Modulation of Thrombin and Heparin Activities by Fibrin

Philip J Hogg; Paul E Bock

doi:10.1055/s-0038-1655982

Thrombosis and Haemostasis, Inhaltsverzeichnis

Thromb Haemost 1997; 77(03): 424-433
DOI: 10.1055/s-0038-1655982

Review Article

Schattauer GmbH Stuttgart

Modulation of Thrombin and Heparin Activities by Fibrin

Autor*innen

Philip J Hogg

¹The Centre for Thrombosis and Vascular Research, School of Pathology, The University of New South Wales, Sydney, Australia
Paul E Bock

²The Vanderbilt University School of Medicine, Department of Pathology, Nashville, Tennessee, USA

Abstract

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Referenzen

References
1 Fenton JW. Thrombin functions and antithrombotic intervention. Thromb Haemost 1995; 74: 0493-0498
2 Binnie C, Lord ST. The fibrinogen sequences that interact with thrombin. Blood 1993; 81: 3186-3189
3 Bjӧrk I, Olson ST, Shore JD. Molecular mechanisms of the accelerating effect of heparin on the reactions between antithrombin and clotting pro-teinases. In: Heparin, Chemical and Biological Properties, Clinical Applications. Lane DA, Lindahl U. eds Boca Raton, FL: CRC Press; 1989. pp 0229-0256
4 Olson ST, Bjӧrk I. Predominant contribution of surface approximation to the mechanism of heparin acceleration of the antithrombin-thrombin reaction:elucidation from salt concentration effects. J Biol Chem 1991; 266: 6353-6364
5 Olson S, Bjork I. Mechanism of action of heparin and heparin-like antithrombotics. Perspectives in Drug Discovery and Design 1993; 1: 0479-0501
6 Hogg PJ, Jackson CM. Heparin promotes the binding of thrombin to fibrin polymer:quantitative characterization of a thrombin-fibrin polymer-hepa-rin ternary complex. J Biol Chem 1990; 265: 0241-0247
7 Hogg PJ, Jackson CM. Formation of a ternary complex between thrombin, fibrin monomer, and heparin influences the action of thrombin on its substrates. J Biol Chem 1990; 265: 0248-0255
8 Hogg PJ, Jackson CM, Labanowski JK, Bock PE. Binding of fibrin monomer and heparin to thrombin in a ternary complex alters the environment of the thrombin catalytic site, reduces affinity for hirudin, and inhibits cleavage of fibrinogen. J Biol Chem 1996; 271: 26088-26095
9 Hogg PJ, Jackson CM. Fibrin monomer protects thrombin from inactivation by heparin-antithrombin III:implications for heparin efficacy. Proc Natl Acad Sci USA 1989; 86: 3619-3623
10 Weitz JI, Hirsh J. New anticoagulant strategies. J Lab Clin Med 1993; 122: 0364-0373
11 Weitz JI. Activation of blood coagulation by plaque rupture:mechanisms and prevention. Am J Cardiol 1995; 75: 018B-022B
12 Stone SR. Thrombin inhibitors:a new generation of antithrombotics. Trend Cardiov Med 1995; 5: 0134-0139
13 Seegers WH, Nieft M, Loomis EC. Note on the adsorption of thrombin on fibrin. Science 1945; 101: 0520-0521
14 Laudano AP, Doolittle RF. Studies on synthetic peptides that bind to fibrinogen and prevent polymerization. Structural requirements, number of binding sites, and species differences. Biochemistry 1980; 19: 1013-1019
15 Naski MC, Shafer JA. A kinetic model for the α-thrombin-catalyzed conversion of plasma levels of fibrinogen to fibrin in the presence of antithrombin III. J Biol Chem 1991; 266: 13003-13010
