Coagulation and innate immune responses: Can we view them separately?

Blood

Volumn 114, Issue 12, 2009, Pages 2367-2374

  Delvaeye, Mieke ^a   Conway, Edward M ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PROTEIN C; ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; FIBRIN; FIBRINOGEN; PLASMIN; PLASMINOGEN; PROTEIN C; PROTEINASE ACTIVATED RECEPTOR; THROMBIN; THROMBOMODULIN;

ANTIPHOSPHOLIPID SYNDROME; BLOOD CLOTTING; BLOOD CLOTTING DISORDER; EVOLUTION; HUMAN; INFLAMMATORY DISEASE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPSIS; THROMBOCYTE; ANIMAL; IMMUNOLOGY; PHYSIOLOGY;

ANIMALS; BLOOD COAGULATION; HUMANS; IMMUNITY, INNATE;

EID: 70350512348     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-05-199208     Document Type: Review

References (89)

1. Mackman N. The role of tissue factor and factor VIIa in hemostasis. Anesth Analg. 2009;108(5):1447-1452.
2. Butenas S, Orfeo T, Mann KG. Tissue factor activity and function in blood coagulation. Thromb Res. 2008;122(suppl 1):S42-S46.
3. Crawley JT, Lane DA. The haemostatic role of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol. 2008;28(2):233-242. (Pubitemid 351161194)
4. Rau JC, Beaulieu LM, Huntington JA, Church FC. Serpins in thrombosis, hemostasis and fibrinolysis. J Thromb Haemost. 2007;5(suppl 1):102-115.
5. Van de Wouwer M, Collen D, Conway EM. Thrombomodulin-Protein C-EPCR System: integrated to regulate coagulation and inflammation. Arterioscler Thromb Vasc Biol. 2004;24(8):1374-1383.
6. Mogensen TH. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev. 2009;22(2):240-273.
7. Beutler BA. TLRs and innate immunity. Blood. 2009;113(7):1399-1407.
8. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81(1):1-5.
9. Sjöberg AP, Trouw LA, Blom AM. Complement activation and inhibition: a delicate balance. Trends Immunol. 2009;30(2):83-90.
10. Huber-Lang M, Sarma JV, Zetoune FS, et al. Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med. 2006;12(6):682-687. (Pubitemid 43865238)
11. Noris M, Remuzzi G. Hemolytic uremic syndrome. J Am Soc Nephrol. 2005;16(4):1035-1050.
12. Iwanaga S, Lee BL. Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol. 2005;38(2):128-150. (Pubitemid 43026214)
13. Iwanaga S. The molecular basis of innate immunity in the horseshoe crab. Curr Opin Immunol. 2002;14(1):87-95. (Pubitemid 34085111)
14. Zhu Y, Thangamani S, Ho B, Ding JL. The ancient origin of the complement system. EMBO J. 2005;24(2):382-394.
15. Krem MM, Di Cera E. Evolution of enzyme cascades from embryonic development to blood coagulation. Trends Biochem Sci. 2002;27(2):67-74.
16. Opal SM, Esmon CT. Bench-to-bedside review: functional relationships between coagulation and the innate immune response and their respective roles in the pathogenesis of sepsis. Crit Care. 2003;7(1):23-38.
17. Busso N, Chobaz-Peclat V, Hamilton J, Spee P, Wagtmann N, So A. Essential role of platelet activation via protease activated receptor 4 in tissue factor-initiated inflammation. Arthritis Res Ther. 2008;10(2):R42. http://arthritis-research.com/content/10/2/R42. Accessed June 2009. (Pubitemid 351611901)
18. 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(4):1342-1347. (Pubitemid 38168646)
19. Sharma L, Melis E, Hickey MJ, et al. The cytoplasmic domain of tissue factor contributes to leukocyte recruitment and death in endotoxemia. Am J Pathol. 2004;165(1):331-340. (Pubitemid 38821839)
20. Abraham E, Reinhart K, Opal S, et al. Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA. 2003;290(2):238-247. (Pubitemid 37430063)
21. Drake WT, Lopes NN, Fenton JW II, Issekutz AC. Thrombin enhancement of interleukin-1 and tumor necrosis factor-alpha induced polymorphonuclear leukocyte migration. Lab Invest. 1992;67(5):617-627.
22. Fujita T, Yamabe H, Shimada M, et al. Thrombin enhances the production of monocyte chemoattractant protein-1 and macrophage inflammatory protein-2 in cultured rat glomerular epithelial cells. Nephrol Dial Transplant. 2008;23(11):3412-3417.
