Blood Reviews
Volume 21, Issue 3 , Pages 131-142 , May 2007

Thrombin generation and fibrin clot structure

References 

  1. Medved LV, Gorkun OV, Privalov PL. Structural organization of C-terminal parts of fibrinogen A alpha-chains. FEBS Lett. 1983;160:291–295
  2. Ferry JD, Morrison PR. Preparation and properties of serum and plasma proteins. VIII. The conversion of human fibrinogen to fibrin under various conditions. J Am Chem Soc. 1947;69:388–400
  3. Betts L, Merenbloom BK, Lord ST. The structure of fibrinogen fragment D with the ’A’ knob peptide GPRVVE. J Thromb Haemost. 2006;4:1139–1141
  4. Rooney MM, Mullin JL, Lord ST. Substitution of tyrosine for phenylalanine in fibrinopeptide A results in preferential thrombin cleavage of fibrinopeptide B from fibrinogen. Biochemistry. 1998;37:13704–13709
  5. Higgins DL, Shafer JA. Fibrinogen Petoskey, a dysfibrinogenemia characterized by replacement of Arg-A alpha 16 by a histidyl residue. Evidence for thrombin-catalyzed hydrolysis at a histidyl residue. J Biol Chem. 1981;256:12013–12017
  6. Blomback B, Hessel B, Hogg D, Therkildsen L. A two-step fibrinogen–fibrin transition in blood coagulation. Nature. 1978;275:501–505
  7. Shen LL, Hermans J, McDonagh J, McDonagh RP. Role of fibrinopeptide B release: comparison of fibrins produced by thrombin and Ancrod. Am J Physiol. 1977;232:H629–H633
  8. Torbet J. Fibrin assembly after fibrinopeptide A release in model systems and human plasma studied with magnetic birefringence. Biochem J. 1987;244:633–637
  9. Blomback B, Carlsson K, Fatah K, Hessel B, Procyk R. Fibrin in human plasma: gel architectures governed by rate and nature of fibrinogen activation. Thromb Res. 1994;75:521–538
  10. Carr ME, Hermans J. Size and density of fibrin fibers from turbidity. Macromolecules. 1978;11:46–50
  11. Hantgan RR, Hermans J. Assembly of fibrin. A light scattering study. J Biol Chem. 1979;254:11272–11281
  12. Carr ME, Shen LL, Hermans J. Mass-length ratio of fibrin fibers from gel permeation and light scattering. Biopolymers. 1977;16:1–15
  13. Wolberg AS, Gabriel DA, Hoffman M. Analyzing fibrin clot structure using a microplate reader. Blood Coagul Fibrin. 2002;13:533–539
  14. Blomback B, Carlsson K, Hessel B, Liljeborg A, Procyk R, Aslund N. Native fibrin gel networks observed by 3D microscopy, permeation and turbidity. Biochim Biophys Acta. 1989;997:96–110
  15. Collet JP, Park D, Lesty C, et al. Influence of fibrin network conformation and fibrin fiber diameter on fibrinolysis speed: dynamic and structural approaches by confocal microscopy. Arterio Thromb Vasc Biol. 2000;20:1354–1361
  16. Wolberg AS, Monroe DM, Roberts HR, Hoffman M. Elevated prothrombin results in clots with an altered fiber structure: a possible mechanism of the increased thrombotic risk. Blood. 2003;101:3008–3013
  17. Wolberg AS, Allen GA, Monroe DM, Hedner U, Roberts HR, Hoffman M. High dose factor VIIa enhances clot stability in a model of hemophilia B. Brit J Haematol. 2005;131:645–655
  18. Hartmann A, Boukamp P, Friedl P. Confocal reflection imaging of 3D fibrin polymers. Blood Cells Mol Dis. 2006;36:191–193
  19. Nair CH, Shah GA, Dhall DP. Effect of temperature, pH and ionic strength and composition on fibrin network structure and its development. Thromb Res. 1986;42:809–816
