Differential actions of PAR2 and PAR1, in stimulating human endothelial cell exocytosis and permeability: The role of Rho-GTPases

Circulation Research

Volumn 92, Issue 3, 2003, Pages 272-278

  Klarenbach, Scott W ^a   Chipiuk, Adam ^a   Nelson, Randy C ^a   Hollenberg, Morley D ^b   Murray, Allan G ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Reperfusion injury; Thrombin receptors Rho GTP binding proteins; Vascular endothelium

Indexed keywords

CLOSTRIDIUM DIFFICILE TOXIN B; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; G PROTEIN COUPLED RECEPTOR; GUANOSINE TRIPHOSPHATASE; JASPAMIDE; PEROXIDASE; PROTEIN CDC42; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; RAC PROTEIN; RHO FACTOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; VON WILLEBRAND FACTOR; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; BACTERIAL PROTEIN; BACTERIAL TOXIN; CALCIUM; CHELATING AGENT; CYCLOPEPTIDE; DEPSIPEPTIDE; DRUG DERIVATIVE; EGTAZIC ACID; NUCLEIC ACID SYNTHESIS INHIBITOR; PEPTIDE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN RECEPTOR; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STIMULATION; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXOCYTOSIS; HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RECEPTOR INTRINSIC ACTIVITY; RECEPTOR UPREGULATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; UMBILICAL VEIN; ARTIFICIAL MEMBRANE; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; METABOLISM; PERMEABILITY; PHYSIOLOGY; SECRETION; VASCULAR ENDOTHELIUM; WEIBEL PALADE BODY;

BACTERIAL PROTEINS; BACTERIAL TOXINS; CALCIUM; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; CHELATING AGENTS; CYTOSKELETON; DEPSIPEPTIDES; EGTAZIC ACID; ENDOTHELIUM, VASCULAR; EXOCYTOSIS; HUMANS; MEMBRANES, ARTIFICIAL; NUCLEIC ACID SYNTHESIS INHIBITORS; PEPTIDES; PEPTIDES, CYCLIC; PERMEABILITY; RECEPTOR, PAR-1; RECEPTOR, PAR-2; RECEPTORS, THROMBIN; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; VON WILLEBRAND FACTOR; WEIBEL-PALADE BODIES;

EID: 0037458275     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000057386.15390.A3     Document Type: Article

References (43)