16 Koopman J, Haverkate F, Lord ST, Grimbergen J, Mannucci PM. Molecular basis of fibrinogen Naples associated with defective thrombin binding and thrombophilia:homozygous substitution of Bp Ala ->Thr. J Clin Invest 1992; 90: 0238-0244
17 Banninger H, Lammle B, Furlan M. Binding of α-thrombin to fibrin depends on the quality of the fibrin network. Biochem J 1994; 298: 0157-0163
18 Liu CY, Nossel HL, Kaplan KL. The binding of thrombin by fibrin. J Biol Chem 1979; 254: 10421-10425
19 Kaminski M, McDonagh J. Studies of the mechanism of thrombin. Interaction with fibrin. J Biol Chem 1983; 258: 10530-10535
20 Naski MC, Shafer JA. α-Thrombin-catalyzed hydrolysis of fibrin I:alternative binding modes and the accessibility of the active site in fibrin I-bound α-thrombin. J Biol Chem 1990; 265: 1401-1407
21 Higgins DL, Lewis SD, Shafer JA. Steady state kinetic parameters for the thrombin-catalyzed conversion of human fibrinogen to fibrin. J Biol Chem 1983; 258: 9276-9282
22 Hofsteenge J, Taguchi H, Stone SR. Effect of thrombomodulin on the kinetics of the interaction of thrombin with substrates and inhibitors. Biochem J 1986; 237: 0243-0251
23 Stubbs MT, Bode W. A player of many parts:the spotlight falls on thrombin’s structure. Thromb Res 1993; 69: 0001-0058
24 Bode W, Turk D, Karshikov A. The refined 1.9-A x-ray crystal structure of D-Phe-Pro-Arg-chloromethyl ketone-inhibited human α-thrombin:structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci 1992; 1: 0426-0471
25 Naski MC, Fenton JW, Maraganore JM, Olson ST, Shafer JA. The COOH-terminal of hirudin. An exosite-directed competitive inhibitor of the action of α-thrombin on fibrinogen. J Biol Chem 1990; 265: 13484-13489
26 Rydel TJ, Ravichandran KG, Tulinsky A, Bode W, Huber R, Roitsch C, Fenton J. 2nd The structure of a complex of recombinant hirudin and human a-thrombin. Science 1990; 249: 0277-0280
27 Rydel TJ, Tulinsky A, Bode W, Huber R. Refined structure of the hirudin-thrombin complex. J Mol Biol 1991; 221: 0583-0601
28 Fenton JW, Olson TA, Zabinski MP, Wilner GD. Anion-binding exosite of human α-thrombin and fibrin(ogen) recognition. Biochemistry 1988; 27: 7106-7112
29 Naski MC, Lorand L, Shafer JA. Characterization of the kinetic pathway for fibrin promotion of α-thrombin-catalyzed activation of plasma factor XIII. Biochemistry 1991; 30: 0934-0941
30 Mihalyi E. Clotting of bovine fibrinogen. Kinetic analysis of the release of fibrinopeptides by thrombin and of the calcium uptake upon clotting at high fibrinogen concentrations. Biochemistry 1988; 27: 0976-0982
31 Lewis SD, Shields PP, Shafer JA. Characterization of the kinetic pathway for liberation of fibrinopeptides during assembly of fibrin. J Biol Chem 1985; 260: 10192-10199
32 Church FC, Pratt CW, Noyes CM, Kalayanamit T, Sherrill GB, Tobin RB, Meade JB. Structure and functional properties of human α-thrombin, phophopyridoxylated α-thrombin, and 7-thrombin. Identification of lysyl residues in α-thrombin that are critical for heparin and fibrin(ogen) interactions. J Biol Chem 1989; 264: 18419-18425
33 Gan ZR, Li Y, Chen Z, Lewis SD, Shafer JA. Identification of basic amino acid residues in thrombin essential for heparin-catalyzed inactivation by antithrombin III. J Biol Chem 1994; 269: 1301-1305
34 Sheehan JP, Sadler JE. Molecular mapping of the heparin-binding exosite of thrombin. Proc Natl Acad Sci USA 1994; 91: 5518-5522
