An ensemble view of thrombin allostery

Biological Chemistry

Volumn 393, Issue 9, 2012, Pages 889-898

  Lechtenberg, Bernhard C ^a   Freund, Stefan M V ^b   Huntington, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Coagulation; NMR spectroscopy; Plasticity; Protease; Zymogen

Indexed keywords

CALCIUM ION; ENZYME PRECURSOR; HIRUGEN; PROTEINASE; PROTHROMBIN; THROMBIN;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ANTICOAGULATION; BLOOD CLOTTING; CARBOXY TERMINAL SEQUENCE; CONFERENCE PAPER; ENZYME ACTIVE SITE; HUMAN; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; THROMBOSIS;

ALLOSTERIC REGULATION; MODELS, MOLECULAR; THROMBIN;

EID: 84869443502     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0178     Document Type: Conference Paper

References (56)

1. 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.
2. 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.
3. 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.
4. Arni, R.K., Padmanabhan, K., Padmanabhan, K.P., Wu, T.P., and Tulinsky, A. (1993). Structures of the noncovalent complexes of human and bovine prothrombin fragment 2 with human PPACKthrombin. Biochemistry 32, 4727-4737.
5. Ayala, Y. and Di Cera, E. (1994). Molecular recognition by thrombin. Role of the slow →fast transition, site-specifi c ion binding energetics and thermodynamic mapping of structural components. J. Mol. Biol. 235, 733-746.
6. Bah, A., Garvey, L.C., Ge, J., and Di Cera, E. (2006). Rapid kinetics of Na+binding to thrombin. J. Biol. Chem. 281, 40049-40056.
7. Bode, W. (1979). The transition of bovine trypsinogen to a trypsinlike state upon strong ligand binding. II. The binding of the pancreatic trypsin inhibitor and of isoleucine-valine and of sequentially related peptides to trypsinogen and to p -guanidinobenzoate- trypsinogen. J. Mol. Biol. 127, 357-374.
8. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S.R., and Hofsteenge, J. (1989). The refi ned 1.9 Å crystal structure of human α-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and signifi cance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475.
9. Boehr, D.D., Dyson, H.J., and Wright, P.E. (2006). An NMR perspective on enzyme dynamics. Chem. Rev. 106, 3055-3079.
10. Boehr, D.D., Nussinov, R., and Wright, P.E. (2009). The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796.
11. Carter, W.J., Cama, E., and Huntington, J.A. (2005). Crystal structure of thrombin bound to heparin. J. Biol. Chem. 280, 2745-2749.
12. Croy, C.H., Koeppe, J.R., Bergqvist, S., and Komives, E.A. (2004). Allosteric changes in solvent accessibility observed in thrombin upon active site occupation. Biochemistry 43, 5246-5255.
13. Davie, E.W. and Ratnoff, O.D. (1964). Waterfall sequence for intrinsic blood clotting. Science 145, 1310-1312.
14. De Cristofaro, R. and Landolfi, R. (1999). Allosteric modulation of BPTI interaction with human α- and ξ-thrombin. Eur. J. Biochem. 260, 97-102.
15. De Cristofaro, R., Picozzi, M., Morosetti, R., and Landolfi, R. (1996). Effect of sodium on the energetics of thrombin-thrombomodulin interaction and its relevance for protein C hydrolysis. J. Mol. Biol. 258, 190-200.
16. De Filippis, V., Colombo, G., Russo, I., Spadari, B., and Fontana, A. (2002). Probing the hirudin-thrombin interaction by incorporation of noncoded amino acids and molecular dynamics simulation. Biochemistry 41, 13556-13569.
17. De Filippis, V., Dea, E.D., Lucatello, F., and Frasson, R. (2005). Effect of Na+ binding on the conformation, stability and molecular recognition properties of thrombin. Biochem. J. 390, 485-492.
18. Di Cera, E., Dang, Q.D., and Ayala, Y.M. (1997). Molecular mechanisms of thrombin function. Cell. Mol. Life Sci. 53, 701-730.
19. Fehlhammer, H., Bode, W., and Huber, R. (1977). Crystal structure of bovine trypsinogen at 1-8 Å resolution. II. Crystallographic refi nement, refi ned crystal structure and comparison with bovine trypsin. J. Mol. Biol. 111, 415-438.
20. Freer, S.T., Kraut, J., Robertus, J.D., Wright, H.T., and Xuong, N.H. (1970). Chymotrypsinogen: 2.5-angstrom crystal structure, comparison with α-chymotrypsin, and implications for zymogen activation. Biochemistry 9, 1997-2009.
21. Friedrich, R., Panizzi, P., Fuentes-Prior, P., Richter, K., Verhamme, I., Anderson, P.J., Kawabata, S.-I., 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.
22. Gianni, S., Ivarsson, Y., Bah, A., Bush-Pelc, L.A., and Di Cera, E. (2007). Mechanism of Na+ binding to thrombin resolved by ultrarapid kinetics. Biophys. Chem. 131, 111-114.
23. Henzler-Wildman, K.A., Thai, V., Lei, M., Ott, M., Wolf-Watz, M., Fenn, T., Pozharski, E., Wilson, M.A., Petsko, G.A., Karplus, M., et al. (2007). Intrinsic motions along an enzymatic reaction trajectory. Nature 450, 838-844.
24. Higashi, S., Nishimura, H., Aita, K., and Iwanaga, S. (1994). Identifi cation of regions of bovine factor VII essential for binding to tissue factor. J. Biol. Chem. 269, 18891-18898.
