Prothrombin activation by platelet-associated prothrombinase proceeds through the prethrombin-2 pathway via a concerted mechanism

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38647-38655

  Haynes, Laura M ^a   Bouchard, Beth A ^a   Tracy, Paula B ^a   Mann, Kenneth G ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED PLATELETS; BINDING FACTORS; COAGULATION PROCESS; CONCERTED MECHANISM; ENZYME COMPLEXES; FACTOR XA; FLOW CHAMBERS; IN-VIVO; KEY ENZYMES; PROTHROMBIN ACTIVATION; PROTHROMBINASE; SYNTHETIC PHOSPHOLIPIDS;

CELL MEMBRANES; COAGULATION; CONFOCAL MICROSCOPY; CYTOLOGY; ENZYMES; GLYCOPROTEINS; LIPOSOMES;

PLATELETS;

BLOOD CLOTTING FACTOR 10A; MEIZOTHROMBIN; PROTHROMBIN;

ADULT; ARTICLE; CELL POPULATION; CONFOCAL MICROSCOPY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME RELEASE; HUMAN; HUMAN CELL; NORMAL HUMAN; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; REACTION ANALYSIS; SHEAR RATE; STEADY STATE; SURFACE PROPERTY; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE MEMBRANE;

ANTICOAGULANTS; BLOOD COAGULATION; BLOOD PLATELETS; CATALYSIS; COLLAGEN; ENZYME PRECURSORS; FACTOR XA; HUMANS; LIPID BILAYERS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; PHOSPHOLIPIDS; PROTHROMBIN; THROMBIN; TIME FACTORS;

EID: 84869015264     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.407791     Document Type: Article

References (57)

