Hemostasis and thrombosis beyond biochemistry: Roles of geometry, flow and diffusion

Thrombosis Research

Volumn 136, Issue 4, 2015, Pages 699-711

  Panteleev, Mikhail A ^a,b,c,d,e   Dashkevich, Natalia M ^a,c   Ataullakhanov, Fazoil I ^a,b,c,d,e  

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

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

^c HemaCore LLC   (Russian Federation)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

^e MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

Author keywords

Blood coagulation; Blood coagulation tests; Blood flow; Diffusion; Enzymatic cascade; Hemostatic plug

Indexed keywords

BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 5; BLOOD CLOTTING FACTOR 7; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9A; PHOSPHOLIPID; PROCOAGULANT; THROMBIN; THROMBOMODULIN; THROMBOPLASTIN;

ARTIFICIAL EMBOLISM; BLOOD BIOCHEMISTRY; BLOOD CLOTTING; HEMOSTASIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRINSIC ACTIVITY; LIPID COMPOSITION; MEMBRANE MICROPARTICLE; MONOCYTE; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; THROMBOCYTE ACTIVATION; THROMBOSIS; VASCULARIZATION; BLOOD; BLOOD CLOTTING TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

BLOOD COAGULATION; BLOOD COAGULATION TESTS; HEMOSTASIS; HUMANS; THROMBOSIS;

EID: 84941873953     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2015.07.025     Document Type: Review

References (90)