25. Hilser, V.J. (2010). An ensemble view of allostery. Science 327, 653-654.
26. Hoffman, M. (2003). Remodeling the blood coagulation cascade. J. Thromb. Thrombolysis 16, 17-20.
27. Hoffman, M. and Monroe, D.M. (2007). Coagulation 2006: a modern view of hemostasis. Hematol. Oncol. Clin. North Am. 21, 1-11.
28. Huntington, J.A. (2005). Molecular recognition mechanisms of thrombin. J. Thromb. Haemost. 3, 1861-1872.
29. Huntington, J.A. (2008a). Structural insights into the life history of thrombin. In: Recent Advances in Thrombosis and Hemostasis, K. Tanaka and E. Davie, eds. (Japan, Tokyo: Springer), pp. 80-106.
30. Huntington, J.A. (2008b). How Na+ activates thrombin - a review of the functional and structural data. Biol. Chem. 389, 1025-1035.
31. 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.
32. Koeppe, J.R. and Komives, E.A. (2006). Amide H/2H exchange reveals a mechanism of thrombin activation. Biochemistry 45, 7724-7732.
33. Koshland, D.E., Némethy, G., and Filmer, D. (1966). Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5, 365-385.
34. Krishnaswamy, S., Mann, K.G., and Nesheim, M.E. (1986). The prothrombinase-catalyzed activation of prothrombin proceeds through the intermediate meizothrombin in an ordered, sequential reaction. J. Biol. Chem. 261, 8977-8984.
35. Kroh, H.K., Tans, G., Nicolaes, G.A.F., Rosing, J., and Bock, P.E. (2007). Expression of allosteric linkage between the sodium ion binding site and exosite I of thrombin during prothrombin activation. J. Biol. Chem. 282, 16095-16104.
36. Lechtenberg, B.C., Johnson, D.J.D., Freund, S.M.V., and Huntington, J.A. (2010). NMR resonance assignments of thrombin reveal the conformational and dynamic effects of ligation. Proc. Natl. Acad. Sci. USA 107, 14087-14092.
37. Liu, L.W., Ye, J., Johnson, A.E., and Esmon, C.T. (1991). Proteolytic formation of either of the two prothrombin activation intermediates results in formation of a hirugen-binding site. J. Biol. Chem. 266, 23633-23636.
38. Macfarlane, R.G. (1964). An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifi er. Nature 202, 498-499.
39. Monod, J., Wyman, J., and Changeux, J.P. (1965). On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12, 88-118.
40. Monroe, D.M. and Hoffman, M. (2006). What does it take to make the perfect clot? Arterioscler. Thromb. Vasc. Biol. 26, 41-48.
41. Orthner, C.L. and Kosow, D.P. (1980). Evidence that human α-thrombin is a monovalent cation-activated enzyme. Arch. Biochem. Biophys. 202, 63-75.
42. Parry, M.A., Stone, S.R., Hofsteenge, J., and Jackman, M.P. (1993). Evidence for common structural changes in thrombin induced by active-site or exosite binding. Biochem. J. 290, 665-670.
43. Renatus, M., Engh, R.A., Stubbs, M.T., Huber, R., Fischer, S., Kohnert, U., and Bode, W. (1997). Lysine 156 promotes the anomalous proenzyme activity of tPA: X-ray crystal structure of single-chain human tPA. EMBO J. 16, 4797-4805.
44. Rezaie, A.R., Cooper, S.T., Church, F.C., and Esmon, C.T. (1995). Protein C inhibitor is a potent inhibitor of the thrombinthrombomodulin complex. J. Biol. Chem. 270, 25336-25339.
45. Rezaie, A.R., He, X., and Esmon, C.T. (1998). Thrombomodulin increases the rate of thrombin inhibition by BPTI. Biochemistry 37, 693-699.
46. Ruf, W. and Dickinson, C.D. (1998). Allosteric regulation of the cofactor-dependent serine protease coagulation factor VIIa. Trends Cardiovasc. Med. 8, 350-356.
47. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
48. Skrzypczak-Jankun, E., Carperos, V.E., Ravichandran, K.G., Tulinsky, A., Westbrook, M., and Maraganore, J.M. (1991). Structure of the hirugen and hirulog 1 complexes of α-thrombin. J. Mol. Biol. 221, 1379-1393.
49. Treuheit, N.A., Beach, M.A., and Komives, E.A. (2011). Thermodynamic compensation upon binding to exosite 1 and the active site of thrombin. Biochemistry 50, 4590-4596.
50. Tsai, C.-J., del Sol, A., and Nussinov, R. (2008). Allostery: absence of a change in shape does not imply that allostery is not at play. J. Mol. Biol. 378, 1-11.
51. Tsai, C.-J., del Sol, A., and Nussinov, R. (2009). Protein allostery, signal transmission and dynamics: a classifi cation scheme of allosteric mechanisms. Mol. Biosyst. 5, 207-216.
52. 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.
53. Vindigni, A., White, C.E., Komives, E.A., and Di Cera, E. (1997). Energetics of thrombin-thrombomodulin interaction. Biochemistry 36, 6674-6681.
54. Wells, C.M. and Di Cera, E. (1992). Thrombin is a Na+-activated enzyme. Biochemistry 31, 11721-11730.
55. Xu, H., Bush, L.A., Pineda, A.O., Caccia, S., and Di Cera, E. (2005). Thrombomodulin changes the molecular surface of interaction and the rate of complex formation between thrombin and protein C. J. Biol. Chem. 280, 7956-7961.
56. Zhang, E. and Tulinsky, A. (1997). The molecular environment of the Na+ binding site of thrombin. Biophys. Chem. 63, 185-200.