Rate-limiting roles of the tenase complex of factors VIII and IX in platelet procoagulant activity and formation of platelet-fibrin thrombi under flow

Haematologica

Volumn 100, Issue 6, 2015, Pages 748-756

  Swieringa, Frauke ^a   Kuijpers, Marijke J E ^a   Lamers, Moniek M E ^a   van der Meijden, Paola E J ^a   Heemskerk, Johan W M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 8; BLOOD CLOTTING FACTOR 9; COLLAGEN; FIBRIN; HEMOSTATIC AGENT; PHOSPHATIDYLSERINE; PROCOAGULANT; RIVAROXABAN; TENASE; THROMBIN; THROMBOPLASTIN; UNCLASSIFIED DRUG; BLOOD CLOTTING FACTOR 8A; BLOOD CLOTTING FACTOR 9A; CANCER PROCOAGULANT; CYSTEINE PROTEINASE; TUMOR PROTEIN;

ANALYTIC METHOD; ARTICLE; BLOOD CLOTTING; FIBRIN FORMATION; FLOW CHAMBER EXPERIMENT; HEMOPHILIA A; HEMOPHILIA B; HUMAN; MOUSE; NONHUMAN; THROMBOCYTE; ANIMAL; BLOOD; C57BL MOUSE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; THROMBOSIS;

ANIMALS; BLOOD COAGULATION; BLOOD PLATELETS; CYSTEINE ENDOPEPTIDASES; FACTOR IXA; FACTOR VIIIA; FIBRIN; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASM PROTEINS; THROMBOSIS;

EID: 84930520496     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2014.116863     Document Type: Article

References (54)

