Homology model of human prothrombinase based on the crystal structure of Pseutarin C

Biological Chemistry

Volumn 395, Issue 10, 2014, Pages 1233-1241

  Pomowski, Anja ^a   Ustok, Fatma Isik ^a   Huntington, James A ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Coagulation; Factor Va; Factor Xa; Protease; Thrombin; Zymogen

Indexed keywords

BLOOD CLOTTING FACTOR 10A; PSEUTARIN C; SNAKE VENOM; UNCLASSIFIED DRUG; BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 5A; PROTHROMBINASE COMPLEX;

CONFERENCE PAPER; CRYSTAL STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMBRANE BINDING; MOLECULAR MODEL; MUTAGENESIS; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; SNAKE; X RAY CRYSTALLOGRAPHY;

PSEUDONAJA TEXTILIS;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; ELAPID VENOMS; FACTOR V; FACTOR VA; FACTOR XA; HUMANS; MODELS, MOLECULAR; SNAKES;

EID: 84926442979     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0165     Document Type: Conference Paper

References (57)

1. Adams, T.E., Hockin, M.F., Mann, K.G., and Everse, S.J. (2004). The crystal structure of activated protein C-inactivated bovine factor Va: Implications for cofactor function. Proc. Natl. Acad. Sci. USA 101, 8918-8923.
2. Autin, L., Steen, M., Dahlback, B., and Villoutreix, B.O. (2006). Proposed structural models of the prothrombinase (FXa-FVa) complex. Proteins 63, 440-450.
3. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S.R., and Hofsteenge, J. (1989). The refined 1.9 Å crystal structure of human α-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475.
4. Bradford, H.N., Orcutt, S.J., and Krishnaswamy, S. (2013). Membrane binding by prothrombin mediates its constrained presentation to prothrombinase for cleavage. J. Biol. Chem. 288, 27789-27800.
5. Brandstetter, H., Bauer, M., Huber, R., Lollar, P., and 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.
6. Chen, V.B., Arendall, W.B., 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S., and Richardson, D.C. (2010). MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21.
7. Davie, E.W. and Ratnoff, O.D. (1964). Waterfall sequence for intrinsic blood clotting. Science 145, 1310-1312.
8. Davis, I.W., Leaver-Fay, A., Chen, V.B., Block, J.N., Kapral, G.J., Wang, X., Murray, L.W., Arendall, W.B., 3rd, Snoeyink, J., Richardson, J.S., et al. (2007). MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383.
9. DiMaio, F., Echols, N., Headd, J.J., Terwilliger, T.C., Adams, P.D., and Baker, D. (2013). Improved low-resolution crystallographic refinement with Phenix and Rosetta. Nat. Methods 10, 1102-1104.
10. Discipio, R.G., Hermodson, M.A., and Davie, E.W. (1977). Activation of human factor-X (Stuart factor) by a protease from Russells viper venom. Biochemistry 16, 5253-5260.
11. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501.
12. Everse, S.J., Adams, T.E., and Mann, K.G. (2008). A molecular model for the human prothrombinase complex. In: Recent Advances in Thrombosis and Hemostasis 2008. K. Tanaka and E.W. Davie, eds. (Japan: Springer), 107-132.
13. Guinto, E.R. and Esmon, C.T. (1982). Formation of a calcium-binding site on bovine activated factor V following recombination of the isolated subunits. J. Biol. Chem. 257, 10038-10043.
14. Guinto, E.R. and Esmon, C.T. (1984). Loss of prothrombin and of factor Xa-factor Va interactions upon inactivation of factor Va by activated protein C. J. Biol. Chem. 259, 13986-13992.
15. Hirbawi, J., Vaughn, J.L., Bukys, M.A., Vos, H.L., and Kalafatis, M. (2010). Contribution of amino acid region 659-663 of Factor Va heavy chain to the activity of factor Xa within prothrombinase. Biochemistry 49, 8520-8534.
