Tissue factor pathway inhibitor: New insights into an old inhibitor

Seminars in Thrombosis and Hemostasis

Volumn 38, Issue 2, 2012, Pages 129-134

  Adams, Murray ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

Author keywords

platelets; protein S; thrombosis; tissue factor; tissue factor pathway inhibitor

Indexed keywords

BLOOD CLOTTING FACTOR 10A; PROTEIN S; RECOMBINANT TISSUE FACTOR PATHWAY INHIBITOR; TISSUE FACTOR PATHWAY INHIBITOR;

ANTICOAGULATION; BLOOD CLOTTING; BLOOD CLOTTING FACTOR DEFICIENCY; CELL SURFACE; COMMUNITY ACQUIRED PNEUMONIA; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; DISSEMINATED INTRAVASCULAR CLOTTING; DRUG HALF LIFE; ENDOTHELIUM CELL; HYPERCOAGULABILITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTE ACTIVATION; THROMBOSIS;

ALTERNATIVE SPLICING; ANIMALS; BLOOD COAGULATION; BLOOD PLATELETS; FACTOR VIIA; HUMANS; LIPOPROTEINS; PROTEIN S; SERINE PROTEINASE INHIBITORS; THROMBOPLASTIN;

EID: 84858119667     PISSN: 00946176     EISSN: 10989064     Source Type: Journal    
DOI: 10.1055/s-0032-1301410     Document Type: Review

References (91)