1. Golino P, Ragni M, Cirillo P, Avvedimento VE, Feliciello A, Esposito N, Scognamiglio A, Trimarco B, Iaccarino G, Condorelli M, Chiariello M, Ambrosio G. Effects of tissue factor induced by oxygen free radicals on coronary flow during reperfusion. Nat Med. 1996;2:35-40.
2. Erlich JH, Boyle EM, Labriola J, Kovacich JC, Santucci RA, Fearns C, Morgan EN, Yun W, Luther T, Kojikawa O, Martin TR, Pohlman TH, Verrier ED, Mackman N. Inhibition of the tissue factor-thrombin pathway limits infarct size after myocardial ischemia-reperfusion injury by reducing inflammation. Am J Pathol. 2000:157:1849-1862.
3. Ejiri S, Eguchi Y, Kishida A, Ishigami F, Kurumi Y, Tani T, Kodama M. Cellular distribution of thrombomodulin as an early marker for warm ischemic liver injury in porcine liver transplantation: protective effect of prostaglandin 12 analogue and tauroursodeoxycholic acid. Transplantation. 2001;71:721-726.
4. Palazzo AJ, Jones SP, Girod WG, Anderson DC, Granger DN, Lefer DJ. Myocardial ischemia-reperfusion injury in CD18- and ICAM-1 -deficient mice. Am J Physiol. 1998;275:H2300-H2307.
5. Yadav SS, Howell DN, Steeber DA, Harland RC, Tedder TF, Clavien PA. P-Selectin mediates reperfusion injury through neutrophil and platelet sequestration in the warm ischemic mouse liver. Hepatology. 1999;29:1494-1502.
6. Singbartl K, Green SA, Ley K. Blocking P-selectin protects from ischemia/reperfusion-induced acute renal failure. FASEB J. 2000;14:48-54.
7. MacFarlane SR, Seatter MJ, Kanke T, Hunter GD. Plevin R. Proteinase-activated receptors. Pharmacol Rev. 2001;53:245-282.
8. Mirza H, Yatsula V, Bahou WF. The proteinase activated receptor-2 (PAR-2) mediates mitogenic responses in human vascular endothelial cells. J Clin Invest. 1996;97:1705-1714.
9. Hamilton JR, Frauman AG, Cocks TM. Increased expression of protease-activated receptor-2 (PAR2) and PAR4 in human coronary artery by inflammatory stimuli unveils endothelium-dependent relaxations to PAR2 and PAR4 agonists. Circ Res. 2001;89:92-98.
10. Fox MT, Harriott P, Walker B, Stone SR. Identification of potential activators of proteinase-activated receptor-2. FEBS Lett. 1997:417:267-269.
11. Riewald M, Ruf W. Mechanistic coupling of protease signaling and initiation of coagulation by tissue factor. Proc Natl Acad Sci U S A. 2001;98:7742-7747.
12. Robinson SD, Frenette PS, Rayburn H, Cummiskey M, Ullman-Cullere MD, Wagner DD, Hynes RO. Multiple, targeted deficiencies in selectins reveal a predominant role for P-selectin in leukocyte recruitment. Proc Natl Acad Sci U S A. 1999;96:11452-11457.
13. Hattori R, Hamilton KK, Fugate RD, McEver RP, Sims PJ. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140. J Biol Chem. 1989;264:7768-7771.
14. Wolff B, Burns AR, Middleton J, Rot A. Endothelial cell "memory" of inflammatory stimulation: human venular endothelial cells store interleukin 8 in Weibel-Palade bodies. J Exp Med. 1998;188:1757-1762.
15. Cirino G, Cicala C, Bucci MR, Sorrentino L, Maraganore JM, Stone SR. Thrombin functions as an inflammatory mediator through activation of its receptor. J Exp Med. 1996;183:821-827.
16. van Nieuw Amerongen GP, van Delft S, Vermeer MA, Collard JG, van Hinsbergh VW. Activation of RhoA by thrombin in endothelial hyper-permeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 2000;87:335-340.
17. Vergnolle N, Hollenberg MD, Sharkey KA. Wallace JL. Characterization of the inflammatory response to proteinase-activated receptor-2 (PAR2)-activating peptides in the rat paw. Br J Pharmacol. 1999;127:1083-1090.
18. Lindner JR, Kahn ML, Coughlan SR, Sambrano GR, Schauble E. Bernstein D, Foy D, Hafezi-Moghadam A, Ley K. Delayed onset of inflammation in protease-activated receptor-2- deficient mice. J Immunol. 2000;165:6505-6510.
19. Storck J, Kusters B, Vahland M, Morys-Wortmann C, Zimmermann ER. Trypsin induced von Willebrand factor release from human endothelial cells in mediated by PAR-2 activation. Thromb Res. 1996;84:463-473.
20. Compton SJ, Cairns JA, Holgate ST, Walls AF. Human mast cell tryptase stimulates the release of an IL-8-dependent neutrophil chemotactic activity from human umbilical vein endothelial cells (HUVEC). Clin Exp Immunol. 2000;121:31-36.
21. Lafleur MA, Hollenberg MD, Atkinson SJ, Knauper V, Murphy G, Edwards DR. Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membrane-type-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63 kDa active species. Biochem J. 2001;357:107-115.
22. Kawabata A, Saifeddine M, Al-Ani B, Leblond L, Hollenberg MD. Evaluation of proteinase-activated receptor-1 (PAR1 ) agonists and antagonists using a cultured cell receptor desensitization assay: activation of PAR2 by PAR1-targeted ligands. J Pharmacol Exp Ther. 1999;288:358-370.
23. Gimbrone MA. Culture of vascular endothelium. Prog Hemost Thromb. 1976;3:1-28.
24. 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.
25. Murray AG, Khodadoust MM, Pober JS, Bothwell AL. Porcine aortic endothelial cells activate human T cells: direct presentation of MHC antigens and costimulation by ligands for human CD2 and CD28. Immunity. 1994;1:57-63.
26. Ren XD, Kiosses WB, Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 1999;18:578-85.
27. Copper JA. Effects of cytochalasin and phalloidin on actin. J Cell Biol. 1987:105:1473-1478.
28. Bubb MR, Senderowicz AM. Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem. 1994;269:14869-14871.
29. Birch KA, Pober JS, Zavoico GB, Means AR, Ewenstein BM. Calcium/calmodulin transduces thrombin-stimulated secretion. J Cell Biol. 1992;118:1501-1510.
30. Draijer R, Atsma DE, Van der Laarse A, van Hinsbergh VW. cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Circ Res. 1995;76:199-208.
31. 2+ entry: evidence for a secretion-like coupling model. Cell. 1999;98:487-499.
32. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley A. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci. 2001:114:1343-1355.
33. Norman JC, Price LS, Ridley AJ, Koffer A. The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol Biol Cell. 1996;7:1429-1442.
34. Kowluru A, Li G, Rabaglia ME, Segu VB, Hofmann F, Aktories K, Metz SA. Evidence for differential roles of the Rho subfamily of GTP-binding proteins in glucose- and calcium-induced insulin secretion from pancreatic beta cells. Biochem Pharmacol. 1997;54:1097-1108.
35. Vergnolle N, Macnaughton WK, Al-Ani B, Saifeddine M, Wallace JL, Hollenberg MD. Proteinase-activated receptor 2 (PAR2)-activating peptides: identification of a receptor distinct from PAR2 that regulates intestinal transport. Proc Natl Acad Sci U S A. 1998;95:7766-7771.
36. Nakata T, Hirokawa N. Organization of cortical cytoskeleton of cultured chromaffin cells and involvement in secretion as revealed by quick-freeze, deep-etching, and double-label immunoelectron microscopy. J Neurosci. 1992;12:2186-2197.
37. Muallem S, Kwiatkowska K, Xu X, Yin HL. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol. 1995;128:589-598.
38. Sullivan R. Price LS, Koffer A. Rho controls cortical F-actin disassembly in addition to, but independently of, secretion in mast cells. J Biol Chem. 1999;274:38140-38146.
39. Trifaro J, Rose SD, Lejen T, Elzagallaai A. Two pathways control chromaffin cell cortical F-actin dynamics during exocytosis. Biochimie. 2000;82:339-352.
40. Hall A. Rho GTPases and the actin cytoskeleton. Cell. 1998;279:509-514.
41. Prepens U, Just I, von Eichel-Streiber C, Aktories K. Inhibition of Fc epsilon-RI-mediated activation of rat basophilic leukemia cells by Clostridium difficile toxin B (monoglucosyltransferase). J Biol Chem. 1996;271:7324-7329.
42. Djouder N, Prepens U, Aktories K, Cavalie A. Inhibition of calcium release-activated calcium current by Rac/Cdc42-inactivating clostridial cytotoxins in RBL cells. J Biol Chem. 2000;275:18732-18738.
43. Vischer UM, Barth H, Wollheim CB. Regulated von Willebrand factor secretion is associated with agonist-specific patterns of cytoskeletal remodeling in cultured endothelial cells. Arterioscler Thromb Vasc Biol. 2000;20:883-891.