Roles of protease-activated receptors in a mouse model of endotoxemia

Blood

Volumn 107, Issue 10, 2006, Pages 3912-3921

  Camerer, Eric ^a   Cornelissen, Ivo ^a   Kataoka, Hiroshi ^a   Duong, Daniel N ^a   Zheng, Yao Wu ^a   Coughlin, Shaun R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTITHROMBIN III; CYTOKINE; ENDOTOXIN; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN ANTITHROMBIN COMPLEX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL COUNT; BLOOD CLOTTING; CONTROLLED STUDY; DEATH; DISSEMINATED INTRAVASCULAR CLOTTING; ENDOTHELIUM CELL; ENDOTOXEMIA; FEMALE; FIBRINOGEN DEFECT; INFLAMMATION; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SURVIVAL; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION; THROMBOCYTOPENIA;

EID: 33646559569     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2005-08-3130     Document Type: Article

References (82)

1. Esmon CT, Fukudome K, Mather T, et al. Inflammation, sepsis, and coagulation. Haematologica. 1999;84:254-259.
2. Camerer E, Kolsto AB, Prydz H. Cell biology of tissue factor, the principal initiator of blood coagulation. Thromb Res. 1996;81:1-41.
3. Pawlinski R, Pedersen B, Schabbauer G, et al. Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood. 2004;103:1342-1347.
4. Drake TA, Cheng J, Chang A, Taylor FBJ. Expression of tissue factor, thrombomodulin, and Eselectin in baboons with lethal Escherichia coli sepsis. Am J Pathol. 1993;142:1458-1470.
5. Esmon CT. Sepsis. A myriad of responses. Lancet. 2001;358(suppl):S61.
6. Taylor FB Jr. Staging of the pathophysiologic responses of the primate microvasculature to Escherichia coli and endotoxin: examination of the elements of the compensated response and their links to the corresponding uncompensated lethal variants. Crit Care Med. 2001;29:S78-S89.
7. Levi M, van der Poll T, ten Cate H, van Deventer SJ. The cytokine-mediated imbalance between coagulant and anticoagulant mechanisms in sepsis and endotoxaemia. Eur J Clin Invest. 1997;27:3-9.
8. Levi M. Current understanding of disseminated intravascular coagulation. Br J Haematol. 2004;124:567-576.
9. Coughlin SR, Camerer E. PARticipation in inflammation. J Clin Invest. 2003;111:25-27.
10. Vergnolle N, Wallace JL, Bunnett NW, Hollenberg MD. Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol Sci. 2001;22:146-152.
11. Esmon CT. Role of coagulation inhibitors in inflammation. Thromb Haemost. 2001;86:51-56.
12. Ruf W. Protease-activated receptor signaling in the regulation of inflammation. Crit Care Med. 2004;32:S287-S292.
13. Pawlinski R, Mackman N. Tissue factor, coagulation proteases, and protease-activated receptors in endotoxemia and sepsis. Crit Care Med. 2004;32:S293-S297.
14. Szaba FM, Smiley ST. Roles for thrombin and fibrin(ogen) in cytokine/chemokine production and macrophage adhesion in vivo. Blood. 2002;99:1053-1059.
15. Johnson LL, Berggren KN, Szaba FM, Chen W, Smiley ST. Fibrin-mediated protection against infection-stimulated immunopathology. J Exp Med. 2003;197:801-806.
16. Degen JL. Hemostatic factors and inflammatory disease. Thromb Haemost. 1999;82:858-864.
17. Joyce DE, Gelbert L, Ciaccia A, DeHoff B, Grinnell BW. Gene expression profile of antithrombotic protein c defines new mechanisms modulating inflammation and apoptosis. J Biol Chem. 2001;276:11199-11203.
18. Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood. 2004;105:3178-3184.
19. Mosnier LO, Griffin JH. Inhibition of staurosporine-induced apoptosis of endothelial cells by activated protein C requires protease-activated receptor-1 and endothelial cell protein C receptor. Biochem J. 2003;373:65-70.
20. Taylor FBJ, Chang A, Ruf W, et al. Lethal E. coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock. 1991;33:127-134.
21. Creasey AA, Chang AC, Feigen L, Wun TC, Taylor FB Jr, Hinshaw LB. Tissue factor pathway inhibitor reduces mortality from Escherichia coli septic shock. J Clin Invest. 1993;91:2850-2860.
22. Taylor FB Jr. The inflammatory-coagulant axis in the host response to gram-negative sepsis: regulatory roles of proteins and inhibitors of tissue factor. New Horiz. 1994;2:555-565.
