Thrombin activity propagates in space during blood coagulation as an excitation wave

Biophysical Journal

Volumn 103, Issue 10, 2012, Pages 2233-2240

  Dashkevich, N M ^a,b   Ovanesov, M V ^c   Balandina, A N ^a,d   Karamzin, S S ^b   Shestakov, P I ^a,b   Soshitova, N P ^b   Tokarev, A A ^d   Panteleev, M A ^a,b,e   Ataullakhanov, F I ^a,b,d,e  

^a CENTER FOR THEORETICAL PROBLEMS OF PHYSICOCHEMICAL PHARMACOLOGY   (Russian Federation)

^b HemaCore (Hematological Corporation)   (Russian Federation)

^c CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^d Federal Research and Clinical Center of Pediatric Hematology   (Russian Federation)

^e MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRIN; PROTEIN C; THROMBIN; THROMBOMODULIN;

ANIMAL; ARTICLE; BIOMECHANICS; BLOOD CLOTTING; FEEDBACK SYSTEM; HEMOSTASIS; HUMAN; METABOLISM; RABBIT;

ANIMALS; BIOMECHANICS; BLOOD COAGULATION; FEEDBACK, PHYSIOLOGICAL; FIBRIN; HEMOSTASIS; HUMANS; PROTEIN C; RABBITS; THROMBIN; THROMBOMODULIN;

EID: 84869410838     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.10.011     Document Type: Article

References (74)