16. Huber, R. and Bode, W. (1978). Structural basis of the activation and action of trypsin. Acc. Chem. Res. 11, 114-122.
17. Huntington, J.A. (2009). Slow thrombin is zymogen-like. J. Thromb. Haemost. 7 (Suppl 1), 159-164.
18. Husten, E.J., Esmon, C.T., and Johnson, A.E. (1987). The active site of blood coagulation factor Xa. Its distance from the phospholipid surface and its conformational sensitivity to components of the prothrombinase complex. J. Biol. Chem. 262, 12953-12961.
19. Isaacs, B.S., Husten, E.J., Esmon, C.T., and Johnson, A.E. (1986). A domain of membrane-bound blood coagulation factor Va is located far from the phospholipid surface. A fluorescence energy transfer measurement. Biochemistry 25, 4958-4969.
20. Jenny, R.J., Pittman, D.D., Toole, J.J., Kriz, R.W., Aldape, R.A., Hewick, R.M., Kaufman, R.J., and Mann, K.G. (1987). Complete cDNA and derived amino acid sequence of human factor V. Proc. Natl. Acad. Sci. USA 84, 4846-4850.
21. Kamata, K., Kawamoto, H., Honma, T., Iwama, T., and Kim, S.H. (1998). Structural basis for chemical inhibition of human blood coagulation factor Xa. Proc. Natl. Acad. Sci. USA 95, 6630-6635.
22. Kane, W.H. and Davie, E.W. (1986). Cloning of a cDNA coding for human factor V, a blood coagulation factor homologous to factor VIII and ceruloplasmin. Proc. Natl. Acad. Sci. USA 83, 6800-6804.
23. Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., Tyka, M., Baker, D., and Karplus, K. (2009). Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77 (Suppl 9), 114-122.
24. Krishnaswamy, S. (1990). Prothrombinase complex assembly. Contributions of protein-protein and protein-membrane interactions toward complex formation. J. Biol. Chem. 265, 3708-3718.
25. 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.
26. Krishnaswamy, S., Russell, G.D., and Mann, K.G. (1989). The reassociation of factor Va from its isolated subunits. J. Biol. Chem. 264, 3160-3168.
27. Krissinel, E. and Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
28. Lechtenberg, B.C., Johnson, D.J., Freund, S.M., 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.
29. Lechtenberg, B.C., Murray-Rust, T.A., Johnson, D.J.D., Adams, T.E., Krishnaswamy, S., Camire, R.M., and Huntington, J.A. (2013). Crystal structure of the prothrombinase complex from the venom of Pseudonaja textilis. Blood 122, 2777-2783.
30. Lee, C.J., Lin, P., Chandrasekaran, V., Duke, R.E., Everse, S.J., Perera, L., and Pedersen, L.G. (2008). Proposed structural models of human factor Va and prothrombinase. J. Thromb. Haemost. 6, 83-89.
31. Lee, C.J., Wu, S., and Pedersen, L.G. (2011). A proposed ternary complex model of prothrombinase with prothrombin: protein-protein docking and molecular dynamics simulations. J. Thromb. Haemost. 9, 2123-2126.
32. Macfarlane, R.G. (1964). An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier. Nature 202, 498-499.
33. Manithody, C. and Rezaie, A.R. (2005). Functional mapping of charged residues of the 82-116 sequence in factor Xa: evidence that lysine 96 is a factor Va independent recognition site for prothrombin in the prothrombinase complex. Biochemistry 44, 10063-10070.
34. Mann, K.G. (2003a). Thrombin formation. Chest 124, 4S-10S.
35. Mann, K.G. and Lawson, J.H. (1992). The role of the membrane in the expression of the vitamin K-dependent enzymes. Arch. Pathol. Lab. Med. 116, 1330-1336.
36. Mann, K.G. and Kalafaatis, M. (2003). Factor V: a combination of Dr Jekyll and Mr Hyde. Blood 101, 20-30.
37. Mann, K.G., Nesheim, M.E., Church, W.R., Haley, P., and Krishnaswamy, S. (1990). Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 76, 1-16.
