Importance of tryptophan 49 of antithrombin in heparin binding and conformational activation

Biochemistry

Volumn 44, Issue 35, 2005, Pages 11660-11668

  Monien, Bernhard H ^a   Krishnasamy, Chandravel ^a   Olson, Steven T ^b   Desai, Umesh R ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CONFORMATIONS; THERMODYNAMICS; X RAYS;

ACTIVATED CONFORMATION; BOUND SACCHARIDE; X-RAY COCRYSTAL STRUCTURE;

CHEMICAL BONDS;

ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; GLUTAMIC ACID; HEPARIN; LYSINE; PENTASACCHARIDE; PROTEINASE; SERINE; SERINE PROTEINASE INHIBITOR; THROMBIN; TRYPTOPHAN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL STRAIN BHK; CHEMICAL MODIFICATION; CONFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; ENERGY; ENZYME ACTIVITY; FLUORESCENCE; IONIC STRENGTH; KINETICS; MUTAGENESIS; MUTATION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; STOICHIOMETRY; THERMODYNAMICS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ANTITHROMBINS; CELLS, CULTURED; CRICETINAE; ENZYME ACTIVATION; HEPARIN; KINETICS; OLIGOSACCHARIDES; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROMETRY, FLUORESCENCE; TRYPTOPHAN;

EID: 24344464774     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050741i     Document Type: Article

References (47)

