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Thromb Haemost 1997; 78(01): 471-477
DOI: 10.1055/s-0038-1657572
Tissue factor pathway inhibitor: a protein in search for a disease
Schattauer GmbH Stuttgart

Tissue Factor Pathway Inhibitor: Potential Therapeutic Applications

Madhu S Bajaj
Department of Internal Medicine, Saint Louis University School of Medicine, Saint Louis, MO, USA
,
S Paul Bajaj
Department of Internal Medicine, Saint Louis University School of Medicine, Saint Louis, MO, USA
› Author Affiliations
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Publication History

Publication Date:
12 July 2018 (online)

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  • References

  • 1 Bajaj MS, Ameri A, Bajaj SP. Tissue factor pathway inhibitor - a regulator of tissue factor induced coagulation. In: Anti-coagulants: Physiologic, pathologic and pharmacologic. Green D. (ed). CRC Press; FL: 1994. p 41-65
    Google Scholar
  • 2 Rapaport SI, Rao LVM. The tissue factor pathway: How it has become a “prima ballerina”. Thromb Haemost 1995; 74: 7-717
    PubMedGoogle Scholar
  • 3 Broze Jr GJ. Tissue factor pathway inhibitor. Thromb Haemost 1995; 74: 90-93
    PubMedGoogle Scholar
  • 4 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 Nad Acad Sci USA 1990; 87: 8869-8873
    CrossrefPubMedGoogle Scholar
  • 5 Broze Jr GJ, Girard TJ, Novotny WF. Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistiy 1990; 29: 7539-7546
    PubMedGoogle Scholar
  • 6 Enjyoji K, Miyata T, Kamikubo Y, Kato H. Effect of heparin on the inhibition of factor Xa by tissue factor pathway inhibitor: a segment, Gly 212-Phe 243, of the third Kunitz domain is a heparin binding site. Biochemistry 1995; 34: 5725-5735
    CrossrefPubMedGoogle Scholar
  • 7 Broze Jr GJ, Lange GW, Duffin KL, MacPhail L. Heterogeneity of plasma tissue factor pathway inhibitor. Blood Coagul Fibrinolysis 1994; 5: 551-559
    PubMedGoogle Scholar
  • 8 Nordfang O, Bjom SE, Valantin S, Nielsen LS, Wildgoose P, Beck TC, Hedner U. The C-terminus of tissue factor pathway inhibitor is essential to its anticoagulant activity. Biochemistry 1991; 30: 10371-10376
    CrossrefPubMedGoogle Scholar
  • 9 Sandset PM, Wam-Cramer BJ, Maki SL, Rapaport SI. Immunodepletion of extrinsic pathway inhibitor sensitizes rabbits to endotoxin-induced intravascular coagulation and the generalized Schwartzman reaction. Blood 1991; 78: 1496-502
    PubMedGoogle Scholar
  • 10 Sandset PM, Wam-Cramer BJ, Rao LVM, Maki SI, Rapaport SI. Depletion of extrinsic pathway inhibitor (EPI) sensitizes rabbits to disseminated intravascular coagulation induced with tissue factor: Evidence supporting a physiologic role for EPI as a natural anticoagulant. Proc Natl Acad Sci USA 1991; 88: 708-12
    CrossrefPubMedGoogle Scholar
  • 11 Girard TJ. Tissue factor pathway inhibitor. In: Novel Therapeutic Agents in Thrombosis and Thrombolysis. Sasahara A, Loscalzo J. (eds). Marcel Dekker; New York: 1997. p 225-260
    Google Scholar
  • 12 Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci USA 1989; 86: 2839-2843
    CrossrefPubMedGoogle Scholar
  • 13 Osterud B, Flaegstad T. Increased thromboplastin activity in monocytes of patients with meningococcal infection: related to an unfavorable prognosis. Thromb Haemost 1983; 49: 5-7
