The factor IXa heparin-binding exosite is a cofactor interactive site: Mechanism for antithrombin-independent inhibition of intrinsic tenase by heparin

Biochemistry

Volumn 44, Issue 9, 2005, Pages 3615-3625

  Yuan, Qiu Ping ^a   Walke, Erik N ^a   Sheehan, John P ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAGULATION; ENZYMES; MUTAGENESIS; SOLVENTS;

COAGULANT ACTIVITY; COFACTOR AFFINITY; LOW MOLECULAR WEIGHT HEPARIN (LMWH); WILD TYPE (WT);

BIOCHEMISTRY;

ANTITHROMBIN; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 8A; BLOOD CLOTTING FACTOR 9A; HEPARIN; LOW MOLECULAR WEIGHT HEPARIN; RECOMBINANT BLOOD CLOTTING FACTOR 9A; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; CONTROLLED STUDY; ENZYME INHIBITION; HYDROLYSIS; KINETICS; MUTATION; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION;

ALANINE; ANTITHROMBINS; BINDING SITES; BLOOD COAGULATION TESTS; CELL LINE; CHROMOGENIC COMPOUNDS; COENZYMES; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; DALTEPARIN; FACTOR IXA; FACTOR VIIIA; FACTOR X; HALF-LIFE; HUMANS; HYDROLYSIS; KINETICS; MUTAGENESIS, SITE-DIRECTED; NEOPLASM PROTEINS; PROTEIN BINDING;

EID: 14644399195     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi047934a     Document Type: Article

References (60)