1. R.G. Macfarlane An enzyme cascade in the blood clotting mechanism, and its function as a biochemical amplifier Nature 202 1964 498 499
2. A. Matafonov, Q. Cheng, Y. Geng, I.M. Verhamme, O. Umunakwe, E.I. Tucker, and et al. Evidence for factor IX-independent roles for factor XIa in blood coagulation J. Thromb. Haemost. 11 2013 2118 2127 10.1111/jth.12435
3. N.V. Zakharova, E.O. Artemenko, N.A. Podoplelova, A.N. Sveshnikova, I.A. Demina, F.I. Ataullakhanov, and et al. Platelet surface-associated activation and secretion-mediated inhibition of coagulation factor XII PLoS One 10 2015 e0116665 10.1371/journal.pone.0116665
4. J.C.M. Meijers Feedback controversy stops here Blood 114 2009 235 10.1182/blood-2009-04-217117
5. V. Johari, and C. Loke Brief overview of the coagulation cascade Dis. Mon. 58 2012 421 423 10.1016/j.disamonth.2012.04.004
6. D. Gailani, C.E. Bane, and A. Gruber Factor XI and contact activation as targets for antithrombotic therapy J. Thromb. Haemost. 2015 10.1111/jth.13005
7. T. Ikezoe Thrombomodulin/activated protein C system in septic disseminated intravascular coagulation J. Intensive Care 3 2015 1 10.1186/s40560-014-0050-7
8. M. Hoffman, and D.M. Monroe A cell-based model of hemostasis Thromb. Haemost. 85 2001 958 965
9. J.J. Hathcock, and Y. Nemerson Platelet deposition inhibits tissue factor activity: in vitro clots are impermeable to factor Xa Blood 104 2004 123 127 10.1182/blood-2003-12-4352
10. S.L. Diamond, and S. Anand Inner clot diffusion and permeation during fibrinolysis Biophys. J. 65 1993 2622 2643 10.1016/S0006-3495(93)81314-6
11. T.J. Stalker, E.A. Traxler, J. Wu, K.M. Wannemacher, S.L. Cermignano, R. Voronov, and et al. Hierarchical organization in the hemostatic response and its relationship to the platelet-signaling network Blood 121 2013 1875 1885 10.1182/blood-2012-09-457739
12. F.I. Ataullakhanov, G.T. Guria, V.I. Sarbash, and R.I. Volkova Spatiotemporal dynamics of clotting and pattern formation in human blood Biochim. Biophys. Acta 1425 1998 453 468
13. M.V. Ovanesov, J.V. Krasotkina, L.I. Ul'yanova, K.V. Abushinova, O.P. Plyushch, S.P. Domogatskii, and et al. Hemophilia A and B are associated with abnormal spatial dynamics of clot growth Biochim. Biophys. Acta 1572 2002 45 57
14. N.M. Dashkevich, T.A. Vuimo, R.A. Ovsepyan, S.S. Surov, N.P. Soshitova, M.A. Panteleev, and et al. Effect of pre-analytical conditions on the thrombodynamics assay Thromb. Res. 133 2014 472 476 10.1016/j.thromres.2013.12.014
15. L. Faxälv, P. Tengvall, and T.L. Lindahl Imaging of blood plasma coagulation and its propagation at surfaces J. Biomed. Mater. Res. A 85 2008 1129 1134 10.1002/jbm.a.31529
16. C.J. Kastrup, M.K. Runyon, F. Shen, and R.F. Ismagilov Modular chemical mechanism predicts spatiotemporal dynamics of initiation in the complex network of hemostasis Proc. Natl. Acad. Sci. U. S. A. 103 2006 15747 15752 10.1073/pnas.0605560103
17. F.I. Ataullakhanov, and M.A. Panteleev Mathematical modeling and computer simulation in blood coagulation Pathophysiol. Haemost. Thromb. 34 2005 60 70 10.1159/000089927
18. H.R. Roberts, M. Hoffman, and D.M. Monroe A cell-based model of thrombin generation Semin. Thromb. Hemost. 32 Suppl. 1 2006 32 38 10.1055/s-2006-939552
19. M.M. Hoffman, and D.M. Monroe Rethinking the coagulation cascade Curr. Hematol. Rep. 4 2005 391 396
20. C.J. Kastrup, M.K. Runyon, E.M. Lucchetta, J.M. Price, and R.F. Ismagilov Using chemistry and microfluidics to understand the spatial dynamics of complex biological networks Acc. Chem. Res. 41 2008 549 558 10.1021/ar700174g
