Caveolae are required for protease-selective signaling by protease-activated receptor-1

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 15, 2009, Pages 6393-6397

  Russo, Angela ^a   Soh, Unice J K ^b   Paing, May M ^a   Arora, Puneeta ^a   Trejo, JoAnn ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

APC; Endothelial; GPCR; Rac1; Thrombin

Indexed keywords

ACTIVATED PROTEIN C; CAVEOLIN 1; GUANOSINE TRIPHOSPHATASE; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR 1; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; PROTEIN C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CAVEOLA; CELL COMPARTMENTALIZATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; CELL CULTURE; ENZYME ACTIVATION; ENZYME SPECIFICITY; GENETICS; METABOLISM; PHOSPHORYLATION;

CAVEOLAE; CELLS, CULTURED; ENZYME ACTIVATION; HUMANS; PHOSPHORYLATION; PROTEIN C; RAC1 GTP-BINDING PROTEIN; RECEPTOR, PAR-1; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; THROMBIN;

EID: 65549087489     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0810687106     Document Type: Article

References (32)

1. Coughlin SR (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost 3:1800-1814.
2. Komarova YA, Mehta D, Malik AB (2007) Dual regulation of endothelial junctional permeability. Sci STKE 2007:re8.
3. Vu TK, Hung DT, Wheaton VI, Coughlin SR (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64:1057-1068.
4. McLaughlin JN, Shen L, Holinstat M, Brooks JD, DiBenedetto E (2005) Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 280:25048-25059.
5. Urban JD, Clarke WP, von Zastrow M, Nichols DE, Kobilka B (2007) Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320:1-13.
6. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF (2001) Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344:699-709.
7. Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT (1996) The endo-thelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci USA 93:10212-10216.
8. Mosnier LO, Griffin JH (2003) Inhibition of staurosporine-induced apoptosis of endo-thelial cells by activated protein C requires protease-activated receptor-1 and endo-thelial cell protein C receptor. Biochem J 373:65-70.
9. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W (2002) Activation of endothelial cell protease activated receptor-1 by the protein C pathway. Science 296:1880-1882.
10. Feistritzer C, Riewald M (2005) Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine-1-phosphate receptor-1 crossactivation. Blood 105:3178-3184.
11. Finigan JH, Dudek SM, Singleton PA, Chiang ET, Jacobson JR (2005) Activated protein C mediates novel lung endothelial barrier enhancement. J Biol Chem 280:17286-17293.
12. Feistritzer C, Schuepbach RA, Mosnier LO, Bush LA, Di Cera E (2006) Protective signaling by activated protein C is mechanistically linked to protein C activation on endothelial cells. J Biol Chem 281:20077-20084.
13. Taylor FB, Stearns-Kurosawa DJ, Kurosawa S, Ferrell GL, Chang AC (2000) The endo-thelial cell protein C receptors aids in host defense against Escherichia coli sepsis. Blood 95:1680-1686.
14. Razani B, Engleman JA, Wang XB, Schubert W, Zhang XL (2001) Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276:38121-38138.
15. Bae J-S, Yang L, Manithody C, Rezaie AR (2007) The ligand occupancy of endothelial protein C receptor switches the protease-activated receptor-1-dependent signaling specificity of thrombin from a permeability-enhancing to a barrier-protective response in endothelial cells. Blood 110:3909-3916.
16. Bae JS, Yang L, Rezaie AR (2007) Receptors of the protein C activation and activated protein C signaling pathways are colocalized in lipid rafts of endothelial cells. Proc Natl Acad Sci USA 104:2867-2872.
17. Arora P, Cuevas B, Russo A, Johnson GL, Trejo J (2008) Persistent transactivation of EGFR and ErbB2/HER2 by protease-activated receptor-1 promotes breast carcinoma cell invasion. Oncogene 27:4434-4445.
18. Schuck S, Manninen A, Honsho M, Fullekrug J, Simons K (2004) Generation of single and double knockdowns in polarized epithelial cells by retrovirus-mediated RNA interference. Proc Natl Acad Sci USA 101:4912-4917.
19. Ishii K, Gerszten R, Zheng YW, Turck CW, Coughlin SR (1995) Determinants of thrombin receptor cleavage: Receptor domains involved, specificity, and role of the P3 aspartate. J Biol Chem 270:16435-16440.
20. Tiruppathi C, Yan W, Sandoval R, Naqvi T, Pronin AN (2000) G protein-coupled receptor kinase-5 regulates thrombin-activated signaling in endothelial cells. Proc Natl Acad Sci USA 97:7440-7445.
21. Trejo J, Coughlin SR (1999) The cytoplasmic tails of protease-activated receptor-1 and substance P receptor specify sorting to lysosomes versus recycling. J Biol Chem 274:2216-2224.
22. Trejo J, Hammes SR, Coughlin SR (1998) Termination of signaling by protease-activated receptor-1 is linked to lysosomal sorting. Proc Natl Acad Sci USA 95:13698-13702.
23. Schuepbach RA, Feistritzer C, Brass LF, Riewald M (2008) Activated protein C-cleaved protease activated receptor-1 is retained on the endothelial cell surface even in the presence of thrombin. Blood 111:2667-2673.
24. Awasthi V, Mandal SK, Papanna V, Rao LVM, Pendurthi UR (2008) Modulation of tissue factor-factor VIIa signaling by lipid rafts and caveolae. Arterioscler Thromb Vasc Biol 27:1447-1455.
25. Carlie-Klusacek ME, Rizzo V (2007) Endothelial cytoskeletal reorganization in response to PAR1 stimulation is mediated by membrane rafts but not caveolae. Am J Physiol Heart Circ Physiol 293:H366-H375.
26. Ludeman MJ, Kataoka H, Srinivasas Y, Esmon NL, Esmon CT (2005) PAR1 cleavage and signaling in response to activated protein C and thrombin. J BiolChem 280:13122-13128.
27. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270:15693-15701.
28. Bae JS, Yang L, Rezaie AR (2008) Lipid raft localization regulates the cleavage specificity of protease activated receptor-1 in endothelial cells. J Thomb Haemost 6:954-961.
29. Paing MM, Johnston CA, Siderovski DP, Trejo J (2006) Clathrin adaptor AP2 regulates thrombin receptor constitutive internalization and endothelial cell resensitization. Mol Cell Biol 28:3221-3242.
30. Edgell CJ, McDonald CC, Graham JB (1983) Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA 12:3734-3737.
31. Paing MM, Stutts AB, Kohout TA, Lefkowitz RJ, Trejo J (2002) β -Arrestins regulate protease-activated receptor-1 desensitization but not internalization or down-regulation. J Biol Chem 277:1292-1300.
32. Hung DT, Vu TK, Wheaton VI, Ishii K, Coughlin SR (1992) Cloned platelet thrombin receptor is necessary for thrombin-induced platelet activation. J Clin Invest 89:1350-1353.