1. Sanders NL, Bajaj SP, Zivelin A, Rapaport SI. Inhibition of tissue factor/factor VIIa activity in plasma requires factor X and an additional plasma component. Blood: 1985; 66 1 204 212 (Pubitemid 15004805)
2. Huang ZF, Broze G Jr. Consequences of tissue factor pathway inhibitor gene-disruption in mice. Thromb Haemost: 1997; 78 1 699 704
3. Huang ZF, Higuchi D, Lasky N, Broze GJ Jr. Tissue factor pathway inhibitor gene disruption produces intrauterine lethality in mice. Blood: 1997; 90 3 944 951 (Pubitemid 27314126)
4. Loeb L, Fleisher MS, Tuttle L. The interaction between blood serum and tissue extract in the coagulation of the blood: I. The combined action of serum and tissue extract on fluoride, hirudin, and peptone plasma; the effect of heating on the serum. J Biol Chem: 1922; 51 461 483
5. Loeb L, Fleisher MS, Tuttle L. The interaction between blood serum and tissue extract in the coagulation of the blood: II. A comparison between the effects of the stroma of erythrocytes and of tissue extracts, unheated and heated, on the coagulation of the blood, and on the mechanism of the interaction of these substances with blood serum. J Biol Chem: 1922; 51 485 506
6. Schneider CL. The active principle of placental toxin; thromboplastin; its inactivator in blood; antithromboplastin. Am J Physiol: 1947; 149 1 123 129
7. Thomas L. Studies on the intravascular thromboplastic effect of tissue suspensions in mice: a factor in normal rabbit serum which inhibits the thromboplastic effect of the sedimentable tissue component. Bull Johns Hopkins Hosp: 1947; 81 1 26 42
8. Marciniak E, Tsukamura S. Two progressive inhibitors of factor Xa in human blood. Br J Haematol: 1972; 22 3 341 351
9. Barrowcliffe TW, Eggleton CA, Stocks J. Studies of anti-Xa activity in human plasma. II: the role of lipoproteins. Thromb Res: 1982; 27 2 185 195 (Pubitemid 12019057)
10. Carson SD. Plasma high density lipoproteins inhibit the activation of coagulation factor X by factor VIIa and tissue factor. FEBS Lett: 1981; 132 1 37 40 (Pubitemid 12248550)
11. Marlar RA, Kleiss AJ, Griffin JH. An alternative extrinsic pathway of human blood coagulation. Blood: 1982; 60 6 1353 1358 (Pubitemid 13211374)
12. Broze GJ Jr, Miletich JP. Isolation of the tissue factor inhibitor produced by HepG2 hepatoma cells. Proc Natl Acad Sci U S A: 1987; 84 7 1886 1890 (Pubitemid 17054118)
13. Hubbard AR, Jennings CA. Inhibition of tissue thromboplastin-mediated blood coagulation. Thromb Res: 1986; 42 4 489 498 (Pubitemid 16073471)
14. Hjort PF. Intermediate reactions in the coagulation of blood with tissue thromboplastin; convertin, accelerin, prothrombinase. Scand J Clin Lab Invest: 1957; 9 Suppl 27 1 183
15. Rao LV, Rapaport SI. Studies of a mechanism inhibiting the initiation of the extrinsic pathway of coagulation. Blood: 1987; 69 2 645 651 (Pubitemid 17022042)
16. Broze GJ Jr, Warren LA, Girard JJ, Miletich JP. Isolation of the lipoprotein associated coagulation inhibitor produced by HepG2 (human hepatoma) cells using bovine factor Xa affinity chromatography. Thromb Res: 1987; 48 2 253 259
17. Wun TC, Kretzmer KK, Girard TJ, Miletich JP, Broze GJ Jr. Cloning and characterization of a cDNA coding for the lipoprotein-associated coagulation inhibitor shows that it consists of three tandem Kunitz-type inhibitory domains. J Biol Chem: 1988; 263 13 6001 6004
18. Broze GJ Jr, Lange GW, Duffin KL, MacPhail L. Heterogeneity of plasma tissue factor pathway inhibitor. Blood Coagul Fibrinolysis: 1994; 5 4 551 559 (Pubitemid 24301576)
19. Hansen JB, Huseby KR, Huseby NE, Ezban M, Nordy A. Tissue factor pathway inhibitor in complex with low density lipoprotein isolated from human plasma does not possess anticoagulant function in tissue factor-induced coagulation in vitro. Thromb Res: 1997; 85 5 413 425 (Pubitemid 27191728)