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Sandset PM, Roise O, Aasen AO, Abildgaard U. Extrinsic pathway inhibitor in post operative/post traumatic septicemia: increased levels in fatal cases. Haemostasis 1989; 19: 189-195
    PubMedGoogle Scholar
  • 15 Rao LVM. Tissue factor as a tumor procoagulant. Cancer Metastasis Rev 1992; 11: 249-266
    CrossrefPubMedGoogle Scholar
  • 16 Idell S. Extravascular coagulation and fibrin deposition in acute lung injury. New Horiz 1994; 2: 566-574
    PubMedGoogle Scholar
  • 17 Tipping PG, Erlich JH, Apostolopoulos J, Mackman N, Loskutoff D, Holdsworth SR. Glomerular tissue factor expression in crescentic glomerulonephritis — correlations between antigen, activity, and mRNA. Am J Pathol 1995; 147: 1736-1748
    PubMedGoogle Scholar
  • 18 Werlin 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: 366-369
    Article in Thieme ConnectPubMedGoogle Scholar
  • 19 Bajaj MS, Sabharwal AK, Kuppuswamy MN, Bajaj SP. Synthesis of tissue factor pathway inhibitor by serum stimulated fibroblasts. Circulation 1996; 94: 1-741
    CrossrefPubMedGoogle Scholar
  • 20 Bajaj MS, Ameri A, Kuppuswamy MN, Bajaj SP. Expression of Tissue Factor Pathway Inhibitor (TFPI) and GATA-2 transcription factor by activated human monocytes. Blood 1993; 82: 343 (a)
    PubMedGoogle Scholar
  • 21 Ameri A, Kuppuswamy MN, Basu S, Bajaj SP. Expression of tissue factor pathway inhibitor by cultured endothelial cells in response to inflammatory mediators. Blood 1992; 79: 3219-3226
    PubMedGoogle Scholar
  • 22 Callander NS, Rao LVM, Nordfang O, Sandset PM, Wam-Cramer B, Rapaport SI. Mechanism of binding of recombinant extrinsic pathway inhibitor (rEPI) to cultured cell surfaces: Evidence that rEPI can bind to and inhibit factor VIIa-tissue factor complexs in the absence of factor Xa. J Biol Chem 1992; 267: 876-882
    PubMedGoogle Scholar
  • 23 Holst J, Lindblad B, Westerlund G, Bregengaard C, Ezban M, Ostergaard PB, Nordfang O, Hedner U. Pharmacokinetics and delayed experimental antithrombotic effect of two domain non-glycosylated tissue factor pathway inhibitor. Thromb Res 1996; 81: 461-470
    CrossrefPubMedGoogle Scholar
  • 24 Fuster V. Mechanisms leading to myocardial infarction: insights from studies of vascular biology. Circulation 1994; 90: 2126-2146
    CrossrefPubMedGoogle Scholar
  • 25 Eisenberg PR, Sherman LA, Schectman K, Perez J, Sobel BE, Jaffe AS. Fibrinopeptide A: a marker of acute coronary thrombosis. Circulation 1985; 71: 912-918
    CrossrefPubMedGoogle Scholar
  • 26 Kruskal JB, Commerford PJ, Franks JJ, Kirsch RE. Fibrin and fibrinogen-related antigens in patients with stable and unstable coronary artery disease. N Engl J Med 1987; 317: 1361-1365
    CrossrefPubMedGoogle Scholar
  • 27 Merlini PA, Bauer KA, Oltrona L, Ardissino D, Cattaneo M, Belli C, Mannucci PM, Rosenberg RD. Persistent activation of coagulation mechanism in unstable angina and myocardial infarction. Circulation 1994; 90: 61-68
    CrossrefPubMedGoogle Scholar
  • 28 Tipping PG, Malliaros J, Holdsworth SR. Procoagulant activity expression by macrophages from atheromatous vascular plaques. Atherosclerosis 1989; 79: 237-243
    CrossrefPubMedGoogle Scholar
  • 29 Femandez-Ortiz A, Badimon J, Falk E, Fuster V, Meyer B, Mailhac A, Weng D, Shah PK, Badimon L. Characterizations of the relative thrombogenicity of atherosclerotic plaque components: implications for consequences of plaque rupture. J Am Coll Cardiol 1994; 23: 1562-1569