1. F.I. Ataullakhanov, and G.T. Guria R.I. Volkova Spatiotemporal dynamics of clotting and pattern formation in human blood Biochim. Biophys. Acta 1425 1998 453 468
2. V.I. Zarnitsina, A.V. Pokhilko, and F.I. Ataullakhanov A mathematical model for the spatio-temporal dynamics of intrinsic pathway of blood coagulation. II. Results Thromb. Res. 84 1996 333 344
3. J. Rinzel, and J.B. Keller Traveling wave solutions of a nerve conduction equation Biophys. J. 13 1973 1313 1337
4. M. Loose, and E. Fischer-Friedrich P. Schwille Spatial regulators for bacterial cell division self-organize into surface waves in vitro Science 320 2008 789 792
5. M.V. Ovanesov, and N.M. Ananyeva E.L. Saenko Initiation and propagation of coagulation from tissue factor-bearing cell monolayers to plasma: initiator cells do not regulate spatial growth rate J. Thromb. Haemost. 3 2005 321 331
6. M.A. Panteleev, and M.V. Ovanesov F.I. Ataullakhanov Spatial propagation and localization of blood coagulation are regulated by intrinsic and protein C pathways, respectively Biophys. J. 90 2006 1489 1500
7. D.M. Monroe, M. Hoffman, and H.R. Roberts Transmission of a procoagulant signal from tissue factor-bearing cell to platelets Blood Coagul. Fibrinolysis 7 1996 459 464
8. R.A. Campbell, and K.A. Overmyer A.S. Wolberg Cellular procoagulant activity dictates clot structure and stability as a function of distance from the cell surface Arterioscler. Thromb. Vasc. Biol. 28 2008 2247 2254
9. E.I. Sinauridze, and R.I. Volkova F.I. Ataullakhanov Dynamics of clot growth induced by thrombin diffusing into nonstirred citrate human plasma Biochim. Biophys. Acta 1425 1998 607 616
10. A.Y. Kondratovich, A.V. Pokhilko, and F.I. Ataullakhanov Spatiotemporal dynamics of contact activation factors of blood coagulation Biochim. Biophys. Acta 1569 2002 86 104
11. A.N. Balandina, and A.M. Shibeko F.I. Ataullakhanov Positive feedback loops for factor V and factor VII activation supply sensitivity to local surface tissue factor density during blood coagulation Biophys. J. 101 2011 1816 1824
12. A.N. Zaikin, and A.M. Zhabotinsky Concentration wave propagation in two-dimensional liquid-phase self-oscillating system Nature 225 1970 535 537
13. D. Gailani, and G.J. Broze Jr. Factor XI activation in a revised model of blood coagulation Science 253 1991 909 912
14. M.A. Panteleev, and A.N. Balandina F.I. Ataullakhanov Task-oriented modular decomposition of biological networks: trigger mechanism in blood coagulation Biophys. J. 98 2010 1751 1761
15. U. Seligsohn Factor XI deficiency in humans J. Thromb. Haemost. 7 Suppl 1 2009 84 87
16. P.A. von dem Borne, J.C. Meijers, and B.N. Bouma Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis Blood 86 1995 3035 3042
17. D.V. Kravtsov, and A. Matafonov D. Gailani Factor XI contributes to thrombin generation in the absence of factor XII Blood 114 2009 452 458
18. A. Gruber, and S.R. Hanson Factor XI-dependence of surface- and tissue factor-initiated thrombus propagation in primates Blood 102 2003 953 955
19. M.J. Davies Pathophysiology of acute coronary syndromes Indian Heart J. 52 2000 473 479
20. Centers for Disease Control and Prevention (CDC) State-specific mortality from sudden cardiac death - United States, 1999 MMWR Morb. Mortal. Wkly. Rep. 51 2002 123 126
21. F. Müller, D. Gailani, and T. Renné Factor XI and XII as antithrombotic targets Curr. Opin. Hematol. 18 2011 349 355
22. H.C. Hemker, and P.L. Giesen S. Béguin The thrombogram: monitoring thrombin generation in platelet-rich plasma Thromb. Haemost. 83 2000 589 591
23. H.C. Hemker, and S. Béguin Thrombin generation in plasma: its assessment via the endogenous thrombin potential Thromb. Haemost. 74 1995 134 138
24. E. Hairer, S.P. Norsett, and G. Wanner Solving Ordinary Differential Equations I: Nonstiff Problems 1993 Springer Berlin
25. H. Meems, and A.B. Meijer G.E. Gilbert Factor VIII C1 domain residues Lys 2092 and Phe 2093 contribute to membrane binding and cofactor activity Blood 114 2009 3938 3946
26. S. Butenas, and A. Undas K.G. Mann Factor XIa and tissue factor activity in patients with coronary artery disease Thromb. Haemost. 99 2008 142 149
