Dynamical view of membrane binding and complex formation of human factor VIIa and tissue factor

Journal of Thrombosis and Haemostasis

Volumn 8, Issue 5, 2010, Pages 1044-1053

  Ohkubo, Y Z ^a,b   Morrissey, J H ^a,b   Tajkhorshid, E ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Coagulation cascade; Factor VIIa; GLA domain; Molecular dynamics simulation; Protein protein interaction; Tissue factor

Indexed keywords

BLOOD CLOTTING FACTOR 7A; THROMBOPLASTIN; PROTEIN BINDING;

ARTICLE; ENZYME ACTIVITY; MEMBRANE BINDING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; SIMULATION; STRUCTURE ANALYSIS; SURFACE PROPERTY; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM;

FACTOR VIIA; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; THROMBOPLASTIN;

EID: 77953786929     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2010.03826.x     Document Type: Article

References (50)

1. Furie B, Furie BC. The molecular basis of blood coagulation. Cell 1988, 53:505-18.
2. Stace CL, Ktistakis NT. Phosphatidic acid- and phosphatidylserine-binding proteins. Biochim Biophys Acta 2006, 176:913-26.
3. Zwaal RFA, Comfurius P, Bevers EM. Lipid-protein interactions in blood coagulation. Biochim Biophys Acta 1998, 1376:433-53.
4. Banner DW, D'Arcy A, Chène C, Winkler FK, Guha A, Konigsberg WH, Nemerson Y. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996, 380:41-6.
5. Harvey SB, Stone MD, Martinez MB, Nelsestuen GL. Mutagenesis of the γ-carboxyglutamic acid domain of human factor VII to generate maximum enhancement of the membrane contact site. J Biol Chem 2003, 278:8363-9.
6. Nelsestuen GL. Enhancement of vitamin-K-dependent protein function by modification of the γ-carboxyglutamic acid domain: studies of protein C and factor VII. Trends Cardiovasc Med 1999, 9:162-7.
7. Huang M, Furie BC, Furie B. Crystal structure of the calcium-stabilized human factor IX Gla domain bound to a conformation-specific anti-factor IX antibody. J Biol Chem 2004, 279:14338-46.
8. Shikamoto Y, Morita T, Fujimoto Z, Mizuno H. Crystal structure of Mg2+- and Ca2+-bound Gla domain of factor IX complexed with binding protein. J Biol Chem 2003, 278:24090-4.
9. Mizuno H, Fujimoto Z, Atoda H, Morita T. Crystal structure of an anticoagulant protein in complex with the Gla domain of factor X. Proc Natl Acad Sci USA 2001, 98:7230-4.
10. Sabharwal AK, Padmanabhan K, Tulinsky A, Mathur A, Gorka J, Bajaj SP. Interaction of calcium with native and decarboxylated human factor X. J Biol Chem 1997, 272:22037-45.
11. Falls LA, Furie BC, Jacobs M, Furie B, Rigby AC. The ω-loop region of the human prothrombin γ-carboxyglutamic acid domain penetrates anionic phospholipid membranes. J Biol Chem 2001, 276:23895-902.
12. Huang M, Rigby AC, Morelli X, Grant MA, Huang G, Furie B, Seaton B, Furie BC. Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat Struct Biol 2003, 10:751-6.
13. Ratcliffe JV, Furie B, Furie BC. The importance of specific γ-carboxyglutamic acid residues in prothrombin - evaluation by site-specific mutagenesis. J Biol Chem 1993, 268:24339-45.
14. Oganesyan V, Oganesyan N, Terzyan S, Qu D, Dauter Z, Esmon NL, Esmon CT. The crystal structure of the endothelial protein C receptor and a bound phospholipid. J Biol Chem 2002, 277:24851-4.
15. Rezende SM, Simmonds RE, Lane DA. Coagulation, inflammation, and apoptosis: different roles for protein S and the protein S-C4b binding protein complex. Blood 2004, 103:1192-201.
16. Lawson JH, Butenas S, Mann KG. The evaluation of complex-dependent alterations in human factor VIIa. J Biol Chem 1992, 267:4834-43.
17. Ruf W, Rehemtullas A, Edgington TS. Phospholipid-independent and -dependent interactions required for tissue factor receptor and cofactor function. J Biol Chem 1991, 266:2158-66.
18. Paborsky LR, Carasli IW, Fisher KL, Gorman CM. Lipid association, but not transmembrane domain, is required for tissue factor activity - substitution of the transmembrane domain with a phosphatidylinositol anchor. J Biol Chem 1991, 266:21911-16.
19. Ruf W, Kalnik MW, Lund-Hansen T, Edgington TS. Characterization of factor VII association with tissue factor in solution - high and low affinity calcium binding sites in factor VII contribute to functionally distinct interactions. J Biol Chem 1991, 266:15719-25.
20. Neuenschwander PF, Morrissey JH. Roles of the membrane-interactive regions of factor VIIa and tissue factor - the factor VIIa Gla domain is dispensable for binding to tissue factor but important for activation of factor X. J Biol Chem 1994, 269:8007-13.
21. McCallum CD, Su B, Neuenschwander PF, Morrissey JH, Johnson AE. Tissue factor positions and maintains the factor VIIa active site far above the membrane surface even in the absence of the factor VIIa Gla domain - a fluorescence resonance energy transfer study. J Biol Chem 1997, 272:30160-6.
22. McCallum CD, Hapak RC, Neuenschwander PF, Morrissey JH, Johnson AE. The location of the active site of blood coagulation factor VIIa above the membrane surface and its reorientation upon association with tissue factor. J Biol Chem 1996, 271:28168-75.