1. Heemskerk JW, Mattheij N, Cosemans JM. Platelet-based coagulation: different populations, different functions. J Thromb Haemost. 2013;11(1):2-11.
2. Mazepa M, Hoffman M, Monroe D. Superactivated platelets: thrombus regulators, thrombin generators, and potential clinical targets. Arterioscler Thromb Vasc Biol. 2013;33(8):1747-1752.
3. Jackson SP. Arterial thrombosis: insidious, unpredictable and deadly. Nat Med. 2011;17(11):1423-1436.
4. Kuijpers MJ, Munnix IC, Cosemans JM, et al. Key role of platelet procoagulant activity in tissue factor- and collagen-dependent thrombus formation in arterioles and venules in vivo. Differential sensitivity to thrombin inhibition. Microcirculation. 2008;15(4):269-282.
5. Furie B, Furie BC. In vivo thrombus formation. J Thromb Haemost. 2007;5(Suppl 1):12-7.
6. Von Brühl ML, Stark K, Steinhart A, et al. Monocytes, neutrophils and platelets cooperate to inititate and propagate venous thrombosis in mice in vivo. J Exp Med. 2012;209(4):819-835.
7. Dubois C, Panicot-Dubois L, Merrill-Skoloff G, Furie B, Furie BC. Glycoprotein VI-dependent and -independent pathways of thrombus formation in vivo. Blood. 2006;107(10):3902-3906.
8. Mangin P, Yap CL, Nonne C, et al. Thrombin overcomes the thrombosis defect associated with platelet GPVI/FcRgamma deficiency. Blood. 2006;107(11):4346-4353.
9. Munnix IC, Kuijpers MJ, Auger J, et al. Segregation of platelet aggregatory and procoagulant microdomains in thrombus formation: regulation by transient integrin activation. Arterioscler Thromb Vasc Biol. 2007;27(11):2484-2490.
10. Renné T, Pozgajova M, Grüner S, et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005;202(2):271-281.
11. Kuijpers MJ, van der Meijden PE, Feijge MA, et al. Factor XIIa regulates the pathological process of thrombus formation on ruptured plaques. Arterioscler Thromb Vasc Biol. 2014;34(8):1674-1680.
12. Day SM, Reeve JL, Pedersen B, et al. Macrovascular thrombosis is driven by tissue factor derived primarily from the blood vessel wall. Blood. 2005;105(1):192-198.
13. Gross PL, Furie BC, Merrill-Skoloff G, Chou J, Furie B. Leukocyte-versus microparticlemediated tissue factor transfer during arteriolar thrombus development. J Leukoc Biol. 2005;78(6):1318-1326.
14. Béguin S, Kumar R. Thrombin, fibrin and platelets, a resonance loop in which von Willebrand factor is a necessary link. Thromb Haemost. 1997;78(1):590-594.
15. Berny MA, Munnix IC, Auger JM, et al. Spatial distribution of factor Xa, thrombin, and fibrin(ogen) on thrombi at venous shear. PloS One. 2010;5(4):e10415.
16. Yang H, Kim A, David T, et al. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell. 2012;151(1): 111-122.
17. Van Kruchten R, Mattheij NJ, Saunders C, et al. Both TMEM16F-dependent and TMEM16F-independent pathways contribute to phosphatidylserine exposure in platelet apoptosis and platelet activation. Blood. 2013;121(10):1850-1857.
18. Cosemans JM, Schols SE, Stefanini L, et al. Key role of glycoprotein Ib/V/IX and von Willebrand factor in platelet activationdependent fibrin formation at low shear flow. Blood. 2011;117(2):651-660.
19. Zwaal RF, Schroit AJ. Pathophysiological implications of membrane phospholipid asymmetry in blood cells. Blood. 1997;89(4): 1121-1132.
20. Monroe DM, Hoffman M. What does it take to make the perfect clot? Arterioscler Thromb Vasc Biol. 2006;26(1):41-48.
21. Mackman N. Triggers, targets and treatments for thrombosis. Nature. 2008;451(7181):914-918.
22. Hovig T, Dodds WJ, Rowsell HC, Mustard JF. The transformation of hemostatic platelet plugs in normal and factor IX deficient dogs. Am J Pathol. 1968;53(3):355-373.
23. 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(4):741-753.
24. Van der Velden P, Giles AR. A detailed morphological evaluation of the evolution of the haemostatic plug in normal, factor VII and factor VIII deficient dogs. Br J Haematol. 1988;70(3):345-355.
25. Mann KG, Jenny RJ, Krishnaswamy S. Cofactor proteins in the assembly and expression of blood clotting enzyme complexes. Annu Rev Biochem. 1988;57:915-956.
26. Hemker HC. Thrombin generation, an essential step in haemostasis and thrombosis. In: Haemostasis and Thrombosis, Vol 1 (Forbes CD, Thomas DP, Tuddenham EGD, Eds) Churchill Livingstone, UK. 1993:477-490.
27. Orfeo T, Brummel-Ziedins KE, Gissel M, Butenas S, Mann KG. The nature of the stable blood clot procoagulant activities. J Biol Chem. 2008;283(15):9776-9786.
28. 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(3):475-480.
29. Bi L, Lawler AM, Antonarakis SE, High KA, Gearhart JD, Kazazian HH. Targeted disruption of the mouse factor VIII gene produces a model of haemophilia A. Nat Genet. 1995;10(1):119-121.
