Molecular recognition mechanisms of thrombin

Journal of Thrombosis and Haemostasis

Volumn 3, Issue 8, 2005, Pages 1861-1872

  Huntington, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cofactor; Exosite; Specificity; Structure; Substrate; Thrombin

Indexed keywords

ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 8; GLYCOPROTEIN IB ALPHA; HEPARIN; HEPARIN COFACTOR II; PROTEIN C; PROTEINASE ACTIVATED RECEPTOR; THROMBIN; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; THROMBOMODULIN;

BLOOD CLOTTING; CONFERENCE PAPER; CRYSTAL STRUCTURE; ENZYME ACTIVITY; FIBRIN CLOT; FIBRINOGEN METABOLISM; HEMOSTASIS; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SITE DIRECTED MUTAGENESIS;

ANIMALS; FACTOR V; FACTOR XI; FACTOR XIII; FIBRINOGEN; HEMOSTASIS; HUMANS; MACROMOLECULAR SUBSTANCES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PROTEINASE-ACTIVATED; SUBSTRATE SPECIFICITY; THROMBIN;

EID: 27144505651     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2005.01363.x     Document Type: Conference Paper

References (99)

1. Ratnoff OD, Ratnoff OD, Forbes CD, eds. The evolution of knowledge about hemostasis. Disorders of Hemostasis. 3rd edn. Philadelphia: WB Saunders Company, 1996;
2. Mann KG, Butenas S, Brummel K. The dynamics of thrombin formation. Arterioscler Thromb Vasc Biol 2003; 23: 17-25.
3. Schechter I, Berger A. On the size of the active site in proteases. I. Papain. Biochem Biophys Res Commun 1967; 27: 157-62.
4. Bode W, Mayr I, Baumann U, Huber R, Stone SR, Hofsteenge J. The refined 1.9 A crystal structure of human alpha-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J 1989; 8: 3467-75.
5. Bode W, Turk D, Karshikov A. The refined 1.9-A X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci 1992; 1: 426-71.
6. Stubbs MT, Bode W. A player of many parts: the spotlight falls on thrombin's structure. Thromb Res 1993; 69: 1-58.
7. Stubbs MT, Bode W. The clot thickens: clues provided by thrombin structure. Trends Biochem Sci 1995; 20: 23-8.
8. Kraulis PJ. Molscript - a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 1991; 24: 946-50.
9. Esnouf RM. An extensively modified version of MolScript that includes greatly enhanced coloring capabilities. J Mol Graph Model 1997; 15: 132.
10. Merritt EA, Murphy MEP. Raster3d version-2.0 - A program for photorealistic molecular graphics. Acta Crystalogr 1994; D50: 869-73.
11. Mosesson MW, Siebenlist KR, Meh DA. The structure and biological features of fibrinogen and fibrin. Ann N Y Acad Sci 2001; 936: 11-30.
12. 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: 9276-82.
13. Tsiang M, Jain AK, Dunn KE, Rojas ME, Leung LL, Gibbs CS. Functional mapping of the surface residues of human thrombin. J Biol Chem 1995; 270: 16854-63.
14. Hall SW, Gibbs CS, Leung LL. Identification of critical residues on thrombin mediating its interaction with fibrin. Thromb Haemost 2001; 86: 1466-74.
15. Martin PD, Robertson W, Turk D, Huber R, Bode W, Edwards BF. The structure of residues 7-16 of the A alpha-chain of human fibrinogen bound to bovine thrombin at 2.3-A resolution. J Biol Chem 1992; 267: 7911-20.
16. Martin PD, Malkowski MG, DiMaio J, Konishi Y, Ni F, Edwards BF. Bovine thrombin complexed with an uncleavable analog of residues 7-19 of fibrinogen A alpha: geometry of the catalytic triad and interactions of the P1′, P2′, and P3′ substrate residues. Biochemistry 1996; 35: 13030-9.