23. Taylor FB, Chang AC, Peer G, Li A, Ezban M, Hedner U. Active site inhibited factor VIIa (DEGR VIIa) attenuates the coagulant and interleukin-6 and -8, but not tumor necrosis factor, responses of the baboon to LD100 Escherichia coli. Blood. 1998;91:1609-1615.
24. Taylor FB Jr, Chang AC, Peer GT, et al. DEGR-factor Xa blocks disseminated intravascular coagulation initiated by Escherichia coli without preventing shock or organ damage. Blood. 1991;78:364-368.
25. Weijer S, Schoenmakers SH, Florquin S, et al. Inhibition of the tissue factor/factor VIIa pathway does not influence the inflammatory or antibacterial response to abdominal sepsis induced by Escherichia coli in mice. J Infect Dis. 2004;189:2308-2317.
26. Taylor F, Chang A, Esmon C, D'Angelo A, Vigano-D'Angelo S, Blick K. Protein C prevents the coagulopathic and lethal effects of E. coli infusion in the baboon. J Clin Invest. 1987;79:918-925.
27. Bernard GR, Vincent JL, Laterre PF, et al. Effi-cacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med. 2001;344:699-709.
28. Esmon CT. The protein C pathway. Chest. 2003;124:26S-32S.
29. Griffin JH, Zlokovic B, Fernandez JA. Activated protein C: potential therapy for severe sepsis, thrombosis, and stroke. Semin Hematol. 2002;39:197-205.
30. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature. 2000;407:258-264.
31. Ruf W. Is APC activation of endothelial cell PAR1 important in severe sepsis? Yes. J Thromb Haemost. 2005;3:1912-1914.
32. Esmon CT. Is APC activation of endothelial cell PAR1 important in severe sepsis? No. J Thromb Haemost. 2005;3:1910-1911.
33. 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.
34. Ishihara H, Connolly AJ, Zeng D, et al. Protease-activated receptor 3 is a second thrombin receptor in humans. Nature. 1997;386:502-506.
35. Kahn ML, Zheng YW, Huang W, et al. A dual thrombin receptor system for platelet activation. Nature. 1998;394:690-694.
36. 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.
37. 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.
38. 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.
39. 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.
40. Kataoka H, Hamilton JR, McKemy DD, et al. Protease-activated receptors 1 and 4 mediate thrombin signaling in endothelial cells. Blood. 2003;102:3224-3231.
41. Camerer E, Kataoka H, 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.
42. McNamara CA, Sarembok IJ, Gimple LW, Fenton JW II, Coughlin SR, Owens GK. Thrombin stimulation of smooth muscle cell proliferation is mediated by a proteolytic, receptor-mediated mechanism. J Clin Invest. 1992;91:94-98.
43. Trejo J, Connolly AJ, Coughlin SR. The cloned thrombin receptor is necessary and sufficient for activation of mitogen-activated protein kinase and mitogenesis in mouse lung fibroblasts. Loss of responses in fibroblasts from receptor knockout mice. J Biol Chem. 1996;271:21536-21541.
44. Lindner JR, Kahn ML, Coughlin SR, et al. Delayed onset of inflammation in protease-activated receptor-2-deficient mice. J Immunol. 2000;165:6504-6510.
45. Suh TT, Holmback K, Jensen NJ, et al. Resolution of spontaneous bleeding events but failure of pregnancy in fibrinogen-deficient mice. Genes Dev. 1995;9:2020-2033.
46. Shivdasani RA, Rosenblatt MF, Zucker FD, et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell. 1995;81:695-704.
47. 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.
48. 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.
49. Riewald M, Petrovan RJ, Donner A, Mueller BM, Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science. 2002;296:1880-1882.
50. Senden NH, Jeunhomme TM, Heemskerk JW, et al. Factor Xa induces cytokine production and expression of adhesion molecules by human umbilical vein endothelial cells. J Immunol. 1998;161:4318-4324.
51. 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.
52. Glantz SA. Primer of Biostatistics. 3rd ed. New York, NY: McGraw-Hill; 1992.
53. Corvera CU, Dery O, McConalogue K, et al. Mast cell tryptase regulates rat colonic myocytes through proteinase-activated receptor 2. J Clin Invest. 1997;100:1383-1393.
54. Molino M, Barnathan ES, Numerof R, et al. Interactions of mast cell tryptase with thrombin receptors and PAR-2. J Biol Chem. 1997;272:4043-4049.
55. Uehara A, Sugawara S, Muramoto K, Takada H. Activation of human oral epithelial cells by neutrophil proteinase 3 through protease-activated receptor-2. J Immunol. 2002;169:4594-4603.
