Inhibition of tissue factor: Factor VIIa-catalyzed factor IX and factor X activation by TFPI and TFPI constructs

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 11, 2014, Pages 1826-1837

  Peraramelli, S ^a   Thomassen, S ^a   Heinzmann, A ^a   Rosing, J ^a   Hackeng, T M ^a   Hartmann, R ^b   Scheiflinger, F ^b   Dockal, M ^b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b BAXTER INNOVATIONS GMBH   (Austria)

Author keywords

Factor IX; Factor X; Phospholipids; Protein S; TFPI

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 10A INHIBITOR; BLOOD CLOTTING FACTOR 7A; BLOOD CLOTTING FACTOR 9A; LIPOPROTEIN; LIPOPROTEIN-ASSOCIATED COAGULATION INHIBITOR; PHOSPHOLIPID; PROTEIN BINDING; PROTEIN S; RECOMBINANT PROTEIN; THROMBOPLASTIN;

ANTAGONISTS AND INHIBITORS; BLOOD CLOTTING; CATALYSIS; DOSE RESPONSE; DRUG EFFECTS; HUMAN; KINETICS; METABOLISM; PROTEIN DOMAIN;

BLOOD COAGULATION; CATALYSIS; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR IXA; FACTOR VIIA; FACTOR XA; FACTOR XA INHIBITORS; HUMANS; KINETICS; LIPOPROTEINS; PHOSPHOLIPIDS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN S; RECOMBINANT PROTEINS; THROMBOPLASTIN;

EID: 84920285249     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12713     Document Type: Article

References (48)

