S., Kain H.E., van der Kammen R.A., Collard J.G. Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading. Nat. Cell Biol. 1:1999;242-248.
121. van Nieuw Amerongen G.P., van Hinsbergh V.W. Cytoskeletal effects of rho-like small guanine nucleotide-binding proteins in the vascular system. Arterioscler. Thromb. Vasc. Biol. 21:2001;300-311.
122. van Nieuw Amerongen G.P., Draijer R., Vermeer M.A., van Hinsbergh V.W. Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ. Res. 83:1998;1115-1123.
123. van Nieuw Amerongen G.P., van Delft S., Vermeer M.A., Collard J.G., van Hinsbergh V.W. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ. Res. 87:2000;335-340.
124. van Nieuw Amerongen G.P., Vermeer M.A., Negre-Aminou P., Lankelma J., Emeis J.J., van Hinsbergh V.W. Simvastatin improves disturbed endothelial barrier function. Circulation. 102:2000;2803-2809.
125. van Nieuw Amerongen G.P., Vermeer M.A., van Hinsbergh V.W. Role of RhoA and Rho kinase in lysophosphatidic acid-induced endothelial barrier dysfunction. Arterioscler. Thromb. Vasc. Biol. 20:2000;E127-E133.
126. van Wetering S., van Buul J.D., Quik S., Mul F.P., Anthony E.C., ten Klooster J.P., Collard J.G., Hordijk P.L. Reactive oxygen species mediate Rac-induced loss of cell-cell adhesion in primary human endothelial cells. J. Cell Sci. 115:2002;1837-1846.
127. Vastrik I., Eicholt B.J., Walsh F.S., Ridley A., Doherty P. Sema3A-induced growth-cone collapse is mediated by rac1 amino acids 17-32. Curr. Biol. 18:1999;991-998.
128. Von Pawel-Rammingen U., Telepnev M.V., Schmidt G., Aktories K., Wolf-Watz H., Rosqvist R. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36:2000;737-748.
129. Vouret-Craviari V., Boquet P., Pouyssegur 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. 9:1998;2639-2653.
130. Vouret-Craviari V., Grall D., Flatau G., Pouyssegur J., Boquet P., Van Obberghen-Schilling E. Effects of cytotoxic necrotizing factor 1 and lethal toxin on actin cytoskeleton and VE-cadherin localization in human endothelial cell monolayers. Infect. Immun. 67:1999;3002-3008.
131. Vouret-Craviari V., Bourcier C., Boulter E., Van Obberghen-Schilling E. Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J. Cell. Sci. 115:2002;2475-2484.
132. Wang P., Verin A.D., Birukova A., Gilbert-McClain L.I., Jacobs K., Garcia J.G. Mechanisms of sodium fluoride-induced endothelial cell barrier dysfunction: role of MLC phosphorylation. Am. J. Physiol., Lung Cell. Mol. Physiol. 281:2001;L1472-L1483.
133. Wojciak-Stothard B., Entwistle A., Garg R., Ridley A.J. 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. 176:1998;150-165.
134. Wojciak-Stothard B., Williams L., Ridley A.J. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J. Cell Biol. 145:1999;1293-1307.
135. Wojciak-Stothard B., Potempa S., Eichholtz T., Ridley A.J. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J. Cell. Sci. 114:2001;1343-1355.
136. Zhao D., Kuhnt-Moore S., Zeng H., Pan A., Wu J.S., Simeonidis S., Moyer M.P., Pothoulakis C. Substance P-stimulated interleukin-8 expression in human colonic epithelial cells involves Rho family small GTPases. Biochem. J. 368:2002;665-672.
137. Zondag G.C., Evers E.E., ten Klooster J.P., Janssen L., van der Kammen R.A., Collard J.G. Oncogenic Ras downregulates Rac activity which leads to increased Rho activity and epithelial-mesenchymal transition. J. Cell Biol. 149:2000;775-782.
138. Zumbihl R., Aepfelbacher M., Andor A., Jacobi C.A., Ruckdeschel K., Rouot B., Heesemann J. The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274:1999;29289-29293.