20. Nordfang O, Bjrn SE, Valentin S., et al. The C-terminus of tissue factor pathway inhibitor is essential to its anticoagulant activity. Biochemistry: 1991; 30 43 10371 10376
21. Valentin S, Nordfang O, Bregengrd C, Wildgoose P. Evidence that the C-terminus of tissue factor pathway inhibitor (TFPI) is essential for its in vitro and in vivo interaction with lipoproteins. Blood Coagul Fibrinolysis: 1993; 4 5 713 720 (Pubitemid 23343394)
22. Wesselschmidt R, Likert K, Girard T, Wun TC, Broze GJ Jr. Tissue factor pathway inhibitor: the carboxy-terminus is required for optimal inhibition of factor Xa. Blood: 1992; 79 8 2004 2010
23. Piro O, Broze GJ Jr. Role for the Kunitz-3 domain of tissue factor pathway inhibitor-alpha in cell surface binding. Circulation: 2004; 110 23 3567 3572 (Pubitemid 39612572)
24. Mine S, Yamazaki T, Miyata T, Hara S, Kato H. Structural mechanism for heparin-binding of the third Kunitz domain of human tissue factor pathway inhibitor. Biochemistry: 2002; 41 1 78 85 (Pubitemid 34049383)
25. Nordfang O, Bjrn SE, Valentin S., et al. The C-terminus of tissue factor pathway inhibitor is essential to its anticoagulant activity. Biochemistry: 1991; 30 43 10371 10376
26. Wesselschmidt R, Likert K, Girard T, Wun TC, Broze GJ Jr. Tissue factor pathway inhibitor: the carboxy-terminus is required for optimal inhibition of factor Xa. Blood: 1992; 79 8 2004 2010
27. Werling RW, Zacharski LR, Kisiel W, Bajaj SP, Memoli VA, Rousseau SM. Distribution of tissue factor pathway inhibitor in normal and malignant human tissues. Thromb Haemost: 1993; 69 4 366 369 (Pubitemid 23103124)
28. Maroney SA, Haberichter SL, Friese P., et al. Active tissue factor pathway inhibitor is expressed on the surface of coated platelets. Blood: 2007; 109 5 1931 1937 (Pubitemid 46348189)
29. 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 31 18832 18837 (Pubitemid 19277636)
30. Sandset PM. Tissue factor pathway inhibitor (TFPI)an update. Haemostasis: 1996; 26 Suppl 4 154 165 (Pubitemid 26417433)
31. McGee MP, Foster S, Wang X. Simultaneous expression of tissue factor and tissue factor pathway inhibitor by human monocytes. A potential mechanism for localized control of blood coagulation. J Exp Med: 1994; 179 6 1847 1854 (Pubitemid 24155665)
32. van der Logt CP, Dirven RJ, Reitsma PH, Bertina RM. Expression of tissue factor and tissue factor pathway inhibitor in monocytes in response to bacterial lipopolysaccharide and phorbolester. Blood Coagul Fibrinolysis: 1994; 5 2 211 220 (Pubitemid 24138055)
33. Petit L, Lesnik P, Dachet C, Moreau M, Chapman MJ. Tissue factor pathway inhibitor is expressed by human monocyte-derived macrophages: relationship to tissue factor induction by cholesterol and oxidized LDL. Arterioscler Thromb Vasc Biol: 1999; 19 2 309 315 (Pubitemid 29072744)
34. 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 U S A: 1990; 87 22 8869 8873 (Pubitemid 120007610)
35. Bajaj MS, Steer S, Kuppuswamy MN, Kisiel W, Bajaj SP. Synthesis and expression of tissue factor pathway inhibitor by serum-stimulated fibroblasts, vascular smooth muscle cells and cardiac myocytes. Thromb Haemost: 1999; 82 6 1663 1672
36. Broze GJ Jr, Girard TJ, Novotny WF. Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistry: 1990; 29 33 7539 7546 (Pubitemid 20279168)
37. Iversen N, Sandset PM, Abildgaard U, Torjesen PA. Binding of tissue factor pathway inhibitor to cultured endothelial cells-influence of glycosaminoglycans. Thromb Res: 1996; 84 4 267 278 (Pubitemid 26417656)
38. Lupu C, Goodwin CA, Westmuckett AD., et al. Tissue factor pathway inhibitor in endothelial cells colocalizes with glycolipid microdomains/ caveolae. Regulatory mechanism(s) of the anticoagulant properties of the endothelium. Arterioscler Thromb Vasc Biol: 1997; 17 11 2964 2974 (Pubitemid 28016049)