1. Lawson, J. H., Kalafatis, M., Stram, S., and Mann, K. G. (1994) A model for the tissue factor pathway to thrombin. I. An empirical study, J. Biol. Chem. 269, 23357-23366.
2. Rand, M. D., Lock, J. B., van't Veer, C., Gaffney, D. P., and Mann, K. G. (1996) Blood clotting in minimally altered whole blood, Blood 88, 3432-3445.
3. van't Veer, C., and Mann, K. G. (1997) 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, 4367-4377.
4. van't Veer, C., Golden, N. J., Kalafatis, M., and Mann, K. G. (1997) 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, 7983-7994.
5. Hockin, M. F., Jones, K. C., Everse, S. J., and Mann, K. G. (2002) A model for the stoichiometric regulation of blood coagulation, J. Biol. Chem. 277, 18322-18333.
6. Lane, D. A., Mannucci, P. M., Bauer, K. A., Bertina, R. M., Bochkov, N. P., Boulyjenkov, V., Chandy, M., Dahlback, B., Ginter, E. K., Miletich, J. P., Rosendaal, F. R., and Seligsohn, U. (1996) Inherited thrombophilia: Part 1, Thromb. Haemostasis 76, 651-662.
7. Lane, D. A., Mannucci, P. M., Bauer, K. A., Bertina, R. M., Bochkov, N. P., Boulyjenkov, V., Chandy, M., Dahlback, B., Ginter, E. K., Miletich, J. P., Rosendaal, F. R., and Seligsohn, U. (1996) Inherited thrombophilia: Part 2, Thromb. Haemostasis 76, 824-834.
8. Bertina, R. M., Koeleman, B. P., Koster, T., Rosendaal, F. R., Dirven, R. J., de Ronde, H., van der Velden, P. A., and Reitsma, P. H. (1994) Mutation in blood coagulation factor V associated with resistance to activated protein C, Nature 369, 64-67.
9. Poort, S. R., Rosendaal, F. R., Reitsma, P. H., and Bertina, R. M. (1996) 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 88, 3698-3703.
10. Koster, T., Blann, A. D., Briet, E., Vandenbroucke, J. P., and Rosendaal, F. R. (1995) Role of clotting factor VIII in effect of von Willebrand factor on occurrence of deep-vein thrombosis, Lancet 345, 152-155.
11. van Hylckama Vlieg, A., van der Linden, I. K., Bertina, R. M., and Rosendaal, F. R. (2000) High levels of factor IX increase the risk of venous thrombosis, Blood 95, 3678-3682.
12. Meijers, J. C., Tekelenburg, W. L., Bouma, B. N., Bertina, R. M., and Rosendaal, F. R. (2000) High levels of coagulation factor XI as a risk factor for venous thrombosis, N. Engl. J. Med. 342, 696-701.
13. Benedict, C. R., Ryan, J., Wolitzky, B., Ramos, R., Gerlach, M., Tijburg, P., and Stern, D. (1991) Active site-blocked factor IXa prevents intravascular thrombus formation in the coronary vasculature without inhibiting extravascular coagulation in a canine thrombosis model, J. Clin. Invest. 88, 1760-1765.
14. Choudhri, T. F., Hoh, B. L., Prestigiacomo, C. J., Huang, J., Kim, L. J., Schmidt, A. M., Kisiel, W., Connolly, E. S., Jr., and Pinsky, D. J. (1999) Targeted inhibition of intrinsic coagulation limits cerebral injury in stroke without increasing intracerebral hemorrhage, J. Exp. Med. 190, 91-99.
15. Spanier, T. B., Chen, J. M., Oz, M. C., Edwards, N. M., Kisiel, W., Stern, D. M., Rose, E. A., and Schmidt, A. M. (1998) Selective anticoagulation with active site-blocked factor IXA suggests separate roles for intrinsic and extrinsic coagulation pathways in cardiopulmonary bypass, J. Thorac. Cardiovasc. Surg. 116, 860-869.
16. Feuerstein, G. Z., Patel, A., Toomey, J. R., Bugelski, P., Nichols, A. J., Church, W. R., Valocik, R., Koster, P., Baker, A., and Blackburn, M. N. (1999) Antithrombotic efficacy of a novel murine antihuman factor IX antibody in rats, Arteriosder. Thromb. Vasc. Biol. 19, 2554-2562.
17. Refino, C. J., Jeet, S., DeGuzman, L., Bunting, S., and Kirchhofer, D. (2002) A human antibody that inhibits factor IX/IXa function potently inhibits arterial thrombosis without increasing bleeding, Arterioscler. Thromb. Vasc. Biol. 22, 517-522.
18. Hopfner, K. P., Lang, A., Karcher, A., Sichler, K., Kopetzki, E., Brandstetter, H., Huber, R., Bode, W., and Engh, R. A. (1999) Coagulation factor IXa: the relaxed conformation of Tyr99 blocks substrate binding, Struct. Folding Des. 7, 989-996.
19. Brandstetter, H., Bauer, M., Huber, R., Lollar, P., and Bode, W. (1995) X-ray structure of clotting factor IXa: active site and module structure related to Xase activity and hemophilia B, Proc. Natl. Acad. Sci. U.S.A. 92, 9796-9800.
