Effect of zymogen domains and active site occupation on activation of prothrombin by von Willebrand factor-binding protein

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 39149-39157

  Kroh, Heather K ^a   Bock, Paul E ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION MECHANISMS; ACTIVE SITE; BLOOD COAGULATION; CATALYTIC DOMAINS; CONFORMATIONAL CHANGE; COOH-TERMINAL; EQUILIBRIUM BINDING; IRREVERSIBLE BINDING; KINETIC MECHANISM; PATHOPHYSIOLOGICAL; PROGRESS CURVES; PROTHROMBIN ACTIVATION; STAPHYLOCOCCUS AUREUS; SUBSTRATE BINDING; TERMINAL RESIDUES;

BACTERIA; CHEMICAL ACTIVATION; KETONES; PROTEINS;

GLYCOPROTEINS;

BLOOD CLOTTING FACTOR; ENZYME PRECURSOR; MEIZOTHROMBIN; PRETHROMBIN 1; PRETHROMBIN 2; PROTHROMBIN; THROMBIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; STRUCTURE ACTIVITY RELATION;

BINDING, COMPETITIVE; BLOOD COAGULATION; CARRIER PROTEINS; CATALYTIC DOMAIN; ENZYME PRECURSORS; FIBRIN; HEK293 CELLS; HUMANS; KINETICS; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTHROMBIN; RECOMBINANT PROTEINS; STAPHYLOCOCCUS AUREUS; THERMODYNAMICS; THROMBIN; VIRULENCE FACTORS; VON WILLEBRAND FACTOR;

STAPHYLOCOCCUS AUREUS;

EID: 84869063151     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.415562     Document Type: Article

References (46)

