The heparin-binding exosite is critical to allosteric activation of factor IXa in the intrinsic tenase complex: The role of arginine 165 and factor X

Biochemistry

Volumn 46, Issue 26, 2007, Pages 7886-7895

  Misenheimer, Tina M ^a   Buyue, Yang ^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

AMINO ACIDS; CATALYSIS; COAGULATION; CONFORMATIONS; HYDROLYSIS;

ALLOSTERIC ACTIVATION; COFACTOR AFFINITY; HEPARIN; HUMAN FACTOR IXA;

ENZYMES;

BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 8A; BLOOD CLOTTING FACTOR 9A; HEPARIN; MUTANT PROTEIN; PHOSPHOLIPID; PROTEINASE; RECOMBINANT BLOOD CLOTTING FACTOR 8; RECOMBINANT BLOOD CLOTTING FACTOR 9; RECOMBINANT HIRUDIN; THROMBIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; BLOOD CLOTTING; COMPLEX FORMATION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; HUMAN; HYDROLYSIS; PRIORITY JOURNAL;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARGININE; BINDING SITES; CYSTEINE ENDOPEPTIDASES; FACTOR IXA; FACTOR VIIIA; FACTOR X; HEPARIN; HUMANS; KINETICS; NEOPLASM PROTEINS; PROTEIN CONFORMATION; RECOMBINANT PROTEINS;

EID: 34347358644     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7004703     Document Type: Article

References (47)