27. S. Butenas, and K.G. Mann Blood coagulation Biochemistry (Mosc.) 67 2002 3 12
28. R.W. Colman Hemostasis and Thrombosis: Basic Principles and Clinical Practice 2006 Lippincott Williams & Wilkins Philadelphia, PA
29. S. Krishnaswamy The interaction of human factor VIIa with tissue factor J. Biol. Chem. 267 1992 23696 23706
30. Y. Nemerson, and R. Gentry An ordered addition, essential activation model of the tissue factor pathway of coagulation: evidence for a conformational cage Biochemistry 25 1986 4020 4033
31. S. Butenas, and K.G. Mann Kinetics of human factor VII activation Biochemistry 35 1996 1904 1910
32. L.V. Rao, T. Williams, and S.I. Rapaport Studies of the activation of factor VII bound to tissue factor Blood 87 1996 3738 3748
33. Y. Komiyama, A.H. Pedersen, and W. Kisiel Proteolytic activation of human factors IX and X by recombinant human factor VIIa: effects of calcium, phospholipids, and tissue factor Biochemistry 29 1990 9418 9425
34. B.J. Warn-Cramer, and S.P. Bajaj Intrinsic versus extrinsic coagulation. Kinetic considerations Biochem. J. 239 1986 757 762
35. D. Gailani, and D. Ho P.N. Walsh Model for a factor IX activation complex on blood platelets: dimeric conformation of factor XIa is essential Blood 97 2001 3117 3122
36. R.J. Baugh, and S. Krishnaswamy Role of the activation peptide domain in human factor X activation by the extrinsic Xase complex J. Biol. Chem. 271 1996 16126 16134
37. J.M. Scandura, and P.N. Walsh Factor X bound to the surface of activated human platelets is preferentially activated by platelet-bound factor IXa Biochemistry 35 1996 8903 8913
38. R. Rawala-Sheikh, and S.S. Ahmad P.N. Walsh Kinetics of coagulation factor X activation by platelet-bound factor IXa Biochemistry 29 1990 2606 2611
39. M.A. Panteleev, and E.L. Saenko F.I. Ataullakhanov Kinetics of factor X activation by the membrane-bound complex of factor IXa and factor VIIIa Biochem. J. 381 2004 779 794
40. R.J. Baugh, G.J. Broze Jr., and S. Krishnaswamy Regulation of extrinsic pathway factor Xa formation by tissue factor pathway inhibitor J. Biol. Chem. 273 1998 4378 4386
41. P.B. Tracy, L.L. Eide, and K.G. Mann Human prothrombinase complex assembly and function on isolated peripheral blood cell populations J. Biol. Chem. 260 1985 2119 2124
42. G. van Dieijen, and G. Tans H.C. Hemker The role of phospholipid and factor VIIIa in the activation of bovine factor X J. Biol. Chem. 256 1981 3433 3442
43. J.F. Keuren, and S.J. Wielders T. Lindhout Synergistic effect of thrombin on collagen-induced platelet procoagulant activity is mediated through protease-activated receptor-1 Arterioscler. Thromb. Vasc. Biol. 25 2005 1499 1505
44. D.L. Higgins, S.D. Lewis, and J.A. Shafer Steady state kinetic parameters for the thrombin-catalyzed conversion of human fibrinogen to fibrin J. Biol. Chem. 258 1983 9276 9282
45. D.C. Hill-Eubanks, and P. Lollar von Willebrand factor is a cofactor for thrombin-catalyzed cleavage of the factor VIII light chain J. Biol. Chem. 265 1990 17854 17858
46. D.D. Monkovic, and P.B. Tracy Activation of human factor V by factor Xa and thrombin Biochemistry 29 1990 1118 1128
47. J.A. Oliver, and D.M. Monroe M. Hoffman Thrombin activates factor XI on activated platelets in the absence of factor XII Arterioscler. Thromb. Vasc. Biol. 19 1999 170 177
48. L. Yang, C. Manithody, and A.R. Rezaie Activation of protein C by the thrombin-thrombomodulin complex: cooperative roles of Arg-35 of thrombin and Arg-67 of protein C Proc. Natl. Acad. Sci. USA 103 2006 879 884
49. L.A. Bush, R.W. Nelson, and E. Di Cera Murine thrombin lacks Na+ activation but retains high catalytic activity J. Biol. Chem. 281 2006 7183 7188
50. M.A. Panteleev, V.I. Zarnitsina, and F.I. Ataullakhanov Tissue factor pathway inhibitor: a possible mechanism of action Eur. J. Biochem. 269 2002 2016 2031
51. S.S. Ahmad, R. Rawala-Sheikh, and P.N. Walsh Comparative interactions of factor IX and factor IXa with human platelets J. Biol. Chem. 264 1989 3244 3251
