Contributions of basic amino acids in the autolysis loop of factor XIa to serpin specificity

Biochemistry

Volumn 45, Issue 31, 2006, Pages 9427-9433

  Rezaie, Alireza R ^a   Sun, Mao Fu ^b   Gailani, David ^b  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASSAYS; CATALYSIS; COAGULATION; ENZYME INHIBITION; HYDROLYSIS; PLASMAS; PROTEINS;

AUTOLYSIS; FACTOR XIA; PLASMA CLOTTING ASSAY; SERPIN SPECIFICITY;

AMINO ACIDS;

ALANINE; ALPHA 1 ANTITRYPSIN; AMINO ACID; ANTITHROMBIN; ARGININE; BLOOD CLOTTING FACTOR 11A; CHROMOGENIC SUBSTRATE; CHYMOTRYPSINOGEN; COMPLEMENT COMPONENT C1S INHIBITOR; LYSINE; PROTEIN Z DEPENDENT PROTEASE INHIBITOR; PROTEINASE INHIBITOR; PYROGLUTAMYLPROLYLARGININE 4 NITROANILIDE; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BLOOD CLOTTING TEST; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN FUNCTION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACIDS, BASIC; ANTITHROMBINS; AUTOLYSIS; COMPLEMENT C1 INHIBITOR PROTEIN; FACTOR XIA; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINANT PROTEINS; SERPINS;

EID: 33747139360     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060820+     Document Type: Article

References (45)