1. Osterud B, Rapaport SI. Activation of factor IX by the reaction product of tissue factor and factor VII: additional pathway for initiating blood coagulation. Proc Natl Acad Sci U S A 1977; 74: 5260-4.
2. Silverberg SA, Nemerson Y, Zur M. Kinetics of the activation of bovine coagulation factor X by components of the extrinsic pathway. Kinetic behavior of two-chain factor VII in the presence and absence of tissue factor. J Biol Chem 1977; 252: 8481-8.
3. 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: 6001-4.
4. Chang JY, Monroe DM, Oliver JA, Roberts HR. TFPIbeta, a second product from the mouse tissue factor pathway inhibitor (TFPI) gene. Thromb Haemost 1999; 81: 45-9.
5. Zhang J, Piro O, Lu L, Broze GJ Jr. Glycosyl phosphatidylinositol anchorage of tissue factor pathway inhibitor. Circulation 2003; 108: 623-7.
6. Maroney SA, Ellery PE, Mast AE. Alternatively spliced isoforms of tissue factor pathway inhibitor. Thromb Res 2010; 125(Suppl 1): S52-6.
7. Broze GJ Jr, Warren LA, Novotny WF, Higuchi DA, Girard JJ, Miletich JP. The lipoprotein-associated coagulation inhibitor that inhibits the factor VII-tissue factor complex also inhibits factor Xa: insight into its possible mechanism of action. Blood 1988; 71: 335-43.
8. 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.
9. Ndonwi M, Tuley EA, Broze GJ Jr. The Kunitz-3 domain of TFPI-alpha is required for protein S-dependent enhancement of factor Xa inhibition. Blood 2010; 116: 1344-51.
10. 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: 2004-10.
11. Huang ZF, Wun TC, Broze GJ Jr. Kinetics of factor Xa inhibition by tissue factor pathway inhibitor. J Biol Chem 1993; 268: 26950-5.
12. Broze GJ Jr, Girard TJ, Novotny WF. Regulation of coagulation by a multivalent Kunitz-type inhibitor. Biochemistry 1990; 29: 7539-46.
13. Pedersen AH, Nordfang O, Norris F, Wiberg FC, Christensen PM, Moeller KB, Meidahl-Pedersen J, Beck TC, Norris K, Hedner U. Recombinant human extrinsic pathway inhibitor. Production, isolation, and characterization of its inhibitory activity on tissue factor-initiated coagulation reactions. J Biol Chem 1990; 265: 16786-93.
14. Callander NS, Rao LV, Nordfang O, Sandset PM, Warn-Cramer B, Rapaport SI. Mechanisms of binding of recombinant extrinsic pathway inhibitor (rEPI) to cultured cell surfaces. Evidence that rEPI can bind to and inhibit factor VIIa-tissue factor complexes in the absence of factor Xa. J Biol Chem 1992; 267: 876-82.
15. Peraramelli S, Thomassen S, Heinzmann A, Rosing J, Hackeng TM, Hartmann R, Scheiflinger F, Dockal M. Direct inhibition of factor VIIa by TFPI and TFPI constructs. J Thromb Haemost 2013; 11: 704-14.
16. Hackeng TM, Sere 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: 3106-11.
17. 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: 1044-6.
18. Peraramelli S, Suylen DP, Rosing J, Hackeng TM. The Kunitz 1 and Kunitz 3 domains of tissue factor pathway inhibitor are required for efficient inhibition of factor Xa. Thromb Haemost 2012; 108: 266-76.
19. Higuchi DA, Wun TC, Likert KM, Broze GJ Jr. The effect of leukocyte elastase on tissue factor pathway inhibitor. Blood 1992; 79: 1712-9.
20. Wesselschmidt R, Likert K, Huang Z, MacPhail L, Broze GJ Jr. Structural requirements for tissue factor pathway inhibitor interactions with factor Xa and heparin. Blood Coagul Fibrinolysis 1993; 4: 661-9.
21. Petersen LC, Bjorn SE, Olsen OH, Nordfang O, Norris F, Norris K. Inhibitory properties of separate recombinant Kunitz-type-protease-inhibitor domains from tissue-factor-pathway inhibitor. Eur J Biochem 1996; 235: 310-6.
22. 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.
23. 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.
24. Broze GJ Jr, Lange GW, Duffin KL, MacPhail L. Heterogeneity of plasma tissue factor pathway inhibitor. Blood Coagul Fibrinolysis 1994; 5: 551-9.
25. Sandset PM, Bendz B. Tissue factor pathway inhibitor: clinical deficiency states. Thromb Haemost 1997; 78: 467-70.
26. Hansen JB, Huseby KR, Huseby NE, Ezban M, Nordoy 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: 413-25.
27. Dahm AE, Andersen TO, Rosendaal F, Sandset PM. A novel anticoagulant activity assay of tissue factor pathway inhibitor I (TFPI). J Thromb Haemost 2005; 3: 651-8.
28. Hamamoto T, Yamamoto M, Nordfang O, Petersen JG, Foster DC, Kisiel W. Inhibitory properties of full-length and truncated recombinant tissue factor pathway inhibitor (TFPI). Evidence that the third Kunitz-type domain of TFPI is not essential for the inhibition of factor VIIa-tissue factor complexes on cell surfaces. J Biol Chem 1993; 268: 8704-10.
29. Valentin S, Reutlingsperger CP, Nordfang O, Lindhout T. Inhibition of factor X activation at extracellular matrix of fibroblasts during flow conditions: a comparison between tissue factor pathway inhibitor and inactive factor VIIa. Thromb Haemost 1995; 74: 1478-85.
30. Baugh RJ, Broze GJ Jr, Krishnaswamy S. Regulation of extrinsic pathway factor Xa formation by tissue factor pathway inhibitor. J Biol Chem 1998; 273: 4378-86.
31. Salemink I, Franssen J, Willems GM, Hemker HC, Lindhout T. Inhibition of tissue factor-factor VIIa-catalyzed factor X activation by factor Xa-tissue factor pathway inhibitor. A rotating disc study on the effect of phospholipid membrane composition. J Biol Chem 1999; 274: 28225-32.
32. Lu G, Broze GJ Jr, Krishnaswamy S. Formation of factors IXa and Xa by the extrinsic pathway: differential regulation by tissue factor pathway inhibitor and antithrombin III. J Biol Chem 2004; 279: 17241-9.
33. Maroney SA, Ellery PE, Wood JP, Ferrel JP, Martinez ND, Mast AE. Comparison of the inhibitory activities of human tissue factor pathway inhibitor (TFPI)alpha and TFPIbeta. J Thromb Haemost 2013; 11: 911-8.
34. Sere KM, Rosing J, Hackeng TM. Inhibition of thrombin generation by protein S at low procoagulant stimuli: implications for maintenance of the hemostatic balance. Blood 2004; 104: 3624-30.
35. Girard TJ, Broze GJ Jr. Tissue factor pathway inhibitor. Methods Enzymol 1993; 222: 195-209.
36. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959; 37: 911-7.
37. Ruggieri S. Separation of the methyl esters of fatty acids by thin layer chromatography. Nature 1962; 193: 1282-3.
38. Hemker HC, Giesen P, Al Dieri R, Regnault V, de Smedt E, Wagenvoord R, Lecompte T, Beguin S. Calibrated automated thrombin generation measurement in clotting plasma. Pathophysiol Haemost Thromb 2003; 33: 4-15.
39. Sere KM, Janssen MP, Willems GM, Tans G, Rosing J, Hackeng TM. Purified protein S contains multimeric forms with increased APC-independent anticoagulant activity. Biochemistry 2001; 40: 8852-60.
40. Sere KM, Willems GM, Rosing J, Hackeng TM. Protein S multimers are generated in vitro and affect protein S structure-function analyses. Semin Hematol 2006; 43: S111-20.
41. Verma AK, Brighton TA. The direct factor Xa inhibitor rivaroxaban. Med J Aust 2009; 190: 379-83.
42. Warn-Cramer BJ, Rao LV, Maki SL, Rapaport SI. Modifications of extrinsic pathway inhibitor (EPI) and factor Xa that affect their ability to interact and to inhibit factor VIIa/tissue factor: evidence for a two-step model of inhibition. Thromb Haemost 1988; 60: 453-6.
43. Willems GM, Janssen MP, Salemink I, Wun TC, Lindhout T. Transient high affinity binding of tissue factor pathway inhibitor-factor Xa complexes to negatively charged phospholipid membranes. Biochemistry 1998; 37: 3321-8.
44. Valentin S, Schousboe I. Factor Xa enhances the binding of tissue factor pathway inhibitor to acidic phospholipids. Thromb Haemost 1996; 75: 796-800.
45. Morrison JF, Walsh CT. The behavior and significance of slow-binding enzyme inhibitors. Adv Enzymol Relat Areas Mol Biol 1988; 61: 201-301.
46. Lindahl AK, Sandset PM, Abildgaard U. The present status of tissue factor pathway inhibitor. Blood Coagul Fibrinolysis 1992; 3: 439-49.
47. Vincent LM, Tran S, Livaja R, Bensend TA, Milewicz DM, Dahlback B. Coagulation factor V(A2440G) causes east Texas bleeding disorder via TFPIalpha. J Clin Invest 2013; 123: 3777-87.
48. Sandset PM, Abildgaard U, Larsen ML. Heparin induces release of extrinsic coagulation pathway inhibitor (EPI). Thromb Res 1988; 50: 803-13.