35 Olson ST, Halvorson HR, Björk I. Quantitative characterization of the thrombin-heparin interaction. Discrimination between specific and nonspecific binding models. J Biol Chem 1991; 266: 6342-6352
36 Grootenhuis PDJ, Westerduin P, Meuleman D, Petitou M, van BoeckelCAA. Rational design of synthetic heparin analogues with tailor-made coagulation factor inhibitory activity. Nature Struct Biol 1995; 2: 0736-0739
37 Bock PE. Active site selective labeling of blood coagulation proteinases with fluorescent probes by the use of thioester peptide chloromethyl ketones. I Specificity of thrombin labeling. J Biol Chem 1992; 267: 14963-14973
38 Bock PE. Active site selective labeling of blood coagulation proteinases with fluorescent probes by the use of thioester peptide chloromethyl ketones. II Properties of thrombin derivatives as reporters of prothrombin fragment 2 binding and specificity of the labeling approach for other proteinases. J Biol Chem 1992; 267: 14974-14981
39 Liu L-W, Vu T-KH, Esmon CT, Coughlin SR. The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J Biol Chem 1991; 266: 16977-16980
40 Linardic CM, Greenberg CS. Inhibition of the anticoagulant properties of antithrombin III and heparin by fibrin. Ann NY Acad Sci 1989; 556: 0459-0461
41 Okwusidi J, Anvari N, Kulczycky M, Blajchman MA, Buchanan MR, Ofosu FA. Fibrin moderates the catalytic action of heparin but not that of dermatan sulfate on thrombin inhibition in human plasma. J Lab Clin Med 1991; 117: 0359-0364
42 Hotchkiss KA, Chesterman CN, Hogg PJ. Inhibition of heparin activity in plasma by soluble fibrin:evidence for ternary thrombin-fibrin-heparin complex formation. Blood 1994; 84: 0498-0503
43 Weitz JI, Hudiba M, Massel D, Maraganore J, Hirsh J. Clot-bound thrombin is protected from inhibition by heparin-antithrombin III but is susceptible to inactivation by antithrombin Ill-independent inhibitors. J Clin Invest 1990; 86: 0385-0391
44 Berry CN, Girardot C, Lecoffre C, Lunven C. Effects of the synthetic thrombin inhibitor argatroban on fibrin-or clot-incorporated thrombin:comparison with heparin and recombinant hirudin. Thromb Haemost 1994; 72: 0381-0386
45 Bendayan P, Boccalon H, Dupouy D, Boneu B. Dermatan sulfate is a more potent inhibitor of clot-bound thrombin than unfractionated and low molecular weight heparins. Thromb Haemost 1994; 71: 0576-0580
46 Esmon CT. The roles of protein C and thrombomodulin in the regulation of blood coagulation. J Biol Chem 1989; 264: 4743-4746
47 Mathews II, Padmanabhan KP, Tulinsky A. Structure of a nonadecapeptide of the fifth EGF domain of thrombomodulin complexed with thrombin. Biochemistry 1994; 33: 13547-13552
48 Ye J, Liu L-W, Esmon CT, Johnson AE. The fifth and sixth growth factorlike domains of thrombomodulin bind to the anion-binding exosite of thrombin and alter its specificity. J Biol Chem 1992; 267: 11023-11028
49 Parkinson JF, Koyama T, Bang NU, Preissner KT. Thrombomodulin:an anticoagulant cell surface proteoglycan with a physiologically relevant glycosaminoglycan moiety. Adv Exp Med Biol 1992; 313: 0177-0188
50 Ye J, Esmon CT, Johnson AE. The chondroitin sulfate moiety of thrombomodulin binds a second molecule of thrombin. J Biol Chem 1993; 268: 2373-2379