  20. Carr ME, Gabriel DA, McDonagh J. Influence of Ca2+ on the structure of reptilase-derived and thrombin-derived fibrin gels. Biochem J. 1986;239:513–516
  21. Glover CJ, McIntire LV, Brown CH, Natelson EA. Rheological properties of fibrin clots. Effects of fibrinogen concentration, Factor XIII deficiency, and Factor XIII inhibition. J Lab Clin Med. 1975;86:644–656
  22. Carr ME, Gabriel DA. The effect of dextran 70 on the structure of plasma-derived fibrin gels. J Lab Clin Med. 1980;96:985–993
  23. Marchi R, Lundberg U, Grimbergen J, et al. Fibrinogen Caracas V, an abnormal fibrinogen with an Aalpha 532 Ser–>Cys substitution associated with thrombosis. Thromb Haemost. 2000;84:263–270
  24. Collet J-P, Soria J, Mirshahi M, et al. Dusart syndrome: a new concept of the relationship between fibrin clot architecture and fibrin clot degradability: hypofibrinolysis related to an abnormal clot structure. Blood. 1993;82:2462–2469
  25. Collet J-P, Woodhead JL, Soria J, et al. Fibrinogen Dusart: electron microscopy of molecules, fibers and clots, and viscoelastic properties of clots. Biophysical J. 1996;70:500–510
  26. Gabriel DA, Muga K, Boothroyd EM. The effect of fibrin structure on fibrinolysis. J Biol Chem. 1992;267:24259–24263
  27. Carr ME, Alving BM. Effect of fibrin structure on plasmin-mediated dissolution of plasma clots. Blood Coag Fibrinol. 1995;6:567–573
  28. Tracy PB, Peterson JM, Nesheim ME, McDuffie FC, Mann KG. Interaction of coagulation factor V and factor Va with platelets. J Biol Chem. 1979;254:10354–10361
  29. Nesheim ME, Pittman DD, Wang JH, Slonosky D, Giles AR, Kaufman RJ. The binding of 35S-labeled recombinant factor VIII to activated and unactivated human platelets. J Biol Chem. 1988;263:16467–16470
  30. Ahmad SS, Rawala-Sheikh R, Walsh PN. Comparative interactions of factor IX and factor IXa with human platelets. J Biol Chem. 1989;264:3244–3251
  31. Rawala-Sheikh R, Ahmad SS, Ashby B, Walsh PN. Kinetics of coagulation factor X activation by platelet-bound factor IXa. Biochemistry. 1990;29:2606–2611
  32. Monroe DM, Hoffman M, Roberts HR. Transmission of a procoagulant signal from tissue factor-bearing cells to platelets. Blood Coag Fibrinol. 1996;7:459–464
  33. Hoffman M, Monroe DM, Oliver JA, Roberts HR. Factors IXa and Xa play distinct roles in tissue factor-dependent initiation of coagulation. Blood. 1995;86:1794–1801
  34. Liu W, Jawerth LM, Sparks EA, et al. Fibrin fibers have extraordinary extensibillity and elasticity. Science. 2006;313:634
  35. van ’t Veer C, Golden NJ, Kalafatis M, Simioni P, Bertina RM, Mann KG. An in vitro analysis of the combination of hemophilia A and factor V(LEIDEN). Blood. 1997;90:3067–3072
  36. Al Dieri R, Peyvandi F, Santagostino E, et al. The thrombogram in rare inherited coagulation disorders: its relation to clinical bleeding. Thromb Haemost. 2002;88:576–582
  37. Allen GA, Wolberg AS, Oliver JA, Hoffman M, Roberts HR, Monroe DM. Impact of procoagulant concentration on rate, peak and total thrombin generation in a model system. J Thromb Haemost. 2004;2:402–413
  38. Dargaud Y, Beguin S, Lienhart A, et al. Evaluation of thrombin generating capacity in plasma from patients with haemophilia A and B. Thromb Haemost. 2005;93:475–480
  39. Wolberg AS. Thrombin Generation Assays: Understanding how the method influences the results. Thromb Res 2006;in press.
