Protease-activated receptors 1 and 4 mediate thrombin signaling in endothelial cells

Blood

Volumn 102, Issue 9, 2003, Pages 3224-3231

  Kataoka, Hiroshi ^b   Hamilton, Justin R ^b   McKemy, David D ^b   Camerer, Eric ^b   Zheng, Yao Wu ^b   Cheng, Abby ^b   Griffin, Courtney ^b   Coughlin, Shaun R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; CALCIUM ION; MITOGEN ACTIVATED PROTEIN KINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIUM CELL; HEMOSTASIS; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL;

EID: 0142183468     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2003-04-1130     Document Type: Article

References (50)

1. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407:258-264.
2. Esmon CT. Role of coagulation inhibitors in inflammation. Thromb Haemost. 2001;86:51-56.
3. Griffin CT, Srinivasan Y, Zheng YW, Huang W, Coughlin SR. A role for thrombin receptor signaling in endothelial cells during embryonic development. Science. 2001;293:1666-1670.
4. 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.
5. Prescott SM, Zimmerman GA, McIntyre TM. Human endothelial cells in culture produce platelet-activating factor (1-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when stimulated with thrombin. Proc Natl Acad Sci U S A. 1984;81:3534-3538.
6. Lorant DE, Patel KD, McIntyre TM, McEver RP, Prescott SM, Zimmerman GA. Coexpression of GMP-140 and PAF by endothelium stimulated by histamine or thrombin: a juxtacrine system for adhesion and activation of neutrophils. J Cell Biol. 1991;115:223-234.
7. Colotta F, Sciacca FL, Sironi M, Luini W, Rabiet MJ, Mantovani A. Expression of monocyte chemotactic protein-1 by monocytes and endothelial cells exposed to thrombin. Am J Pathol. 1994; 144:975-985.
8. Ueno A, Murakami K, Yamanouchi K, Watanabe M, Kondo T. Thrombin stimulates production of interleukin-8 in human umbilical vein endothelial cells. Immunology. 1996;88:76-81.
9. Subramaniam M, Frenette PS, Saffaripour S, Johnson RC, Hynes RO, Wagner DD. Defects in hemostasis in P-selectin-deficient mice. Blood. 1996;87:1238-1242.
10. Frenette PS, Mayadas TN, Rayburn H, Hynes RO, Wagner DD. Susceptibility to infection and altered hematopoiesis in mice deficient in both P- and E-selectins. Cell. 1996;84:563-574.
11. Denis C, Methia N, Frenette PS, et al. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci U S A. 1998;95:9524-9529.
12. Ley K. Molecular mechanisms of leukocyte recruitment in the inflammatory process. Cardiovasc Res. 1996;32:733-742.
13. Lum H, Malik AB. Regulation of vascular endothelial barrier function. Am J Physiol. 1994;267: L223-241.
14. Rabiet MJ, Plantier JL, Rival Y, Genoux Y, Lampugnani MG, Dejana E. Thrombin-induced increase in endothelial permeability is associated with changes in cell-to-cell junction organization. Arterioscler Thromb Vasc Biol. 1996;16:488-496.
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. Vouret-Craviari V, Grall D, Flatau G, Pouysségur 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. 1999;67:3002-3008.
17. Daniel TO, Gibbs VC, Milfay DF, Garovoy MR, Williams LT. Thrombin stimulates c-sis gene expression in microvascular endothelial cells. J Biol Chem. 1986;261:9579-9582.
18. Papadimitriou E, Manolopoulos VG, Hayman GT, et al. Thrombin modulates vectorial secretion of extracellular matrix proteins in cultured endothelial cells. Am J Physiol. 1997;272:C1112-C1122.
19. Zucker S, Conner C, DiMassmo BI, et al. Thrombin induces the activation of progelatinase A in vascular endothelial cells: physiologic regulation of angiogenesis. J Biol Chem. 1995;270:23730-23738.
20. Tsopanoglou NE, Maragoudakis ME. On the mechanism of thrombin-induced angiogenesis: potentiation of vascular endothelial growth factor activity on endothelial cells by up-regulation of its receptors. J Biol Chem. 1999;274:23969-23976.
21. Nakanishi-Matsui M, Zheng YW, Sulciner DJ, Weiss EJ, Ludeman MJ, Coughlin SR. PAR3 is a cofactor for PAR4 activation by thrombin. Nature. 2000;404:609-613.
22. Sambrano GR, Coughlin SR. The carboxyl tail of protease-activated receptor-1 is required for chemotaxis: correlation of signal termination and directional migration. J Biol Chem. 1999;274: 20178-20184.
23. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 1991;64:1057-1068.
24. Coughlin SR. How the protease thrombin talks to cells. Proc Natl Acad Sci U S A. 1999;96:11023-11027.
25. Connolly AJ, Ishihara H, Kahn ML, Farese RV Jr, Coughlin SR. Role of the thrombin receptor in development and evidence for a second receptor. Nature. 1996;381:516-519.