20. The Columbus Investigators (1997) Low-molecular-weight heparin in the treatment of patients with venous thromboembolism, N. Engl. J. Med. 337, 657-662.
21. Koopman, M. M., Prandoni, P., Piovella, F., Ockelford, P. A., Brandjes, D. P., van der Meer, J., Gallus, A. S., Simonneau, G., Chesterman, C. H., and Prins, M. H. (1996) Treatment of venous thrombosis with intravenous unfractionated heparin administered in the hospital as compared with subcutaneous low-molecular-weight heparin administered at home, N. Engl. J. Med. 334, 682-687.
22. Levine, M., Gent, M., Hirsh, J., Leclerc, J., Anderson, D., Weitz, J., Ginsberg, J., Turpie, A. G., Demers, C., and Kovacs, M. (1996) A comparison of low-molecular-weight heparin administered primarily at home with unfractionated heparin administered in the hospital for proximal deep-vein thrombosis, N. Engl. J. Med. 334, 677-681.
23. Bedsted, T., Swanson, R., Chuang, Y. J., Bock, P. E., Bjork, I., and Olson, S. T. (2003) Heparin and calcium ions dramatically enhance antithrombin reactivity with factor IXa by generating new interaction exosites, Biochemistry 42, 8143-8152.
24. Izaguirre, G., Zhang, W., Swanson, R., Bedsted, T., and Olson, S. T. (2003) Localization of an antithrombin exosite that promotes rapid inhibition of factors Xa and IXa dependent on heparin activation of the serpin, J. Biol. Chem. 278, 51433-51440.
25. Miletich, J. P., Jackson, C. M., and Majerus, P. W. (1978) Properties of the factor Xa binding site on human platelets, J. Biol. Chem. 253, 6908-6916.
26. Rezaie, A. R. (2001) Prothrombin protects factor Xa in the prothrombinase complex from inhibition by the heparin-antithrombin complex, Blood 97, 2308-2313.
27. Barrow, R. T., Parker, E. T., Krishnaswamy, S., and Lollar, P. (1994) Inhibition by heparin of the human blood coagulation intrinsic pathway factor X activator, J. Biol. Chem. 269, 26796-26800.
28. Gray, E., Cesmeli, S., Lormeau, J. C., Davies, A. B., and Lane, D. A. (1994) Low affinity heparin is an antithrombotic agent, Thromb. Haemostasis 71, 203-207.
29. Sheehan, J., and Lan, H. (1998) Phosphorothioate oligonucleotides inhibit the intrinsic tenase complex, Blood 92, 1617-1625.
30. Sheehan, J. P., and Phan, T. M. (2001) Phosphorothioate oligonucleotides inhibit the intrinsic tenase complex by an allosteric mechanism, Biochemistry 40, 4980-4989.
31. Sheehan, J. P., Kobbervig, C. E., and Kirkpatrick, H. M. (2003) Heparin inhibits the intrinsic tenase complex by interacting with an exosite on factor IXa, Biochemistry 42, 11316-11325.
32. MacDonald, R. C., MacDonald, R. I., Menco, B. P., Takeshita, K., Subbarao, N. K., and Hu, L. R. (1991) Small-volume extrusion apparatus for preparation of large, unilamellar vesicles, Biochim. Biophys. Acta 1061, 297-303.
33. Chen, P., Toribara, T., and Warner, H. (1956) Anal. Chem. 28, 1756-1758.
34. Chang, J., Jin, J., Lollar, P., Bode, W., Brandstetter, H., Hamaguchi, N., Straight, D. L., and Stafford, D. W. (1998) Changing residue 338 in human factor IX from arginine to alanine causes an increase in catalytic activity, J. Biol. Chem. 273, 12089-12094.
35. Southern, P. J., and Berg, P. (1982) Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter, J. Mol. Appl. Genet. 1, 327-341.
36. Yan, S. C., Razzano, P., Chao, Y. B., Walls, J. D., Berg, D. T., McClure, D. B., and Grinnell, B. W. (1990) Characterization and novel purification of recombinant human protein C from three mammalian cell lines, Biotechnology (New York) 8, 655-661.
37. Cote, H. C., Stevens, W. K., Bajzar, L., Banfield, D. K., Nesheim, M. E., and MacGillivray, R. T. (1994) Characterization of a stable form of human meizotnrombin derived from recombinant prothrombin (R155A, R271A, and R284A), J. Biol. Chem. 269, 11374-11380.
38. Lozier, J. N., Monroe, D. M., Stanfield-Oakley, S., Lin, S. W., Smith, K. J., Roberts, H. R., and High, K. A. (1990) Factor IX New London: substitution of proline for glutamine at position 50 causes severe hemophilia B, Blood 75, 1097-1104.