  40. Shah GA, Nair CH, Dhall DP. Comparison of fibrin networks in plasma and fibrinogen solution. Thromb Res. 1987;45:257–264
  41. Carr ME. Fibrin formed in plasma is composed of fibers more massive than those formed from purified fibrinogen. Thrombosis and Haemostasis. 1988;59:535–539
  42. Torbet J. Fibrin assembly in human plasma and fibrinogen/albumin mixtures. Biochemistry. 1986;25:5309–5314
  43. Naski MC, Shafer JA. A kinetic model for the alpha-thrombin-catalyzed conversion of plasma levels of fibrinogen to fibrin in the presence of antithrombin III. J Biol Chem. 1991;266:13003–13010
  44. Elgue G, Sanchez J, Fatah K, Olsson P, Blomback B. The effect of plasma antithrombin concentration on thrombin generation and fibrin gel structure. Thromb Res. 1994;75:203–212
  45. Wilf J, Gladner JA, Minton AP. Acceleration of fibrin gel formation by unrelated proteins. Thromb Res. 1985;37:681–688
  46. Braaten JV, Jerome WG, Hantgan RR. Uncoupling fibrin from integrin receptors hastens fibrinolysis at the platelet-fibrin interface. Blood. 1994;83:982–993
  47. Jerome WG, Handt S, Hantgan RR. Endothelial cells organize fibrin clots into structures that are more resistant to lysis. Microsc Microanal. 2005;11:268–277
  48. Handt S, Jerome WG, Tietze L, Hantgan RR. Plasminogen activator inhibitor-1 secretion of endothelial cells increases fibrinolytic resistance of an in vitro fibrin clot: evidence for a key role of endothelial cells in thrombolytic resistance. Blood. 1996;87:4204–4213
  49. Reed GL, Matsueda GR, Haber E. Platelet factor XIII increases the fibrinolytic resistance of platelet-rich clots by accelerating the crosslinking of alpha 2-antiplasmin to fibrin. Thrombosis and Haemostasis. 1992;68:315–320
  50. Mosnier LO, Buijtenhuijs P, Marx PF, Meijers JC, Bouma BN. Identification of thrombin activatable fibrinolysis inhibitor (TAFI) in human platelets. Blood. 2003;101:4844–4846
  51. Pham TD, Kaplan KL, Butler VP. Immunoelectron microscopic localization of platelet factor 4 and fibrinogen in the granules of human platelets. J Histochem Cytochem. 1983;31:905–910
  52. Xi M, Beguin S, Hemker HC. The relative importance of the factors II, VII, IX and X for the prothrombinase activity in plasma of orally anticoagulated patients. Thromb Haemost. 1989;62:788–791
  53. Xi M, Beguin S, Hemker HC. Importance of factor-IX-dependent prothrombinase formation–the Josso pathway–in clotting plasma. Haemostasis. 1989;19:301–308
  54. Sumner WT, Monroe DM, Hoffman M. Variability in platelet procoagulant activity in healthy volunteers. Thromb Res. 1996;81:533–543
  55. Butenas S, van’t Veer C, Mann KG. “Normal” thrombin generation. Blood. 1999;94:2169–2178
  56. Kempton CL, Hoffman M, Roberts HR, Monroe DM. Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler Thromb Vasc Biol. 2005;25:861–866
  57. Aird WC. Spatial and temporal dynamics of the endothelium. J Thromb Haemost. 2005;3:1392–1406
  58. Kumar R, Beguin S, Hemker HC. The effect of fibrin clots and clot-bound thrombin on the development of platelet procoagulant activity. Thromb Haemost. 1995;74:962–968
  59. Weitz JI, Hudoba M, Massel D, Maraganore J, Hirsh J. Clot-bound thrombin is protected from inhibition by heparin-antithrombin III but is susceptible to inactivation by antithrombin III-independent inhibitors. J Clin Invest. 1990;86:385–391
  60. Weitz JI, Leslie B, Hudoba M. Thrombin binds to soluble fibrin degradation products where it is protected from inhibition by heparin-antithrombin but susceptible to inactivation by antithrombin-independent inhibitors. Circulation. 1998;97:544–552
  61. Torbet J. The thrombin activation pathway modulates the assembly, structure and lysis of human plasma clots in vitro. Thromb Haemost. 1995;73:785–792
  62. von dem Borne PA, Meijers JC, Bouma BN. Feedback activation of factor XI by thrombin in plasma results in additional formation of thrombin that protects fibrin clots from fibrinolysis. Blood. 1995;86:3035–3042
  63. Panteleev MA, Ovanesov MV, Kireev DA, et al. Spatial propagation and localization of blood coagulation are regulated by intrinsic and protein C pathways, respectively. Biophys J. 2006;90:1489–1500
  64. Rodgers GM, Greenberg CS, Shuman MA. Characterization of the effects of cultured vascular cells on the activation of blood coagulation. Blood. 1983;61:1155–1162
