Comparative Analysis of Haemostatic Proteinases: Structural Aspects of Thrombin, Factor Xa, Factor IXa and Protein C

• References

• 1 Davie EW, Fujikawa K, and Kisiel W. The coagulation cascade: Initiation, maintenance, and regulation. Biochemistry 30: 10364-10370 1991;
• 2 Ruf W, and Edgington TS. Structural biology of tissue factor, the initiator of thrombogenesis in vivo. FASEB J 8: 385-390 1994;
• 3 Mann KG. The assembly of blood clotting complexes on membranes. Trends Biochem. Sci 12: 229-233 1987;
• 4 Esmon CT. The roles of protein C and thrombomodulin in the regulation of blood coagulation. J. Biol. Chem. 264: 4743-4746 1989;
• 5 Stubbs MT, & Bode W. Coagulation factors and their inhibitors. Curr. Op. Struct. Biol. 1994; 4: 823-832
• 6 Bode W, Mayr I, Baumann U, Huber R, Stone SR, & Hofeteenge J. The refined 1.9Acrystal structure of human a-thrombin: Interaction with D-Phe-Pro-Arg chloromethlyketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J 8: 3467-3475 1989;
• 7 Bode W, Turk D, and Karshikov A. The refined 1.9 Å X-ray crystal structure of D-PheProArg chloromethylketone inhibited human a-thrombin. Structure analysis, overall structure, electrostatic properties, detailed active site geometry, structure-function relationships. Protein Sci 1: 426-471 1992;
• 8 Stubbs MT, & Bode W. A player of many parts: the spotlight falls on thrombin’s structure. Thrombosis Research 69: 1-58 1993;
• 9 Stubbs MT, & Bode W. 1995; The clot thickens… clues provided by thrombin structure. Trends Biochem. Sci 20: 23-28
• 10 Padmanabhan K, Padmanabhan KP, Tulinsky A, Park CH, Bode W, Huber R, Blankenship DT, Cardin AD, & Kisiel W. 1993; Structure of human des(l-45) Factor Xa at 2.2 Å resolution. J. Mol. Biol 232: 947-966
• 11 Brandstetter H, Kühne A, Bode W, Huber R, von der Saal W, Wirthensohn K, & Engh RA. 1996; X-ray structure of the active site inhibited clotting factor Xa: Implications for drug design and substrate recognition. J. Biol. Chem 271: 29988-29992
• 12 Brandstetter H, Bauer M, Huber R, Lollar P, & Bode W. 1995; X-ray structure of clotting factor IXa: Active site and module structure related to Xase activity and hemophilia B. Proc. Natl. Acad. Sci. USA 92: 9796-9800
• 13 Mather T, Oganessyan V, Hof P, Huber R, Foundling S, Esmon C, and Bode W. 1996; The 2.8Acrystal structure of Gla-domainless activated protein C. EMBO J 15: 6822-6831
• 14 Banner DW, D’Arcy A, Chene C, Winkler FW, Guha A, Konigsberg WH, Nemerson Y, & Kirchhofer D. 1996; The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 380: 41-46
• 15 Banner DW. (this volume, p. 512)
• 16 Carrell RW. (this volume, ;p. 516)
• 17 Seshadri TP, Tulinsky A, Skrzypczak-Jankun E, and Park CH. Structure of bovine prothrombin fragment 1 refined at 2.25Aresolution. J. Mol. Biol 220: 481-494 1991;
• 18 Sunnerhagen M, Forsen S, Hoffren AM, Drakenberg T, Teleman O, & Stenflo J. 1995; Structure of the Ca²⁺free Gla domain sheds light on membrane binding of blood coagulation factors. Nature Struct. Biol 2: 504-509
• 19 Freedman SJM, Furie BC, Furie B, & Baleja JD. 1995; Structure of the metal-free gamma-carboxyglutamic acid-rich membrane binding region of factor IX by two-dimensional NMR spectroscopy. J. Biol. Chem 270: 7980-7989
• 20 Soriano-Garcia M, Padmanabhan K, deVos AM, and Tulinsky A. The Ca²⁺ion and membrane binding structure of the Gla domain of Ca-prothrombin fragment 1. Biochemistry 5i: 2554-2566 1992;
• 21 Freedman SJ, Furie BC, Furie B, Baleja JD. 1995; Structure of the calcium ion-bound gamma-carboxyglutamic acid-rich domain of factor IX. Biochemistry 34: 12126-12137
• 22 Freedman SJ, Blostein MD, Baleja JD, Jacobs M, Furie BC, Furie B. 1996; Identification of the phospholipid binding site in the vitamin K-dependent blood coagulation protein factor IX. Biol. Chem 271: 16227-16236