23. Morrissey JH, Neuenschwander PF, Huang Q, McCallum CD, Su B, Johnson AE. Factor VIIa-tissue factor: functional importance of protein-membrane interactions. Thromb Haemost 1997, 78:112-16.
24. Huang Q, Neuenschwander PF, Rezaie AR, Morrissey JH. Substrate recognition by tissue factor-factor VIIa - evidence for interaction of residues Lys165 and Lys166 of tissue factor with the 4-carboxyglutamate-rich domain of factor X. J Biol Chem 1996, 271:21752-7.
25. Carlsson K, Freskgård P, Persson E, Carlsson U, Svensson M. Probing the interface between factor Xa and tissue factor in the quaternary complex tissue factor-factor VIIa-factor Xa-tissue factor pathway inhibitor. Eur J Biochem 2003, 270:2576-82.
26. Kirchhofer D, Eigenbrot C, Lipari MT, Moran P, Peek M, Kelley RF. The tissue factor region that interacts with factor Xa in the activation of factor VII. Biochemistry 2001, 40:675-82.
27. Kirchhofer D, Lipari MT, Moran P, Eigenbrot C, Kelley RF. The tissue factor region that interacts with substrates factor IX and factor X. Biochemistry 2000, 39:7380-7.
28. Manithody C, Yang L, Rezaie AR. Identification of a basic region on tissue factor that interacts with the first epidermal growth factor-like domain of factor X. Biochemistry 2007, 46:3193-9.
29. Colina CM, Venkateswarlu D, Duke R, Perera L, Pedersen LG. What causes the enhancement of activity of factor VIIa by tissue factor? J Thromb Haemost 2006, 4:2726-9.
30. Hoffman M, Colina CM, McDonald AG, Arepally GM, Pedersen L, Monroe DM. Tissue factor around dermal vessels has bound factor VII in the absence of injury. J Thromb Haemost 2007, 5:1403-8.
31. Norledge BV, Petrovan RJ, Ruf W, Olson AJ. The tissue factor/factor VIIa/factor Xa complex: a model built by docking and site-directed mutagenesis. Proteins 2003, 53:640-8.
32. Venkateswarlu D, Duke R, Perera L, Darden TA, Pedersen LG. An all-atom solution-equilibrated model for human extrinsic blood coagulation complex (sTF-VIIa-Xa): a protein-protein docking and molecular dynamics refinement study. J Thromb Haemost 2003, 1:2577-88.
33. Olsen OE, Rand KD, Ostergaard H, Persson E. A combined structural dynamics approach identifies a putative switch in factor VIIa employed by tissue factor to initiate blood coagulation. Prot Sci 2007, 16:671-82.
34. Harlos K, Martin DMA, O'Brien DP, Jones EY, Stuart DI, Polikarpov I, Miller A, Tuddenham EGD, Boys CWG. Crystal structure of the extracellular region of human tissue factor. Nature 1994, 370:662-6.
35. Yves A, Muller MHU, de Vos AM. The crystal structure of the extracellular domain of human tissue factor refined to 1.7 Å resolution. J Mol Biol 1999, 289:103-12.
36. Pike ACW, Brzozowski AM, Roberts SM, Olsen OH, Persson E. Structure of human factor VIIa and its implications for the triggering of blood coagulation. Proc Natl Acad Sci USA 1999, 96:8925-30.
37. Murakami MT, Rios-Steiner J, Weaver SE, Tulinsky A, Geiger JH, Arni RK. Intermolecular interactions and characterization of the novel factor Xa exosite involved in macromolecular recognition and inhibition: crystal structure of human Gla-domainless factor Xa complexed with the anticoagulant protein NAPc2 from the hematophagous nematode Ancylostoma caninum. J Mol Biol 2007, 366:602-10.
38. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990, 215:403-10.
39. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Ohkubo YZ, Tajkhorshid E. Blood clotting reactions on nanoscale phospholipid bilayers. Thromb Res 2008, 122:S23-6.
40. Ohkubo YZ, Tajkhorshid E. Distinct structural and adhesive roles of Ca2+ in membrane binding of blood coagulation factors. Structure 2008, 16:72-81.
41. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K. Scalable molecular dynamics with NAMD. J Comp Chem 2005, 26:1781-802.
42. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck J, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher IWE. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 1998, 102:3586-616.
43. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys 1983, 79:926-35.
44. Feller SE, Zhang YH, Pastor RW, Brooks BR. Constant pressure molecular dynamics simulation - the Langevin piston method. J Chem Phys 1995, 103:4613-21.
45. Martyna GJ, Tobias DJ, Klein ML. Constant pressure molecular dynamics algorithms. J Chem Phys 1994, 101:4177-89.
46. Darden T, York D, Pedersen L. Particle mesh Ewald. An N log(N) method for Ewald sums in large systems. J Chem Phys 1993, 98:10089-92.
47. Waxman E, Laws WR, Laue TM, Nemerson Y, Ross JBA. Human factor VIIa and its complex with soluble tissue factor: evaluation of asymmetry and conformational dynamics by ultracentrifugation and fluorescence anisotropy decay methods. Biochemistry 1993, 32:3005-12.
48. Wang Y, Ohkubo YZ, Tajkhorshid E. Gas conduction of lipid bilayers and membrane channels. Current Topics in Membranes: Computational Modeling of Membrane Bilayers 2008, 343-67. Feller S, In, ed, Oxford, Elsevier
49. Bach RR. Tissue factor encryption. Arterioscler Thromb Vasc Biol 2006, 26:456-61.
50. Morrissey JH, Pureza V, Davis-Harrison RL, Sligar SG, Rienstra CM, Kijak AZ, Ohkubo YZ, Tajkhorshid E. Protein-membrane interactions: blood clotting on nanoscale bilayers. J Thromb Haemost 2009, 7(S1):169-72.