Thrombin activatable fibrinolysis inhibitor (TAFI) - How does thrombin regulate fibrinolysis?

Annals of Medicine

Volumn 38, Issue 6, 2006, Pages 378-388

  Bouma, Bonno N ^a,b   Mosnier, Laurent O ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Carboxypeptidase; Coagulation; Fibrinolysis; TAFI

Indexed keywords

ACTIVATED PROTEIN C; AMINOCAPROIC ACID; ANTIFIBRINOLYTIC AGENT; BLOOD CLOTTING FACTOR 10A INHIBITOR; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9; CARBOXYPEPTIDASE; ENZYME INHIBITOR; FIBRIN; FIBRINOGEN; FIBRINOLYTIC AGENT; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBIN INHIBITOR; TISSUE FACTOR PATHWAY INHIBITOR; TISSUE PLASMINOGEN ACTIVATOR;

ARTERIOSCLEROSIS; ARTERY THROMBOSIS; BLEEDING DISORDER; BLOOD CLOT LYSIS; BLOOD CLOTTING; BLOOD CLOTTING FACTOR 11 DEFICIENCY; BLOOD PRESSURE; CARBOXY TERMINAL SEQUENCE; DENTURE; DISEASE SEVERITY; DOWN REGULATION; FIBRINOLYSIS; FIBRINOLYTIC THERAPY; HEART INFARCTION; HEMOPHILIA; HEMOPHILIA A; HEMOPHILIA B; HUMAN; IN VIVO STUDY; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; THROMBIN TIME; THROMBOCYTE; THROMBOEMBOLISM; THROMBOSIS; VEIN THROMBOSIS; WOUND HEALING;

ANIMALS; BLOOD COAGULATION DISORDERS, INHERITED; BLOOD PLATELETS; CARBOXYPEPTIDASE U; FIBRINOLYSIS; HUMANS; INFLAMMATION; PROTEIN C; THROMBIN; THROMBOSIS;

EID: 33749257998     PISSN: 07853890     EISSN: 16512219     Source Type: Journal    
DOI: 10.1080/07853890600852898     Document Type: Review

References (91)