39. Sevinsky JR, Rao LV, Ruf W. Ligand-induced protease receptor translocation into caveolae: a mechanism for regulating cell surface proteolysis of the tissue factor-dependent coagulation pathway. J Cell Biol: 1996; 133 2 293 304 (Pubitemid 26131614)
40. Lupu C, Lupu F, Dennehy U, Kakkar VV, Scully MF. Thrombin induces the redistribution and acute release of tissue factor pathway inhibitor from specific granules within human endothelial cells in culture. Arterioscler Thromb Vasc Biol: 1995; 15 11 2055 2062
41. Marutsuka K, Hatakeyama K, Yamashita A, Sato Y, Sumiyoshi A, Asada Y. Adrenomedullin augments the release and production of tissue factor pathway inhibitor in human aortic endothelial cells. Cardiovasc Res: 2003; 57 1 232 237 (Pubitemid 36009455)
42. Hansen JB, Svensson B, Olsen R, Ezban M, Osterud B, Paulssen RH. Heparin induces synthesis and secretion of tissue factor pathway inhibitor from endothelial cells in vitro. Thromb Haemost: 2000; 83 6 937 943 (Pubitemid 30411697)
43. Lupu C, Poulsen E, Roquefeuil S, Westmuckett AD, Kakkar VV, Lupu F. Cellular effects of heparin on the production and release of tissue factor pathway inhibitor in human endothelial cells in culture. Arterioscler Thromb Vasc Biol: 1999; 19 9 2251 2262 (Pubitemid 29422260)
44. Bara L, Bloch MF, Zitoun D., et al. Comparative effects of enoxaparin and unfractionated heparin in healthy volunteers on prothrombin consumption in whole blood during coagulation, and release of tissue factor pathway inhibitor. Thromb Res: 1993; 69 5 443 452 (Pubitemid 23102564)
45. Kijowski R, Hoppensteadt D, Walenga J, Borris L, Lassen MR, Fareed J. Role of tissue factor pathway inhibitor in post surgical deep venous thrombosis (DVT) prophylaxis in patients treated with low molecular weight heparin. Thromb Res: 1994; 74 1 53 64 (Pubitemid 24257428)
46. Samama MM, Bara L, Gerotziafas GT. Mechanisms for the antithrombotic activity in man of low molecular weight heparins (LMWHs). Haemostasis: 1994; 24 2 105 117 (Pubitemid 24234488)
47. Hansen JB, Huseby KR, Huseby NE, Ezban M, Nordy A. Tissue factor pathway inhibitor in complex with low density lipoprotein isolated from human plasma does not possess anticoagulant function in tissue factor-induced coagulation in vitro. Thromb Res: 1997; 85 5 413 425 (Pubitemid 27191728)
48. Lesnik P, Vonica A, Gurin M, Moreau M, Chapman MJ. Anticoagulant activity of tissue factor pathway inhibitor in human plasma is preferentially associated with dense subspecies of LDL and HDL and with Lp(a). Arterioscler Thromb: 1993; 13 7 1066 1075 (Pubitemid 23195809)
49. Ellery PE, Hardy K, Oostryck R, Adams MJ. Further insight into the heparin-releasable and glycosylphosphatidylinositollipid-anchored forms of tissue factor pathway inhibitor. Clin Appl Thromb Hemost: 2008; 14 3 267 278 (Pubitemid 351871936)
50. Maroney SA, Cunningham AC, Ferrel J., et al. A GPI-anchored co-receptor for tissue factor pathway inhibitor controls its intracellular trafficking and cell surface expression. J Thromb Haemost: 2006; 4 5 1114 1124
51. 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 12 2099 2104 (Pubitemid 36025221)
52. Ott I, Miyagi Y, Miyazaki K., et al. Reversible regulation of tissue factor-induced coagulation by glycosyl phosphatidylinositol-anchored tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol: 2000; 20 3 874 882 (Pubitemid 30151706)
53. Zhang J, Piro O, Lu L, Broze GJ Jr. Glycosyl phosphatidylinositol anchorage of tissue factor pathway inhibitor. Circulation: 2003; 108 5 623 627 (Pubitemid 36961180)
54. Maroney SA, Ellery PE, Mast AE. Alternatively spliced isoforms of tissue factor pathway inhibitor. Thromb Res: 2010; 125 Suppl 1 S52 S56