  65. Rodgers GM, Broze GJ, Shuman MA. The number of receptors for factor VII correlates with the ability of cultured cells to initiate coagulation. Blood. 1984;63:434–438
  66. Zwaginga JJ, de Boer HC, MJ IJ, et al. Thrombogenicity of vascular cells. Comparison between endothelial cells isolated from different sources and smooth muscle cells and fibroblasts. Arteriosclerosis. 1990;10:437–448
  67. Ovanesov MV, Ananyeva NM, Panteleev MA, Ataullakhanov FI, Saenko EL. Initiation and propagation of coagulation from tissue factor-bearing cell monolayers to plasma: initiator cells do not regulate spatial growth rate. J Thromb Haemost. 2005;3:321–331
  68. Carr ME, Dent RM, Carr SL. Abnormal fibrin structure and inhibition of fibrinolysis in patients with multiple myeloma. J Lab Clin Med. 1996;128:83–88
  69. Collet JP, Mishal Z, Lesty C, et al. Abnormal fibrin clot architecture in nephrotic patients is related to hypofibrinolysis: influence of plasma biochemical modifications: a possible mechanism for the high thrombotic tendency?. Thromb Haemost. 1999;82:1482–1489
  70. Sugo T, Nakamikawa C, Yoshida N, et al. End-linked homodimers in fibrinogen Osaka VI with a B beta-chain extension lead to fragile clot structure. Blood. 2000;96:3779–3785
  71. Dunn EJ, Ariens RA, Grant PJ. The influence of type 2 diabetes on fibrin structure and function. Diabetologia. 2005;48:1198–1206
  72. Dunn EJ, Philippou H, Ariens RA, Grant PJ. Molecular mechanisms involved in the resistance of fibrin to clot lysis by plasmin in subjects with type 2 diabetes mellitus. Diabetologia. 2006;49:1071–1080
  73. Sixma JJ, van den Berg A. 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. 1984;58:741–753
  74. Cawthern KM, van’t Veer C, Lock JB, Di Lorenzo ME, Branda RF, Mann KG. Blood coagulation in hemophilia A and hemophilia C. Blood. 1998;91:4581–4592
  75. Englert JM, Moen JL, Wolberg AS. Altered fibrinopeptide release produces thicker fibrin fibers and an abnormal fibrin clot structure in an in vitro model of hemophilia B. International Fibrinogen Workshop. 2004.
  76. Bettigole RE, Hampton JW, Bird RM. Abnormal plasma clots in hemophilia. Thromb Diath Haemorrh. 1964;12:331–337
  77. He S, Blomback M, Jacobsson Ekman G, Hedner U. The role of recombinant factor VIIa (FVIIa) in fibrin structure in the absence of FVIII/FIX. J Thromb Haemost. 2003;1:1215–1219
  78. Broze GJ, Higuchi DA. Coagulation-dependent inhibition of fibrinolysis: role of carboxypeptidase-U and the premature lysis of clots from hemophilic plasma. Blood. 1996;88:3815–3823
  79. Mosnier LO, Lisman T, van den Berg HM, Nieuwenhuis HK, Meijers JC, Bouma BN. The defective down regulation of fibrinolysis in haemophilia A can be restored by increasing the TAFI plasma concentration. Thromb Haemost. 2001;86:1035–1039
  80. Lisman T, Mosnier LO, Thierry Lambert T, et al. Inhibition of fibrinolysis by recombinant factor VIIa in plasma from patients with severe hemophilia A. Blood. 2002;99:175–179
  81. Negrier C, Hay CR. The treatment of bleeding in hemophilic patients with inhibitors with recombinant factor VIIa. Semin Thromb Hemost. 2000;26:407–412
  82. Monroe DM, Hoffman M, Oliver JA, Roberts HR. Platelet activity of high-dose factor VIIa is independent of tissue factor. Brit J Haematol. 1997;99:542–547
  83. Poort SR, Rosendaal FR, Reitsma PH, Bertina RM. A common genetic variation in the 3′-untranslated region of the prothrombin gene is associated with elevated plasma prothrombin levels and an increase in venous thrombosis. Blood. 1996;88:3698–3703
  84. Rosendaal FR, Siscovick DS, Schwartz SM, Psaty BM, Raghunathan TE, Vos HL. A common prothrombin variant (20210 G to A) increases the risk of myocardial infarction in young women. Blood. 1997;90:1747–1750
  85. Giordano P, De Lucia D, Coppola B, Iolascon A. Homozygous prothrombin gene mutation and ischemic cerebrovascular disease: a case report. Acta Haematologica. 1999;102:101–103
  86. Kyrle PA, Mannhalter C, Beguin S, et al. Clinical studies and thrombin generation in patients homozygous or heterozygous for the G20210A mutation in the prothrombin gene. Arterio Thromb Vasc Biol. 1998;18:1287–1291