21. F. Shen, C.J. Kastrup, and R.F. Ismagilov Using microfluidics to understand the effect of spatial distribution of tissue factor on blood coagulation Thromb. Res. 122 Suppl. 1 2008 S27 S30 10.1016/S0049-3848(08)70015-X
22. M.A. Panteleev, A.N. Balandina, E.N. Lipets, M.V. Ovanesov, and F.I. Ataullakhanov Task-oriented modular decomposition of biological networks: trigger mechanism in blood coagulation Biophys. J. 98 2010 1751 1761 10.1016/j.bpj.2010.01.027
23. K.G. Mann Thrombin generation in hemorrhage control and vascular occlusion Circulation 124 2011 225 235 10.1161/CIRCULATIONAHA.110.952648
24. S. Butenas, T. Orfeo, and K.G. Mann Tissue factor in coagulation: Which? Where? When? Arterioscler. Thromb. Vasc. Biol. 29 2009 1989 1996 10.1161/ATVBAHA.108.177402
25. S.L. Diamond Tissue factor activity under flow Thromb. Res. 125 Suppl. 1 2010 S29 S30 10.1016/j.thromres.2010.01.029
26. J.J. Hathcock Flow effects on coagulation and thrombosis Arterioscler. Thromb. Vasc. Biol. 26 2006 1729 1737 10.1161/01.ATV.0000229658.76797.30
27. S.M. Slack, Y. Cui, and V.T. Turitto The effects of flow on blood coagulation and thrombosis Thromb. Haemost. 70 1993 129 134
28. Y. Nemerson, and V.T. Turitto The effect of flow on hemostasis and thrombosis Thromb. Haemost. 66 1991 272 276
29. D. Basmadjian The effect of flow and mass transport in thrombogenesis Ann. Biomed. Eng. 18 1990 685 709
30. K. Guria, and G.T. Guria Spatial aspects of blood coagulation: two decades of research on the self-sustained traveling wave of thrombin Thromb. Res. 135 2015 423 433 10.1016/j.thromres.2014.12.014
31. K.G. Mann, K. Brummel, and S. Butenas What is all that thrombin for? J. Thromb. Haemost. 1 2003 1504 1514
32. M.A. Panteleev, M.V. Ovanesov, D.A. Kireev, A.M. Shibeko, E.I. Sinauridze, N.M. Ananyeva, and et al. Spatial propagation and localization of blood coagulation are regulated by intrinsic and protein C pathways, respectively Biophys. J. 90 2006 1489 1500 10.1529/biophysj.105.069062
33. S. Butenas, C. van 't Veer, and K.G. Mann Evaluation of the initiation phase of blood coagulation using ultrasensitive assays for serine proteases J. Biol. Chem. 272 1997 21527 21533
34. M.A. Khanin, and V.V. Semenov A mathematical model of the kinetics of blood coagulation J. Theor. Biol. 136 1989 127 134
35. A.M. Shibeko, E.S. Lobanova, M.A. Panteleev, and F.I. Ataullakhanov Blood flow controls coagulation onset via the positive feedback of factor VII activation by factor Xa BMC Syst. Biol. 4 2010 5 10.1186/1752-0509-4-5
36. F. Shen, C.J. Kastrup, Y. Liu, and R.F. Ismagilov Threshold response of initiation of blood coagulation by tissue factor in patterned microfluidic capillaries is controlled by shear rate Arterioscler. Thromb. Vasc. Biol. 28 2008 2035 2041 10.1161/ATVBAHA.108.173930
37. A.N. Balandina, A.M. Shibeko, D.A. Kireev, A.A. Novikova, I.I. Shmirev, M.A. Panteleev, and et al. 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 10.1016/j.bpj.2011.08.034
38. F. Shen, R.R. Pompano, C.J. Kastrup, and R.F. Ismagilov Confinement regulates complex biochemical networks: initiation of blood clotting by "diffusion acting." Biophys. J. 97 2009 2137 2145 10.1016/j.bpj.2009.08.004
39. T. Orfeo, S. Butenas, K.E. Brummel-Ziedins, and K.G. Mann The tissue factor requirement in blood coagulation J. Biol. Chem. 280 2005 42887 42896 10.1074/jbc.M505506200
40. T. Orfeo, K.E. Brummel-Ziedins, M. Gissel, S. Butenas, and K.G. Mann The nature of the stable blood clot procoagulant activities J. Biol. Chem. 283 2008 9776 9786 10.1074/jbc.M707435200
41. M.V. Ovanesov, N.M. Ananyeva, M.A. Panteleev, F.I. Ataullakhanov, and 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 10.1111/j.1538-7836.2005.01128.x