17. Malkowski MG, Martin PD, Lord ST, Edwards BF. Crystal structure of fibrinogen-Aalpha peptide 1-23 (F8Y) bound to bovine thrombin explains why the mutation of Phe-8 to tyrosine strongly inhibits normal cleavage at Arg-16. Biochem J 1997; 326: 815-22.
18. Maurer MC, Trosset JY, Lester CC, DiBella EE, Scheraga HA. New general approach for determining the solution structure of a ligand bound weakly to a receptor: structure of a fibrinogen Aalpha-like peptide bound to thrombin (S195A) obtained using NOE distance constraints and an ECEPP/3 flexible docking program. Proteins 1999; 34: 29-48.
19. Krishnan R, Sadler JE, Tulinsky A. Structure of the Ser195Ala mutant of human alpha-thrombin complexed with fibrinopeptide A(7-16): evidence for residual catalytic activity. Acta Crystallogr D Biol Crystallogr 2000; 56: 406-10.
20. Pechik I, Madrazo J, Mosesson MW, Hernandez I, Gilliland GL, Medved L. Crystal structure of the complex between thrombin and the central "E" region of fibrin. Proc Natl Acad Sci USA 2004; 101: 2718-23.
21. Duga S, Asselta R, Tenchini ML. Coagulation factor V. Int J Biochem Cell Biol 2004; 36: 1393-9.
22. Fay PJ. Activation of factor VIII and mechanisms of cofactor action. Blood Rev 2004; 18: 1-15.
23. 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: 13882-7.
24. Myles T, Yun TH, Hall SW, Leung LL. An extensive interaction interface between thrombin and factor V is required for factor V activation. J Biol Chem 2001; 276: 25143-9.
25. Myles T, Yun TH, Leung LL. Structural requirements for the activation of human factor VIII by thrombin. Blood 2002; 100: 2820-6.
26. Ariens RA, Lai TS, Weisel JW, Greenberg CS, Grant PJ. Role of factor XIII in fibrin clot formation and effects of genetic polymorphisms. Blood 2002; 100: 743-54.
27. Janus TJ, Lewis SD, Lorand L, Shafer JA. Promotion of thrombin-catalyzed activation of factor XIII by fibrinogen. Biochemistry 1983; 22: 6269-72.
28. Philippou H, Rance J, Myles T, Hall SW, Ariens RA, Grant PJ, Leung L, Lane DA. Roles of low specificity and cofactor interaction sites on thrombin during factor XIII activation: competition for cofactor sites on thrombin determines its fate. J Biol Chem 2003; 278: 32020-6.
29. Sadasivan C, Yee VC. Interaction of the factor XIII activation peptide with alpha -thrombin. Crystal structure of its enzyme-substrate analog complex. J Biol Chem 2000; 275: 36942-8.
30. Andrews RK, Gardiner EE, Shen Y, Whisstock JC, Berndt MC. Glycoprotein Ib-IX-V. Int J Biochem Cell Biol 2003; 35: 1170-4.
31. Brass LF. Thrombin and platelet activation. Chest 2003; 124: 18S-25S.
32. Dumas JJ, Kumar R, Seehra J, Somers WS, Mosyak L. Crystal structure of the GpIbalpha-thrombin complex essential for platelet aggregation. Science 2003; 301: 222-6.
33. Celikel R, McClintock RA, Roberts JR, Mendolicchio GL, Ware J, Varughese KI, Ruggeri ZM. Modulation of alpha-thrombin function by distinct interactions with platelet glycoprotein Ibalpha. Science 2003; 301: 218-21.
34. Sadler JE. Structural biology. A menage a trois in two configurations. Science 2003; 301: 177-9.
35. Vanhoorelbeke K, Ulrichts H, Romijn RA, Huizinga EG, Deckmyn H. The GPIbalpha-thrombin interaction: far from crystal clear. Trends Mol Med 2004; 10: 33-9.
36. Li CQ, Vindigni A, Sadler JE, Wardell MR. Platelet glycoprotein Ib alpha binds to thrombin anion-binding exosite II inducing allosteric changes in the activity of thrombin. J Biol Chem 2001; 276: 6161-8.
