Tissue factor pathway inhibitor is an inhibitor of factor VII-activating protease

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 6, 2012, Pages 1165-1171

  Stephan, F ^a   Dienava Verdoold, I ^b   Bulder, I ^a   Wouters, D ^a   Mast, A E ^c   Te Velthuis, H ^d   Aarden, L A ^a   Zeerleder, S ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c BLOOD RESEARCH INSTITUTE   (United States)

^d Reagents Division   (Netherlands)

Author keywords

Apoptosis; Factor VII activating protease; Hyaluronic acid binding protein 2; Inflammation; Nucleosomes; Tissue factor pathway inhibitor

Indexed keywords

BLOOD CLOTTING FACTOR 10A INHIBITOR; BLOOD CLOTTING FACTOR 7; BLOOD CLOTTING FACTOR 7A INHIBITOR; MONOCLONAL ANTIBODY; TISSUE FACTOR PATHWAY INHIBITOR;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; FLOW CYTOMETRY; INCUBATION TIME; MOUSE; NONHUMAN; NUCLEOSOME; PLASMA; PRIORITY JOURNAL;

ALPHA-2-ANTIPLASMIN; ANTIBODIES, MONOCLONAL; APOPTOSIS; CATALYTIC DOMAIN; COMPLEMENT C1 INACTIVATOR PROTEINS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMANS; JURKAT CELLS; LIPOPROTEINS; NUCLEOSOMES; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS;

EID: 84861685399     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04712.x     Document Type: Article

References (37)

1. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, Manogue KR, Faist E, Abraham E, Andersson J, Andersson U, Molina PE, Abumrad NN, Sama A, Tracey KJ. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999; 285: 248-51.
2. Wang H, Yang H, Czura CJ, Sama AE, Tracey KJ. HMGB1 as a late mediator of lethal systemic inflammation. Am J Respir Crit Care Med 2001; 164: 1768-73.
3. Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, Brinkmann V, Lorenz M, Bidzhekov K, Khandagale AB, Konrad I, Kennerknecht E, Reges K, Holdenrieder S, Braun S, Reinhardt C, Spannagl M, Preissner KT, Engelmann B. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887-96.
4. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, Taylor FB, Esmon NL, Lupu F, Esmon CT. Extracellular histones are major mediators of death in sepsis. Nat Med 2009; 15: 1318-21.
5. Zeerleder S, Zwart B, Wuillemin WA, Aarden LA, Groeneveld AB, Caliezi C, van Nieuwenhuijze AE, van Mierlo GJ, Eerenberg AJ, Lammle B, Hack CE. Elevated nucleosome levels in systemic inflammation and sepsis. Crit Care Med 2003; 31: 1947-51.
6. van Till JW, van Veen SQ, den Broeder V, Bresser P, Lutter R, Out TA, Schultz MJ, Gouma DJ, Boermeester MA. Compartmental apoptosis and neutrophil accumulation in severe peritonitis. J Surg Res 2010; 164: 321-8.
7. Xu J, Zhang X, Monestier M, Esmon NL, Esmon CT. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J Immunol 2011; 187: 2626-31.
8. van Nieuwenhuijze AE, van Lopik T, Smeenk RJ, Aarden LA. Time between onset of apoptosis and release of nucleosomes from apoptotic cells: putative implications for systemic lupus erythematosus. Ann Rheum Dis 2003; 62: 10-14.
9. Zeerleder S, Zwart B, te Velthuis H, Manoe R, Bulder I, Rensink I, Aarden LA. A plasma nucleosome releasing factor (NRF) with serine protease activity is instrumental in removal of nucleosomes from secondary necrotic cells. FEBS Lett 2007; 581: 5382-8.
10. Zeerleder S, Zwart B, te Velthuis H, Stephan F, Manoe R, Rensink I, Aarden LA. Nucleosome-releasing factor: a new role for factor VII-activating protease (FSAP). FASEB J 2008; 22: 4077-84.
11. Etscheid M, Hunfeld A, Konig H, Seitz R, Dodt J. Activation of proPHBSP, the zymogen of a plasma hyaluronan binding serine protease, by an intermolecular autocatalytic mechanism. Biol Chem 2000; 381: 1223-31.
12. Choi-Miura NH, Saito K, Takahashi K, Yoda M, Tomita M. Regulation mechanism of the serine protease activity of plasma hyaluronan binding protein. Biol Pharm Bull 2001; 24: 221-5.
13. Romisch J, Vermohlen S, Feussner A, Stohr H. The FVII activating protease cleaves single-chain plasminogen activators. Haemostasis 1999; 29: 292-9.
14. Hunfeld A, Etscheid M, Konig H, Seitz R, Dodt J. Detection of a novel plasma serine protease during purification of vitamin K-dependent coagulation factors. FEBS Lett 1999; 456: 290-4.
15. Wygrecka M, Morty RE, Markart P, Kanse SM, Andreasen PA, Wind T, Guenther A, Preissner KT. Plasminogen activator inhibitor-1 is an inhibitor of factor VII-activating protease in patients with acute respiratory distress syndrome. J Biol Chem 2007; 282: 21671-82.
16. Stephan F, Hazelzet JA, Bulder I, Boermeester MA, van Till JO, van der Poll T, Wuillemin WA, Aarden LA, Zeerleder S. Activation of factor VII-activating protease in human inflammation: a sensor for cell death. Crit Care 2011; 15: R110.
17. Bajaj MS, Kuppuswamy MN, Saito H, Spitzer SG, Bajaj SP. Cultured normal human hepatocytes do not synthesize lipoprotein-associated coagulation inhibitor: evidence that endothelium is the principal site of its synthesis. Proc Natl Acad Sci USA 1990; 87: 8869-73.
18. Novotny WF, Girard TJ, Miletich JP, Broze GJ Jr. Platelets secrete a coagulation inhibitor functionally and antigenically similar to the lipoprotein associated coagulation inhibitor. Blood 1988; 72: 2020-5.
19. Maroney SA, Haberichter SL, Friese P, Collins ML, Ferrel JP, Dale GL, Mast AE. Active tissue factor pathway inhibitor is expressed on the surface of coated platelets. Blood 2007; 109: 1931-7.
20. Novotny WF, Girard TJ, Miletich JP, Broze GJ Jr. Purification and characterization of the lipoprotein-associated coagulation inhibitor from human plasma. J Biol Chem 1989; 264: 18832-7.
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: 2850-60.
22. Carr C, Bild GS, Chang AC, Peer GT, Palmier MO, Frazier RB, Gustafson ME, Wun TC, Creasey AA, Hinshaw LB. Recombinant E. coli-derived tissue factor pathway inhibitor reduces coagulopathic and lethal effects in the baboon gram-negative model of septic shock. Circ Shock 1994; 44: 126-37.
23. Abraham E, Reinhart K, Svoboda P, Seibert A, Olthoff D, Dal NA, Postier R, Hempelmann G, Butler T, Martin E, Zwingelstein C, Percell S, Shu V, Leighton A, Creasey AA. Assessment of the safety of recombinant tissue factor pathway inhibitor in patients with severe sepsis: a multicenter, randomized, placebo-controlled, single-blind, dose escalation study. Crit Care Med 2001; 29: 2081-9.
24. Girard TJ, Warren LA, Novotny WF, Likert KM, Brown SG, Miletich JP, Broze GJ Jr. Functional significance of the Kunitz-type inhibitory domains of lipoprotein-associated coagulation inhibitor. Nature 1989; 338: 518-20.
25. Nuijens JH, Huijbregts CC, Eerenberg-Belmer AJ, Abbink JJ, Strack van Schijndel RJ, Felt-Bersma RJ, Thijs LG, Hack CE. Quantification of plasma factor XIIa-Cl(-)-inhibitor and kallikrein-Cl(-)-inhibitor complexes in sepsis. Blood 1988; 72: 1841-8.
26. Warshawsky I, Bu G, Mast A, Saffitz JE, Broze GJ Jr, Schwartz AL. The carboxy terminus of tissue factor pathway inhibitor is required for interacting with hepatoma cells in vitro and in vivo. J Clin Invest 1995; 95: 1773-81.
27. Lockett JM, Mast AE. Contribution of regions distal to glycine-160 to the anticoagulant activity of tissue factor pathway inhibitor. Biochemistry 2002; 41: 4989-97.
28. Cheng Y, Prusoff WH. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 1973; 22: 3099-108.
29. Harenberg J, Malsch R, Heene DL. Tissue factor pathway inhibitor: proposed heparin recognition region. Blood Coagul Fibrinolysis 1995; 6(Suppl 1): S50-6.
30. Sandset PM, Abildgaard U, Larsen ML. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res 1988; 50: 803-13.
31. Cunningham AC, Hasty KA, Enghild JJ, Mast AE. Structural and functional characterization of tissue factor pathway inhibitor following degradation by matrix metalloproteinase-8. Biochem J 2002; 367: 451-8.
32. Kanse SM, Declerck PJ, Ruf W, Broze G, Etscheid M. Factor VII-activating protease promotes the proteolysis and inhibition of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol 2012; 32: 427-33.
33. Broze GJ Jr. Tissue factor pathway inhibitor and the current concept of blood coagulation. Blood Coagul Fibrinolysis 1995; 6(Suppl 1): S7-13.
34. Broze GJ Jr, Lange GW, Duffin KL, MacPhail L. Heterogeneity of plasma tissue factor pathway inhibitor. Blood Coagul Fibrinolysis 1994; 5: 551-9.
35. Mast AE, Acharya N, Malecha MJ, Hall CL, Dietzen DJ. Characterization of the association of tissue factor pathway inhibitor with human placenta. Arterioscler Thromb Vasc Biol 2002; 22: 2099-104.
36. Abraham E, Reinhart K, Opal S, Demeyer I, Doig C, Rodriguez AL, Beale R, Svoboda P, Laterre PF, Simon S, Light B, Spapen H, Stone J, Seibert A, Peckelsen C, De DC, Postier R, Pettila V, Artigas A, Percell SR, et al. Efficacy and safety of tifacogin (recombinant tissue factor pathway inhibitor) in severe sepsis: a randomized controlled trial. JAMA 2003; 290: 238-47.
37. de Jonge E, Dekkers PE, Creasey AA, Hack CE, Paulson SK, Karim A, Kesecioglu J, Levi M, van Deventer SJ, van der Poll T. Tissue factor pathway inhibitor dose-dependently inhibits coagulation activation without influencing the fibrinolytic and cytokine response during human endotoxemia. Blood 2000; 95: 1124-9.