38. Mann, K.G., Brummel, K., and Butenas, S. (2003a). What is all that thrombin for? J. Thromb. Haemost. 1, 1504-1514.
39. Mann, K.G., Butenas, S., and Brummel, K. (2003b). The dynamics of thrombin formation. Arterioscler. Thromb. Vasc. Biol. 23, 17-25.
40. Mizuno, H., Fujimoto, Z., Atoda, H., and Morita, T. (2001). Crystal structure of an anticoagulant protein in complex with the Gla domain of factor X. Proc. Natl. Acad. Sci. USA 98, 7230-7234.
41. Nesheim, M.E., Taswell, J.B., and Mann, K.G. (1979). Contribution of Bovine Factor-V and Factor-Va to the Activity of Prothrombinase. J. Biol. Chem. 254, 952-962.
42. Nesheim, M.E., Foster, W.B., Hewick, R., and Mann, K.G. (1984). Characterization of factor-V activation intermediates. J. Biol. Chem. 259, 3187-3196.
43. Norstrom, E.A., Tran, S., Steen, M., and Dahlback, B. (2006). Effects of factor Xa and protein S on the individual activated protein C-mediated cleavages of coagulation factor Va. J. Biol. Chem. 281, 31486-31494.
44. Pittman, D.D., Tomkinson, K.N., Michnick, D., Selighsohn, U., and Kaufman, R.J. (1994). Posttranslational sulfation of factor V is required for efficient thrombin cleavage and activation and for full procoagulant activity. Biochemistry 33, 6952-6959.
45. Rezaie, A.R. (2000). Identification of basic residues in the heparinbinding exosite of factor Xa critical for heparin and factor Va binding. J. Biol. Chem. 275, 3320-3327.
46. Rosing, J., Tans, G., Govers-Riemslag, J.W., Zwaal, R.F., and Hemker, H.C. (1980). The role of phospholipids and factor Va in the prothrombinase complex. J. Biol. Chem. 255, 274-283.
47. Rudolph, A.E., Porche-Sorbet, R., and Miletich, J.P. (2000). Substitution of asparagine for arginine 347 of recombinant factor Xa markedly reduces factor Va binding. Biochemistry 39, 2861-2867.
48. Rudolph, A.E., Porche-Sorbet, R., and Miletich, J.P. (2001). Definition of a factor Va binding site in factor Xa. J. Biol. Chem. 276, 5123-5128.
49. Sanchez, R. and Sali, A. (2000). Comparative protein structure modeling. Introduction and practical examples with modeller. Methods Mol. Biol. 143, 97-129.
50. Schrodinger, L.L.C. (2010). The PyMOL Molecular Graphics System, Version 1.3r1.
51. Spencer, F.A. and Becker, R.C. (1997). The prothrombinase complex: assembly and function. J.Thromb. Thrombolysis 4, 357-364.
52. Steen, M., Villoutreix, B.O., Norstrom, E.A., Yamazaki, T., and Dahlback, B. (2002). Defining the factor Xa-binding site on factor Va by site-directed glycosylation. J. Biol. Chem. 277, 50022-50029.
53. Steen, M., Tran, S., Autin, L., Villoutreix, B.O., Tholander, A.-L., and Dahlback, B. (2008). Mapping of the factor Xa binding site on factor Va by site-directed mutagenesis. J. Biol. Chem. 283, 20805-20812.
54. Stenflo, J. (1991). Structure-function relationships of epidermal growth factor modules in vitamin K-dependent clotting factors. Blood 78, 1637-1651.
55. Villoutreix, B.O. and Dahlback, B. (1998). Structural investigation of the A-domains of human blood coagulation factor V by molecular modeling. Protein Sci. 7, 1317-1325.
56. Yegneswaran, S., Wood, G.M., Esmon, C.T., and Johnson, A.E. (1997). Protein S alters the active site location of activated protein C above the membrane surface. A fluorescence resonance energy transfer study of topography. J. Biol. Chem. 272, 25013-25021.
57. Zaitseva, I., Zaitsev, V., Card, G., Moshkov, K., Bax, B., Ralph, A., and Lindley, P. (1996). The X-ray structure of human serum ceruloplasmin at 3.1 Å: nature of the copper centres. J. Biol. Inorg. Chem. 1, 15-23.