1. Wiggins, R. C., Bouma, B. N., Cochrane, C. G., and Griffin, J. H. (1977) Role of high molecular-weight kininogen in surface-binding and activation of coagulation factor XI and prekallikrein, Proc. Natl. Acad. Sci. (U.S.A.) 74, 4636-4640.
2. Walsh, P. N., and Griffin, J. H. (1981) Contributions of human platelets to the proteolytic activation of blood coagulation factors XII and XI, Blood 57, 106-118.
3. Kurachi, K., and Davie, E. W. (1977) Activation of human factor XI (plasma thromboplastin antecedent) by factor XIIa (activated Hageman factor), Biochemistry 16, 5831-5839.
4. Gailani, D., and Broze, G. J., Jr. (1991) Factor XI activation in a revised model of blood coagulation, Science 253, 909-912.
5. Ragni, M. V., Sinha, D., Seaman, F., Lewis, J. H., Spero, J. A., and Walsh, P. N. (1985) Comparison of bleeding tendency, factor XI coagulant activity, and factor XI antigen in 25 factor XI-deficient kindreds, Blood 65, 719-724.
6. Asakai, R., Chung, D. W., Davie, E. W., and Seligsohn, U. (1991) Factor XI deficiency in Ashkenazi Jews in Israel, N. Engl. J. Med. 325, 153-158.
7. Walsh, P. N. (1999) Platelets and factor XI bypass the contact system of blood coagulation, Thromb. Haemostasis 8, 234-242.
8. Bouma, B. N., and Griffin, J. H. (1977) Human blood coagulation factor XI. Purification, properties, and mechanism of activation by activated factor XII, J. Biol. Chem. 252, 6432-6437.
9. Fujikawa, K., Chung, D., Hendrickson, L., and Davie, E. (1986) Amino acid sequence of human factor XI, a blood coagulation factor with four tandem repeats that are highly homologous with plasma prekallikrein, Biochemistry 25, 2417-2424.
10. Naito, K., and Fujikawa, K. (1991) Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces, J. Biol. Chem. 266, 7353-7358.
11. Walsh, P. N., Baglia, F. A., and Jameson, B. A. (1993) Factor XI and platelets: Activation and regulation, Thromb. Haemostasis 70, 75-79.
12. Sun, M. F., Zhao, M., and Gailani, D. (1999) Identification of amino acids in the factor XI apple 3 domain required for activation of factor IX, J. Biol. Chem. 274, 36373-36378.
13. Sun, M. F., and Gailani, D. (1996) Identification of a factor IX binding site on the third apple domain of activated factor XI, J. Biol. Chem. 271, 29023-29028.
14. Meijers, J. C. M., Vlooswikj, R. A. A., and Bouma, B. N. (1988) Inhibition of human blood coagulation factor XIa by C1 inhibitor, Biochemistry 27, 959-963.
15. Patston, P. A., Gettins, P., Beechem, J., and Schapira, M. (1991) Mechanism of serpin action: Evidence that C1 inhibitor functions as a suicide substrate, Biochemistry 30, 8876-8882.
16. Zhao, M., Abdel-Razek, T., Sun, M., Gailani, D. (1998) J. Biol. Chem. 273, 31153-31159.
17. Wuillemin, W. A., Eldering, E., Citarella, F., de Ruig, C. P., ten Cate, H., and Hack, C. E. (1996) Modulation of cotact system proteases by glycosaminoglycans, J. Biol. Chem. 271, 12913-12918.
18. Olson, S. T., Swanson, R., Raub-Segall, E., Bedsted, T., Sadri, M., Petitou, M., Herault, J. P., Herbert, J. M., and Björk, I. (2004) Accelerating ability of synthetic oligosaccharides on antithrombin inhibition of proteinases of the clotting and fibrinolytic systems. Comparison with heparin and low-molecular-weight heparin, Thromb. Haemostasis 92, 929-939.
19. Scott, C. F., Schapira, M., James, H. L., Cohen, A. B., and Colman, R. W. (1982) Inactivation of factor XIa by plasma protease inhibitors: predominant role of alpha 1-protease inhibitor and protective effect of high molecular weight kininogen, J. Clin. Invest. 69, 844-852.
20. Berrettini, M., Schleef, R. R., Espana, F., Loskutoff, D. J., and Griffin, J. H. (1989) Interaction of type 1 plasminogen activator inhibitor with the enzymes of the contact activation system, J. Biol. Chem. 264, 11738-11743.
21. Meijers, J. C., Kanters, D. H., Vlooswijk, R. A., van Erp, H. E., Hessing, M., and Bouma, B. N. (1988) Inactivation of human plasma kallikrein and factor XIa by protein C inhibitor, Biochemistry 27, 4231-4237.
22. Knauer, D. J., Majumdar, D., Fong, P.-C., and Knauer, M. F. (2000) Serpin regulation of factor XIa, J. Biol. Chem. 275, 37340-37346.
23. Gettins, P. G. W., Patston, P. A., and Olson, S. T. (1996) Mechanism of action of serpins as suicide substrate inhibitors, in Serpins: Structure, Function and Biology, pp 33-63, R. G. Lands Company, Austin, TX.
24. Tabatabai, A., Fiehler, R., and Broze, G. J., Jr. (2001) Protein Z circulates in plasma in a complex with protein Z-dependent protease inhibitor, Thromb. Haemostasis 85, 655-660.