1. Sakata Y, Aoki N. Significance of cross-linking of alpha 2-plasmin inhibitor to fibrin in inhibition of fibrinolysis and in hemostasis. J Clin Invest. 1982;69:536-42.
2. Lorand L. Sol Sherry Lecture in Thrombosis: research on clot stabilization provides clues for improving thrombolytic therapies. Arterioscler Thromb Vasc Biol. 2000;20:2-9.
3. Butt C, Zheng H, Randell E, Robb D, Parfrey P, Xie YG. Combined carrier status of prothrombin 20210A and factor XIII-A Leu34 alleles as a strong risk factor for myocardial infarction: evidence of a gene-gene interaction. Blood. 2003;101:3037-41.
4. Balogh I, Szoke G, Karpati L, Wartiovaara U, Katona E, Komaromi I, et al. Val34Leu polymorphism of plasma factor XIII: biochemistry and epidemiology in familial thrombophilia. Blood. 2000;96:2479-86.
5. Collet JP, Soria J, Mirshahi M, Hirsch M, Dagonnet FB, Caen J, et al. Dusart syndrome: a new concept of the relationship between fibrin clot architecture and fibrin clot degradability: hypofibrinolysis related to an abnormal clot structure. Blood. 1993;82:2462-9.
6. Wolberg AS, Monroe DM, Roberts HR, Hoffman M. Elevated prothrombin results in clots with an altered fiber structure: a possible mechanism of the increased thrombotic risk. Blood. 2003;101:3008-13.
7. Bouma BN, Von dem Borne PAK, Meijers JCM. Factor XI and protection of the fibrin clot against lysis. A role for the intrinsic pathway of coagulation in fibrinolysis. Thromb Haemost. 1998;80:24-7.
8. Bajzar L, Manuel R, Nesheim ME. Purification and characterization of TAFI, a thrombin-activable fibrinolysis inhibitor. J Biol Chem. 1995;270:14477-84.
9. Eaton DL, Malloy BE, Tsai SP, Henzel W, Drayna D. Isolation, molecular cloning, and partial characterization of a novel carboxypeptidase B from human plasma. J Biol Chem. 1991;266:21833-8.
10. Wang W, Hendriks DF, Scharpé SS. Carboxypeptidase U, a plasma carboxypeptidase with high affinity for plasminogen. J Biol Chem. 1994;269:15937-44.
11. Campbell W, Okada H. An arginine specific carboxypeptidase generated in blood during coagulation or inflammation which is unrelated to carboxypeptidase N or its subunits. Biochem Biophys Res Commun. 1989;162:933-9.
12. Bouma BN, Marx PF, Mosnier LO, Meijers JCM. Thrombin-activatable fibrinolysis inhibitor (TAFI, plasma procarboxypeptidase B, procarboxypeptidase R, procarboxypeptidase U). Thromb Res. 2001;101:329-54.
13. Marx PF. Thrombin-activatable fibrinolysis inhibitor. Curr Med Chem. 2004;11:2335-48.
14. Hoylaerts M, Rijken DC, Lijnen HR, Collen D. Kinetics of the activation of plasminogen by tissue plasminogen activator. Role of fibrin. J Biol Chem. 1982;257:2912-9.
15. Christensen U. C-terminal lysine residues of fibrinogen fragments essential for binding to plasminogen. FEBS Lett. 1985;182:43-6.
16. Fleury V, Angles Cano E. Characterization of the binding of plasminogen to fibrin surfaces: the role of carboxy-terminal lysines. Biochemistry. 1991;30:7630-8.
17. Sakharov DV, Rijken DC. Superficial accumulation of plasminogen during plasma clot lysis. Circulation. 1995;92:1883-90.
18. Wang W, Boffa PB, Bajzar L, Walker JB, Nesheim ME. A study of the mechanism of inhibition of fibrinolysis by activated thrombin-activable fibrinolysis inhibitor. J Biol Chem. 1998;273:27176-81.
19. Redlitz A, Tan AK, Eaton DL, Plow EF. Plasma carboxypeptidases as regulators of the plasminogen system. J Clin Invest. 1995;96:2534-8.
20. Leurs J, Nerme V, Sim Y, Hendriks D. Carboxypeptidase U (TAFIa) prevents lysis from proceeding into the propagation phase through a threshold-dependent mechanism. J Thromb Haemost. 2004;2:416-23.
21. Walker JB, Bajzar L. The intrinsic threshold of the fibrinolytic system is modulated by basic carboxypeptidases, but the magnitude of the antifibrinolytic effect of activated thrombin-activable fibrinolysis inhibitor is masked by its instability. J Biol Chem. 2004;279:27896-904.
22. Boffa MB, Wang W, Bajzar L, Nesheim ME. Plasma and recombinant thrombin-activable fibrinolysis inhibitor (TAFI) and activated TAFI compared with respect to glycosylation, thrombin/thrombomodulin-dependent activation, thermal stability, and enzymatic properties. J Biol Chem. 1998;273:2127-35.
23. Boffa MB, Bell R, Stevens WK, Nesheim ME. Roles of thermal instability and proteolytic cleavage in regulation of activated thrombin-activable fibrinolysis inhibitor. J Biol Chem. 2000;275:12868-78.
