GIT1 Mediates Thrombin Signaling in Endothelial Cells: Role in Turnover of RhoA-Type Focal Adhesions

Circulation Research

Volumn 94, Issue 8, 2004, Pages 1041-1049

  Van Nieuw Amerongen, Geerten P ^a,b   Natarajan, Kanchana ^a   Yin, Guoyong ^a   Hoefen, Ryan J ^a   Osawa, M ^a   Haendeler, Judith ^a   Ridley, A J ^d,e   Fujiwara, K ^a   Van Hinsbergh, Victor W M ^b,c   Berk, Bradford C ^a,f  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c TNO   (Netherlands)

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

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Contractility; Endothelium; Focal adhesion kinase; Thrombin

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ANTISENSE OLIGONUCLEOTIDE; FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR KINASE; G PROTEIN COUPLED RECEPTOR KINASE INTERACTING PROTEIN; GIT1 PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN TYROSINE KINASE; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; UNCLASSIFIED DRUG; VINCULIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SHAPE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPLETION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE; FOCAL ADHESION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MEMBRANE PERMEABILITY; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; UMBILICAL VEIN;

EID: 2342482455     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000125627.77235.0C     Document Type: Article

References (40)

1. Burridge K, Chrzanowska W-M. Focal adhesions, contractility, and signaling. Ann Rev Cell Dev Biol. 1996;12:463-518.
2. Katoh K, Kano Y, Amano M, Onishi H, Kaibuchi K, Fujiwara K. Rho-kinase-mediated contraction of isolated stress fibers. J Cell Biol. 2001;153:569-584.
3. Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K. Isolation and contraction of the stress fiber. Mol Biol Cell. 1998;9:1919-1938.
4. Goeckeler ZM, Wysolmerski RB. Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation. J Cell Biol. 1995;130:613-627.
5. Moy AB, Van Engelenhoven J, Bodmer J, Kamath J, Keese C, Giaever I, Shasby S, Shasby DM. Histamine and thrombin modulate endothelial focal adhesion through centripetal and centrifugal forces. J Clin Invest. 1996;97:1020-1027.
6. van Nieuw Amerongen GP, van Hinsbergh VW. Cytoskeletal effects of rho-like small guanine nucleotide-binding proteins in the vascular system. Arterioscler Thromb Vasc Biol. 2001;21:300-311.
7. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 2000;87:335-340.
8. 2+, and junctions in endothelial hyperpermeability. Circ Res. 2000;87:268-271.
9. Carbajal JM, Gratrix ML, Yu CH, Schaeffer RC, Jr. ROCK mediates thrombin's endothelial barrier dysfunction. Am J Physiol Cell Physiol. 2000;279:C195-C204.
10. van Nieuw Amerongen GP, Draijer R, Vermeer MA, van Hinsbergh VW. Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ Res. 1998;83:1115-1123.
11. Essler M, Amano M, Kruse HJ, Kaibuchi K, Weber PC, Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem. 1998;273:21867-21874.
12. Ridley AJ, Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992;70:389-399.
13. Flinn HM, Ridley AJ. Rho stimulates tyrosine phosphorylation of focal adhesion kinase, p130 and paxillin. J Cell Sci. 1996;109:1133-1141.
14. Chrzanowska WM, Burridge K. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J Cell Biol. 1996;133:1403-1415.
15. Needham LK, Rozengurt E. Gα12 and Gα13 stimulate Rho-dependent tyrosine phosphorylation of focal adhesion kinase, paxillin, and p130 Crk-associated substrate. J Biol Chem. 1998;273:14626-14632.
16. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD. FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol. 2000;2:249-256.
17. Ruest PJ, Roy S, Shi E, Mernaugh RL, Hanks SK. Phosphospecific antibodies reveal focal adhesion kinase activation loop phosphorylation in nascent and mature focal adhesions and requirement for the autophosphorylation site. Cell Growth Differ. 2000;11:41-48.
18. Ren XD, Kiosses WB, Sieg DJ, Otey CA, Schlaepfer DD, Schwartz MA. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J Cell Sci. 2000;113:3673-3678.