1. Olson, S. T., and Björk, I. (1994) Regulation of thrombin activity by antithrombin and heparin, Semin. Thromb. Hemostasis 20, 373-409.
2. Björk, I., and Olson, S. T. (1997) Antithrombin. A bloody important serpin, in Chemistry and Biology of Serpins (Church, F. C., Cunningham, D. D., Ginsburg, D., Hoffman, M., Stone, S. R., and Tollefsen, D. M., Eds.) pp 17-33, Plenum Press, New York.
3. Gettins, P. G. (2002) Serpin structure, mechanism, and function, Chem. Rev. 102, 4751-4803.
4. Olson, S. T., Björk, I., and Shore, J. D. (1993) Kinetic characterization of heparin-catalyzed and uncatalyzed inhibition of blood coagulation proteinases by antithrombin, Methods Enzymol. 222, 525-559.
5. Bedsted, T., Swanson, R., Chuang, Y. J., Bock, P. E., Björk, 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.
6. Olson, S. T., Swanson, R., Raub-Segall, E., Bedsted, T., Sadri, M., Petitou, M., Herault, J. P., Herbert, J. M., and Björk, I. 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.
7. Linhardt, R. J., and Loganathan D. (1990) Heparin, heparinoids and heparin oligosaccharides: Structure and biological activities in Biomimetic Polymers (Gebelein, C. G., Ed.) pp 135-173, Plenum Press, New York.
8. Rabenstein, D. L. (2002) Heparin and heparan sulfate: Structure and function, Nat. Prod. Rep. 19, 312-331.
9. Olson, S. T., and Chuang, Y. J. (2002) Heparin activates antithrombin anticoagulant function by generating new interaction sites (exosites) for blood clotting proteinases, Trends Cardiovasc. Med. 12, 331-338.
10. Langdown, J., Johnson, D. J. D., Baglin, T. P., and Huntington, J. A. (2004) Allosteric activation of antithrombin critically depends upon hinge region extension, Biochemistry 279, 47288-47297.
11. Olson, S. T., and Shore, J. D. (1982) Demonstration of a two-step reaction mechanism for inhibition of α-thrombin by antithrombin III and identification of the step affected by heparin, J. Biol. Chem. 257, 14891-14895.
12. Danielsson, A., Raub, E., Lindahl, U., and Björk, I. (1986) Role of ternary complexes, in which heparin binds both antithrombin and proteinase, in the acceleration of the reactions between antithrombin and thrombin or factor Xa, J. Biol. Chem. 261, 15467-15473.
13. Olson, S. T. (1988) Transient kinetics of heparin-catalyzed protease inactivation by antithrombin III. Linkage of protease-inhibitor-heparin interactions in the reaction with thrombin, J. Biol. Chem. 263, 1698-1708.
14. Rezaie, A. R. (1998) Calcium enhances heparin catalysis of the antithrombin-factor Xa reaction by a template mechanism. Evidence that calcium alleviates Gla domain antagonism of heparin binding to factor Xa, J. Biol. Chem. 273, 16824-16827.
15. Rezaie, A. R., and Olson, S. T. (2000) Calcium enhances heparin catalysis of the antithrombin-factor Xa reaction by promoting the assembly of an intermediate heparin-antithrombin-factor Xa bridging complex. Demonstration by rapid kinetics studies, Biochemistry 39, 12083-12090.
16. Jin, L., Abrahams, J.-P., Skinner, R., Petitou, M., Pike, R. N., and Carrell, R. W. (1997) The anticoagulant activation of antithrombin by heparin, Proc. Natl. Acad. Sci. U.S.A. 94, 14683-14688.
17. Desai, U. R., Swanson, R. S., Bock, S. C., Björk, I., and Olson, S. T. (2000) The role of arginine 129 in heparin binding and activation of antithrombin, J. Biol. Chem. 275, 18976-18984.
18. Arocas, V., Bock, S. C., Raja, S., Olson, S. T., and Björk, I. (2001) Lysine 114 of antithrombin is of crucial importance for the affinity and kinetics of heparin pentasaccharide binding, J. Biol. Chem. 276, 43809-43817.
19. Schedin-Weiss, S., Desai, U. R., Bock, S. C., Gettins, P. G. W., Olson, S. T., and Björk, I. (2002) Importance of Lysine 125 for heparin binding and activation of antithrombin, Biochemistry 41, 4779-4788.
20. Arocas, V., Turk, B., Bock, S. C., Olson, S. T., and Björk, I. (2000) The region of antithrombin interacting with full-length heparin chains outside the high-affinity pentasaccharide sequence extends to Lys136 but not to Lys139, Biochemistry 39, 8512-8518.
21. Olson, S. T., Björk, I., Sheffer, R., Craig, P. A., Shore, J. D., and Choay, J. (1992) Role of the antithrombin binding pentasaccharide in heparin acceleration of antithrombin-proteinase reactions, J. Biol. Chem. 267, 12528-12538.
22. Chang, J. Y., and Tran, T. H. (1986) Antithrombin III Basel. Identification of a Pro-Leu substitution in a hereditary abnormal antithrombin with impaired heparin cofactor activity, J. Biol. Chem. 261, 1174-1176.
23. Blackburn, M. N., Smith, R. L., Carson, J., and Sibley, C. C. (1984) The heparin-binding site of antithrombin III. Identification of a critical tryptophan in the amino acid sequence, J. Biol. Chem. 259, 939-941.
24. Björk, I., and Nordling, K. (1979) Evidence by chemical modification for the involvement of one or more tryptophanyl residues of bovine antithrombin in the binding of high-affinity heparin, Eur. J. Biochem. 102, 497-502.