1. Goodey, N. M., and Benkovic, S. J. (2008) Allosteric regulation and catalysis emerge via a common route. Nat. Chem. Biol. 4, 474-482 (Pubitemid 352019763)
2. Bock, P. E., Panizzi, P., and Verhamme, I. M. (2007) Exosites in the substrate specificity of blood coagulation reactions. J. Thromb. Haemost. 5, (Suppl. 1), 81-94 (Pubitemid 46958821)
3. Huber, R., and Bode, W. (1978) Structural basis of the activation and action of trypsin. Acc. Chem. Res. 11, 114-122
4. Anderson, P. J., Nesset, A., and Bock, P. E. (2003) Effects of activation peptide bond cleavage and fragment 2 interactions on the pathway of exosite I expression during activation of human prethrombin 1 to thrombin. J. Biol. Chem. 278, 44482-44488 (Pubitemid 37377200)
5. Anderson, P. J., Nesset, A., Dharmawardana, K. R., and Bock, P. E. (2000) Characterization of proexosite I on prothrombin. J. Biol. Chem. 275, 16428-16434 (Pubitemid 30398862)
6. Monteiro, R. Q., Bock, P. E., Bianconi, M. L., and Zingali, R. B. (2001) Characterization of bothrojaracin interaction with human prothrombin. Protein Sci. 10, 1897-1904 (Pubitemid 32848786)
7. Doyle, M. F., and Mann, K. G. (1990) Multiple active forms of thrombin IV. Relative activities of meizothrombins. J. Biol. Chem. 265, 10693-10701
8. Verhamme, I. M., Olson, S. T., Tollefsen, D. M., and Bock, P. E. (2002) Binding of exosite ligands to human thrombin: re-evaluation of allosteric linkage between thrombin exosites I and II. J. Biol. Chem. 277, 6788-6798 (Pubitemid 34953060)
9. Petrera, N. S., Stafford, A. R., Leslie, B. A., Kretz, C. A., Fredenburgh, J. C., and Weitz, J. I. (2009) Long range communication between exosites 1 and 2 modulates thrombin function. J. Biol. Chem. 284, 25620-25629
10. Ye, J., Liu, L. W., Esmon, C. T., and Johnson, A. E. (1992) 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. 267, 11023-11028
11. Panizzi, P., Friedrich, R., Fuentes-Prior, P., Kroh, H. K., Briggs, J., Tans, G., Bode, W., and Bock, P. E. (2006) Novel fluorescent prothrombin analogs as probes of staphylocoagulase-prothrombin interactions. J. Biol. Chem. 281, 1169-1178
12. Panizzi, P., Friedrich, R., Fuentes-Prior, P., Richter, K., Bock, P. E., and Bode, W. (2006) Fibrinogen substrate recognition by staphylocoagulase-(pro) thrombin complexes. J. Biol. Chem. 281, 1179-1187
13. Kroh, H. K., Panizzi, P., and Bock, P. E. (2009) Von Willebrand factor binding-protein is a hysteretic conformational activator of prothrombin. Proc. Natl. Acad. Sci. U.S.A. 106, 7786-7791
14. Friedrich, R., Panizzi, P., Fuentes-Prior, P., Richter, K., Verhamme, I., Anderson, P. J., Kawabata, S., Huber, R., Bode, W., and Bock, P. E. (2003) Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature 425, 535-539 (Pubitemid 37237051)
15. Frieden, C. (1970) Kinetic aspects of regulation of metabolic processes: the hysteretic enzyme concept. J. Biol. Chem. 245, 5788-5799
16. Frieden, C. (1979) Slow transitions and hysteretic behavior in enzymes. Annu. Rev. Biochem. 48, 471-489
17. Bock, P. E., Olson, S. T., and Björk, I. (1997) Inactivation of thrombin by antithrombin is accompanied by inactivation of regulatory exosite I. J. Biol. Chem. 272, 19837-19845 (Pubitemid 27340078)
18. Bock, P. (1992) Active-site-selective labeling of blood coagulation proteinases with fluorescence probes by the use of thioester peptide chloromethyl ketones. I. Specificity of thrombin labeling. J. Biol. Chem. 267, 14963-14973
19. Carlisle, T. L., Bock, P. E., and Jackson, C. M. (1990) Kinetic intermediates in prothrombin activation: bovine prethrombin 1 conversion to thrombin by factor X. J. Biol. Chem. 265, 22044-22055 (Pubitemid 120023918)
20. Kamath, P., and Krishnaswamy, S. (2008) Fate of membrane-bound reactants and products during the activation of human prothrombin by prothrombinase. J. Biol. Chem. 283, 30164-30173
21. Orcutt, S. J., and Krishnaswamy, S. (2004) Binding of substrate in two conformations to human prothrombinase drives consecutive cleavage at two sites in prothrombin. J. Biol. Chem. 279, 54927-54936 (Pubitemid 40053239)
22. Newell-Caito, J. L., Laha, M., Tharp, A. C., Creamer, J. I., Xu, H., Maddur, A. A., Tans, G., and Bock, P. E. (2011) Notecarin D binds human factor V and factor Va with high affinity in the absence of membranes. J. Biol. Chem. 286, 38286-38297