19. Zhao ZS, Manser E, Loo TH, Lim L. Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol Cell Biol. 2000;20:6354-6363.
20. Bagrodia S, Bailey D, Lenard Z, Hart M, Guan JL, Premont RT, Taylor SJ, Cerione RA. A tyrosine-phosphorylated protein that binds to an important regulatory region on the Cool family of p21-activated kinase-binding proteins. J Biol Chem. 1999;274:22393-22400.
21. Haendeler J, Yin G, Hojo Y, Saito Y, Melaragno M, Yan C, Sharma VK, Heller M, Aebersold R, Berk BC. GIT1 mediates Src-dependent activation of phospholipase Cγ by angiotensin II and epidermal growth factor. J Biol Chem. 2003;278:49936-49944.
22. van Nieuw Amerongen GP, Vermeer MA, Negre-Aminou P, Lankelma J, Emeis JJ, van Hinsbergh VW. Simvastatin improves disturbed endothelial barrier function. Circulation. 2000;102:2803-2809.
23. Mazald Y, Hashimoto S, Okawa K, Tsubouchi A, Nakamura K, Yagi R, Yano H, Kondo A, Iwamatsu A, Mizoguchi A, Sabe H. An ADP-ribosylation factor GTPase-activating protein Git2-short/KIAA0148 is involved in subcellular localization of paxillin and actin cytoskeletal organization. Mol Biol Cell. 2001;12:645-662.
24. Turner CE, Brown MC, Perrotta JA, Riedy MC, Nikolopoulos SN, McDonald AR, Bagrodia S, Thomas S, Leventhal PS. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J Cell Biol. 1999;145:851-863.
25. 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.
26. Schmitz U, Ishida M, Ishida T, Berk BC. Angiotensin II stimulates tyrosine phosphorylation of PLC-γ associated proteins: characterization of a c-Src-dependent 97 kD protein in vascular smooth muscle cells. Circ Res. 1997;81:550-557.
27. 2-mediated injury of human endothelial cells. J Biol Chem. 2000;275:37187-37193.
28. Igishi T, Gutkind JS. Tyrosine kinases of the Src family participate in signaling to MAP kinase from both Gq and Gi-coupled receptors. Biochem Biophys Res Commun. 1998;244:5-10.
29. Yan C, Takahashi M, Okuda M, Lee JD, Berk BC. Fluid shear stress stimulates big mitogen-activated protein kinase 1 (BMK1) activity in endothelial cells: dependence on tyrosine kinases and intracellular calcium. J Biol Chem. 1999;274:143-150.
30. Young MA, Gonfloni S, Superti-Furga G, Roux B, Kuriyan J. Dynamic coupling between the SH2 and SH3 domains of c-Src and Hck underlies their inactivation by C-terminal tyrosine phosphorylation. Cell. 2001;105:115-126.
31. Yin G, Haendeler J, Yan C, Berk BC. GIT1 functions as a scaffold for MEK1-extracellular signal-regulated kinase 1 and 2 activation by angiotensin II and epidermal growth factor. Mol Cell Biol. 2004;24:875-885.
32. Shikata Y, Birukov KG, Garcia JG. S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J Appl Physiol. 2003;94:1193-1203.
33. Shikata Y, Birukov KG, Birukova AA, Verin A, Garcia JG. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J. 2003;17:2240-2249.
34. Schaphorst KL, Pavalko FM, Patterson CE, Garcia JG. Thrombin-mediated focal adhesion plaque reorganization in endothelium: role of protein phosphorylation. Am J Respir Cell Mol Biol. 1997;17:443-455.
35. Mehta D, Tiruppathi C, Sandoval R, Minshall RD, Holinstat M, Malik AB. Modulatory role of focal adhesion kinase in regulating human pulmonary arterial endothelial barrier function. J Physiol. 2002;539:779-789.
36. Brown MC, Turner CE. Roles for the tubulin- and PTP-PEST-binding paxillin LIM domains in cell adhesion and motility. Int J Biochem Cell Biol. 2002;34:855-863.
37. Fincham VJ, Frame MC. The catalytic activity of Src is dispensable for translocation to focal adhesions but controls the turnover of these structures during cell motility. EMBO J. 1998;17:81-92.
38. van Nieuw Amerongen GP, Vermeer MA, van Hinsbergh VW. Role of RhoA and Rho kinase in lysophosphatidic acid-induced endothelial barrier dysfunction. Arterioscler Thromb Vasc Biol. 2000;20: E127-E133.
39. Geiger B, Bershadsky A. Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell. 2002;110:139-142.
40. Rodriguez-Fernandez JL. Why do so many stimuli induce tyrosine phosphorylation of FAK? Bioessays. 1999;21:1069-1075.