25. Chowdhury, V., Mille, B., Olds, R. J., Lane, D. A., Watton, J., Barrowcliffe, T. W., Pabinger, I., Woodcock, B. E., and Thein, S. L. (1995) Antithrombins Southport (Leu 99 to Val) and Vienna (Gln 118 to Pro): Two novel antithrombin variants with abnormal heparin binding, Br. J. Haematol. 89, 602-609.
26. Okajima, K., Abe, H., Maeda, S., Motomura, M., Tsujihata, M., Nagataki, S., Okabe, H., and Takatsuki, K. (1993) Antithrombin III Nagasaki (Serl16-Pro): A heterozygous variant with defective heparin binding associated with thrombosis, Blood 81, 1300-1305.
27. Watton, J., Longstaff, C., Lane, D. A., and Barrowcliffe, T. W. (1993) Heparin binding affinity of normal and genetically modified antithrombin III measured using a monoclonal antibody to the heparin binding site of antithrombin III, Biochemistry 32, 7286-7293.
28. Gettins, P., Choay, J., Crews, B. C., and Zettlmeiss, G. (1992) Role of tryptophan 49 in the heparin cofactor activity of human antithrombin III, J. Biol. Chem. 267, 21946-21953.
29. Johnson, D. J. D., and Huntington, J. A. (2003) Crystal structure of antithrombin in a heparin-bound intermediate state, Biochemistry 42, 8712-8719.
30. Backovic, M., and Gettins, P. G. (2002) Insight into residues critical for antithrombin function from analysis of an expanded database of sequences that includes frog, turtle, and ostrich antithrombins, J. Proteome Res. 1, 367-373.
31. Meagher, J. L., Beechem, J. M., Olson, S. T., and Gettins, P. C. (1998) Deconvolution of the fluorescence emission spectrum of human antithrombin and identification of the tryptophan residues that are responsive to heparin binding, J. Biol. Chem. 273, 23283-23289.
32. Desai, U. R., Petitou, M., Björk, I., and Olson, S. T. (1998) Mechanism of heparin activation of antithrombin. Role of individual residues of the pentasaccharide activating sequence in the recognition of native and activated states of antithrombin, J. Biol. Chem. 273, 7478-7487.
33. Turk, B., Brieditis, I., Bock, S. C., Olson, S. T., and Björk, I. (1997) The oligosaccharide side chain on Asn-135 of α-antithrombin, absent in β-antithrombin, decreases the heparin affinity of the inhibitor by affecting the heparin-induced conformational change, Biochemistry 36, 6682-6691.
34. Olson, S. T., Halvorson, H. R., and Björk, I. (1991) Quantitative characterization of the thrombin-heparin interaction. Discrimination between specific and nonspecific binding models, J. Biol. Chem. 266, 6342-6352.
35. Olson, S. T., and Björk, I. (1991) Predominant contribution of surface approximation to the mechanism of heparin acceleration of the antithrombin-thrombin reaction. Elucidation from salt concentration effects, J. Biol. Chem. 266, 6353-6364.
36. Mascotti, D. P., and Lohman, T. M. (1995) Thermodynamics of charged oligopeptide-heparin interactions, Biochemistry 34, 2908-2915.
37. Olson, S. T., Srinivasan, K. R., Björk, I., and Shore, J. D. (1981) Binding of high affinity heparin to antithrombin III. Stopped flow kinetic studies of the binding interaction, J. Biol. Chem. 256, 11073-11079.
38. Manning, G. S. (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides, Q. Rev. Biophys. 11, 179-249.
39. Fan, B., Crews, B. C., Turko, I. V., Choay, J., Zettlmeissl, G., and Gettins, P. (1993) Heterogeneity of recombinant human antithrombin III expressed in baby hamster kidney cells. Effect of glycosylation differences on heparin binding and structure, J. Biol. Chem. 268, 17588-17596.
40. Jairajpuri, M. A., Lu, A., Desai, U. R., Olson, S. T., Björk, I., and Bock, S. C. (2003) Antithrombin III phenylalanines 122 and 121 contribute to its high affinity for heparin and its conformational activation, J. Biol. Chem. 278, 15941-15950.
41. Arocas, V., Bock, S. C., Olson, S. T., and Björk, I. (1999) The role of Arg46 and Arg47 of antithrombin in heparin binding, Biochemistry 38, 10196-10204.
42. Schedin-Weiss, S., Desai, U. R., Bock, S. C., Olson, S. T., and Björk, I. (2004) Roles of N-terminal region residues Lys11, Arg13, and Arg24 of antithrombin in heparin recognition and in promotion and stabilization of the heparin-induced conformational change, Biochemistry 43, 675-683.
43. Lakowicz, J. R. (2000) On spectral relaxation in proteins, Photochem. Photobiol. 72, 421-437.
44. Koide, T., Odani, S., Takahashi, K., Ono, T., and Sakuragawa, N. (1984) Antithrombin III Toyama: Replacement of arginine-47 by cysteine in hereditary abnormal antithrombin III that lacks heparin-binding ability, Proc. Natl. Acad. Sci. U.S.A. 81, 289-293.
45. Owen, M. C., Borg, J. Y., Soria, C., Soria, J., Caen, J., and Carrell, R. W. (1987) Heparin binding defect in a new antithrombin III variant: Rouen, 47 Arg to His, Blood 69, 1275-1279.
46. Borg, J. Y., Owen, M. C., Soria, C., Soria, J., Caen, J., and Carrell, R. W. (1988) Proposed heparin binding site in antithrombin based on arginine 47. A new variant Rouen-II, 47 Arg to Ser, J. Clin. Invest. 81, 1292-1296.
47. Wolf, M., Boyer-Neumann, C., Molho-Sabatier, P., Neumann, C., Meyer, D., and Larrieu, M. J. (1990) Familial variant of antithrombin III (AT III Bligny, 47Arg to His) associated with protein C deficiency, Thromb. Haemostasia 63, 215-219.