42. N.M. Dashkevich, M.V. Ovanesov, A.N. Balandina, S.S. Karamzin, P.I. Shestakov, N.P. Soshitova, and et al. Thrombin activity propagates in space during blood coagulation as an excitation wave Biophys. J. 103 2012 2233 2240 10.1016/j.bpj.2012.10.011
43. J.E. Ferrell Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability Curr. Opin. Cell Biol. 14 2002 140 148
44. E. Beltrami, and J. Jesty Mathematical analysis of activation thresholds in enzyme-catalyzed positive feedbacks: application to the feedbacks of blood coagulation Proc. Natl. Acad. Sci. U. S. A. 92 1995 8744 8748
45. J. Jesty, and E. Beltrami Positive feedbacks of coagulation: their role in threshold regulation Arterioscler. Thromb. Vasc. Biol. 25 2005 2463 2469 10.1161/01.ATV.0000187463.91403.b2
46. J. Jesty, J. Rodriguez, and E. Beltrami Demonstration of a threshold response in a proteolytic feedback system: control of the autoactivation of factor XII Pathophysiol. Haemost. Thromb. 34 2005 71 79 10.1159/000089928
47. J. Müller, S. Brandt, K. Mayerhofer, T. Tjardes, and M. Maegele Tolerance and threshold in the extrinsic coagulation system Math. Biosci. 211 2008 226 254 10.1016/j.mbs.2007.07.007
48. F.I. Ataullakhanov, R.I. Volkova, A.V. Pokhilko, and E.I. Sinauridze Threshold behavior of the blood coagulation system upon changes in calcium concentration Biofizika 39 1994 713 720
49. C. van 't Veer, and K.G. Mann Regulation of tissue factor initiated thrombin generation by the stoichiometric inhibitors tissue factor pathway inhibitor, antithrombin-III, and heparin cofactor-II J. Biol. Chem. 272 1997 4367 4377
50. C. van 't Veer, N.J. Golden, M. Kalafatis, and K.G. Mann Inhibitory mechanism of the protein C pathway on tissue factor-induced thrombin generation. Synergistic effect in combination with tissue factor pathway inhibitor J. Biol. Chem. 272 1997 7983 7994
51. C.J. Kastrup, F. Shen, M.K. Runyon, and R.F. Ismagilov Characterization of the threshold response of initiation of blood clotting to stimulus patch size Biophys. J. 93 2007 2969 2977 10.1529/biophysj.107.109009
52. C.J. Kastrup, J.Q. Boedicker, A.P. Pomerantsev, M. Moayeri, Y. Bian, R.R. Pompano, and et al. Spatial localization of bacteria controls coagulation of human blood by "quorum acting." Nat. Chem. Biol. 4 2008 742 750
53. U.M. Okorie, W.S. Denney, M.S. Chatterjee, K.B. Neeves, and S.L. Diamond Determination of surface tissue factor thresholds that trigger coagulation at venous and arterial shear rates: amplification of 100 f. circulating tissue factor requires flow Blood 111 2008 3507 3513 10.1182/blood-2007-08-106229
54. P. Gasque Complement: a unique innate immune sensor for danger signals Mol. Immunol. 41 2004 1089 1098 10.1016/j.molimm.2004.06.011
55. K.E. Brummel, S.G. Paradis, S. Butenas, and K.G. Mann Thrombin functions during tissue factor-induced blood coagulation Blood 100 2002 148 152
56. G.J. Broze Tissue factor pathway inhibitor and the revised theory of coagulation Annu. Rev. Med. 46 1995 103 112 10.1146/annurev.med.46.1.103
57. M. Hoffman, D.M. Monroe, J.A. Oliver, and H.R. Roberts Factors IXa and Xa play distinct roles in tissue factor-dependent initiation of coagulation Blood 86 1995 1794 1801
58. D.M. Monroe, M. Hoffman, and H.R. Roberts Transmission of a procoagulant signal from tissue factor-bearing cell to platelets Blood Coagul. Fibrinolysis Int. J. Haemost. Thromb. 7 1996 459 464
59. M.K. Runyon, B.L. Johnson-Kerner, C.J. Kastrup, T.G. Van Ha, and R.F. Ismagilov Propagation of blood clotting in the complex biochemical network of hemostasis is described by a simple mechanism J. Am. Chem. Soc. 129 2007 7014 7015 10.1021/ja072602p