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. Duffy, E. J., and Lollar, P. (1992) Intrinsic pathway activation of factor X and its activation peptide-deficient derivative, factor Xdes-143-191, J. Biol. Chem. 267, 7821-7827.
4. McRae, B. J., Kurachi, K., Heimark, R. L., Fujikawa, K., Davie, E. W., and Powers, J. C. (1981) Mapping the active sites of bovine thrombin, factor IXa, factor Xa, factor XIa, factor XIIa, plasma kallikrein, and trypsin with amino acid and peptide thioesters: development of new sensitive substrates, Biochemistry 20, 7196-7206.
5. Fay, P. J., Beattie, T. L., Regan, 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. Jenkins, P. V., Dill, J. L., Zhou, Q., and Fay, P. J. (2004) Contribution of factor VIIIa A2 and A3-C1-C2. subunits to the affinity for factor IXa in factor Xase, Biochemistry 43, 5094-5101.
11. 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 (Part 2), 217-221.
12. 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 Villa, J. Biol. Chem. 274, 18477-18486.
13. Bajaj, S. P., Schmidt, A. E., Mathur, A., Padmanabhan, K., Zhong, D., Mastri, M., and Fay, P. J. (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.
14. 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.
15. 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.
16. 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.
17. Yang, L., Manithody, C., and Rezaie, A. R. (2002) Localization of the heparin binding exosite of factor IXa, J. Biol. Chem. 277, 50756-50760.
18. Yuan, Q. P., Walke, E. N., and Sheehan, J. P. (2005) The factor IXa heparin-binding exosite is a cofactor interactive site: mechanism for antithrombin-independent inhibition of intrinsic tenase by heparin, Biochemistry 44, 3615-3625.
19. Sheehan, J. P., and Walke, E. N. (2006) Depolymerized holothurian glycosaminoglycan and heparin inhibit the intrinsic tenase complex by a common antithrombin-independent mechanism, Blood 107, 3876-3882.
20. 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.
21. Chen, P., Toribara, T., and Warner, H. (1956) Anal. Chem. 28, 1756-1758.
22. 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.
23. 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.
24. Duffy, E. J., Parker, E. T., Mutucumarana, V. P., Johnson, A. E., and Lollar, P. (1992) Binding of factor VIIIa and factor VIII to factor IXa on phospholipid vesicles, J. Biol. Chem. 267, 17006-17011.
25. Limbird, L. (1995) Cell Surface Receptors: A Short Course on Theory and Methods, 2nd ed., Kluwer Academic Publishers, Boston.
26. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (150) of an enzymatic reaction, Biochem. Pharmacol. 22, 3099-3108.
27. Chou, T. (1974) Relationships between inhibition constants and fractional inhibition in enzyme-catalyzed reactions with different numbers of reactants, different reaction mechanisms, and different types and mechanisms of inhibition, Mol. Pharmacol. 10, 235-247.
28. 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 meizothrombin derived from recombinant prothrombin (R155A, R271A, and R284A), J. Biol. Chem. 269, 11374-11380.
29. 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 (NY) 8, 655-661.
30. 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.
31. Lollar, P., and Parker, C. G. (1990) pH-dependent denaturation of thrombin-activated porcine factor VIII, J. Biol. Chem. 265, 1688-1692.
32. Sichler, K., Banner, D. W., D'Arcy, A., Hopfner, K. P., Huber, R., Bode, W., Kresse, G. B., Kopetzki, E., and Brandstetter, H. (2002) Crystal structures of uninhibited factor VIIa link its cofactor and substrate-assisted activation to specific interactions, J. Mol. Biol. 322, 591-603.
33. Sichler, K., Kopetzki, E., Huber, R., Bode, W., Hopfner, K. P., and Brandstetter, H. (2003) Physiological fIXa activation involves a cooperative conformational rearrangement of the 99-loop, J. Biol. Chem. 278, 4121-4126.
34. Sheehan, J. P., and Phan, T. M. (2001) Phosphorothioate oligonucleotides inhibit the intrinsic tenase complex by an allosteric mechanism, Biochemistry 40, 4980-4989.
35. Panteleev, M. A., Ananyeva, N. M., Greco, N. J., Ataullakhanov, F. I., and Saenko, E. L. (2006) Factor VIIIa regulates substrate delivery to the intrinsic factor X-activating complex, FEBS J. 273, 374-387.
36. Lollar, P., Parker, E. T., Curtis, J. E., Helgerson, S. L., Hoyer, L. W., Scott, M. E., and Scandella, D. (1994) Inhibition of human factor VIIIa by anti-A2 subunit antibodies, J. Clin. Invest. 93, 2497-2504.
37. Mathur, A., Zhong, D., Sabharwal, A. K., Smith, K. J., and Bajaj, S. P. (1997) Interaction of factor IXa with factor VIIIa. Effects of protease domain Ca2+ binding site, proteolysis in the autolysis loop, phospholipid, and factor X, J. Biol. Chem. 272, 23418-23426.
38. Green, P. M., Giannelli, F., Sommer, S. S., Poon, M.-C., Ludwig, M., Schwaab, R., Rietsma, P. H., Goossens, M., Yoshioka, A., Figueiredo, M. S., Tagariello, G., and Brownlee, G. G. (2004) Haemophilia B mutation database, version 13 ed., www.kcl.ac.uk/ip/petergreen/haemBdatabase.html.
39. 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.
40. Neuenschwander, P. F. (2004) Exosite occupation by heparin enhances the reactivity of blood coagulation factor IXa, Biochemistry 43, 2978-2986.
41. Neuenschwander, P. F., Williamson, S. R., Nalian, A., and Baker-Deadmond, K. J. (2006) Heparin modulates the 99-loop of factor IXa: effects on reactivity with isolated Kunitz-type inhibitor domains, J. Biol. Chem. 281, 23066-23074.
42. Rohlena, J. (2004) in Department of Plasma Proteins of Sanquin Research, pp 1-111, University of Utrecht and Sanquin Research at CLB, Amsterdam.
43. 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.
44. 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.
45. Hopfner, K. P., Brandstetter, H., Karcher, A., Kopetzki, E., Huber, R., Engh, R. A., and Bode, W. (1997) Converting blood coagulation factor IXa into factor Xa: dramatic increase in amidolytic activity identifies important active site determinants, EMBO J. 16, 6626-6635.
46. 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, Structure 7, 989-996.
47. DeLano, W. L. (2006), DeLano Scientific, San Carlos, CA.