1. Mann, K. G., Nesheim, M. E., Church, W. R., Haley, P., and Krishnaswamy, S. (1990) Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 76, 1-16 (Pubitemid 20220784)
2. Krishnaswamy, S., Mann, K. G., and Nesheim, M. E. (1986) The prothrombinase-catalyzed activation of prothrombin proceeds through the intermediate meizothrombin in an ordered, sequential reaction. J. Biol. Chem. 261, 8977-8984 (Pubitemid 17205103)
3. Downing, M. R., Butkowski, R. J., Clark, M. M., and Mann, K. G. (1975) Human prothrombin activation. J. Biol. Chem. 250, 8897-8906
4. Petrovan, R. J., Govers-Riemslag, J. W., Nowak, G., Hemker, H. C., Tans, G., and Rosing, J. (1998) Autocatalytic peptide bond cleavages in prothrombin and meizothrombin. Biochemistry 37, 1185-1191 (Pubitemid 28135703)
5. Wood, J. P., Silveira, J. R., Maille, N. M., Haynes, L. M., and Tracy, P. B. (2011) Prothrombin activation on the activated platelet surface optimizes expression of procoagulant activity. Blood 117, 1710-1718
6. Fager, A. M., Tracy, P. B., and Everse, S. J. (2009) Unique structural models of prothrombinase assembled on the activated platelet membrane. J. Thromb. Haemost. 7, 198a
7. Tracy, P. B., Nesheim, M. E., and Mann, K. G. (1981) Coordinate binding of factor Va and factor Xa to the unstimulated platelet. J. Biol. Chem. 256, 743-751 (Pubitemid 11151447)
8. Tracy, P. B., and Mann, K. G. (1983) Prothrombinase complex assembly on the platelet surface is mediated through the 74,000-dalton component of factor Va. Proc. Natl. Acad. Sci. U.S.A. 80, 2380-2384 (Pubitemid 13097193)
9. Tracy, P. B., Eide, L. L., and Mann, K. G. (1985) Human prothrombinase complex assembly and function on isolated peripheral blood cell populations. J. Biol. Chem. 260, 2119-2124 (Pubitemid 15112069)
10. Nesheim, M. E., Furmaniak-Kazmierczak, E., Henin, C., and Côté, G. (1993) On the existence of platelet receptors for factor V(a) and factor VIII(a). Thromb. Haemost. 70, 80-86 (Pubitemid 23225456)
11. Bouchard, B. A., Catcher, C. S., Thrash, B. R., Adida, C., and Tracy, P. B. (1997) Effector cell protease receptor-1, a platelet activation-dependent membrane protein, regulates prothrombinase-catalyzed thrombin generation. J. Biol. Chem. 272, 9244-9251 (Pubitemid 27154934)
12. Tracy, P. B., Eide, L. L., Bowie, E. J., and Mann, K. G. (1982) Radioimmunoassay of factor V in human plasma and platelets. Blood 60, 59-63 (Pubitemid 12085920)
13. Monković, D. D., and Tracy, P. B. (1990) Functional characterization of human platelet-released factor V and its activation by factor Xa and thrombin. J. Biol. Chem. 265, 17132-17140
14. Beumer, S., Heijnen, H. F., IJsseldijk, M. J., Orlando, E., de Groot, P. G., and Sixma, J. J. (1995) Platelet adhesion to fibronectin in flow: the importance of von Willebrand factor and glycoprotein Ib. Blood 86, 3452-3460
15. Hathcock, J. J. (2006) Flow effects on coagulation and thrombosis. Arterioscler. Thromb. Vasc. Biol. 26, 1729-1737
16. Moroi, M., Jung, S. M., Shinmyozu, K., Tomiyama, Y., Ordinas, A., and Diaz-Ricart, M. (1996) Analysis of platelet adhesion to a collagen-coated surface under flow conditions: the involvement of glycoprotein VI in the platelet adhesion. Blood 88, 2081-2092 (Pubitemid 26307910)
17. Moroi, M., Jung, S. M., Okuma, M., and Shinmyozu, K. (1989) A patient with platelets deficient in glycoprotein VI that lack both collagen-induced aggregation and adhesion. J. Clin. Invest. 84, 1440-1445 (Pubitemid 19272230)
18. Santoro, S. A. (1986) Identification of a 160,000 dalton platelet membrane protein that mediates the initial divalent cation-dependent adhesion of platelets to collagen. Cell 46, 913-920
19. Brass, L. F. (2003) Thrombin and platelet activation. Chest 124, 18S-25S
20. Ruggeri, Z. M., Bader, R., and de Marco, L. (1982) Glanzmann thrombasthenia: deficient binding of von Willebrand factor to thrombin-stimulated platelets. Proc. Natl. Acad. Sci. U.S.A. 79, 6038-6041 (Pubitemid 13249974)