24. Marx PF, Hackeng TM, Dawson PE, Griffin JH, Meijers JCM, Bouma BN. Inactivation of active thrombin-activable fibrinolysis inhibitor takes place by a process that involves conformational instability rather than proteolytic cleavage. J Biol Chem. 2000;275:12410-5.
25. Marx PF, Dawson PE, Bouma BN, Meijers JCM. Plasmin-mediated activation and inactivation of thrombin-activatable fibrinolysis inhibitor. Biochemistry. 2002;41:6688-96.
26. Schneider M, Boffa M, Stewart R, Rahman M, Koschinsky M, Nesheim ME. Two naturally occurring variants of TAFI (Thr 325 and Ile 325) differ substantially with respect to thermal stability and antifibrinolytic activity of the enzyme. J Biol Chem. 2002;277:1021-30.
27. Cote HC, Bajzar L, Stevens WK, Samis JA, Morser J, MacGillivray RT, et al. Functional characterization of recombinant human meizothrombin and Meizothrombin(desF1). Thrombomodulin-dependent activation of protein C and thrombin-activatable fibrinolysis inhibitor (TAFI), platelet aggregation, antithrombin-III inhibition. J Biol Chem. 1997;272:6194-200.
28. Bajzar L, Morser J, Nesheim ME. TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem. 1996;271:16603-8.
29. Mann KG, Butenas S, Brummel K. The dynamics of thrombin formation. Arterioscler Thromb Vasc Biol. 2003;23:17-25.
30. Keularts IM, Zivelin A, Seligsohn U, Hemker HC, Beguin S. The role of factor XI in thrombin generation induced by low concentrations of tissue factor. Thromb Haemost. 2001;85:1060-5.
31. Von dem Borne PAK, Bajzar L, Meijers JCM, Nesheim ME, Bouma BN. Thrombin-mediated activation of factor XI results in a thrombin-activatable fibrinolysis inhibitor-dependent inhibition of fibrinolysis. J Clin Invest. 1997;99:2323-7.
32. Rosing J, van Rijn JL, Bevers EM, van Dieijen G, Comfurius P, Zwaal RF. The role of activated human platelets in prothrombin and factor X activation. Blood. 1985;65:319-32.
33. Oliver JA, Monroe DM, Roberts HR, Hoffman M. Thrombin activates factor XI on activated platelets in the absence of factor XII. Arterioscler Thromb Vasc Biol. 1999;19:170-7.
34. Mosnier LO, Buijtenhuijs P, Marx PF, Meijers JCM, Bouma BN. Identification of thrombin activatable fibrinolysis inhibitor in human platelets. Blood. 2003;101:4844-6.
35. Mosnier LO, Von dem Borne PAK, Meijers JCM, Bouma BN. Plasma TAFI levels influence the clot lysis time in healthy individuals in the presence of an intact pathway of coagulation. Thromb Haemost. 1998;80:829-35.
36. Bajzar L, Nesheim ME, Tracy PB. The profibrinolytic effect of activated protein C in clots formed from plasma is TAFI-dependent. Blood. 1996;88:2093-100.
37. Mosnier LO, Meijers JCM, Bouma BN. Regulation of fibrinolysis in plasma by TAFI and protein C is dependent on the concentration of thrombomodulin. Thromb Haemost. 2001;85:5-11.
38. Gresele P, Momi S, Berrettini M, Nenci GG, Schwarz HP, Semeraro N, et al. Activated human protein C prevents thrombin-induced thromboembolism in mice-Evidence that activated protein C reduces intravascular fibrin accumulation through the inhibition of additional thrombin generation. J Clin Invest. 1998;101:667-76.
39. Bertina RM, Koeleman BPC, Koster T, Rosendaal FR, Dirven RJ, de Ronde H, et al. Mutations in blood coagulation factor V associated with resistance to activated protein C. Nature. 1994;369:64-7.
40. Colucci M, Simioni P, Piro D, Prandoni P, Pagnan A, Semeraro N. An antifibrinolytic effect associated with an anti-factor V antibody in a patient with severe thrombophilia. Haematologica. 2003;88:1383-9.
41. Parker AC, Mundada LV, Schmaier AH, Fay WP. Factor VLeiden inhibits fibrinolysis in vivo. Circulation. 2004;110:3594-8.
42. Griffin JH. The thrombin paradox. Nature. 1995;378:337-8.
43. Hanson SR, Griffin JH, Harker LA, Kelly LA, Esmon CT, Gruber A. Antithrombotic effects of thrombin-induced activation of endogenous protein C in primates. J Clin Invest. 1993;92:2003-12.
44. Bauer KA, Rosenberg RD. The pathophysiology of the prethrombotic state in humans: insight gained from studies using markers of hemostatic system activation. Blood. 1987;70:343-50.
45. Redlitz A, Nicolini FA, Malycky JL, Topol EJ, Plow EF. Inducible carboxypeptidase activity. A role in clot lysis in vivo. Circulation. 1996;93:1328-30.
46. Minnema MC, Friederich PW, Levi M, Von dem Borne PAK, Mosnier LO, Meijers JCM, et al. Enhancement of rabbit jugular vein thrombolysis by neutralization of factor XI-In vivo evidence for a role of factor XI as an anti-fibrinolytic factor. J Clin Invest. 1998;101:10-4.