23. Wadgaonkar R, Somnay K, Garcia JG. Thrombin induced secretion of macrophage migration inhibitory factor (MIF) and its effect on nuclear signaling in endothelium. J Cell Biochem. 2008;105(5):1279-1288.
24. Clark A, Weymann A, Hartman E, et al. Evidence for non-traditional activation of complement factor C3 during murine liver regeneration. Mol Immunol. 2008;45(11):3125-3132.
25. Naldini A, Aarden L, Pucci A, Bernini C, Carraro F. Inhibition of interleukin-12 expression by alpha=thrombin in human peripheral blood mononuclear cells: a potential mechanism for modulating Th1/Th2 responses. Br J Pharmacol. 2003;140(5):980-986. (Pubitemid 37464082)
26. Feistritzer C, Riewald M. Endothelial barrier protection by activated protein C through PAR1-dependent sphingosine 1-phosphate receptor-1 crossactivation. Blood. 2005;105(8):3178-3184. (Pubitemid 40504337)
27. Krupiczojc MA, Scotton CJ, Chambers RC. Coagulation signalling following tissue injury: focus on the role of factor Xa. Int J Biochem Cell Biol. 2008;40(6-7):1228-1237.
28. Sutherland MR, Friedman HM, Pryzdial EL. Herpes simplex virus type 1-encoded glycoprotein C enhances coagulation factor VIIa activity on the virus. Thromb Haemost. 2004;92(5):947-955.
29. Matsushita K, Imamura T, Tomikawa M, Tancharoen S, Tatsuyama S, Maruyama I. DX-9065a inhibits proinflammatory events induced by gingipains and factor Xa. J Periodontal Res. 2006;41(2):148-156.
30. Shpacovitch V, Feld M, Hollenberg MD, Luger TA, Steinhoff M. Role of protease-activated receptors in inflammatory responses, innate and adaptive immunity. J Leukoc Biol. 2008;83(6):1309-1322. (Pubitemid 351960309)
31. Trivedi V, Boire A, Tchernychev B, et al. Platelet matrix metalloprotease-1 mediates thrombogenesis by activating PAR1 at a cryptic ligand site. Cell. 2009;137(2):332-343.
32. Rallabhandi P, Nhu QM, Toshchakov VY, et al. Analysis of proteinase-activated receptor 2 and TLR4 signal transduction: a novel paradigm for receptor cooperativity. J Biol Chem. 2008;283(36):24314-24325.
33. Camerer E, Cornelissen I, Kataoka H, Duong DN, Zheng YW, Coughlin SR. Roles of protease-activated receptors in a mouse model of endotoxemia. Blood. 2006;107(10):3912-3921. (Pubitemid 43726796)
34. Niessen F, Schaffner F, Furlan-Freguia C, et al. Dendritic cell PAR1-S1P3 signalling couples coagulation and inflammation. Nature. 2008;452(7187):654- 658.
35. Kaneider NC, Leger AJ, Agarwal A, et al. 'Role reversal' for the receptor PAR1 in sepsis-induced vascular damage. Nat Immunol. 2007;8(12):1303-1312. (Pubitemid 350131169)
36. Niessen F, Furlan-Freguia C, Fernandez JA, et al. Endogenous EPCR/aPC-PAR1 signaling prevents inflammation-induced vascular leakage and lethality. Blood. 2009;113(12):2859-2866.
37. Kerschen EJ, Fernandez JA, Cooley BC, et al. Endotoxemia and sepsis mortality reduction by non-anticoagulant activated protein C. J Exp Med. 2007;204(10):2439-2448.
38. Kahn ML. Counteracting clotting in sepsis. Nat Med. 2008;14(9):918-919.
39. Wiedermann C, Romisch J. The anti-inflammatory actions of antithrombin-a review. Acta Med Austriaca. 2002;29(3):89-92.
40. Jackson CJ, Xue M. Activated protein C: an anticoagulant that does more than stop clots. Int J Biochem Cell Biol. 2008;40(12):2692-2697.
41. Riewald M, Petrovan RJ, Donner A, Ruf W. Activated protein C signals through the thrombin receptor PAR1 in endothelial cells. J Endotoxin Res. 2003;9(5):317-321. (Pubitemid 37193040)
42. Yang XV, Banerjee Y, Fernandez JA, et al. Activated protein C ligation of ApoER2 (LRP8) causes Dab1-dependent signaling in U937 cells. Proc Natl Acad Sci U S A. 2009;106(1):274-279.
43. Villegas-Mendez A, Montes R, Ambrose LR, Warrens AN, Laffan M, Lane DA. Proteolysis of the endothelial cell protein C receptor by neutrophil proteinase 3. J Thromb Haemost. 2007;5(5):980-988. (Pubitemid 46691727)
44. Bernard GR. Drotrecogin alfa (activated) (recombinant human activated protein C) for the treatment of severe sepsis. Crit Care Med. 2003;31(3):S85-S93. (Pubitemid 36143481)