• 23 Huber R, & Bode W. 1978; Structural basis of the activation and action of trypsin. Accounts of Chemical Research 11: 114-122
• 24 van DieijenG, Tans G, Rosing J, & Hemker HC. 1981; The role of phospholipid and factor Villa in the activation of bovine factor X. J. Biol. Chem 256: 34333-3442
• 25 Mann KG, Nesheim ME, Church WR, Haley P, & Krishnaswamy S. Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 16: 1-16 1990;
• 26 Coughlin SR. 1994; Thrombin receptor function and cardiovascular disease. Trends Cardiovasc. Med 4: 77-83
• 27 Olson ST, & Björk I. 1992. Regulation of thrombin by antithrombin and heparin cofactor II. In Thrombin: Structure and function. Ed. Berliner LJ. New York: Plenum Press; pp 159-217
• 28 Ascenzi P, Coletta M, Amiconi G, De CristofaroR, Bolognesi M, Guarneri M, & Menegatti E. 1988; Binding of the bovine pancreatic trypsin inhibitor (Kunitz) to human a-, b- and g-thrombin; a kinetic and thermodynamic study. Biochim. Biophys. Acta 956: 156-161
• 29 Priestle JP, Rahuel J, Rink H, Tones M, & Grütter MG. 1993; Changes in interactions in complexes of hirudin derivatives and human a-thrombin due to different crystal forms. Protein Science 2: 1630-1642
• 30 Engh R, Brandstetter H, Sucher G, Baumann U, Kühne A, Eichinger A, Bode W, Huber R, Poll T, Rudolph R, & von derSaal W. 1996; Enzyme flexibility, solvent and ‘weak’ interactions characterize thrombin-ligand interactions: implications for drug design. Structure 15: 1353-1362
• 31 Rydel TJ, Tulinsky A, Bode W, & Huber R. 1991; Refined Structure of the Hirudin - Thrombin Complex. J. Mol. Biol 221: 583-601
• 32 van de, Locht A, Lamba D, Bauer M, Huber R, Friedrich T, Kröger B, Höffken W, & Bode W. 1995; Two heads are better than one: crystal structure of the insect derived double domain Kazal inhibitor rhodniin in complex with thrombin. EMBOJ 14: 5149-5157
• 33 van de, Locht A, Stubbs MT, Bode W, Friedrich T, Bollschweiler C, Höffken W, & Huber R. 1996; The Omithodorin:Thrombin Crystal Structure, a Key to the TAP Enigma. EMBO 15: 6011-6017
• 34 Stubbs MT, Oschkinat H, Mayr I, Huber R, Angliker H, Stone SR, & Bode W. The interaction of thrombin with fibrinogen - a structural basis for its specificity. Eur. J. Biochem 206: 187-195 1992;
• 35 Martin RD, Robertson W, Turk D, Bode W, & Edwards FP. 1992; The structure of residues 7-16 of the Aa-chain of human fibrinogen bound to bovine thrombin at 2.3 A resolution. J. Biol. Chem 267: 7911-7920
• 36 Stubbs MT, & Bode W. 1993; A model for the specificity of fibrinogen cleavage by thrombin. Semin. Thromb. Hemost 19: 344-351
• 37 Qiu X, Padmanabhan K, Carperos VE, Tulinsky A, Kline T, Maraganore JM, and Fenton II J.W. The structure of the hirulog3-thrombin complex and the nature of the S ’ subsites of substrates and inhibitors. Biochemistry 31: 11689-11697 1992;
• 38 Martin PD, Malkowski MG, DiMaio J, Konishi Y, Ni F, & Edwards B.FP. 1996; Bovine thrombin complexed with an uncleavable analog of residues 7-19 of fibrinogen Aa: Geometry of the catalytic triad and interactions of the PI’, P2’ and P3’ substrate residues. Biochemistry 35: 13030-13039
• 39 Stephens AW, Thalley BS, & Hirs C.HW. 1987; Anti-thrombin-in Denver, a reactive site variant. J. Biol Chem 262: 1044-1048
• 40 Stephens AW, Siddiqui A, & Hirs C.HW. 1988; Site directed mutagenesis of the reactive center (Serine 394) of antithrombin III.J. Biol. Chem 263: 15849-15852
• 41 Theunissen HJ.M, Dijkema R, Grootenhuis P.D.J, Swinkels JC, Poorter TL, Carati P, and Visser A. 1993; Dissociation of heparin-dependent thrombin and factor Xa inhibitory activities of antithrombin-III by mutations in the reactive site. J. Biol. Chem 268: 9035-9040
• 42 Morenweiser R, Auerswald EA, van deLocht A, Fritz H, Stürzebecher J, & Stubbs MT. Structure-based design of a potent chimeric thrombin inhibitor. Submitted for publication.