37. De Cristofaro R, De Candia E, Landolfi R, Rutella S, Hall SW. Structural and functional mapping of the thrombin domain involved in the binding to the platelet glycoprotein Ib. Biochemistry 2001; 40: 13268-73.
38. Marchese P, Murata M, Mazzucato M, Pradella P, De Marco L, Ware J, Ruggeri ZM. Identification of three tyrosine residues of glycoprotein Ib alpha with distinct roles in von Willebrand factor and alpha-thrombin binding. J Biol Chem 1995; 270: 9571-8.
39. De Marco L, Mazzucato M, Masotti A, Ruggeri ZM. Localization and characterization of an alpha-thrombin-binding site on platelet glycoprotein Ib alpha. J Biol Chem 1994; 269: 6478-84.
40. Ofosu FA. Protease activated receptors 1 and 4 govern the responses of human platelets to thrombin. Transfus Apheresis Sci 2003; 28: 265-8.
41. Liu LW, Vu TK, Esmon CT, Coughlin SR. The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J Biol Chem 1991; 266: 16977-80.
42. Jacques SL, LeMasurier M, Sheridan PJ, Seeley SK, Kuliopulos A. Substrate-assisted catalysis of the PAR1 thrombin receptor. Enhancement of macromolecular association and cleavage. J Biol Chem 2000; 275: 40671-8.
43. Vu TK, Wheaton VI, Hung DT, Charo I, Coughlin SR. Domains specifying thrombin-receptor interaction. Nature 1991; 353: 674-7.
44. Ayala YM, Cantwell AM, Rose T, Bush LA, Arosio D, Di Cera E. Molecular mapping of thrombin-receptor interactions. Proteins 2001; 45: 107-16.
45. Mathews II, PadmanabhanKP, Ganesh V, Tulinsky A, Ishii M, Chen J, Turck CW, Coughlin SR, Fenton JW. Crystallographic structures of thrombin complexed with thrombin receptor peptides: existence of expected and novel binding modes. Biochemistry 1994; 33: 3266-79.
46. Li W, Johnson DJ, Esmon CT, Huntington JA. Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol 2004; 11: 857-62.
47. Brunger AT, Adams PD, Clore GM, Delano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Cryst 1998; D54: 905-21.
48. De Candia E, Hall SW, Rutella S, Landolfi R, Andrews RK, De Cristofaro R. Binding of thrombin to glycoprotein Ib accelerates the hydrolysis of Par-1 on intact platelets. J Biol Chem 2001; 276: 4692-8.
49. Gailani D, Broze GJJ. Factor XI activation in a revised model of blood coagulation. Science 1991; 253: 909-12.
50. Naito K, Fujikawa K. Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J Biol Chem 1991; 266: 7353-8.
51. Baglia FA, Walsh PN. Prothrombin is a cofactor for the binding of factor XI to the platelet surface and for platelet-mediated factor XI activation by thrombin. Biochemistry 1998; 37: 2271-81.
52. Baglia FA, Walsh PN. Thrombin-mediated feedback activation of factor XI on the activated platelet surface is preferred over contact activation by factor XIIa or factor XIa. J Biol Chem 2000; 275: 20514-9.
53. Walsh PN. Roles of factor XI, platelets and tissue factor-initiated blood coagulation. J Thromb Haemost 2003; 1: 2081-6.
54. Yun TH, Baglia FA, Myles T, Navaneetham D, Lopez JA, Walsh PN, Leung LL. Thrombin activation of factor XI on activated platelets requires the interaction of factor XI and platelet glycoprotein Ib alpha with thrombin anion-binding exosites I and II, respectively. J Biol Chem 2003; 278: 48112-9.
55. Baglia FA, Walsh PN. A binding site for thrombin in the apple 1 domain of factor XI. J Biol Chem 1996; 271: 3652-8.
56. Esmon NL, Owen WG, Esmon CT. Isolation of a membrane-bound cofactor for thrombin-catalyzed activation of protein C. J Biol Chem 1982; 257: 859-64.
57. Esmon CT. The protein C pathway. Chest 2003; 124: 26S-32S.