60. O.A. Fadeeva, M.A. Panteleev, S.S. Karamzin, A.N. Balandina, I.V. Smirnov, and F.I. Ataullakhanov Thromboplastin immobilized on polystyrene surface exhibits kinetic characteristics close to those for the native protein and activates in vitro blood coagulation similarly to thromboplastin on fibroblasts Biochem. Biokhimiia 75 2010 734 743
61. M.V. Ovanesov, E.G. Lopatina, E.L. Saenko, N.M. Ananyeva, L.I. Ul'yanova, O.P. Plyushch, and et al. Effect of factor VIII on tissue factor-initiated spatial clot growth Thromb. Haemost. 89 2003 235 242 10.1267/THRO03020235
62. D. Gailani, and G.J. Broze Factor XI activation in a revised model of blood coagulation Science 253 1991 909 912
63. I.M. Keularts, A. Zivelin, U. Seligsohn, H.C. Hemker, and S. Béguin The role of factor XI in thrombin generation induced by low concentrations of tissue factor Thromb. Haemost. 85 2001 1060 1065
64. S.J.H. Wielders, S. Béguin, H.C. Hemker, and T. Lindhout Factor XI-dependent reciprocal thrombin generation consolidates blood coagulation when tissue factor is not available Arterioscler. Thromb. Vasc. Biol. 24 2004 1138 1142 10.1161/01.ATV.0000128125.80559.9c
65. J.J. Sixma, and A. van den Berg The haemostatic plug in haemophilia A: a morphological study of haemostatic plug formation in bleeding time skin wounds of patients with severe haemophilia A Br. J. Haematol. 58 1984 741 753
66. M. Hoffman, H.C. Whinna, and D.M. Monroe Circulating tissue factor accumulates in thrombi, but not in hemostatic plugs J. Thromb. Haemost. 4 2006 2092 2093 10.1111/j.1538-7836.2006.02085.x
67. E. Lipets, O. Vlasova, E. Urnova, O. Margolin, A. Soloveva, O. Ostapushchenko, and et al. Circulating contact-pathway-activating microparticles together with factors IXa and XIa induce spontaneous clotting in plasma of hematology and cardiologic patients PLoS One 9 2014 e87692 10.1371/journal.pone.0087692
68. U.J.H. Sachs, and B. Nieswandt In vivo thrombus formation in murine models Circ. Res. 100 2007 979 991 10.1161/01.RES.0000261936.85776.5f
69. M. Hoffman, A. Harger, A. Lenkowski, U. Hedner, H.R. Roberts, and D.M. Monroe Cutaneous wound healing is impaired in hemophilia B Blood 108 2006 3053 3060 10.1182/blood-2006-05-020495
70. M.K. Runyon, C.J. Kastrup, B.L. Johnson-Kerner, T.G.V. Ha, and R.F. Ismagilov Effects of shear rate on propagation of blood clotting determined using microfluidics and numerical simulations J. Am. Chem. Soc. 130 2008 3458 3464 10.1021/ja076301r
71. L.M. Haynes, B.A. Bouchard, P.B. Tracy, and K.G. Mann Prothrombin activation by platelet-associated prothrombinase proceeds through the prethrombin-2 pathway via a concerted mechanism J. Biol. Chem. 287 2012 38647 38655 10.1074/jbc.M112.407791
72. L.M. Haynes, T. Orfeo, and K.G. Mann Rivaroxaban delivery and reversal at a venous flow rate Arterioscler. Thromb. Vasc. Biol. 32 2012 2877 2883 10.1161/ATVBAHA.112.300053
73. L.M. Haynes, Y.C. Dubief, and K.G. Mann Membrane binding events in the initiation and propagation phases of tissue factor-initiated zymogen activation under flow J. Biol. Chem. 287 2012 5225 5234 10.1074/jbc.M111.302075
74. K. Korsan-Bengtsen Routine tests as measures of the total intrinsic blood clotting potential. A comparison of whole blood clotting time (WBCT), recalcification time of citrated plasma (RTST), partial thromboplastin time (PTT), and activated partial thromboplastin time (APTT) Scand. J. Haematol. 8 1971 359 368