45. Levi M. Activated protein C in sepsis: a critical review. Curr Opin Hematol. 2008;15(5):481-486.
46. Nadel S, Goldstein B, Williams MD, et al. Drotrecogin alfa (activated) in children with severe sepsis: a multicentre phase III randomised controlled trial. Lancet. 2007;369(9564):836-843. (Pubitemid 46365900)
47. Mosnier LO, Zlokovic BV, Griffin JH. The cytoprotective protein C pathway. Blood. 2007;109(8):3161-3172.
48. Regnault V, Boehlen F, Ozsahin H, et al. Antiprotein S antibodies following a varicella infection: detection, characterization and influence on thrombin generation. J Thromb Haemost. 2005;3(6):1243-1249. (Pubitemid 41725249)
49. Rezende SM, Simmonds RE, Lane DA. Coagulation, inflammation, and apoptosis: different roles for protein S and the protein S-C4b binding protein complex. Blood. 2004;103(4):1192-1201.
50. Weiler H, Lindner V, Kerlin B, et al. Characterization of a mouse model for thrombomodulin deficiency. Arterioscler Thromb Vasc Biol. 2001;21(19):1531-1537. (Pubitemid 34219820)
51. Van de Wouwer M, Plaisance S, DeVries A, et al. The lectin-like domain of thrombomodulin interferes with complement activation and protects against arthritis. J Thromb Haemost. 2006;4(8):1813-1824. (Pubitemid 44144810)
52. Shi CS, Shi GY, Hsiao SM, et al. Lectin-like domain of thrombomodulin binds to its specific ligand Lewis Y antigen and neutralizes lipopolysaccharide-induced inflammatory response. Blood. 2008;112(90):3661-3670.
53. Abeyama K, Stern DM, Ito Y, et al. The N-terminal domain of thrombomodulin sequesters high-mobility group-B1 protein, a novel antiinflammatory mechanism. J Clin Invest. 2005;115(5):1267-1274. (Pubitemid 40629045)
54. Myles T, Nishimura T, Yun TH, et al. Thrombin activatable fibrinolysis inhibitor: a potential regulator of vascular inflammation. J Biol Chem. 2003;278(51):51059-51067. (Pubitemid 38020340)
55. Yerkovich ST, Roponen M, Smith ME, et al. Allergen-enhanced thrombomodulin (blood dendritic cell antigen 3, CD141) expression on dendritic cells is associated with a TH2-skewed immune response. J Allergy Clin Immunol. 2009;123(1):209-216.
56. Ikeguchi H, Maruyama S, Morita Y, et al. Effects of human soluble thrombomodulin on experimental glomerulonephritis. Kidney Int. 2002;61(2):490-501. (Pubitemid 34102589)
57. Geudens N, Van de Wouwer M, Banaudenaerde B, et al. The lectin-like domain of thrombomodulin protects against ischemia-reperfusion lung injury. Eur Resp Journal. 2008;32(4):862-870.
58. Sharfuddin AA, Sandoval RM, Berg DT, et al. Soluble thrombomodulin protects ischemic kidneys. J Am Soc Nephrol. 2009;20(3):524-534.
59. Saito H, Maruyama I, Shimazaki S, et al. Efficacy and safety of recombinant human soluble thrombomodulin (ART-123) in disseminated intravascular coagulation: results of a phase III, randomized, double-blind clinical trial. J Thromb Haemost. 2007;5(1):31-41. (Pubitemid 44921064)
60. Smiley ST, King JA, Hancock WW. Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol. 2001;167(5):2887-2894.
61. Adams RA, Schachtrup C, Davalos D, Tsigelny I, Akassoglou K. Fibrinogen signal transduction as a mediator and therapeutic target in inflammation: lessons from multiple sclerosis. Curr Med Chem. 2007;14(27):2925-2936. (Pubitemid 350201659)
62. Kay AB, Pepper DS, McKenzie R. The identification of fibrinopeptide B as a chemotactic agent derived from human fibrinogen. Br J Haematol. 1974;27(4):669-677.
63. Flick MJ, Du X, Witte DP, et al. Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest. 2004;113(11):1596-1606. (Pubitemid 39071683)
64. Krarup A, Wallis R, Presanis JS, Gal P, Sim RB. Simultaneous activation of complement and coagulation by MBL-associated serine protease 2. PLoS ONE. 2007;2:e623. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone. 0000623. Accessed June 2009. (Pubitemid 351279928)
65. Hajela K, Kojima M, Ambrus G, et al. The biological functions of MBL-associated serine proteases (MASPs). Immunobiology. 2002;205(4-5):467-475. (Pubitemid 35153962)