58. Dahlback B, Villoutreix BO. Molecular recognition in the protein C anticoagulant pathway. J Thromb Haemost 2003; 1: 1525-34.
59. Weiler H, Isermann BH. Thrombomodulin. J Thromb Haemost 2003; 1: 1515-24.
60. Zushi M, Gomi K, Yamamoto S, Maruyama I, Hayashi T, Suzuki K. The last three consecutive epidermal growth factor-like structures of human thrombomodulin comprise the minimum functional domain for protein C-activating cofactor activity and anticoagulant activity. J Biol Chem 1989; 264: 10351-3.
61. Fuentes-Prior P, Iwanaga Y, Huber R, Pagila R, Rumennik G, Seto M, Morser J, Light DR, Bode W. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 2000; 404: 518-25.
62. Kurosawa S, Stearns DJ, Jackson KW, Esmon CT. A 10-kDa cyanogen bromide fragment from the epidermal growth factor homology domain of rabbit thrombomodulin contains the primary thrombin binding site. J Biol Chem 1988; 263: 5993-6.
63. Ye J, Liu LW, Esmon CT, Johnson AE. The fifth and sixth growth factor-like domains of thrombomodulin bind to the anion-binding exosite of thrombin and alter its specificity. J Biol Chem 1992; 267: 11023-8.
64. Nagashima M, Lundh E, Leonard JC, Morser J, Parkinson JF. Alanine-scanning mutagenesis of the epidermal growth factor-like domains of human thrombomodulin identifies critical residues for its cofactor activity. J Biol Chem 1993; 268: 2888-92.
65. Tolkatchev D, Ng A, Zhu B, Ni F. Identification of a thrombin-binding region in the sixth epidermal growth factor-like repeat of human thrombomodulin. Biochemistry 2000; 39: 10365-72.
66. Baerga-Ortiz A, Rezaie AR, Komives EA. Electrostatic dependence of the thrombin-thrombomodulin interaction. J Mol Biol 2000; 296: 651-8.
67. Tsiang M, Lentz SR, Sadler JE. Functional domains of membrane-bound human thrombomodulin. EGF-like domains four to six and the serine/threonine-rich domain are required for cofactor activity. J Biol Chem 1992; 267: 6164-70.
68. Lin JH, McLean K, Morser J, Young TA, Wydro RM, Andrews WH, Light DR. Modulation of glycosaminoglycan addition in naturally expressed and recombinant human thrombomodulin. J Biol Chem 1994; 269: 25021-30.
69. 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, 97, and 101. J Biol Chem 1994; 269: 17965-70.
70. Vindigni A, White CE, Komives EA, Di Cera E. Energetics of thrombin-thrombomodulin interaction. Biochemistry 1997; 36: 6674-81.
71. Nawa K, Sakano K, Fujiwara H, Sato Y, Sugiyama N, Teruuchi T, Iwamoto M, Marumoto Y. Presence and function of chondroitin-4-sulfate on recombinant human soluble thrombomodulin. Biochem Biophys Res Commun 1990; 171: 729-37.
72. 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: 243-51.
73. Esmon CT, Esmon NL, Harris KW. Complex formation between thrombin and thrombomodulin inhibits both thrombin-catalyzed fibrin formation and factor V activation. J Biol Chem 1982; 257: 7944-7.
74. Esmon NL, Carroll RC, Esmon CT. Thrombomodulin blocks the ability of thrombin to activate platelets. J Biol Chem 1983; 258: 12238-42.
75. Yang L, Rezaie AR. The fourth epidermal growth factor-like domain of thrombomodulin interacts with the basic exosite of protein C. J Biol Chem 2003; 278: 10484-90.
76. Hayashi T, Zushi M, Yamamoto S, Suzuki K. Further localization of binding sites for thrombin and protein C in human thrombomodulin. J Biol Chem 1990; 265: 20156-9.
77. Fukudome K, Esmon CT. Identification, cloning, and regulation of a novel endothelial cell protein C/activated protein C receptor. J Biol Chem 1994; 269: 26486-91.