47. Nagashima M, Werner M, Wang M, Zhao L, Light DR, Pagila R, et al. An inhibitor of activated thrombin-activatable fibrinolysis inhibitor potentiates tissue-type plasminogen activator-induced thrombolysis in a rabbit jugular vein thrombolysis model. Thromb Res. 2000;98:333-42.
48. Refino CJ, DeGuzman L, Schmitt D, Smyth R, Jeet S, Lipari MT, et al. Consequences of inhibition of plasma carboxypeptidase B on in vivo thrombolysis, thrombosis and hemostasis. Fibrinolysis Proteolysis. 2000;14:305-14.
49. Klement P, Liao P, Bajzar L. A novel approach to arterial thrombolysis. Blood. 1999;94:2735-43.
50. Bjorkman JA, Abrahamsson TI, Nerme VK, Mattsson CJ. Inhibition of carboxypeptidase U (TAFIa) activity improves rt-PA induced thrombolysis in a dog model of coronary artery thrombosis. Thromb Res. 2005;116:519-24.
51. Sakharov DV, Plow EF, Rijken DC. On the mechanism of the antifibrinolytic activity of plasma carboxypeptidase B. J Biol Chem. 1997;272:14477-82.
52. Biemond BJ, Friederich PW, Levi M, Vlasuk GB, Buller HR, ten Cate JW. Comparison of sustained antithrombotic effects of inhibitors of thrombin and factor Xa in experimental thrombosis. Circulation. 1996;93:153-60.
53. Mattsson C, Bjorkman JA, Abrahamsson T, Nerme V, Schatteman K, Leurs J, et al. Local proCPU (TAFI) activation during thrombolytic treatment in a dog model of coronary artery thrombosis can be inhibited with a direct, small molecule thrombin inhibitor (melagatran). Thromb Haemost. 2002;87:557-62.
54. Gruber A, Hanson SR. Factor XI-dependence of surface- and tissue factor-initiated thrombus propagation in primates. Blood. 2003;102:953-5.
55. Yamashita A, Nishihira K, Kitazawa T, Soeda T, Esaki K, Imamura T. Factor XI contributes to thrombus propagation on injured neointima of the rabbit Iliac artery. J Thromb Haemost. 2006;4:1496-1501.
56. Wagenaar GT, Girma M, Havik SR, Voskuilen MC, Bouma BN, Meijers JCM. Generation and characterization of thrombin activatable fibrinolysis inhibitor deficient mice. Thromb Haemost. 2001;Suppl July:OC1759 (abstract).
57. Nagashima M, Yin ZF, Zhao L, White K, Zhu Y, Lasky N, et al. Thrombin-activatable fibrinolysis inhibitor (TAFI) deficiency is compatible with murine life. J Clin Invest. 2002;109:101-10.
58. Swaisgood CM, Schmitt D, Eaton D, Plow EF. In vivo regulation of plasminogen function by plasma carboxypeptidase B. J Clin Invest. 2002;110:1275-82.
59. Biemond BJ, Havik SR, Meijers JCM. Absence of enhanced lysis of pulmonary microemboli in TAFI deficient mice. Blood. 2001;98 (255a), 1070 (abstract).
60. te Velde EA, Wagenaar GT, Reijerkerk A, Roose-Girma M, Borel-Rinkes I, Voest EE, et al. Impaired healing of cutaneous wounds and colonic anastomoses in mice lacking thrombin-activatable fibrinolysis inhibitor. J Thromb Haemost. 2003;1:2087-96.
61. Romer J, Bugge TH, Pyke C, Lund LR, Flick MJ, Degen JL, et al. Impaired wound healing in mice with a disrupted plasminogen gene. Nat Med. 1996;2:287-92.
62. Drew AF, Liu H, Davidson JM, Daugherty CC, Degen JL. Wound-healing defects in mice lacking fibrinogen. Blood. 2001;97:3691-8.
63. Myles T, Nishimura T, Yun TH, Nagashima M, Morser J, Patterson AJ, et al. Thrombin activatable fibrinolysis inhibitor, a potential regulator of vascular inflammation. J Biol Chem. 2003;278:51059-67.
64. Liaw L, Birk DE, Ballas CB, Whitsitt JS, Davidson JM, Hogan BL. Altered wound healing in mice lacking a functional osteopontin gene (spp1). J Clin Invest. 1998;101:1468-78.
65. Smith LL, Giachelli CM. Structural requirements for alpha 9 beta 1-mediated adhesion and migration to thrombin-cleaved osteopontin. Exp Cell Res. 1998;242:351-60.
66. Smith LL, Cheung HK, Ling LE, Chen J, Sheppard D, Pytela R, et al. Osteopontin N-terminal domain contains a cryptic adhesive sequence recognized by alpha9beta1 integrin. J Biol Chem. 1996;271:28485-91.
67. Asakai R, Chung DW, Davie EW, Seligsohn U. Factor XI deficiency in Ashkenazi Jews in Israel. N Engl J Med. 1991;325:153-8.
68. Berliner S, Horowitz I, Martinowitz U, Brenner B, Seligsohn U. Dental surgery in patients with severe factor XI deficiency without plasma replacement. Blood Coagul Fibrinolysis. 1992;3:465-8.