55. O'Brien LM, Mastri M, Fay PJ. Regulation of factor VIIIa by human activated protein C and protein S: inactivation of cofactor in the intrinsic factor Xase. Blood: 2000; 95 5 1714 1720 (Pubitemid 30120834)
56. Rosing J, Hoekema L, Nicolaes GA., et al. Effects of protein S and factor Xa on peptide bond cleavages during inactivation of factor Va and factor VaR506Q by activated protein C. J Biol Chem: 1995; 270 46 27852 27858
57. Comp PC, Esmon CT. Recurrent venous thromboembolism in patients with a partial deficiency of protein S. N Engl J Med: 1984; 311 24 1525 1528 (Pubitemid 15223250)
58. Comp PC, Nixon RR, Cooper MR, Esmon CT. Familial protein S deficiency is associated with recurrent thrombosis. J Clin Invest: 1984; 74 6 2082 2088 (Pubitemid 15197352)
59. Schwarz HP, Fischer M, Hopmeier P, Batard MA, Griffin JH. Plasma protein S deficiency in familial thrombotic disease. Blood: 1984; 64 6 1297 1300 (Pubitemid 15224546)
60. van't Veer C, Hackeng TM, Biesbroeck D, Sixma JJ, Bouma BN. Increased prothrombin activation in protein S-deficient plasma under flow conditions on endothelial cell matrix: an independent anticoagulant function of protein S in plasma. Blood: 1995; 85 7 1815 1821
61. Hackeng TM, Ser KM, Tans G, Rosing J. Protein S stimulates inhibition of the tissue factor pathway by tissue factor pathway inhibitor. Proc Natl Acad Sci U S A: 2006; 103 9 3106 3111 (Pubitemid 43346432)
62. Ndonwi M, Broze G Jr. Protein S enhances the tissue factor pathway inhibitor inhibition of factor Xa but not its inhibition of factor VIIa-tissue factor. J Thromb Haemost: 2008; 6 6 1044 1046 (Pubitemid 351689932)
63. Castoldi E, Simioni P, Tormene D, Rosing J, Hackeng TM. Hereditary and acquired protein S deficiencies are associated with low TFPI levels in plasma. J Thromb Haemost: 2010; 8 2 294 300
64. Giesen PL, Rauch U, Bohrmann B., et al. Blood-borne tissue factor: another view of thrombosis. Proc Natl Acad Sci U S A: 1999; 96 5 2311 2315 (Pubitemid 29117911)
65. Mast AE, Stadanlick JE, Lockett JM, Dietzen DJ, Hasty KA, Hall CL. Tissue factor pathway inhibitor binds to platelet thrombospondin-1. J Biol Chem: 2000; 275 41 31715 31721
66. Crawley JT, Lane DA. The haemostatic role of tissue factor pathway inhibitor. Arterioscler Thromb Vasc Biol: 2008; 28 2 233 242 (Pubitemid 351161194)
67. Arins RA, Alberio G, Moia M, Mannucci PM. Low levels of heparin-releasable tissue factor pathway inhibitor in young patients with thrombosis. Thromb Haemost: 1999; 81 2 203 207 (Pubitemid 29078303)
68. Dahm A, Van Hylckama Vlieg A, Bendz B, Rosendaal F, Bertina RM, Sandset PM. Low levels of tissue factor pathway inhibitor (TFPI) increase the risk of venous thrombosis. Blood: 2003; 101 11 4387 4392 (Pubitemid 36857803)
69. Llobet D, Falkon L, Mateo J., et al. Low levels of tissue factor pathway inhibitor (TFPI) in two out of three members of a family with thrombophilia. Thromb Res: 1995; 80 5 413 418
70. Adams MJ, Oostryck R. A comparative study of functional assays for tissue factor pathway inhibitor using normal plasma and clinical samples. Blood Coagul Fibrinolysis: 2000; 11 4 327 333 (Pubitemid 30396478)
71. Bognacki J, Hammelburger J. Functional and immunologic methods for the measurement of human tissue factor pathway inhibitor. Blood Coagul Fibrinolysis: 1995; 6 Suppl 1 S65 S72
72. Skretting G, Stavik B, Landvik NE., et al. Functional characterization of polymorphisms in the human TFPI gene. Biochem Biophys Res Commun: 2010; 397 1 106 111
73. Amini Nekoo A, Iles D. Analysis of a T-287C polymorphism in the tissue factor pathway inhibitor gene and identification of a repressor element in the promoter. Thromb Res: 2008; 121 6 813 819 (Pubitemid 351491295)