78. Fukudome K, Kurosawa S, Stearns-Kurosawa DJ, He X, Rezaie AR, Esmon CT. The endothelial cell protein C receptor. Cell surface expression and direct ligand binding by the soluble receptor. J Biol Chem 1996; 271: 17491-8.
79. Stearns-Kurosawa DJ, Kurosawa S, Mollica JS, Ferrell GL, Esmon CT. The endothelial cell protein C receptor augments protein C activation by the thrombin-thrombomodulin complex. Proc Natl Acad Sci USA 1996; 93: 10212-6.
80. Hall SW, Nagashima M, Zhao L, Morser J, Leung LL. Thrombin interacts with thrombomodulin, protein C, and thrombin-activatable fibrinolysis inhibitor via specific and distinct domains. J Biol Chem 1999; 274: 25510-6.
81. Bajzar L. Thrombin activatable fibrinolysis inhibitor and an antifibrinolytic pathway. Arterioscler Thromb Vasc Biol 2000; 20: 2511-8.
82. Marx PF. Thrombin-activatable fibrinolysis inhibitor. Curr Med Chem 2004; 11: 2335-48.
83. Nesheim M. Thrombin and fibrinolysis. Chest 2003; 124: 33S-9S.
84. Kokame K, Zheng X, Sadler JE. Activation of thrombin-activable fibrinolysis inhibitor requires epidermal growth factor-like domain 3 of thrombomodulin and is inhibited competitively by protein C. J Biol Chem 1998; 273: 12135-9.
85. Sheehan JP, Sadler JE. Molecular mapping of the heparin-binding exosite of thrombin. Proc Natl Acad Sci USA 1994; 91: 5518-22.
86. 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: 1301-5.
87. Tsiang M, Jain AK, Gibbs CS. Functional requirements for inhibition of thrombin by antithrombin III in the presence and absence of heparin. J Biol Chem 1997; 272: 12024-9.
88. Carter WJ, Cama E, Huntington JA. Crystal structure of thrombin bound to heparin. J Biol Chem 2005; 280: 2745-9.
89. Olson ST, Halvorson HR, Bjork I. Quantitative characterization of the thrombin-heparin interaction. Discrimination between specific and nonspecific binding models. J Biol Chem 1991; 266: 6342-52.
90. Huntington JA. Mechanisms of glycosaminoglycan activation of the serpins in hemostasis. J Thromb Haemost 2003; 1: 1535-49.
91. Huntington JA, Read RJ, Carrell RW. Structure of a serpin-protease complex shows inhibition by deformation. Nature 2000; 407: 923-6.
92. Tollefsen DM. Heparin cofactor II. Adv Exp Med Biol 1997; 425: 35-44.
93. Baglin TP, Carrell RW, Church FC, Esmon CT, Huntington JA. Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proc Natl Acad Sci USA 2002; 99: 11079-84.
94. Verhamme IM, Bock PE, Jackson CM. The preferred pathway of glycosaminoglycan-accelerated inactivation of thrombin by heparin cofactor II. J Biol Chem 2004; 279: 9785-95.
95. Olson ST, Bjork I, Shore JD. Kinetic characterization of heparin-catalyzed and uncatalyzed inhibition of blood coagulation proteinases by antithrombin. Methods Enzymol 1993; 222: 525-59.
96. Olson ST, Bjork 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: 6353-64.
97. Stone SR, Le Bonniec BF. Inhibitory mechanism of serpins. Identification of steps involving the active-site serine residue of the protease. J Mol Biol 1997; 265: 344-62.
98. Karshikov A, Bode W, Tulinsky A, Stone SR. Electrostatic interactions in the association of proteins: an analysis of the thrombin-hirudin complex. Protein Sci 1992; 1: 727-35.
99. Myles T, Le Bonniec BF, Betz A, Stone SR. Electrostatic steering and ionic tethering in the formation of thrombin-hirudin complexes: the role of the thrombin anion-binding exosite-I. Biochemistry 2001; 40: 4972-9.