• 43 Wu Q, Sheehan JP, Tsiang M, Lentz SR, Birktoft JJ, & Sadler JE. 1991; Single amino acid substitutions dissociate fibrinogen-clotting and thrombomodulin-binding activities of human thrombin. Proc. Natl. Acad. Sci. USA 88: 6775-6779
• 44 Tsiang M, Jain AK, Dunn KE, Rojas ME, Leung L.L.K, & Gibbs CS. 1995; Functional mapping of the surface residues of human thrombin. J. Biol. Chem 270: 16854-16863
• 45 Le BonniecB F, Myles T, Johnson T, Knight CG, Tapparelli C, & Stone SR. 1996; Characterization of the P2’ and P3’ specificities of thrombin using fluorescence-quenched substrates and mapping of the subsites by mutagenesis. Biochemistry 35: 7114-7122
• 46 Le BonniecB F, & Esmon CT. 1991; Glul92®Gln substitution in thrombin mimics the catalytic switch induced by thrombomodulin. Proc. Natl. Acad. Sci. USA 88: 7371-1315
• 47 Le BonniecB F, MacGillivray RT, & Esmon CT. 1991; Thrombin Glu39 restricts the P3¹specificity to nonacidic residues. J. Biol. Chem 266: 13796-13803
• 48 Griffith MJ, Noyes CM, Tyndall JA, & Church FC. 1985; Structural evidence for leucine at the reactive site of heparin cofactor II. Biochemistry 24: 6777-6782
• 49 Ragg H. 1986; A new member of the plasma protease inhibitor gene family. Nucleic Acids Research 14: 1073-1088
• 50 Van DeerlinV M.D, andTollefsen DM. 1991; The N-terminal acidic domain of heparin cofactor II mediates the inhibition of a-thrombin in the presence of glycosaminoglycans. J. Biol. Chem 266: 20223-20231
• 51 Ragg H, Ulshofer T, and Gerewitz J. 1990; On the activation of human Leuserpin-2, a thrombin inhibitor, by glycosaminoglycans. J. Biol. Chem 265: 5211-5218
• 52 Rogers SJ, Pratt CW, Whinna HC, and Church FC. 1992; Role of thrombin exosites in inhibition by heparin cofactor II. J. Biol. Chem 267: 3613-3617
• 53 Gershkovich AA. 1996; Regulation of thrombin activity by ligand-induced conformational changes: a review. Biochemistry (Moscow) 61: 817-824
• 54 Wells CM, & di Cera E. 1992; Thrombin is a Na⁺-activated enzyme. Biochemistry, 31: 11721-11730
• 55 Ayala Y, & di Cera E. 1994; Molecular recognition by thrombin: role of the slow Æfast transition, site-specific ion binding eregetics and thermodynamic mapping of structural components. J. Mol. Biol 235: 733-746
• 56 di Cera E, Guinto ER, Vindigni A, Dang QD, Ayala YM, Wuyi M, & Tulinsky A. 1995; The Na⁺binding site of thrombin. J. Biol. Chem 270: 22089-22092
• 57 Gibbs CS, Coutre SE, Tsiang M, Li W.-X, Jain AK, Dunn KE, Law VS, Mao CT, Matsumura SY, Mejza SJ, Paborsky LR, & Leung L.L.K. 1995; Conversion of thrombin into an anticoagulant by protein engineering. Nature 378: 413-416
• 58 Miyata T, Aruga R, Umeyama H, Bezeaud A, Guillin MC, & Iwanaga S. 1992; Prothrombin Salakta: Substitution of glutamic acid-466 by alanine reduces the fibrinogen clotting activity and the esterase activity. Biochemistry 31: 7457-7462
• 59 Le BonniecB F, Guinto GR, and Esmon CT. Interaction of thrombin des-ETW with antithrombin III, the Kunitz inhibitors, thrombomodulin and protein C. Structural link between the autolysis loop and the Tyr-Pro-Pro-Tip insertion of thrombin. J.Biol. Chem 267: 19341-19348 1992;
• 60 Parry M.A.A, Stone SR, Hofsteenge J, & Jackman P. 1993; Evidence for common structural changes in thrombin induced by active-site or exosite binding. Biochem. J 290: 665-670
• 61 de CristofaroR, Rocca B, Bizzi B, & Landolfi R. 1993; The linkage between binding of the C-terminal domain of hirudin and amidase activity in human a-thrombin. Biochemical Journal 289: 475-80
