Effect of sodium on the energetics of thrombin-thrombomodulin interaction and its relevance for protein C hydrolysis

Journal of Molecular Biology

Volumn 258, Issue 1, 1996, Pages 190-200

  De Cristofaro, Raimondo ^a   Picozzi, Matilde ^a   Morosetti, Roberta ^a   Landolfi, Raffaele ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

Linkage; Protein c; Sodium; Thrombin; Thrombomodulin

Indexed keywords

PROTEIN C; SODIUM ION; THROMBIN; THROMBOMODULIN;

ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENERGY TRANSFER; ENTHALPY; ENTROPY; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME SUBSTRATE COMPLEX; HUMAN; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TEMPERATURE SENSITIVITY; THERMODYNAMICS;

FELIS CATUS;

EID: 0029928918     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0242     Document Type: Article

References (57)

1. Ayala, Y. & Di Cera, E. (1994). Molecular recognition by thrombin. Role of the slow → fast transition, site-specific ion binding energetics and thermodynamic mapping of structural components. J. Mol. Biol. 235, 733-746.
2. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S. R. & Hofsteenge, J. (1989). The refined 1.9 Å crystal structure of human α-thombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475.
3. Castagnola, M., Cassiano, L., De Cristofaro, R., Landolfi, R., Rossetti, D. V. & Marini Bettolo, G. B. (1988). High performance liquid chromatography in protein sequence determinations. J. Chromatog. 440, 231-251.
4. Cleland, W. W. (1986). In Investigations of Rates and Mechanisms of Reactions (Bernasconi, C. F., ed.), vol. 6, pp. 791-870, Wiley, New York.
5. Dang, Q. D., Vindigni, A. & Di Cera, E. (1995). An allosteric switch controls the procoagulant and anticoagulant activities of thrombin, Proc. Natl Acad. Sci. USA, 92, 5977-5981.
6. De Cristofaro, R. & Di Cera, E. (1990). Effect of protons on the amidase activity of human α-thrombin. J. Mol. Biol. 226, 1077-1085.
7. De Cristofaro, R. & Di Cera, E. (1992). Modulation of thrombin-fibrinogen interaction by specific ion effects. Biochemistry, 31, 257-265.
8. De Cristofaro, R. & Landolfi, R. (1994). Thermodynamics of substrates and reversible inhibitors binding to the active site cleft of human α-thrombin. J. Mol. Biol. 239, 569-577.
9. De Cristofaro, R., Fenton, J. W., II & Di Cera, E. (1992a). Modulation of thrombin-hirudin interaction by specific ion effects. J. Mol. Biol. 226, 263-269.
10. De Cristofaro, R., Fenton, J. W., II & Di Cera, E. (1992b). Linkage between proton binding and amidase activity in human γ-thrombin. Biochemistry, 31, 1147-1153.
11. De Cristofaro, R., Rocca, B., Bizzi, B. & Landolfi, R. (1993). The linkage between binding of the C-terminal domain of hirudin and amidase activity of human α-thrombin. Biochem. J. 289, 475-480.
12. De Cristofaro, R., Picozzi, M., De Candia, E., Rocca, B. & Landolfi, R. (1995). Thrombin-thrombomodulin interaction: energetics and potential role of water as an allosteric effector. Biochem. J. 310, 49-53.
13. Di Cera, E., De Cristofaro, R., Albright, D. J. & Fenton, J. W., II (1991). Linkage between proton binding and amidase activity in human α-thrombin: effects of ions and temperature. Biochemistry, 30, 7913-7924.
14. + binding site of thrombin. J. Biol. Chem. 270, 22089-22092.
15. Eftink, M. R., Anusiem, A. C. & Biltonen, R. L. (1983). Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry, 22, 3884-3896.
16. Esmon, C. T. (1989). The roles of Protein C in the regulation of blood coagulation. J. Biol. Chem. 264, 4743-4746.
17. Fersht, A. R. (1985). In Enzyme Structure and Mechanisms, pp. 159-161, Freeman, New York.
18. Foster, D. C., Yoshitake, S. & Davie, E. W. (1985). The nucleotide sequence of the gene for human Protein C. Proc. Natl Acad. Sci. USA, 82, 4673-4677.
19. Galvin, J. B., Kurosawa, S., Moore, K., Esmon, C. T. & Esmon, N. L. (1987). Reconstitution of rabbit thrombomodulin into phospholipid vesicles. J. Biol. Chem. 262, 2199-2205.
20. Griffin, J. H., Evatt, B. & Zimmermann, T. S. (1981). Deficiency of Protein C in congenital thrombotic disease. J. Clin. Invest. 68, 1370-1373.