75. Z. Olah, M. Szarvas, Z. Bereczky, A. Kerenyi, J. Kappelmayer, and Z. Boda Direct thrombin inhibitors and factor xa inhibitors can influence the diluted prothrombin time used as the initial screen for lupus anticoagulant Arch. Pathol. Lab. Med. 137 2013 967 973 10.5858/arpa.2012-0236-OA
76. M.A. Panteleev, and H.C. Hemker Global/integral assays in hemostasis diagnostics: promises, successes, problems and prospects Thromb. J. 13 2015 5 10.1186/s12959-014-0032-y
77. 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
78. P.A. Evans, K. Hawkins, M. Lawrence, R.L. Williams, M.S. Barrow, N. Thirumalai, and et al. Rheometry and associated techniques for blood coagulation studies Med. Eng. Phys. 30 2008 671 679 10.1016/j.medengphy.2007.08.005
79. Y. Dargaud, H.M.H. Spronk, P. Leenders, H.C. Hemker, and H. Ten Cate Monitoring platelet dependent thrombin generation in mice Thromb. Res. 126 2010 436 441 10.1016/j.thromres.2010.08.007
80. M.A. Gracheva, E.S. Urnova, E.I. Sinauridze, I.D. Tarandovskiy, E.B. Orel, A.V. Poletaev, and et al. Thromboelastography, thrombin generation test and thrombodynamics reveal hypercoagulability in patients with multiple myeloma Leuk. Lymphoma 1-35 2015 10.3109/10428194.2015.1041385
81. W. Potze, J. Adelmeijer, R.J. Porte, and T. Lisman Preserved clot formation detected by the Thrombodynamics analyzer in patients with cirrhosis Thromb. Res. 135 2015 1012 1016
82. N. Tynngård, T.L. Lindahl, and S. Ramström Assays of different aspects of haemostasis - what do they measure? Thromb. J. 13 2015 8 10.1186/s12959-015-0036-2
83. E.N. Lipets, and F.I. Ataullakhanov Global assays of hemostasis in the diagnostics of hypercoagulation and evaluation of thrombosis risk Thromb. J. 13 2015 4 10.1186/s12959-015-0038-0
84. T.L. Lindahl, M. Wallstedt, K.M. Gustafsson, E. Persson, and A. Hillarp More efficient reversal of dabigatran inhibition of coagulation by activated prothrombin complex concentrate or recombinant factor VIIa than by four-factor prothrombin complex concentrate Thromb. Res. 135 2015 544 547 10.1016/j.thromres.2014.12.019
85. L.A. Parunov, N.P. Soshitova, O.A. Fadeeva, A.N. Balandina, K.G. Kopylov, M.A. Kumskova, and et al. Drug-drug interaction of the anti-TFPI aptamer BAX499 and factor VIII: studies of spatial dynamics of fibrin clot formation in hemophilia A Thromb. Res. 133 2014 112 119 10.1016/j.thromres.2013.10.036
86. L.A. Parunov, O.A. Fadeeva, A.N. Balandina, N.P. Soshitova, K.G. Kopylov, M.A. Kumskova, and et al. Improvement of spatial fibrin formation by the anti-TFPI aptamer BAX499: changing clot size by targeting extrinsic pathway initiation J. Thromb. Haemost. 9 2011 1825 1834 10.1111/j.1538-7836.2011.04412.x
87. C.S. Ivo, M.B. Ivo, P.G.O. de Salles, R.C.V. do Rosário, and T.A. Nunes Effect of the period of extrinsic mechanical compression following sclerotherapy in veins in rabbit ears Acta Cir. Bras. 26 2011 165 173 10.1590/S0102-86502011000300003
88. J.D. Welsh, T.J. Stalker, R. Voronov, R.W. Muthard, M. Tomaiuolo, S.L. Diamond, and et al. A systems approach to hemostasis: 1. The interdependence of thrombus architecture and agonist movements in the gaps between platelets Blood 124 2014 1808 1815 10.1182/blood-2014-01-550335
89. N.P. Soshitova, S.S. Karamzin, A.N. Balandina, O.A. Fadeeva, A.V. Kretchetova, G.M. Galstian, and et al. Predicting prothrombotic tendencies in sepsis using spatial clot growth dynamics Blood Coagul. Fibrinolysis Int. J. Haemost. Thromb. 23 2012 498 507 10.1097/MBC.0b013e328352e90e
90. E.A. Seregina, O.F. Nikulina, N.V. Tsvetaeva, M.N. Rodionova, I.V. Gribkova, E.B. Orel, and et al. Laboratory tests for coagulation system monitoring in a patient with β-thalassemia Int. J. Hematol. 99 2014 588 596 10.1007/s12185-014-1559-1