• 62 de CristofaroR, de Candia E, Picozzi M, & Landolfi R. 1995; Conformational transformations linked to active site ligation in human thrombin: effect on the interaction with fibrinogen and the cleavable platelet receptor. J. Mol. Biol., 245: 447-458
• 63 Skrzypczak-Jankun E, Carperos V, Ravichandran KG, Tulinsky A, Westbrook M, and Maraganore J. The structure of the hirugen and hirulog 1 complexes of a-thrombin. J. Mol. Biol 221: 1379-1393 1991;
• 64 Mathews II, Padmanabhan KP, und Tulinsky A. 1994; Structure of a nonadecapeptide of the fifth EGF domain of thrombomodulin complexed with thrombin. Biochemistry 33: 13547-13552
• 65 Vijayalakshmi J, Padmanabhan KP, Mann KG, & Tulinsky A. 1994; The isomorphous structures of prethrombin 2, hirugen-, and PPACK-thrombin: changes accompanying activation and exosite binding to thrombin. Protein Sci 3: 2254-2271
• 66 Ye J, Esmon NL, Esmon CT, & Johnson AE. 1991; The active site of thrombin is altered upon binding to thrombomodulin. J. Biol. Chem 266: 23016-23021
• 67 Guinto ER, Ye J, Le BonniecB F, & Esmon CT. 1994; Glu¹⁹²→Gin substitution in thrombin yields an enzyme that is effectively inhibited by bovine pancreatic trypsin inhibitor and tissue factor pathway inhibitor. J. Biol Chem 269: 18395-18400
• 68 Rezaie AR, & Esmon CT. 1995; Contribution of residue 192 in factor Xa to enzyme specificity and function. J. Biol. Chem 270: 16176-16181
• 69 Neuenschwander PF, & Morrissey JH. 1995; Alteration of the substrate and inhibitor specificities of blood coagulation factor VIIa: Importance of amino acid residue K192. Biochemistry 34: 8701-8707
• 70 Rezaie A, and Esmon C. 1993; Conversion of glutamic acid 192 to glutamine in activated protein C changes the substrate specificity and increases reactivity toward macromolecular inhibitors. Biol. Chem 268: 19943-19948
• 71 Duffy EJ, Angliker H, Le BonniecB F, & Stone SR. 1997; Allosteric modulation of the activity of thrombin. Biochem. J 321: 361-365
• 72 Friedrich T, Kröger B, Biolajan S, Lemaire HG, Höffken HW, Reuschenbach P, Otte M, and Dodt J. 1993; AKazal- type inhibitor with thrombin specificity fromRhodniusprolixus. J. Biol. Chem 268: 16216-16222
• 73 Le BonniecB F, Guinto ER, MacGillivray RT, Stone SR, & Esmon CT. 1993; The role of thrombin’s Tyr-Pro-Pro-Trp motif in the interaction with fibrinogen, thrombomodulin, protein C, antithrombin III, and the Kunitz inhibitors. J. Biol. Chem 268: 19055-19061
• 74 van deLochtA, Bode W, Huber R, Le BonniecB F, Stone SR, Esmon CT, & Stubbs MT. 1997. The thrombin E192Q:BPTI-complex reveals gross structural rearrangements: implications for the interaction with antithrombin. EMBO J. in the press
• 75 Engh RA, Huber R, Bode W, & Schulze AJ. 1995; Divining the serpin inhibition mechanism: a suicide substrate ‘springe’. Trends Biotech 13: 503-510
• 76 Le BonniecB F, Guinto ER, & Stone SR. 1995; Identification of thrombin residues that modulate its interactions with antithrombin III and a₁-antitrypsin. Biochemistry 34: 12241-12248
• 77 Rezaie AR. 1996; Tryptophan 60D in the B-insertion loop of thrombin modulates the thrombin-antithrombin reaction. Biochemistry 35: 1918-1924
• 78 Krishnaswamy S, Church WR, Nesheim ME, & Mann KG. 1987; Activation of human prothrombin by prothrombinase. Influence of factor Va on the reaction mechanism. J. Biol. Chem 262: 3291-3299
• 79 Doyle MF, & Mann KG. 1990; Multiple active forms of thrombin. IV. Relative activities of meizothrombins. J. Biol. Chem 265: 10693-10701