51 Ye J, Rezaie AR, Esmon CT. Glycosaminoglycan contributions to both protein C activation and thrombin inhibition involve a common arginine-rich site in thrombin that includes residues arginine 93, and 101. J Biol Chem 1994; 269: 17965-17970
52 Esmon CT. Thrombomodulin as a model of molecular mechanisms that modulate protease specificity and function at the vessel surface. FASEB J 1995; 9: 0946-0955
53 Bajzar L, Morser J, Nesheim M. TAFI, or plasma procarboxypeptidase B couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem 1996; 271: 16603-16608
54 Rezaie AR, Cooper ST, Church FC, Esmon CT. Protein C inhibitor is a potent inhibitor of the thrombin-thrombomodulin complex. J Biol Chem 1995; 270: 25336-25339
55 Mathews II, Padmanabhan KP, Ganesh V, Tulinsky A, Ishii M, Chen J, Turck CW, Coughlin SR, Fenton J. 2nd Crystallographic structures of thrombin complexed with thrombin receptor peptides:existence of expected and novel binding modes. Biochemistry 1994; 33: 3266-3279
56 Tollefsen DM. Insight into the mechanism of action of heparin cofactor II. Thromb Haemost 1995; 74: 1209-1214
57 Ofosu FA, Fenton J, Maraganore J, Blajchman MA, Yang X, Smith L, Anvari N, Buchanan MR, Hirsh J. 2nd Inhibition of the amplification reactions of blood coagulation by site-specific inhibitors of α-thrombin. Biochem J 1992; 283: 0893-0897
58 Esmon CT, Lollar P. Involvement of thrombin anion-binding exosites 1 and 2 in the activation of factor V and factor VIII. J Biol Chem 1996; 271: 13882-13887
59 Gailani D, Broze GJ. Factor XI activation by thrombin and factor XIa. Sem Thromb Hemost 1993; 19: 0396-0404
60 Lewis SD, Janus TJ, Lorand L, Shafer JA. Regulation of formation of factor XllIa by its substrates. Biochemistry 1985; 24: 6772-6777
61 Awbery BJ, Hoak JC, Owen WG. Binding of human thrombin to cultured human endothelial cells. J Biol Chem 1979; 254: 4092-4095
62 Hatton MWC, Dejana E, Cazenave JP, Regoeczi E, Mustard JF. Heparin inhibits thrombin binding to rabbit thoracic aorta endothelium. J Lab Clin Med 1980; 96: 0861-0870
63 Shimada K, Ozawa T. Evidence that cell-surface heparan sulphate is involved in the high affinity thrombin binding to cultured porcine aortic endothelial cells. J Clin Invest 1985; 75: 1308-1316
64 Marcum JA, Rosenberg RD. Anticoagulantly active heparan sulfate proteoglycan and the vascular endothelium. Sem Thromb Hemostas 1987; 13: 0464-0474
65 Bar-Shavit R, Eldor A, Vlodavsky I. Binding of thrombin to subendothelial extracellular matrix:protection and expression of functional properties. J Clin Invest 1989; 84: 1096-1104
66 Zammit A, Dawes J. Fibrinogen inhibits the heparin cofactor II-mediated antithrombin activity of dermatan sulphate. Blood 1995; 85: 0720-0726
67 Liu CY, Nossel HL, Kaplan KL. Defective thrombin binding by abnormal fibrin associated with recurrent thrombosis. Thromb Haemost 1979; 42: 079
68 Haverkate F, Koopman J, Kluft C, D’Angelo A, Cattaneo M, Manucci PM. Fibrinogen Milano II:a congenital dysfibrinogenaemia associated with juvenile arterial and venous thrombosis. Thromb Haemost 1986; 55: 0131-0135
69 Lensing AW, Prins MH, Davidson BL, Hirsh J. Treatment of deep venous thrombosis with low-molecular-weight heparins. A meta-analysis. Arc Int Med 1995; 155: 0601-0607
70 Coller BS, Anderson K, Weisman HF. New antiplatelet agents:platelet GPIIb/IIIa antagonists. Thromb Haemost 1995; 74: 0302-0338