23. Bock, P. E. (1992) Active-site-selective labeling of blood coagulation proteinases with fluorescence 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. 267, 14974-14981
24. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global Kinetic Explorer: A new computer program for dynamic simulation and fitting of kinetic data. Anal. Biochem. 387, 20-29
25. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) FitSpace Explorer: An algorithm to evaluate multi-dimensional parameter space in fitting kinetic data. Anal. Biochem. 387, 30-41
26. Mac Sweeney, A., Birrane, G., Walsh, M. A., O'Connell, T., Malthouse, J. P., and Higgins, T. M. (2000) Crystal structure of δ-chymotrypsin bound to a peptidyl chloromethyl ketone inhibitor. Acta Crystallogr.DBiol. Crystallogr. 56, 280-286 (Pubitemid 30147178)
27. Panizzi, P., Friedrich, R., Fuentes-Prior, P., Bode, W., and Bock, P. E. (2004) The staphylocoagulase family of zymogen activator and adhesion proteins. Cell. Mol. Life Sci. 61, 2793-2798 (Pubitemid 40064327)
28. Huang, M., Rigby, A. C., Morelli, X., Grant, M. A., Huang, G., Furie, B., Seaton, B., and Furie, B. C. (2003) Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat. Struct. Biol. 10, 751-756 (Pubitemid 37052415)
29. 2+ prothrombin fragment 1 including the conformation of the Gla domain. Biochemistry 28, 6805-6810
30. 2+ ion and membrane binding structure of the Gla domain of Ca-prothrombin fragment 1. Biochemistry 31, 2554-2566
31. Chen, Z., Pelc, L. A., and Di Cera, E. (2010) Crystal structure of prethrombin-1. Proc. Natl. Acad. Sci. U.S.A. 107, 19278-19283
32. Church, F. C., Lundblad, R. L., Noyes, C. M.Tarvers, R. C. (1985) Effect of divalent cations on the limited proteolysis of prothrombin by thrombin. Arch. Biochem. Biophys. 240, 607-612 (Pubitemid 15250072)
33. 56 and catalytic activity. J. Biol. Chem. 271, 8062-8067
34. 155 promotes the release of thrombin from the catalytic surface during the activation of bovine prothrombin. J. Biol. Chem. 263, 1037-1044
35. Anderson, P. J., and Bock, P. E. (2003) Role of prothrombin fragment 1 in the pathway of regulatory exosite I formation during conversion of human prothrombin to thrombin. J. Biol. Chem. 278, 44489-44495 (Pubitemid 37377201)
36. Kamath, P., Huntington, J. A., and Krishnaswamy, S. (2010) Ligand binding shuttles thrombin along a continuum of zymogen- and proteinase-like states. J. Biol. Chem. 285, 28651-28658
37. Changeux, J. P., and Edelstein, S. (2011) Conformational selection or induced fit? 50 years of debate resolved. F1000 Biol. Rep. 3, 19
38. Khan, A. R., and James, M. N. (1998) Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Protein Sci. 7, 815-836 (Pubitemid 28216525)
39. Narayana, S. V., Carson, M., el-Kabbani, O., Kilpatrick, J. M., Moore, D., Chen, X., Bugg, C. E., Volanakis, J. E., and DeLucas, L. J. (1994) Structure of human factor D: A complement system protein at 2.0 Ä resolution. J. Mol. Biol. 235, 695-708
40. Page, M. J., Macgillivray, R. T., and Di Cera, E. (2005) Determinants of specificity in coagulation proteases. J. Thromb. Haemost. 3, 2401-2408 (Pubitemid 41727155)
41. Petrovan, R. J., and Ruf, W. (2002) Role of zymogenicity-determining residues of coagulation factor VII/VIIa in cofactor interaction and macromolecular substrate recognition. Biochemistry 41, 9302-9309 (Pubitemid 34810004)
42. Olsen, O. H., and Persson, E. (2008) Cofactor-induced and mutational activity enhancement of coagulation factor VIIa. Cell Mol. Life Sci. 65, 953-963
43. Eigenbrot, C., and Kirchhofer, D. (2002)Newinsight into how tissue factor allosterically regulates factor VIIa. Trends Cardiovasc. Med. 12, 19-26 (Pubitemid 34048707)
44. Vijayalakshmi, J., Padmanabhan, K. P., Mann, K. G., and Tulinsky, A. (1994) The isomorphous structures of prethrombin2, hirugen-, and PPACK-thrombin: Changes accompanying activation and exosite binding to thrombin. Protein Sci. 3, 2254-2271
45. Petrovan, R. J., Govers-Riemslag, J. W., Nowak, G., Hemker, H. C., Tans, G., and Rosing, J. (1998) Autocatalytic peptide bond cleavages in prothrombin and meizothrombin. Biochemistry 37, 1185-1191 (Pubitemid 28135703)
46. Atkinson, B. T., Jasuja, R., Chen, V. M., Nandivada, P., Furie, B., and Furie, B. C. (2010) Laser-induced endothelial cell activation supports fibrin formation. Blood 116, 4675-4683