• 80 Kaczmarek E, Kaminski M, & McDonagh J. 1987; Fibrino-gen-sepharose interaction with prothrombin, prethrombin 1, prethrombin 2 and thrombin. Biochim. Biophys. Acta 914: 275-282
• 81 Arni RK, Padmanabhan K, Padmanabhan KP, Wu TP, & Tulinsky A. Structures of the non-covalent complexes of human and bovine prothrombin fragment 2 with human PPACK-thrombin. Biochemistry 32: 4727-4737 1993;
• 82 Liu L.-W, Ye J, Johnson AE, & Esmon CT. Proteolytic formation of either of the two prothrombin activation intermediates results in formation of a hirugen binding site. J. Biol. Chem 266: 23632-23636 1991;
• 83 Ni F, Ning Q, Jackson CM, & Fenton II J.W. 1993; Thrombin exosite for fibrinogen recognition is partially accessible in prothrombin. J. Biol. Chem 268: 16899-16902
• 84 van de, Locht A, Stubbs MT, Bauer M, & Bode W. 1996; Crystallographic evidence that the F2 Kringle catalytic domain linker of prothrombin does not cover the fibrinogen recognition exosite. J. Biol. Chem 03: 3413-3416
• 85 Burgering MJ M, Orbons L.P.M, van derDoelen A, Mulders J, Theunissen H.J.M, Grootenhuis PJ.M, Bode W, Huber R, & Stubbs MT. 1997 The second Kunitz domain of human tissue factor pathway inhibitor. Cloning, structure determination and interaction with factor Xa. J. Mol. Biol in the press
• 86 Stubbs MT, Huber R, & Bode W. 1995; Crystal structures of factor Xa specific inhibitors in complex with trypsin: Structural grounds for inhibition of factor Xa and selectivity against thrombin. FEBS Lett 375: 103-107
• 87 Stubbs MT. 1996; Structural aspects of factor Xa inhibition. Current Pharmaceutical Design 02: 543-552
• 88 Broze Jr GJ. (1995) Tissue factor pathway inhibitor. Thromb. Haemost 14: 90-93
• 89 Castillo MJ, Kurachi K, Nishino N, Okkubo F, & Powers JC. 1983; Reactivity of bovine blood coagulation factor IXa beta, factor Xa beta, and factor XIa toward fluorogenic peptides containing the activation site sequences of bovine factor IX and factor X. Biochemistry 22: 1021-1029
• 90 Kam CM, Kerrigan JE, Plaskon RR, Duffy EJ, Lollar P, Suddath FL, & Powers JC. 1994; Mechanism-based isocoumarin inhibitors for blood coagulation serine proteases. Effect of the 7-substituent in 7-amino-4-chloro-3- (isothioureidoalkoxy)isocoumarins on inhibitory and anticoagulant potency. J. Med. Chem 37: 1298-1306
• 91 Sunnerhagen M, Olah GA, Stenflo J, Forsen S, Drakenberg T, & Trewhella J. 1996; The relative orientation of Gla and EGF domains in coagulation factor X is altered by Ca²⁺binding to the first EGF domain. A combined NMR-small angle X-ray scattering study. Biochemistry 35: 11547-11559
• 92 Bottema CD, Ketterling RP, Ii S, Yoon HS, Phillips III J.A, & Sommer SS. 1991; Missense mutations and evolutionary conservation of amino acids: evidence that many of the amino acids in factor IX function as “spacer” elements. Am. J. Hum. Genet 49: 820-838
• 93 Roberts HR. 1993; Molecular biology of hemophilia B. Thromb. Haemost 70: 1-9
• 94 Gianelli F, Green PM, Sommer SS, Lillicrap DP, Ludwig M, Schwaab R, Reitsma PH, Goossens M, & Brownlee GG. 1994; Haemophilia B: database of point mutations and short additions and deletions, fifth edition, 1994. Nucleic Acids Res 22: 3534-3546
• 95 Pratt CW, Whinna HC, & Church FC. 1992; A comparison of three heparin-binding serine protease inhibitors. J. Biol. Chem 267: 8795-8801
• 96 Hermans JM, & Stone SR. 1993; Interaction of activated protein C with serpins. Biochem. J 295: 239-245
• 97 Holly R, & Foster DC. 1994; Resistance to inhibition by al-antitrypsin and species specificity of a chimeric human/ bovine protein C. Biochemistry 33: 1876-1880