    CrossrefPubMedGoogle Scholar
  • 30 Chesebro JH, Toschi V, Lettino M, Gallo R, Badimon JJ, Fallon JT, Fuster V. Evolving concepts in the pathogenesis and treatment of arterial thrombosis (Grand rounds). Mt. Sinai J Med 1995; 62: 275-286
    PubMedGoogle Scholar
  • 31 Jang IK, Gold HK, Leinbach RC, Fallon JT, Collen D, Wilcox JN. Antithrombotic effect of a monoclonal antibody against tissue factor in a rabbit model of platelet-mediated arterial thrombosis. Arterioscler Thromb 1992; 12: 948-954
    CrossrefPubMedGoogle Scholar
  • 32 Pawashe AB, Golino P, Ambrosio G, Migliaccio F, Ragni M, Pascucci I, Chiariello M, Bach R, Garen A, Konigsberg WK, Ezekowitz MD. A monoclonal antibody against rabbit tissue factor inhibits thrombus formation in stenotic injured rabbit carotid arteries. Circ Res 1994; 74: 56-63
    CrossrefPubMedGoogle Scholar
  • 33 Speidel CM, Eisenberg PR, Ruf W, Edgington TS, Abendschein DR. Tissue factor mediates prolonged procoagulant activity on the luminal surface of balloon-injured aortas in rabbits. Circulation 1995; 92: 3323-3330
    CrossrefPubMedGoogle Scholar
  • 34 Van’TVeer C, Hackeng TM, Delahaye C, Sixma JJ, Bouma BN. Activated factor X and thrombin formation triggered by tissue factor on endothelial cell matrix in a flow model: Effect of tissue factor pathway inhibitor. Blood 1994; 84: 1132-1142
    PubMedGoogle Scholar
  • 35 Haskel EJ, Torr SR, Day KC, Palmier MO, Wun T-C, Sobel BE, Abendschein DR. Prevention of arterial reocclusion after thrombolysis with recombinant lipoprotein- associated coagulation inhibitor. Circulation 1991; 84: 821-827
    CrossrefPubMedGoogle Scholar
  • 36 Abendschein DR, Meng YY, Torr-Brown S, Sobel BE. Maintenance of coronary patency after fibrinolysis with tissue factor pathway inhibitor. Circulation 1995; 92: 944-999
    CrossrefPubMedGoogle Scholar
  • 37 Eisenberg PR. Current concepts in coronary thrombolysis (Review). Hematol Oncol Clin North Am 1992; 06: 1161-1170
    CrossrefPubMedGoogle Scholar
  • 38 Jang Y, Guzman LA, Lincoff M, Gottsauner WM, Forudi F, Hart CE, Courtman DW, Ezban M, Ellis SG, Topol EJ. Influence of blockade at specific levels of the coagulation cascade on restenosis in a rabbit atherosclerotic femoral artery injury model. Circulation 1995; 92: 3041-3050
    CrossrefPubMedGoogle Scholar
  • 39 Khouri RK, Brown DM, Choi ET, Kania NM, Pasia EN, Lantieri LA. Local applications of tissue factor pathway inhibitor (TFPI) inhibits intimal hyperplasia induced by arterial interventions. Surgical Forum 1995; 46: 389-391
    PubMedGoogle Scholar
  • 40 Khouri RK, Koudsi B, Kaiding F, Omberg RL, Wun T-C. Prevention of thrombosis by topical application of tissue factor pathway inhibitor in a rabbit model of vascular trauma. Ann Plast Surg 1993; 30: 398-404
    CrossrefPubMedGoogle Scholar
  • 41 Ozbeck MR, Brown DM, Deune EG, Lantieri LA, Kania NM, Pasia EN, Cooley BC, Wun TC, Khouri RK. Topical tissue factor pathway inhibitor improves free-flap survival in a model simu-lating free-flap errors. J. Reconstr Microsurg 1995; 11: 185-188
    Article in Thieme ConnectPubMedGoogle Scholar
  • 42 Dumanian GA, Heil BV, Khouri RK, Hong C, Labadie K, Wun T-C, Johnson PC. Tissue factor and its inhibition at the human microvascular anastomosis. J Surg Res 1996; 60: 263-269
    CrossrefPubMedGoogle Scholar