52. S.S. Ahmad, J.M. Scandura, and P.N. Walsh Structural and functional characterization of platelet receptor-mediated factor VIII binding J. Biol. Chem. 275 2000 13071 13081
53. S.J. Koppelman, and T.M. Hackeng B.N. Bouma Inhibition of the intrinsic factor X activating complex by protein S: evidence for a specific binding of protein S to factor VIII Blood 86 1995 1062 1071
54. T.M. Hackeng, and C. van 't Veer B.N. Bouma Human protein S inhibits prothrombinase complex activity on endothelial cells and platelets via direct interactions with factors Va and Xa J. Biol. Chem. 269 1994 21051 21058
55. J.M. Scandura, S.S. Ahmad, and P.N. Walsh A binding site expressed on the surface of activated human platelets is shared by factor X and prothrombin Biochemistry 35 1996 8890 8902
56. P.B. Tracy, M.E. Nesheim, and K.G. Mann Platelet factor Xa receptor Methods Enzymol. 215 1992 329 360
57. J. Pieters, and G. Willems T. Lindhout Inhibition of factor IXa and factor Xa by antithrombin III/heparin during factor X activation J. Biol. Chem. 263 1988 15313 15318
58. A.R. Rezaie Calcium enhances heparin catalysis of the antithrombin-factor Xa reaction by a template mechanism. Evidence that calcium alleviates Gla domain antagonism of heparin binding to factor Xa J. Biol. Chem. 273 1998 16824 16827
59. V. Ellis, and M. Scully V. Kakkar Inhibition of human factor Xa by various plasma protease inhibitors Biochim. Biophys. Acta 701 1982 24 31
60. F. España, M. Berrettini, and J.H. Griffin Purification and characterization of plasma protein C inhibitor Thromb. Res. 55 1989 369 384
61. V. Ellis, M.F. Scully, and V.V. Kakkar Inhibition of prothrombinase complex by plasma proteinase inhibitors Biochemistry 23 1984 5882 5887
62. M.R. Downing, J.W. Bloom, and K.G. Mann Comparison of the inhibition of thrombin by three plasma protease inhibitors Biochemistry 17 1978 2649 2653
63. V.M. Derechin, M.A. Blinder, and D.M. Tollefsen Substitution of arginine for Leu444 in the reactive site of heparin cofactor II enhances the rate of thrombin inhibition J. Biol. Chem. 265 1990 5623 5628
64. P. Lollar, E.T. Parker, and P.J. Fay Coagulant properties of hybrid human/porcine factor VIII molecules J. Biol. Chem. 267 1992 23652 23657
65. S. Solymoss, M.M. Tucker, and P.B. Tracy Kinetics of inactivation of membrane-bound factor Va by activated protein C. Protein S modulates factor Xa protection J. Biol. Chem. 263 1988 14884 14890
66. W.A. Wuillemin, and E. Eldering C.E. Hack Modulation of contact system proteases by glycosaminoglycans. Selective enhancement of the inhibition of factor XIa J. Biol. Chem. 271 1996 12913 12918
67. J.C. Meijers, R.A. Vlooswijk, and B.N. Bouma Inhibition of human blood coagulation factor XIa by C-1 inhibitor Biochemistry 27 1988 959 963
68. M.J. Heeb, A. Gruber, and J.H. Griffin Identification of divalent metal ion-dependent inhibition of activated protein C by alpha 2-macroglobulin and alpha 2-antiplasmin in blood and comparisons to inhibition of factor Xa, thrombin, and plasmin J. Biol. Chem. 266 1991 17606 17612
69. M.J. Heeb, and R. Bischoff J.H. Griffin Inhibition of activated protein C by recombinant alpha 1-antitrypsin variants with substitution of arginine or leucine for methionine358 J. Biol. Chem. 265 1990 2365 2369
70. M.A. Panteleev, and N.M. Ananyeva E.L. Saenko Factor VIIIa regulates substrate delivery to the intrinsic factor X-activating complex FEBS J. 273 2006 374 387
71. A. Baerga-Ortiz, A.R. Rezaie, and E.A. Komives Electrostatic dependence of the thrombin-thrombomodulin interaction J. Mol. Biol. 296 2000 651 658
72. J.B. Galvin, and S. Kurosawa N.L. Esmon Reconstitution of rabbit thrombomodulin into phospholipid vesicles J. Biol. Chem. 262 1987 2199 2205
73. M. Aritomi, and N. Watanabe I. Maruyama Recombinant human soluble thrombomodulin delivers bounded thrombin to antithrombin III: thrombomodulin associates with free thrombin and is recycled to activate protein c Thromb. Haemost. 70 1993 418 422
74. A.R. Rezaie, and S.T. Cooper C.T. Esmon Protein C inhibitor is a potent inhibitor of the thrombin-thrombomodulin complex J. Biol. Chem. 270 1995 25336 25339