30. Chauhan AK, Kisucka J, Lamb CB, Bergmeier W, Wagner DD. Von Willebrand factor and factor VIII are independently required to form stable occlusive thrombi in injured veins. Blood. 2007;109(6):2424-2429.
31. Neyman M, Gewirtz J, Poncz M. Analysis of the spatial and temporal characteristics of platelet-delivered factor VIII-based clots. Blood. 2008;112(4):1101-1108.
32. Ogawa S, Szlam F, Dunn AL, et al. Evaluation of a novel flow chamber system to assess clot formation in factor VIII-deficient mouse and anti-factor IXa-treated human blood. Haemophilia. 2012;18(6):926-932.
33. Lin HF, Maeda N, Smithies O, Straight DL, Stafford DW. A coagulation factor IX-deficient mouse model for human hemophilia B. Blood. 1997;90(10):3962-3966.
34. Kundu RK, Sangiorgi F, Wu LY, et al. Targeted inactivation of the coagulation factor IX gene causes hemophilia B in mice. Blood. 1998;92(1):168-174.
35. Wang X, Cheng Q, Xu L, et al. Effects of factor IX and factor XI deficiency on ferric chloride- induced carotid artery occlusion in mice. J Thromb Haemost. 2005;3(4):695-702.
36. Munnix IC, Cosemans JM, Auger JM, Heemskerk JW. Platelet response heterogeneity in thrombus formation. Thromb Haemost. 2009;102(6):1149-1156.
37. De Witt SM, Swieringa F, Cavill R, et al. Identification of platelet function defects by multi-parameter assessment of thrombus formation. Nat Commun. 2014;5:4257.
38. Van der Meijden PE, Munnix IC, Auger JM, et al. Dual role of collagen in factor XIIdependent thrombus formation. Blood. 2009;114(4):881-890.
39. Kuijpers MJ, Schulte V, Oury C, et al. Facilitating roles of murine platelet glycoprotein Ib and aIIbb3 in phosphatidylserine exposure during vWF-collagen-induced thrombus formation. J Physiol. 2004;558(2): 403-415.
40. Bauer KA. Recent progress in anticoagulant therapy: oral direct inhibitors of thrombin and factor Xa. J Thromb Haemost. 2011;9 (Suppl 1):12-19.
41. Van der Meijden PE, Feijge MA, Swieringa F, et al. Key role of integrin αIIbβ3 signaling to Syk kinase in tissue factor-induced thrombin generation. Cell Mol Life Sci. 2012;69(20): 3481-3492.
42. Curtis JE, Helgerson SL, Parker ET, Lollar P. Isolation and characterization of thrombinactivated human factor VIII. J Biol Chem. 1994;269(8):6246-6251.
43. Lamphear BJ, Fay PJ. Factor IXa enhances reconstitution of factor VIIIa from isolated A2 subunit and A1/A3-C1-C2 dimer. J Biol Chem. 1992;267(6):3725-3730.
44. Doi M, Sugimoto M, Matsui H, Matsunari Y, Shima M. Coagulation potential of immobilised factor VIII in flow-dependent fibrin generation on platelet surfaces. Thromb Haemost. 2013;110(2):316-322.
45. Du LM, Nurden P, Nurden AT, et al. Platelettargeted gene therapy with human factor VIII establishes haemostasis in dogs with haemophilia A. Nat Commun. 2013;4:2773.
46. Milanov P, Ivanciu L, Abriss D, et al. Engineered factor IX variants bypass FVIII and correct hemophilia A phenoype in mice. Blood. 2014;119(2):602-611.
47. Hill-Eubanks DC, Lollar P. von Willebrand factor is a cofactor for thrombin-catalyzed cleavage of the factor VIII light chain. J Biol Chem. 1990;265(29):17854-17858.
48. Colman RW, Hirsh J, Marder VJ, Clowes AW, George JN. Hemostasis and Thrombosis. Philadelphia: Lippincott Williams & Wilkins; 2001.
49. Billy D, Speijer H, Willems G, Hemker HC, Lindhout T. Prothrombin activation by prothrombinase in a tubular flow reactor. J Biol Chem. 1995;270(3):1029-1034.
50. Wartiovaara-Kautto U, Joutsi-Korhonen L, Ilveskero S, Armstrong E, Lassila R. Platelets significantly modify procoagulant activities in haemophilia A. Haemophilia. 2011;17(5):743-751.
51. Sugita C, Yamashita A, Moriguchi-Goto S, et al. Factor VIII contributes to platelet-fibrin thrombus formation via thrombin generation under low shear conditions. Thromb Res. 2009;124(5):601-607.
52. Weiss HJ, Turitto VT, Vicic WJ, Baumgartner HR. Fibrin formation, fibrinopeptide A release, and platelet thrombus dimensions on subendothelium exposed to flowing native blood: greater in factor XII and XI than in factor VIII and IX deficiency. Blood. 1984;63(5):1004-1014.
53. Onasoga-Jarvis AA, Leiderman K, Fogelson AL, et al. The effect of factor VIII deficiencies and replacement and bypass therapies on thrombus formation under venous flow conditions in microfluidic and computational models. PloS One. 2013;8(11):e78732.
54. Colace TV, Fogarty PF, Panckeri KA, Diamond SL. Microfluidic assay of hemophilic blood clotting: distinct deficits in platelet and fibrin deposition at low factor levels. J Thromb Haemost. 2014;12(2):147-158.