  87. Colucci M, Binetti BM, Tripodi A, Chantarangkul V, Semeraro N. Hyperprothrombinemia associated with prothrombin G20210A mutation inhibits plasma fibrinolysis through a TAFI-mediated mechanism. Blood. 2004;103:2157–2161
  88. Fatah K, Hamsten A, Blomback B, Blomback M. Fibrin gel network characteristics and coronary heart disease: relations to plasma fibrinogen concentration, acute phase protein, serum lipoproteins and coronary atherosclerosis. Thromb Haemost. 1992;68:130–135
  89. Fatah K, Silveira A, Tornvall P, Karpe F, Blomback M, Hamsten A. Proneness to formation of tight and rigid fibrin gel structures in men with myocardial infarction at a young age. Thromb Haemost. 1996;76:535–540
  90. Mills J, Mansfield M, Grant P. Elevated fibrinogen in the healthy male relatives of patients with severe, premature coronary artery disease. Eur Heart J. 2002;23:1276–1281
  91. Collet JP, Allali Y, Lesty C, et al. Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis. Arterioscler Thromb Vasc Biol. 2006;26:2567–2573
  92. Greilich PE, Carr ME, Zekert SL, Dent RM. Quantitative assessment of platelet function and clot structure in patients with severe coronary artery disease. American Journal of the Medical Sciences. 1994;307:15–20
  93. Mills JD, Ariens RA, Mansfield MW, Grant PJ. Altered fibrin clot structure in the healthy relatives of patients with premature coronary artery disease. Circulation. 2002;106:1938–1942
  94. Aoki I, Shimoyama K, Aoki N, et al. Platelet-dependent thrombin generation in patients with diabetes mellitus: effects of glycemic control on coagulability in diabetes. J Am Coll Cardiol. 1996;27:560–566
  95. Nair CH, Azhar A, Wilson JD, Dhall DP. Studies on fibrin network structure in human plasma. Part II–Clinical application: diabetes and antidiabetic drugs. Thromb Res. 1991;64:477–485
  96. Jorneskog G, Egberg N, Fagrell B, et al. Altered properties of the fibrin gel structure in patients with IDDM. Diabetologia. 1996;39:1519–1523
  97. Meh DA, Siebenlist KR, Mosesson MW. Identification and characterization of the thrombin binding sites on fibrin. Journal of Biological Chemistry. 1996;271:23121–23125
  98. Mutch NJ, Robbie LA, Booth NA. Human thrombi contain an abundance of active thrombin. Thromb Haemost. 2001;86:1028–1034
  99. Hogg PJ, Jackson CM. Fibrin monomer protects thrombin from inactivation by heparin-antithrombin III: implications for heparin efficacy. Proc Natl Acad Sci U S A. 1989;86:3619–3623
  100. Kumar R, Beguin S, Hemker HC. The influence of fibrinogen and fibrin on thrombin generation–evidence for feedback activation of the clotting system by clot bound thrombin. Thrombosis and Haemostasis. 1994;72:713–721
  101. de Bosch NB, Mosesson MW, Ruiz-Saez A, Echenagucia M, Rodriquez-Lemoin A. Inhibition of thrombin generation in plasma by fibrin formation (antithrombin 1). Thromb Haemost. 2002;88:253–258
  102. Owen J, Friedman KD, Grossman BA, Wilkins C, Berke AD, Powers ER. Thrombolytic therapy with tissue plasminogen activator or streptokinase induces transient thrombin activity. Blood. 1988;72:616–620
  103. Badimon L, Chesebro JH, Badimon JJ. Thrombus formation on ruptured atherosclerotic plaques and rethrombosis on evolving thrombi. Circulation. 1992;86:III74–III85
  104. Banninger H, Lammle B, Furlan M. Binding of alpha-thrombin to fibrin depends on the quality of the fibrin network. Biochem J. 1994;298:157–163
  105. Nehls V, Herrmann R. The configuration of fibrin clots determines capillary morphogenesis and endothelial cell migration. Microvasc Res. 1996;51:347–364
  106. Shats EA, Nair CH, Dhall DP. Interaction of endothelial cells and fibroblasts with modified fibrin networks: role in atherosclerosis. Atherosclerosis. 1997;129:9–15
  107. Collen A, Koolwijk P, Kroon M, van Hinsbergh VW. Influence of fibrin structure on the formation and maintenance of capillary-like tubules by human microvascular endothelial cells. Angiogenesis. 1998;2:153–165
  108. Weisel JW, Nagaswami C. Computer modeling of fibrin polymerization kinetics correlated with electron microscope and turbidity observations: clot structure and assembly are kinetically controlled. Biophys J. 1992;63:111–128

PII: S0268-960X(06)00066-X

doi: 10.1016/j.blre.2006.11.001

Blood Reviews
Volume 21, Issue 3 , Pages 131-142 , May 2007