  • 43 Del ZoppoGJ, Copelan BR, Harker LA, Waltz TA, Zyroff J, Hanson SR, Battenberg E. Experimental acute thrombotic stroke in baboons. Stroke 1986; 17: 1254-1265
    CrossrefPubMedGoogle Scholar
  • 44 Thomas WS, Mori E, Copeland BR, Yu JQ, Morrissey JH, Del Zoppo GJ. Tissue factor contributes to microvascular defects after focal cerebral ischemia. Stroke 1993; 24: 847-854
    CrossrefPubMedGoogle Scholar
  • 45 Ragni M, Cirillo P, Pascucci I, Scognamiglio A, D’Andrea D, Eramo N, Ezekowitz MD, Pawashe AB, Chiariello M, Golino P. Monoclonal antibody against tissue factor shortens tissue plasminogen activater lysis time and prevents reocclusion in a rabbit model of carotid artery thrombosis. Circulation 1996; 93: 1913-1918
    CrossrefPubMedGoogle Scholar
  • 46 Koudsi B, Chatman DM, Ballinger BA, Ferguson EW, Kraemer BA, Miller GA, Wun T-C, Farr G, Money SR. Tissue factor pathway inhibitor protects the ischemic spinal cord. J Surg Res 1996; 63: 174-178
    CrossrefPubMedGoogle Scholar
  • 47 Kraemer BA, Yu CD, Omberg RL, Wun T-C, Koudsi BM. The effects of tissue factor pathway inhibitor (TFPI) on tissue ischemia and reperfusion in a rabbit ear model. Surgical Forum 1995; 46: 738-740
    PubMedGoogle Scholar
  • 48 Taylor Jr FB. Studies on the inflammatory-coagulant axis in the baboon response toE.coli: Regulatory roles of proteins C, S, C4bBP and of inhibitors of tissue factor. Prog Clin Biol Res 1994; 388: 175-194
    PubMedGoogle Scholar
  • 49 Wildgoose P, Bregengard C, Nordfang O. Infusion of inactivated factor VIIa inhibits endotoxin-induced disseminated intravascular coagulation in rabbits. Thromb Haemost 1993; 69: 852 (a)
    Article in Thieme ConnectPubMedGoogle Scholar
  • 50 Bregengard 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 coagula-tion in rabbits. Blood Coagul Fibrinolysis 1993; 4: 699-706
    CrossrefPubMedGoogle Scholar
  • 51 Taylor Jr FB, Chang A, Ruf W, Morrissey JH, Hinshaw L, Catlett R, Blick K, Edgington TS. Lethal E.coli septic shock is prevented by blocking tissue factor with monoclonal antibody. Circ Shock 1991; 33: 127-134
    PubMedGoogle Scholar
  • 52 Creasey AA, Chang ACK, Feigen L, Wun T-C, Taylor Jr FB, Hinshaw LB. Tissue factor pathway inhibitor reduces mortality fromEscherichia coliseptic shock. J Clin Invest 1993; 91: 2850-2860
    CrossrefPubMedGoogle Scholar
  • 53 Carr C, Bild GS, Chang ACK, Peer GT, Palmier MO, Frazier RB, Gustafson ME, Wun T-C, Creasey AA, Hinshaw LB, Taylor Jr FB, Galluppi GR. RecombinantE.coli-derived tissue factor pathway inhibitor reduces coagulopathic and lethal effects in the baboon gram-negative model of septic shock. Circ Shock 1995; 44: 126-137
    PubMedGoogle Scholar
  • 54 Levi M, ten CateH, Bauer KA, van der Poll T, Edgington TS, Buller HR, van Deventer SJH, Hack CE, ten Cate JW, Rosenberg RD. Inhibition of Endotoxin-induced activation of coagulation and fibrinolysis by Pentoxifylline or by a monoclonal anti-tissue factor antibody in chimpanzees. J Clin Invest 1994; 93: 114-120
    CrossrefPubMedGoogle Scholar
  • 55 Biemond BJ, Levi M, ten Cate H, Soule HR, Morris LD, Foster DL, Bogowitz CA, van der Poll T, Buller HR, ten Cate JW. Complete inhibition of endotoxin-induced coagulation activation in chimpanzees with a monoclonal Fab fragment against factor VII/VIIa. Thromb Haemost 1995; 73: 223-230
    Article in Thieme ConnectPubMedGoogle Scholar