39. Myszka, D. G. (2000) Kinetic, equilibrium, and thermodynamic analysis of macromolecular interactions with BIACORE, Methods Enzymol. 323, 325-340.
40. Limbird, L. (1995) Cell Surface Receptors: A Short Course on Theory and Methods, Kluwer Academic Publishers, Boston, MA.
41. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, John Wiley and Sons, New York.
42. Dixon, M., and Webb, E. (1979) Enzymes, Academic Press, New York.
43. Rezaie, A. R. (2000) Identification of basic residues in the heparin-binding exosite of factor Xa critical for heparin and factor Va binding, J. Biol. Chem. 275, 3320-3327.
44. Sheehan, J. P., and Sadler, J. E. (1994) Molecular mapping of the heparin-binding exosite of thrombin, Proc. Natl. Acad. Sci. U.S.A. 91, 5518-5522.
45. Sturzebecher, J., Kopetzki, E., Bode, W., and Hopfner, K. P. (1997) Dramatic enhancement of the catalytic activity of coagulation factor IXa by alcohols, FEBS Lett. 412, 295-300.
46. Mathur, A., and Bajaj, S. P. (1999) Protease and EGF1 domains of factor IXa play distinct roles in binding to factor VIIIa. Importance of helix 330 (helix 162 in chymotrypsin) of protease domain of factor IXa in its interaction with factor VIIIa, J. Biol. Chem. 274, 18477-18486.
47. Kolkman, J. A., Lenting, P. J., and Mertens, K. (1999) Regions 301-303 and 333-339 in the catalytic domain of blood coagulation factor IX are factor VIII-interactive sites involved in stimulation of enzyme activity, Biochem. J. 339, 217-221.
48. Bajaj, S. P., Schmidt, A. E., Mathur, A., Padmanabhan, K., Zhong, D., Mastri, M., and Fay, P. I. (2001) Factor IXa:factor VIIIa interaction, helix 330-338 of factor ixa interacts with residues 558-565 and spatially adjacent regions of the a2 subunit of factor VIIIa, J. Biol. Chem. 276, 16302-16309.
49. Lollar, P., and Parker, C. G. (1990) pH-dependent denaturation of thrombin-activated porcine factor VIII, J. Biol. Chem. 265, 1688-1692.
50. Lollar, P., Knutson, G. J., and Fass, D. N. (1984) Stabilization of thrombin-activated porcine factor VIII:C by factor IXa phospholipid, Blood 63, 1303-1308.
51. Fay, P. J., Beattie, T. L., Regans, L. M. O., Brien, L. M., and Kaufman, R. J. (1996) Model for the factor VIIIa-dependent decay of the intrinsic factor Xase. Role of subunit dissociation and factor IXa-catalyzed proteolysis, J. Biol. Chem. 271, 6027-6032.
52. Green, P. M., Giannelli, F., Sommer, S. S., Poon, M.-C., Ludwig, M., Schwaab, R., Rietsma, P. H., Goossens, M., Yoshioka, A., Figueriredo, M. S., Tagariello, G., and Brownlee, G. G. (2003) Haemophilia B Mutation Database (www.kcl.ac.uk/ip/petergreen/ haemBdatabase.html).
53. Jenkins, P. V., Dill, J. L., Zhou, Q., and Fay, P. J. (2004) Clustered basic residues within segment 484-510 of the factor VIIIa A2 subunit contribute to the catalytic efficiency for factor Xa generation, J. Thromb. Haemostasis 2, 452-458.
54. Walker, R. K., and Krishnaswamy, S. (1994) The activation of prothrombin by the prothrombinase complex. The contribution of the substrate-membrane interaction to catalysis, J. Biol. Chem. 269, 27441-27450.
55. Krishnaswamy, S., Field, K. A., Edgington, T. S., Morrissey, J. H., and Mann, K. G. (1992) Role of the membrane surface in the activation of human coagulation factor X, J. Biol. Chem. 267, 26110-26120.
56. Yang, L., Manithody, C., and Rezaie, A. R. (2002) Localization of the heparin binding exosite of factor IXa, J. Biol. Chem. 277, 50756-50760.
57. Rudolph, A. E., Porche-Sorbet, R., and Miletich, J. P. (2001) Definition of a factor Va binding site in factor Xa, J. Biol. Chem. 276, 5123-5128.
58. Fay, P. J., Koshibu, K., and Mastri, M. (1999) The A1 and A2 subunits of factor VIIIa synergistically stimulate factor IXa catalytic activity, J. Biol. Chem. 274, 15401-15406.
59. Lenting, P. J., Donath, M. J., van Mourik, J. A., and Mertens, K. (1994) Identification of a binding site for blood coagulation factor IXa on the light chain of human factor VIII, J. Biol. Chem. 269, 7150-7155.
60. Fay, P. J., and Koshibu, K. (1998) The A2 subunit of factor VIIIa modulates the active site of factor IXa, J. Biol. Chem. 273, 19049-19054.