21. Savage, B., Almus-Jacobs, F., and Ruggeri, Z. M. (1998) Specific synergy of multiple substrate-receptor interactions in platelet thrombus formation under flow. Cell 94, 657-666 (Pubitemid 28427584)
22. Shen, Y., Romo, G. M., Dong, J. F., Schade, A., McIntire, L. V., Kenny, D., Whisstock, J. C., Berndt, M. C., López, J. A., and Andrews, R. K. (2000) Requirement of leucine-rich repeats of glycoprotein (GP) Ibα for shear-dependent and static binding of von Willebrand factor to the platelet membrane GP Ib-IX-V complex. Blood 95, 903-910 (Pubitemid 30062712)
23. Haynes, L. M., Dubief, Y. C., Orfeo, T., and Mann, K. G. (2011) Dilutional control of prothrombin activation at physiologically relevant shear rates. Biophys. J. 100, 765-773
24. Billy, D., Briedé, J., Heemskerk, J. W., Hemker, H. C., and Lindhout, T. (1997) Prothrombin conversion under flow conditions by prothrombinase assembled on adherent platelets. Blood Coagul. Fibrinolysis 8, 168-174 (Pubitemid 27241509)
25. Higgins, D. L., and Mann, K. G. (1983) The interaction of bovine factor V and factor V-derived peptides with phospholipid vesicles. J. Biol. Chem. 258, 6503-6508 (Pubitemid 13106824)
26. Butenas, S., Orfeo, T., Lawson, J. H., and Mann, K. G. (1992) Aminonaphthalenesulfonamides, a new class of modifiable fluorescent detecting groups and their use in substrates for serine protease enzymes. Biochemistry 31, 5399-5411
27. Butenas, S., DiLorenzo, M. E., and Mann, K. G. (1997) Ultrasensitive fluorogenic substrates for serine proteases. Thromb. Haemost. 78, 1193-1201 (Pubitemid 27464585)
28. Katzmann, J. A., Nesheim, M. E., Hibbard, L. S., and Mann, K. G. (1981) Isolation of functional human coagulation factor V by using a hybridoma antibody. Proc. Natl. Acad. Sci. U.S.A. 78, 162-166 (Pubitemid 11131257)
29. Bajaj, S. P., and Mann, K. G. (1973) Simultaneous purification of bovine prothrombin and factor X. Activation of prothrombin by trypsin-activated factor X. J. Biol. Chem. 248, 7729-7741
30. Griffith, M. J., Noyes, C. M., and Church, F. C. (1985) Reactive site peptide structural similarity between heparin cofactor II and antithrombin III. J. Biol. Chem. 260, 2218-2225 (Pubitemid 15105719)
31. Lundblad, R. L., Kingdon, H. S., and Mann, K. G. (1976) Thrombin. Methods Enzymol. 45, 156-176
32. Heldebrant, C. M., Butkowski, R. J., Bajaj, S. P., and Mann, K. G. (1973) The activation of prothrombin. II. Partial reactions, physical and chemical characterization of the intermediates of activation. J. Biol. Chem. 248, 7149-7163
33. Monkovic, D. D., and Tracy, P. B. (1990) Activation of human factor V by factor Xa and thrombin. Biochemistry 29, 1118-1128 (Pubitemid 20053831)
34. Mustard, J. F., Perry, D. W., Ardlie, N. G., and Packham, M. A. (1972) Preparation of suspensions of washed platelets from humans. Br. J. Haematol. 22, 193-204
35. Camire, R. M., Kalafatis, M., Cushman, M., Tracy, R. P., Mann, K. G., and Tracy, P. B. (1995) The mechanism of inactivation of human platelet factor Va from normal and activated protein C-resistant individuals. J. Biol. Chem. 270, 20794-20800
36. Kalb, E., Frey, S., and Tamm, L. K. (1992) Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers. Biochim. Biophys. Acta 1103, 307-316
37. Tamm, L. K., and McConnell, H. M. (1985) Supported phospholipid bilayers. Biophys. J. 47, 105-113
38. Haynes, L. M., Dubief, Y. C., and Mann, K. G. (2012) Membrane binding events in the initiation and propagation phases of tissue factor-initiated zymogen activation under flow. J. Biol. Chem. 287, 5225-5234
39. Côté, H. C., Bajzar, L., Stevens, W. K., Samis, J. A., Morser, J., MacGillivray, R. T., and Nesheim, M. E. (1997) Functional characterization of recombinant human meizothrombin and Meizothrombin(desF1). Thrombomodulin-dependent activation of protein C and thrombin-activatable fibrinolysis inhibitor (TAFI), platelet aggregation, antithrombin-III inhibition. J. Biol. Chem. 272, 6194-6200 (Pubitemid 27118088)
