The regulation of factor IXa by supersulfated low molecular weight heparin

Biochemistry

Volumn 49, Issue 46, 2010, Pages 9997-10005

  Misenheimer, Tina M ^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

ALANINE SUBSTITUTION; ANTITHROMBIN; BINDING AFFINITIES; BINDING ASSAYS; COFACTOR AFFINITY; COFACTORS; ENZYME COMPLEXES; FACTOR IXA; FACTOR VIIIA; FACTOR X; HEPARIN AFFINITY; HEPARIN BINDING; LOW-MOLECULAR WEIGHT HEPARINS; PROTEASE ACTIVITIES; WILD TYPES;

AMINO ACIDS; BINDING ENERGY; BIOCHEMISTRY; COMPLEXATION; ENZYME INHIBITION; MOLECULAR WEIGHT; PHOSPHOLIPIDS; POLYSACCHARIDES;

BINDING SITES;

ALANINE; BLOOD CLOTTING FACTOR 10; BLOOD CLOTTING FACTOR 9A; LOW MOLECULAR WEIGHT HEPARIN; PHOSPHOLIPID; PROTEINASE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CATALYSIS; COMPLEX FORMATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DOMAIN; SULFATION;

ALLOSTERIC REGULATION; ANTITHROMBINS; BINDING SITES; FACTOR IXA; HEPARIN, LOW-MOLECULAR-WEIGHT; HYDROLYSIS; KINETICS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 78649305395     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi100906q     Document Type: Article

References (40)

1. 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
2. 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
3. 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
4. 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
5. Anderson, J. A., Fredenburgh, J. C., Stafford, A. R., Guo, Y. S., Hirsh, J., Ghazarossian, V., and Weitz, J. I. (2001) Hypersulfated low molecular weight heparin with reduced affinity for antithrombin acts as an anticoagulant by inhibiting intrinsic tenase and prothrombinase J. Biol. Chem. 9755-9761
6. 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
7. 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
8. 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
9. 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
10. Ngo, J. C., Huang, M., Roth, D. A., Furie, B. C., and Furie, B. (2008) Crystal structure of human factor VIII: implications for the formation of the factor IXa-factor VIIIa complex Structure 16, 597-606
11. 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, King's College, London.
12. Misenheimer, T. M., Buyue, Y., and Sheehan, J. P. (2007) 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 46, 7886-7895
13. Blostein, M. D., Furie, B. C., Rajotte, I., and Furie, B. (2003) The Gla domain of factor IXa binds to factor VIIIa in the tenase complex J. Biol. Chem. 278, 31297-31302
14. Nishimura, H., Takeya, H., Miyata, T., Suehiro, K., Okamura, T., Niho, Y., and Iwanaga, S. (1993) Factor IX Fukuoka. Substitution of ASN92 by His in the second epidermal growth factor-like domain results in defective interaction with factors VIIa/X J. Biol. Chem. 268, 24041-24046
15. Hughes, P. E., Morgan, G., Rooney, E. K., Brownlee, G. G., and Handford, P. (1993) Tyrosine 69 of the first epidermal growth factor-like domain of human factor IX is essential for clotting activity J. Biol. Chem. 268, 17727-17733
16. 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
17. 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
18. Buyue, Y., Whinna, H. C., and Sheehan, J. P. (2008) The heparin-binding exosite of factor IXa is a critical regulator of plasma thrombin generation and venous thrombosis Blood 112, 3234-3241
19. Buyue, Y. and Sheehan, J. P. (2009) Fucosylated chondroitin sulfate inhibits plasma thrombin generation via targeting of the factor IXa heparin-binding exosite Blood 114, 3092-3100
20. Wakabayashi, H., Griffiths, A. E., and Fay, P. J. (2009) Combining mutations of charged residues at the A2 domain interface enhances factor VIII stability over single point mutations J. Thromb. Haemostasis 7, 438-444
21. 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
22. Gilbert, G. E. and Arena, A. A. (1998) Unsaturated phospholipid acyl chains are required to constitute membrane binding sites for factor VIII Biochemistry 37, 13526-13535
23. Needham, D., McIntosh, T. J., and Evans, E. (1988) Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers Biochemistry 27, 4668-4673
24. Blume, A. (1980) Thermotropic behavior of phosphatidylethanolamine- cholesterol and phosphatidylethanolamine-phosphatidylcholine-cholesterol mixtures Biochemistry 19, 4908-4913
25. Chen, P., Toribara, T., and Warner, H. (1956) Anal. Chem. 28, 1756-1758
26. 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
27. Limbird, L. (1996) Complex binding phenomena, in Cell Surface Receptors: A Short Course on Theory and Methods, 2 nd ed., pp 123 - 167, Kluwer Academic Publishers, Boston.
28. DeLean, A., Munson, P. J., and Rodbard, D. (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves Am. J. Physiol. 235, E97-102
29. 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
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. Segel, I. H. (1975) Rapid equilibrium partial and mixed-type inhibition, in Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, pp 160 - 226, John Wiley and Sons, New York.
32. Gandhi, N. S., Coombe, D. R., and Mancera, R. L. (2008) Platelet endothelial cell adhesion molecule 1 (PECAM-1) and its interactions with glycosaminoglycans: 1. Molecular modeling studies Biochemistry 47, 4851-4862
33. van Dieijen, G., Tans, G., Rosing, J., and Hemker, H. C. (1981) The role of phospholipid and factor VIIIa in the activation of bovine factor X J. Biol. Chem. 256, 3433-3442
34. 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
35. 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
36. Yang, L., Manithody, C., and Rezaie, A. R. (2002) Localization of the heparin binding exosite of factor IXa J. Biol. Chem. 277, 50756-50760
37. Wakabayashi, H. and Fay, P. J. (2008) Identification of residues contributing to A2 domain-dependent structural stability in factor VIII and factor VIIIa J. Biol. Chem. 283, 11645-11651
38. Wakabayashi, H., Varfaj, F., Deangelis, J., and Fay, P. J. (2008) Generation of enhanced stability factor VIII variants by replacement of charged residues at the A2 domain interface Blood 112, 2761-2769
39. Johnson, D. J., Langdown, J., and Huntington, J. A. (2010) Molecular basis of factor IXa recognition by heparin-activated antithrombin revealed by a 1.7-Å structure of the ternary complex Proc. Natl. Acad. Sci. U.S.A. 107, 645-650
40. Neuenschwander, P. F. (2004) Exosite occupation by heparin enhances the reactivity of blood coagulation factor IXa Biochemistry 43, 2978-2986