  • 56 Johnson K, Aarden L, Choi Y, Groot Ed, Creasey A. The proinflammatory cytokine response to coagulation and endotoxin in whole blood. Blood 1996; 87: 5051-5060
    PubMedGoogle Scholar
  • 57 Bone RC, Francis PB, Pierce AK. Intravascular coagulation associated with adult respiratory distress syndrome. Am J Med 1976; 61: 585-589
    CrossrefPubMedGoogle Scholar
  • 58 Idell S, James KK, Levin EG, Schwartz BS, Manchanda N, Maunder RJ, Martin TR, McLarty J, Fair DS. Local abnor-malities in coagulation and fibrinolytic pathways predispose to alveolar fibrin deposition in the adult respiratory distress syndrome. J Clin Invest 1989; 84: 695-705
    CrossrefPubMedGoogle Scholar
  • 59 Sabharwal AK, Bajaj SP, Ameri A, Tricomi SM, Hyers TM, Dahms TE, Taylor Jr FB, Bajaj MS. Tissue factor pathway inhibitor and von Willebrand factor antigen levels in adult respiratory distress syndrome and in a primate model of sepsis. Am J Respir Crit Care Med 1995; 151: 758-767
    CrossrefPubMedGoogle Scholar
  • 60 Spokas EG, Wun T-C. Venous thrombosis produced in the vena cava of rabbits by vascular damage and stasis. J Pharmacol Toxicol Methods 1992; 27: 225-232
    CrossrefPubMedGoogle Scholar
  • 61 Holst J, Lindblad B, Bergqvist D, Nordfang O, Ostergaard PB, Petersen JG, Nielsen G, Hedner U. Antithrombotic effect of recombinant truncated tissue factor pathway inhibitor (TFPI 10-161) in experimental venous thrombosis — a comparison with low molecular weight heparin. Thromb Haemost 1994; 71: 214-219
    Article in Thieme ConnectPubMedGoogle Scholar
  • 62 Holst J, Lindblad B, Bergqvist D, Nordfang O, Ostergaard PB, Petersen JG, Nielsen G, Hedner U. Antithrombotic properties of a truncated recombinant tissue factor pathway inhibitor in an experimental venous thrombosis model. Haemostasis 1993; 23 (Suppl. 01) 112-117
    PubMedGoogle Scholar
  • 63 Callander NS, Varki N, Rao LV. Immunohistochemical identification of tissue factor in solid tumors. Cancer 1992; 70: 1194-1201
    CrossrefPubMedGoogle Scholar
  • 64 Lindahl AK, Sandset PM, Abildgaard U. Indices of hyper-coagulation in cancer as compared with those in acute inflammation and acute infarction. Haemostasis 1990; 20: 253-262
    PubMedGoogle Scholar
  • 65 Kakkar AK, DeRuvo N, Chinswangwatanakul V, Tebbutt S, Williamson RC. Extrinsic-pathway activation in cancer with high factor VIIa and tissue factor. Lancet 1995; 346: 1004-1005
    CrossrefPubMedGoogle Scholar
  • 66 Lindahl AK, Sandset PM, Abildgaard V, Andersson TR, Harbitz TB. High plasma levels of extrinsic pathway inhibitor and low levels of other coagulation inhibitors in advanced cancer. Acta Chir Scand 1989; 155: 389-393
    PubMedGoogle Scholar
  • 67 Contrino J, Hair G, Kreutzer DL, Rickies FR. In situ detection of tissue factor in vascular endothelial cells: correlation with malignant phenotype of human breast disease. Nat Med 1996; 2: 209-215
    CrossrefPubMedGoogle Scholar
  • 68 Zhang Y, Deng Y, Luther T, Muller M, Ziegler R, Waldherr R, Stem DM. Tissue factor controls the balance of angiogenic and antiangiogenic properties of tumor cells in mice. J Clin Invest 1994; 94: 1320-1327
    CrossrefPubMedGoogle Scholar
  • 69 Bromberg ME, Konisberg WH, Madison JF, Pawashe A, Goren A. Tissue factor promotes melanoma metastases by a pathway independent of blood coagulation. Proc Natl Acad Sci USA 1995; 92: 8205-8209
    CrossrefPubMedGoogle Scholar