Mutations in the fourth EGF-like domain affect thrombomodulin-induced changes in the active site of thrombin

Biochemistry

Volumn 47, Issue 41, 2008, Pages 10933-10939

  Koeppe, Julia R ^a   Beach, Muneera A ^a   Baerga Ortiz, Abel ^a   Kerns, S Jordan ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; GLYCOPROTEINS; NUCLEAR MAGNETIC RESONANCE; STORAGE ALLOCATION (COMPUTER);

ACTIVE SITES; ALANINE MUTATIONS; MISFOLDING; STRUCTURAL DEFECTS; THROMBIN BINDING; THROMBOMODULIN; WILD-TYPE;

CRYSTAL STRUCTURE;

MUTANT PROTEIN; PROTEIN C; THROMBIN; THROMBOMODULIN;

AMINO ACID SUBSTITUTION; ARTICLE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; EPIDERMAL GROWTH FACTOR; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, FLUORESCENCE; SURFACE PLASMON RESONANCE; THROMBIN; THROMBOMODULIN;

EID: 53749094150     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8008278     Document Type: Article

References (26)

1. Esmon, C. T. (2000) Regulation of blood coagulation. Biochim. Biophys. Acta 1477, 349-360.
2. Stearns, D. J., Kurosawa, S., and Esmon, C. T. (1989) Microthrombomodulin. Residues 310-486 from the epidermal growth factor precursor homology domain of thrombomodulin will accelerate protein C activation. J. Biol. Chem. 264, 3352-3356.
3. Hayashi, T., Zushi, M., Yamamoto, S., and Suzuki, K. (1990) Further localization of binding sites for thrombin and protein C in human thrombomodulin. J. Biol. Chem. 265, 20156-20159.
4. Kurosawa, S., Stearns, D. J., Jackson, K. W., and Esmon, C. T. (1988) A 10-kDa cyanogen bromide fragment from the epidermal growth factor homology domain of rabbit thrombomodulin contains the primary thrombin binding site. J. Biol. Chem. 263, 5993-5996.
5. White, C. E., Hunter, M. J., Meininger, D. P., White, L. R., and Komives, E. A. (1995) Large-scale expression, purification and characterization of small fragments of thrombomodulin: The roles of the sixth domain and of methionine 388. Protein Eng. 8, 1177-1187.
6. Nagashima, M., Lundh, E., Leonard, J. C., Morser, J., and Parkinson, J. F. (1993) Alanine-scanning mutagenesis of the epidermal growth factor-like domains of human thrombomodulin identifies critical residues for its cofactor activity. J. Biol. Chem. 268, 2888-2892.
7. Hall, S. W., Nagashima, M., Zhao, L., Morser, J., and Leung, L. L. K. (1999) Thrombin interacts with thrombomodulin, protein C, and thrombin-activatable fibrinolysis inhibitor via specific and distinct domains. J. Biol. Chem. 274, 25510-25516.
8. Mandell, J. G., Falick, A. M., and Komives, E. A. (1998) Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl. Acad. Sci. U.S.A. 95, 14705-14710.
9. Fuentes-Prior, P., Iwanaga, Y., Huber, R., Pagila, R., Rumennik, G., Seto, M., Morser, J., Light, D. R., and Bode, W. (2000) Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature 404, 518-525.
10. Ye, J., Liu, L. W., Esmon, C. T., and Johnson, A. E. (1992) The 5th and 6th Growth Factor-Like Domains of Thrombomodulin Bind to the Anion-Binding Exosite of Thrombin and Alter Its Specificity. J. Biol. Chem. 267, 11023-11028.
11. Mandell, J. G., Baerga-Ortiz, A., Akashi, S., Takio, K., and Komives, E. A. (2001) Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306, 575-589.
12. Koeppe, J. R., Seitova, A., Mather, T., and Komives, E. A. (2005) Thrombomodulin tightens the thrombin active site loops to promote protein C activation. Biochemistry 44, 14784-14791.
13. Rezaie, A. R., and Yang, L. (2003) Thrombomodulin allosterically modulates the activity of the anticoagulant thrombin. Proc. Natl. Acad. Sci. U.S.A. 100, 12051-12056.
14. Rezaie, A. R., and Yang, L. (2005) Mutagenesis studies toward understanding the mechanism of the cofactor function of thrombomodulin. Biophys. Chem. 117, 255-261.
15. Wood, M. J., Sampoli Benitez, B. A., and Komives, E. A. (2000) Solution structure of the smallest cofactor-active fragment of thrombomodulin. Nat. Struct. Biol. 7, 200-204.
16. Prieto, J. H., Sampoli Benitez, B. A., Melacini, G., Johnson, D. A., Wood, M. J., and Komives, E. A. (2005) Dynamics of the fragment of thrombomodulin containing the fourth and fifth epidermal growth factor-like domains correlate with function. Biochemistry 44, 1225-1233.
17. Yang, L., Manithody, C., and Rezaie, A. R. (2006) Activation of protein C by the thrombin-thrombomodulin complex: Cooperative roles of Arg-35 of thrombin and Arg-67 of protein C. Proc. Natl. Acad. Sci. U.S.A. 103, 879-884.
18. Baerga-Ortiz, A., Rezaie, A. R., and Komives, E. A. (2000) Electrostatic dependence of the thrombin-thrombomodulin interaction. J. Mol. Biol. 296, 651-658.
19. Baerga-Ortiz, A., Bergqvist, S. P., Mandell, J. G., and Komives, E. A. (2004) Two different proteins that compete for binding to thrombin have opposite kinetic and thermodynamic profiles. Protein Sci. 13, 166-176.
20. Ye, J., Esmon, N. L., Esmon, C. T., and Johnson, A. E. (1991) The active site of thrombin is altered upon binding to thrombomodulin. Two distinct structural changes are detected by fluorescence, but only one correlates with protein C activation. J. Biol. Chem. 266, 23016-23021.
21. Wood, M. J., and Komives, E. A. (1999) Production of large quantities of isotopically labeled protein in Pichia pastoris by fermentation. J. Biomol. NMR 13, 149-159.
22. Croy, C. H., Koeppe, J. R., Bergqvist, S., and Komives, E. A. (2004) Allosteric Changes in Solvent Accessibility Observed in Thrombin upon Active Site Occupation. Biochemistry 43, 5246-5255.
23. Wood, M. J., Becvar, L. A., Prieto, J. H., Melacini, G., and Komives, E. A. (2003) NMR structures reveal how oxidation inactivates thrombomodulin. Biochemistry 42, 11932-11942.
24. 2Cl. Biochemistry 27, 6633-6639.
25. Blaber, M., Baase, W. A., Gassner, N., and Matthews, B. W. (1995) Alanine scanning mutagenesis of the α helix 115-123 of phage T4 lysozyme: Effects on structure, stability and the binding of solvent. J. Mol. Biol. 246, 317-330.
26. Clarke, J. H., Light, D. R., Blasko, E., Parkinson, J. F., Nagashima, M., McLean, K., Vilander, L., Andrews, W. H., Morser, J., and Glaser, C. B. (1993) The short loop between epidermal growth factor-like domains 4 and 5 is critical for human thrombomodulin function. J. Biol. Chem. 268, 6309-6315.