26. Sambrano GR, Weiss EJ, Zheng YW, Huang W, Coughlin SR. Role of thrombin signalling in platelets in haemostasis and thrombosis. Nature. 2001;413:74-78.
27. Dong QG, Bernasconi S, Lostaglio S, et al. A general strategy for isolation of endothelial cells from murine tissues: characterization of two endothelial cell lines from the murine lung and subcutaneous sponge implants. Arterioscler Thromb Vasc Biol. 1997;17:1599-1604.
28. Schlaeger TM, Bartunkova S, Lawitts JA, et al. Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc Natl Acad Sci U S A. 1997;94: 3058-3063.
29. Ishii K, Hein L, Kobilka B, Coughlin SR. Kinetics of thrombin receptor cleavage on intact cells: relation to signaling. J Biol Chem. 1993;268:9780-9786.
30. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997;389:816-824.
31. Hamilton JR, Nguyen PB, Cocks TM. Atypical protease-activated receptor mediates endothelium-dependent relaxation of human coronary arteries. Circ Res. 1998;82:1306-1311.
32. 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.
33. Kahn ML, Zheng YW, Huang W, et al. A dual thrombin receptor system for platelet activation. Nature. 1998;394:690-694
34. Ngaiza JR, Jaffe EA. A 14 amino acid peptide derived from the amino terminus of the cleaved thrombin receptor elevates intracellular calcium and stimulates prostacyclin production in human endothelial cells. Biochem Biophys Res Commun. 1991;179:1656-1661.
35. Nystedt S, Emilsson K, Wahlestedt C, Sundelin J, Molecular cloning of a potential proteinase activated receptor [see comments]. Proc Natl Acad Sci U S A. 1994;91:9208-9212.
36. Vouret-Craviari V, Van Obberghen-Schilling E, Scimeca JC, Van Obberghen E, Pouyssegur J. Differential activation of p44mapk (ERK1) by alpha-thrombin and thrombin-receptor peptide agonist. Biochem J. 1993:209-214.
37. Serkkola E, Hurme M. Synergism between protein-kinase C and cAMP-dependent pathways in the expression of the interleukin-1 beta gene is mediated via the activator-protein-1 (AP-1) enhancer activity. Eur J Biochem. 1993;213:243-249.
38. Rhoades KL, Golub SH, Economou JS. The regulation of the human tumor necrosis factor alpha promoter region in macrophage, T cell, and B cell lines. J Biol Chem. 1992;267:22102-22107.
39. Khachigian LM, Williams AJ. Collins T. Interplay of Sp1 and Egr-1 in the proximal platelet-derived growth factor A-chain promoter in cultured vascular endothelial cells. J Biol Chem. 1995;270: 27679-27686.
40. Cui MZ, Parry GC, Oeth P, et al. Transcriptional regulation of the tissue factor gene in human epithelial cells is mediated by Sp1 and EGR-1. J Biol Chem. 1996;271:2731-2739.
41. O'Brien PJ, Prevost N, Molino M, et al. Thrombin responses in human endothetial cells: contributions from receptors other than PAR1 include the transactivation of PAR2 by thrombin-cleaved PAR1. J Biol Chem. 2000;275:13502-13509.
42. Hollenberg MD, Saifeddine M, Al-Ani B, Gui Y. Proteinase-activated receptor 4 (PAR4): action of PAR4-activating peptides in vascular and gastric tissue and lack of cross-reactivity with PAR1 and PAR2. Can J Physiol Pharmacol. 1999;77:458-464.
43. Vergnolle N, Derian CK, D'Andrea MR, Steinhoff M, Andrade-Gordon P. Characterization of thrombin-induced leukocyte rolling and adherence: a potential proinflammatory role for proteinase-activated receptor-4. J Immunol. 2002;169:1467-1473.
44. Sambrano GR, Huang W, Faruqi T, Mahrus S, Craik C, Coughlin SR. Cathepsin G activates protease-activated receptor-4 in human platelets. J Biol Chem. 2000;275:6819-6823.
45. Shapiro MJ, Weiss EJ, Faruqi TR, Coughlin SR. Protease-activated receptors 1 and 4 are shut off with distinct kinetics after activation by thrombin. J Biol Chem. 2000;275:25216-25221.
46. D'Andrea MR, Derian CK, Leturcq D, et al. Characterization of protease-activated receptor-2 immunoreactivity in normal human tissues. J Histochem Cytochem. 1998;46:157-164.
47. Camerer E, Kataoka H, Zheng YW, Kahn M, Lease K, Coughlin SR. Genetic evidence that protease-activated receptors mediate Factor Xa signaling in endothelial cells. J Biol Chem. 2002; 277:16081-16087.
48. Damiano BP, Cheung WM, Santulli RJ, et al. Cardiovascular responses mediated by protease-activated receptor-2 (PAR-2) and thrombin receptor (PAR-1) are distinguished in mice deficient in PAR-2 or PAR-1. J Pharmacol Exp Ther. 1999; 288:671-678.
49. Camerer E, Huang W, Coughlin SR. Tissue factor- and factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc Natl Acad Sci U S A. 2000;97:5255-5260.
50. 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.