40. Brooks, E. G., Trotman, W., Wadsworth, M. P., Taatjes, D. J., Evans, M. F., Ittleman, F. P., Callas, P. W., Esmon, C. T., and Bovill, E. G. (2009) Valves of the deep venous system: an overlooked risk factor. Blood 114, 1276-1279
41. Miletich, J. P., Jackson, C. M., and Majerus, P. W. (1977) Interaction of coagulation factor Xa with human platelets. Proc. Natl. Acad. Sci. U.S.A. 74, 4033-4036 (Pubitemid 8197769)
42. Tracy, P. B., Peterson, J. M., Nesheim, M. E., McDuffie, F. C., and Mann, K. G. (1979) Interaction of coagulation factor V and factor Va with platelets. J. Biol. Chem. 254, 10354-10361 (Pubitemid 10180977)
43. Fager, A. M., Wood, J. P., Bouchard, B. A., Feng, P., and Tracy, P. B. (2010) Properties of procoagulant platelets: defining and characterizing the subpopulation binding a functional prothrombinase. Arterioscler. Thromb. Vasc. Biol. 30, 2400-2407
44. Boskovic, D. S., Bajzar, L. S., and Nesheim, M. E. (2001) Channeling during prothrombin activation. J. Biol. Chem. 276, 28686-28693
45. Brufatto, N., and Nesheim, M. E. (2003) Analysis of the kinetics of prothrombin activation and evidence that two equilibrating forms of prothrombinase are involved in the process. J. Biol. Chem. 278, 6755-6764 (Pubitemid 36800663)
46. Kim, P. Y., and Nesheim, M. E. (2007) Further evidence for two functional forms of prothrombinase each specific for either of the two prothrombin activation cleavages. J. Biol. Chem. 282, 32568-32581 (Pubitemid 350159285)
47. Bianchini, E. P., Orcutt, S. J., Panizzi, P., Bock, P. E., and Krishnaswamy, S. (2005) Ratcheting of the substrate from the zymogen to proteinase conformations directs the sequential cleavage of prothrombin by prothrombinase. Proc. Natl. Acad. Sci. U.S.A. 102, 10099-10104 (Pubitemid 41023332)
48. Lee, C. J., Wu, S., and Pedersen, L. G. (2011) A proposed ternary complex model of prothrombinase with prothrombin: protein-protein docking and molecular dynamics simulations. J. Thromb. Haemost. 9, 2123-2126
49. Topalov, N. N., Kotova, Y. N., Vasil'ev, S. A., and Panteleev, M. A. (2012) Br. J. Haematol. 157, 105-115
50. Lee, C. J., Wu, S., Eun, C., and Pedersen, L. G. (2010) A revisit to the one form kinetic model of prothrombinase. Biophys. Chem. 149, 28-33
51. Kim, P. Y., and Nesheim, M. E. (2012) A revisit of the two-form kinetic model of prothrombinase: A rebuttal. Biophys. Chem. 160, 75-76; author reply 77-78
52. Schoen, P., Lindhout, T., Willems, G., and Hemker, H. C. (1990) Continuous flow and the prothrombinase-catalyzed activation of prothrombin. Thromb. Haemost. 64, 542-547
53. Fuster, V., Stein, B., Ambrose, J. A., Badimon, L., Badimon, J. J., and Chesebro, J. H. (1990) Atherosclerotic plaque rupture and thrombosis. Evolving concepts. Circulation 82, II47-59
54. Alberio, L., Safa, O., Clemetson, K. J., Esmon, C. T., and Dale, G. L. (2000) Surface expression and functional characterization of alpha-granule factorVin human platelets: effects of ionophore A23187, thrombin, collagen, and convulxin. Blood 95, 1694-1702 (Pubitemid 30120831)
55. Batar, P., and Dale, G. L. (2001) Simultaneous engagement of thrombin and Fc gamma RIIA receptors results in platelets expressing high levels of procoagulant proteins. J. Lab. Clin. Med. 138, 393-402 (Pubitemid 34010023)
56. Kempton, C. L., Hoffman, M., Roberts, H. R., and Monroe, D. M. (2005) Platelet heterogeneity: variation in coagulation complexes on platelet subpopulations. Arterioscler. Thromb. Vasc. Biol. 25, 861-866 (Pubitemid 40463882)
57. Panteleev, M. A., Ananyeva, N. M., Greco, N. J., Ataullakhanov, F. I., and Saenko, E. L. (2005) Two subpopulations of thrombin-activated platelets differ in their binding of the components of the intrinsic factor X-activating complex. J. Thromb. Haemost. 3, 2545-2553 (Pubitemid 41727172)