56. Uehara A, Muramoto K, Takada H, Sugawara S. Neutrophil serine proteinases activate human nonepithelial cells to produce inflammatory cytokines through protease-activated receptor 2. J Immunol. 2003;170:5690-5696.
57. Laubach VE, Shesely EG, Smithies O, Sherman PA. Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death. Proc Natl Acad Sci U S A. 1995;92:10688-10692.
58. Vergnolle N. Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo. J Immunol. 1999;163:5064-5069.
59. 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.
60. Schoenmakers SH, Groot AP, Florquin S, Reitsma PH, Spek CA. Blood cell-derived tissue factor influences host response during murine endotoxemia. Blood Cells Mol Dis. 2004;32:325-333.
61. Corral J, Yelamos J, Hernandez-Espinosa D, et al. Role of lipopolysaccharide and cecal ligation and puncture on blood coagulation and inflammation in sensitive and resistant mice models. Am J Pathol. 2005;166:1089-1098.
62. Schoenmakers SH, Versteeg HH, Groot AP, Reitsma PH, Spek CA. Tissue factor haploinsufficiency during endotoxin induced coagulation and inflammation in mice. J Thromb Haemost. 2004;2:2185-2193.
63. Shivdasani RA, Rosenblatt MF, Zucker-Franklin D, et al. Transcription factor NF-E2 is required for platelet formation independent of the actions of thrombopoietin/MGDF in megakaryocyte development. Cell. 1995;81:695-704.
64. Garcia JG, Liu F, Verin AD, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001;108:689-701.
65. Peng X, Hassoun PM, Sammani S, et al. Protective effects of sphingosine 1-phosphate in murine endotoxin-induced inflammatory lung injury. Am J Respir Crit Care Med. 2004;169:1245-1251.
66. Kahn ML, Nakanishi-Matsui M, Shapiro MJ, Ishihara H, Coughlin SR. Protease-activated receptors 1 and 4 mediate activation of human platelets by thrombin. J Clin Invest. 1999;103:879-887.
67. Weiss EJ, Hamilton JR, Lease KE, Coughlin SR. Protection against thrombosis in mice lacking PAR3. Blood. 2002;100:3240-3244.
68. Hamilton JR, Cornelissen I, Coughlin SR. Impaired hemostasis and protection against thrombosis in protease-activated receptor 4-deficient mice is due to lack of thrombin signaling in platelets. J Thromb Haemost. 2004;2:1429-1435.
69. Derian CK, Damiano BP, Addo MF, et al. Blockade of the thrombin receptor protease-activated receptor-1 with a small-molecule antagonist prevents thrombus formation and vascular occlusion in nonhuman primates. J Pharmacol Exp Ther. 2003;304:855-861.
70. Vergnolle N, Wallace JL, Bunnett NW, Hollenberg MD. Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol Sci. 2001;22:146-152.
71. Levi M, van der Poll T, Buller HR. Bidirectional relation between inflammation and coagulation. Circulation. 2004;109:2698-2704.
72. Levi M, Keller TT, van Gorp E, ten Cate H. Infection and inflammation and the coagulation system. Cardiovasc Res. 2003;60:26-39.
73. Riewald M, Ruf W. Science review: role of coagulation protease cascades in sepsis. Crit Care. 2003;7:123-129.
74. Aird WC. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood. 2003;101:3765-3777.
75. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional toll-like receptor-4 (TLR4). Blood. 2005;106:2417-2423.
76. 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.
77. Vergnolle N. Proteinase-activated receptor-2-activating peptides induce leukocyte rolling, adhesion, and extravasation in vivo. J Immunol. 1999;163:5064-5069.
78. Su X, Camerer E, Hamilton JR, Coughlin SR, Matthay MA. Protease-activated receptor-2 activation induces acute lung inflammation by neuropeptide-dependent mechanisms. J Immunol. 2005;175:2598-2605.
79. 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.
80. Kawabata A, Kuroda R, Nishikawa H, Asai T, Kataoka K, Taneda M. Enhancement of vascular permeability by specific activation of protease-activated receptor-1 in rat hindpaw: a protective role of endogenous and exogenous nitric oxide. Br J Pharmacol. 1999;126:1856-1862.
81. 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.
82. Feistritzer C, Lenta R, Riewald M. Protease-activated receptors-1 and -2 can mediate endothelial barrier protection: role in factor Xa signaling. J Thromb Haemost. 2005;3:2798-2805.