25. Jin, L., Pandey, P., Babine, R. E., Weaver, D. T., Abdel-Meguid, S. S., and Strickler, J. E. (2005) Mutations of surface residues to promote crystallization of active factor XI as a complex with benzamidine an essential step for the iterative structure-based design factor XI inhibitors, Acta Crystallogr., Sect. D 61, 1418-1425.
26. Jin, J., Pandey, P., Babine, R. E., Gorga, J. C., Seidl, K. J., Gelfand, E., Weaver, D. T., Abdel-Meguid, S. S., and Strickler, J. E. (2005) Crystal structures of the factor XIa catalytic domain in complex with ecotin mutants reveal substrate-like interactions, J. Biol. Chem. 280, 4704-4712.
27. Navaneetham, D., Jin, L., Pandey, P., Strickler, J. E., Babine, R. E., Abdel-Meguid, S. S., and Walsh, P. N. (2005) Structural and mutational analyses of the molecular interactions between the catalytic domain of factor XIa and the Kunitz protease inhibitor domain of protease nexin 2, J. Biol. Chem. 280, 36165-36175.
28. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S. R., and Hofsteenge, J. (1989) The refined 1.9 Å crystal structure of human α-thrombin: interaction with D-Phe-Pro-Arg chlorometheylketone and significance of the Tyr-Pro-Pro-Trp insertion segment, EMBO J. 8, 3467-3475.
29. Manithody, C., Yang, L., and Rezaie, A. R. (2002) Role of basic residues of the autolysis loop in the catalytic function of factor Xa, Biochemistry 41, 6780-6788.
30. Yang, L., Manithody, C., Olson, S. T., and Rezaie, A. R. (2003) Contribution of basic residues of the autolysis loop to the substrate and inhibitor specificity of factor IXa, J. Biol. Chem. 278, 25032-25038.
31. Rezaie, A. R., Manithody, C., and Yang, L. (2005) Identification of factor Xa residues critical for interaction with protein Z-dependent protease inhibitor, J. Biol. Chem. 280, 32722-32728.
32. Smirnov, M. D., and Esmon, C. T. (1994) Phosphatidylethanolamine incorporation into vesicles selectively enhances factor Va inactivation by activated protein C, J. Biol. Chem. 269, 816-819.
33. Ogawa, T., Verhamme, I. M., Sun, M. F., Bock, P. E., and Gailani, D. Exosite-mediated substrate recognition of factor IX by factor XIa: The factor XIa heavy chain is required for initial recognition of factor IX, J. Biol. Chem. 280, 23523-23530.
34. Lottenberg, R., Hall, J. A., Blinder, M., Binder, E. P., and Jackson, C. M. (1983) The action of thrombin on peptide p-nitroanilide substrates. Substrate selectivity and examination of hydrolysis under different reaction conditions, Biochim. Biophys. Acta. 742, 539-557.
35. Han, X., Fiehler, R., and Broze, G. J., Jr. (1998) Isolation a protein Z-dependent plasma protease inhibitor, Proc. Natl. Acad. Sci. (U.S.A.) 95, 9250-9255.
36. Han, X., Fiehler, R., and Broze, G. J., Jr. (2000) Characterization of the protein Z-dependent protease inhibitor, Blood 96, 3049-3055.
37. Yang, L., Manithody, C., and Rezaie, A. R. (2002) Localization of the heparin binding exosite of factor IXa, J. Biol. Chem. 277, 50756-50760.
38. Wiebe, E. M., Stafford, A. R., Fredenburgh, J. C., and Weitz, J. I. Mechanism of catalysis of inhibition of factor IXa by antithrombin in the presence of heparin or pentasaccharide, J. Biol. Chem. 278, 35767-35774.
39. Olson, S. T., Björk, I., Sheffer, R., Craig, P. A., Shore, J. D., and Choay, J. Role of the antithrombin-binding pentasaccharide in heparin acceleration of antithrombin-proteinase reactions. Resolution of the antithrombin conformational change contribution to heparin rate enhancement, J. Biol. Chem. 267, 12528-12538.
40. Rezaie, A. R., Yang, L., and Manithody, C. (2004) Mutagenesis studies toward understanding the mechanism of differential reactivity of factor Xa with the native and heparin activated antithrombin, Biochemistry 43, 2898-2905.
41. Mauron, T., Lammle, B., Wuillemin, W. A. (1998) Influence of low molecular weight heparin and low molecular weight dextran sulfate on the inhibition of coagulation factor XIa by serpins, Thromb. Haemostasis 80, 82-86.
42. Pixley, R. A., Schapira, M., and Colman, R. W. (1985) The regulation of human factor XIIa by plasma proteinase inhibitors, J. Biol. Chem. 260, 1723-1729.
43. Schapira, M., Scott, C. F., and Colman, R. W. (1981) Protection of human plasma kallikrein from inactivation by C1-inhibitor and other protease inhibitors: The role of high molecular weight kininogen, Biochemistry 20, 2738-2743.
44. Bos, I. G. A., Hack, C. E., and Abrahams, J. P. (2002) Structural and functional aspects of C1-inhibitor, Immunobiology 205, 518-533.
45. Johnson, D. J. D., Li, W., Adams, T. E., and Huntington, J. A. (2006) Antithrombin-S195A factor Xa-heparin structure reveals the allosteric mechanism of antithrombin activation, EMBO J. 25, 2029-2037.