69. Chan JC, Ganopolsky JG, Cornelissen I, Suckow MA, Sandoval-Cooper MJ, Brown EC, et al. The characterization of mice with a targeted combined deficiency of protein c and factor XI. Am J Pathol. 2001;158:469-79.
70. Broze GJ Jr, Higuchi DA. Coagulation-dependent inhibition of fibrinolysis: role of carboxypeptidase-U and the premature lysis of clots from hemophilic plasma. Blood. 1996;88:3815-23.
71. Mosnier LO, Lisman T, van den Berg HM, Nieuwenhuis HK, Meijers JCM, Bouma BN. The defective down regulation of fibrinolysis in haemophilia A can be restored by increasing the TAFI plasma concentration. Thromb Haemost. 2001;86:1035-9.
72. Sixma JJ, van den Berg A. The haemostatic plug in haemophilia A: a morphological study of haemostatic plug formation in bleeding time skin wounds of patients with severe haemophilia A. Br J Haematol. 1984;58:741-53.
73. Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues: implications for disorders of hemostasis and thrombosis. Am J Pathol. 1989;134:1087-97.
74. Walsh PN, Rizza CR, Matthews JM, Eipe J, Kernoff PB, Coles MD, et al. Epsilon-Aminocaproic acid therapy for dental extractions in haemophilia and Christmas disease: a double blind controlled trial. Br J Haematol. 1971;20:463-75.
75. Koster T, Blann AD, Vandenbroucke JP, Rosendaal FR. Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis. Lancet. 2000;345:152-5.
76. Vlieg AV, van der Linden IK, Bertina RM, Rosendaal FR. High levels of factor IX increase the risk of venous thrombosis. Blood. 2000;95:3678-82.
77. Meijers JCM, Tekelenburg WL, Bouma BN, Bertina RM, Rosendaal FR. High levels of coagulation factor XI as a risk factor for venous thrombosis. N Engl J Med. 2000;342:696-701.
78. Colucci M, Binetti BM, Tripodi A, Chantarangkul V, Semeraro N. Hyperprothrombinemia associated with prothrombin G20210A mutation inhibits plasma fibrinolysis through a TAFI-mediated mechanism. Blood. 2004;103:2157-61.
79. van Tilburg NH, Rosendaal FR, Bertina RM. Thrombin activatable fibrinolysis inhibitor and the risk for deep vein thrombosis. Blood. 2000;95:2855-9.
80. Eichinger S, Schonauer V, Weltermann A, Minar E, Bialonczyk C, Hirschl M, et al. Thrombin-activatable fibrinolysis inhibitor and the risk for recurrent venous thromboembolism. Blood. 2004;103:3773-6.
81. Silveira A, Schatteman KA, Goossens F, Moor E, Scharpé SS, Strömqvist M, et al. Plasma procarboxypeptidase U in men with symptomatic coronary artery disease. Thromb Haemost. 2000;84:364-8.
82. Juhan-Vague I, Morange PE, Aubert H, Henry M, Aillaud MF, Alessi MC, et al. Plasma thrombin-activatable fibrinolysis inhibitor antigen concentration and genotype in relation to myocardial infarction in the north and south of Europe. Arterioscler Thromb Vasc Biol. 2002;22:867-73.
83. Juhan-Vague I, Morange PE. Very high TAFI antigen levels are associated with a lower risk of hard coronary events: the PRIME Study. J Thromb Haemost. 2003;1:2243-4.
84. Leebeek FW, Goor MP, Guimaraes AH, Brouwers GJ, Maat MP, Dippel DW, et al. High functional levels of thrombin-activatable fibrinolysis inhibitor are associated with an increased risk of first ischemic stroke. J Thromb Haemost. 2005;3:2211-8.
85. Salomon O, Steinberg DM, Dardik R, Rosenberg N, Zivelin A, Tamarin I, et al. Inherited factor XI deficiency confers no protection against acute myocardial infarction. J Thromb Haemost. 2003;1:658-61.
86. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-74.
87. Shinohara T, Sakurada C, Suzuki T, Takeuchi O, Campbell W, Ikeda S, et al. Pro-carboxypeptidase R cleaves bradykinin following activation. Int Arch Allergy Immunol. 1994;103:400-4.
88. Ueno A, Oh-ishi S. Roles for the kallikrein-kinin system in inflammatory exudation and pain: lessons from studies on kininogen-deficient rats. J Pharmacol Sci. 2003;93:1-20.
89. Koschinsky ML, Boffa MB, Nesheim ME, Zinman B, Hanley AJ, Harris SB, et al. Association of a single nucleotide polymorphism in CPB2 encoding the thrombin-activable fibrinolysis inhibitor (TAF1) with blood pressure. Clin Genet. 2001;60:345-9.
90. Campbell WD, Lazoura E, Okada N, Okada H. Inactivation of C3a and C5a octapeptides by carboxypeptidase R and carboxypeptidase N. Microbiol Immunol. 2002;46:131-4.
91. Bouma BN, Meijers JCM. New insights into factors affecting clot stability: A role for thrombin activatable fibrinolysis inhibitor (TAFI; plasma procarboxypeptidase B, plasma procarboxypeptidase U, procarboxypeptidase R). Semin Hematol. 2004;41:13-9.