66. Sárváry A, Szucs S, Balogh I, et al. Possible role of factor XIII subunit A in Fcgamma and complement receptor-mediated phagocytosis. Cell Immunol. 2004;228(2):81-90. (Pubitemid 38813331)
67. Birnbaum J, Hein OV, Luhrs C, et al. Effects of coagulation factor XIII on intestinal functional capillary density, leukocyte adherence and mesenteric plasma extravasation in experimental endotoxemia. Crit Care. 2006;10(1):R29. http://ccforum.com/content/10/1/R29. Accessed June 2009. (Pubitemid 47079792)
68. Degen JL, Bugge TH, Goguen JD. Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost. 2007;5(suppl 1):24-31.
69. Mondino A, Blasi F. uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol. 2004;25(8):450-455. (Pubitemid 38951087)
70. Rijneveld AW, Levi M, Florquin S, Speelman P, Carmeliet P, van Der Poll T. Urokinase receptor is necessary for adequate host defense against pneumococcal pneumonia. J Immunol. 2002;168(7):3507-3511. (Pubitemid 34250418)
71. Yepes M, Roussel BD, Ali C, Vivien D. Tissue-type plasminogen activator in the ischemic brain: more than a thrombolytic. Trends Neurosci. 2009;32(1):48-55.
72. Gong Y, Hart E, Shchurin A, Hoover-Plow J. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest. 2008;118(9):3012-3024.
73. Weyrich AS, Zimmerman GA. Platelets: signaling cells in the immune continuum. Trends Immunol. 2004;25(9):489-495.
74. Ma AC, Kubes P. Platelets, neutrophils, and neutrophil extracellular traps (NETs) in sepsis. J Thromb Haemost. 2008;6(3):415-420. (Pubitemid 351280107)
75. von Hundelshausen P, Koenen RR, Weber C. Platelet-mediated enhancement of leukocyte adhesion. Microcirculation. 2009;16(1):84-96.
76. Rizvi M, Pathak D, Freedman JE, Chakrabarti S. CD40-CD40 ligand interactions in oxidative stress, inflammation and vascular disease. Trends Mol Med. 2008;14(12):530-538.
77. Danese S, de la Motte C, Reyes BM, Sans M, Levine AD, Fiocchi C. Cutting edge: T cells trigger CD40-dependent platelet activation and granular RANTES release: a novel pathway for immune response amplification. J Immunol. 2004;172(4):2011-2015. (Pubitemid 38182345)
78. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood. 2005;106(7):2417-2423. (Pubitemid 41510815)
79. Del Conde I, Cruz MA, Zhang H, Lopez JA, Afshar-Kharghan V. Platelet activation leads to activation and propagation of the complement system. J Exp Med. 2005;201(6):871-879. (Pubitemid 40524457)
80. Wiedmer T, Esmon CT, Sims PJ. Complement proteins C5b-9 stimulate procoagulant activity through platelet prothrombinase. Blood. 1986;68(4):875-880. (Pubitemid 17183846)
81. Yin W, Ghebrehiwet B, Peerschke EI. Expression of complement components and inhibitors on platelet microparticles. Platelets. 2008;19(3):225-233. (Pubitemid 351574446)
82. Blair P, Rex S, Vitseva O, et al. Stimulation of Toll-like receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ Res. 2009;104(3):346-354.
83. Kyriakides C, Woodcock SA, Wang Y, et al. Soluble P-selectin moderates complement-dependent reperfusion injury of ischemic skeletal muscle. Am J Physiol Cell Physiol. 2000;279(2):C520-C528. (Pubitemid 30679591)
84. Polgar J, Matuskova J, Wagner DD. The P-selectin, tissue factor, coagulation triad. J Thromb Haemost. 2005;3(8):1590-1596. (Pubitemid 41716543)
85. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463-469.
86. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532-1535. (Pubitemid 38314426)
87. Girardi G, Berman J, Redecha P, et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest. 2003;112(11):1644-1654. (Pubitemid 38063722)
88. Li W, Zheng X, Gu JM, et al. Extra-embryonic expression of EPCR is essential for embryonic viability. Blood. 2005;106(8):2716-2722. (Pubitemid 41510745)
89. Hurtado V, Montes R, Gris JC, et al. Autoantibodies against EPCR are found in antiphospholipid syndrome and are a risk factor for fetal death. Blood. 2004;104(5):1369-1374. (Pubitemid 39166513)