74. Eitzman DT, Westrick RJ, Bi X., et al. Lethal perinatal thrombosis in mice resulting from the interaction of tissue factor pathway inhibitor deficiency and factor V Leiden. Circulation: 2002; 105 18 2139 2142 (Pubitemid 34517155)
75. Lincz LF, Adams MJ, Scorgie FE, Thom J, Baker RI, Seldon M. Polymorphisms of the tissue factor pathway inhibitor gene are associated with venous thromboembolism in the antiphospholipid syndrome and carriers of factor V Leiden. Blood Coagul Fibrinolysis: 2007; 18 6 559 564 (Pubitemid 47344304)
76. Bajaj MS, Bajaj SP. Tissue factor pathway inhibitor: potential therapeutic applications. Thromb Haemost: 1997; 78 1 471 477 (Pubitemid 27289287)
77. Holst J, Lindblad B, Bergqvist D., et al. Antithrombotic effect of recombinant truncated tissue factor pathway inhibitor (TFPI1-161) in experimental venous thrombosisa comparison with low molecular weight heparin. Thromb Haemost: 1994; 71 2 214 219 (Pubitemid 24047330)
78. Spokas EG, Wun TC. Venous thrombosis produced in the vena cava of rabbits by vascular damage and stasis. J Pharmacol Toxicol Methods: 1992; 27 4 225 232
79. Bregengrd C, Nordfang O, Wildgoose P, Svendsen O, Hedner U, Diness V. The effect of two-domain tissue factor pathway inhibitor on endotoxin-induced disseminated intravascular coagulation in rabbits. Blood Coagul Fibrinolysis: 1993; 4 5 699 706 (Pubitemid 23343392)
80. Camerota AJ, Creasey AA, Patla V, Larkin VA, Fink MP. Delayed treatment with recombinant human tissue factor pathway inhibitor improves survival in rabbits with gram-negative peritonitis. J Infect Dis: 1998; 177 3 668 676 (Pubitemid 28099881)
81. Abendschein DR, Meng YY, Torr-Brown S, Sobel BE. Maintenance of coronary patency after fibrinolysis with tissue factor pathway inhibitor. Circulation: 1995; 92 4 944 949
82. Badimon JJ, Lettino M, Toschi V., et al. Local inhibition of tissue factor reduces the thrombogenicity of disrupted human atherosclerotic plaques: effects of tissue factor pathway inhibitor on plaque thrombogenicity under flow conditions. Circulation: 1999; 99 14 1780 1787 (Pubitemid 29181404)
83. Brown DM, Kania NM, Choi ET., et al. Local irrigation with tissue factor pathway inhibitor inhibits intimal hyperplasia induced by arterial interventions. Arch Surg: 1996; 131 10 1086 1090 (Pubitemid 26338104)
84. Haskel EJ, Torr SR, Day KC., et al. Prevention of arterial reocclusion after thrombolysis with recombinant lipoprotein-associated coagulation inhibitor. Circulation: 1991; 84 2 821 827
85. Khouri RK, Sherman R, Buncke HJ Jr., et al. A phase II trial of intraluminal irrigation with recombinant human tissue factor pathway inhibitor to prevent thrombosis in free flap surgery. Plast Reconstr Surg: 2001; 107 2 408 415, discussion 416-418 (Pubitemid 32125282)
86. de Jonge E, Dekkers PE, Creasey AA., et al. Tissue factor pathway inhibitor dose-dependently inhibits coagulation activation without influencing the fibrinolytic and cytokine response during human endotoxemia. Blood: 2000; 95 4 1124 1129 (Pubitemid 30099814)
87. Abraham E, Reinhart K, Opal S., et al. OPTIMIST Trial Study Group. 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)
88. Abraham E, Reinhart K, Svoboda P., et al. 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 11 2081 2089 (Pubitemid 33063534)
89. Laterre PF. Beyond antibiotics in severe community-acquired pneumonia: the role and rationale for tissue factor pathway inhibition. Crit Care: 2008; 12 Suppl 6 S4
90. Wunderink RG, Laterre PF, Francois B., et al. CAPTIVATE Trial Group. Recombinant tissue factor pathway inhibitor in severe community-acquired pneumonia: a randomized trial. Am J Respir Crit Care Med: 2011; 183 11 1561 1568
91. Adams M. Novel considerations in the pathogenesis of the antiphospholipid syndrome: involvement of the tissue factor pathway of blood coagulation. Semin Thromb Hemost: 2008; 34 3 251 255