21. Hofsteenge, J. & Stone, S. R. (1987). The effect of thrombomodulin on the cleavage of fibrinogen and fibrinogen fragments by thrombin. Eur. J. Biochem. 168, 49-56.
22. Jakubowski, H. V. & Owen, W. G. (1989). Macromolecular specificity determinants on thrombin for fibrinogen and thrombomodulin. J. Biol. Chem. 264, 11117-11121.
23. ++ binding to a high affinity site that does not contain carboxyglutamic acid. J. Biol. Chem. 258, 5554-5560.
24. Kisiel, W., Ericsson, L. H. & Davie, E. W. (1976). Proteolytic activation of Protein C from bovine plasma. Biochemistry, 15, 4893-4900.
25. Kurosawa, S., Galvin, J. B., Esmon, N. L. & Esmon, C. T. (1987). Proteolytic formation and properties of functional domains of thrombomodulin. J. Biol. Chem. 262, 2206-2212.
26. Kurosawa, S., Stearns, D. J., Jackson, J. B. & 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. 262, 2206-2212.
27. Landis, B. H., Koeheler, K. A. & Fenton, J. W., II. (1981). Human thrombins. J. Biol. Chem. 256, 4604-4610.
28. LeBonniec, B. F. & Esmon, C. T. (1991). Glu192 → Gln substitution in thrombin mimics the catalytic switch induced by thrombomodulin. Proc. Natl Acad. Sci. USA, 88, 7371-7375.
29. Lentz, S. R., Chen, Y. & Sadler, J. E. (1993). Sequences required for thrombomodulin cofactor activity within the fourth epidermal growth factor-like domain of human thrombomodulin. J. Biol. Chem. 268, 15312-15317.
30. Levina, N. B. & Nazimov, I. V. (1984). High performance liquid chromatography of Dns-amino acids in the purity control of peptides. J. Chromatog. 286, 207-216.
31. Lougheed, J. C., Bowman, C. L., Meininger, D. P. & Komives, E. (1995). Thrombin inhibition by cyclic peptides from thrombomodulin. Protein Sci. 4, 773-780.
32. Lumry R. (1995). The new paradigm for protein research. In Protein-Solvent Interactions (Gregory, R. B., ed.), pp. 1-141, Marcel Dekker, Basel.
33. Mathews, I. I., Padmanabhan, K. P., Tulinsky A. & Sadler, J. E. (1994a). Structure of a nonadecapeptide of the fifth EGF domain of thrombomodulin complexed with thrombin. Biochemistry, 33, 13547-13552.
34. Mathews, I. I., Padmanabhan, K. P., Ganesh, V., Tulinsky, A., Ishii, M., Chen, J., Turck, C. W., Coughlin, S. R. & Fenton, J. W., II (1994b). Crystallographic structures of thrombin complexed with thrombin receptor peptides: existence of expected and novel binding modes. Biochemistry, 33, 3266-3279.
35. Meininger, D. P., Hunter, M. J. & Komives, E. A. (1995). Synthesis, activity and preliminary structure of the fourth EGF-like domain of thrombomodulin. Protein Sci. 4, 1683-1695.
36. Miller-Andersson, M., Borg, H. & Andersson, L. O. (1974). Purification of antithrombin III by affinity chromatrography. Thromb. Res. 5, 439-452.
37. Nagashima, M., Lundh, E., Leonard, J. C., Morser, J. & 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.
38. Nishioka, J., Taneda, H. & Suzuki, K. (1993). Estimation of the possible recognition sites for thrombomodulin, procoagulant and anticoagulant proteins around the active center of α-thrombin. J. Biochem. 114, 148-155.
39. 2+ dependence of the interactions between Protein C, thrombin, and the elastase fragment of thrombomodulin. Analysis by ultracentrifugation. Biochemistry, 31, 746-754.
40. Orthner, C. L. & Kosow, D. P. (1980). Evidence that human α-thrombin is a monovalent cation-activated enzyme. Arch. Biochem. Biophys. 202, 63-75.
41. Owen, W. G. & Esmon, C. T. (1981). Functional properties of and endothelial cell cofactor for thrombin-catalyzed activation of Protein C. J. Biol. Chem. 256, 5532-5535.
42. Salem, H. H., Maruyama, I., Ishii, H. & Majerus, P. W. (1984). Isolation and characterization of thrombomodulin from human placenta. J. Biol. Chem. 259, 12246-12251.
43. Skrzypczak-Jankun, E., Carperos, V. E., Ravichandran, K. G., Tulinsky A., Westbrook, M. & Maraganore, J. M. (1991). Structure of the hirugen and hirulog 1 complexes of α-thrombin. J. Mol. Biol. 221, 1379-1393.
44. Srinivasan, J., Hu, S., Hrabal, R., Zhu, Y., Komives, E. A. & Ni, F. (1994). Thrombin-bound structure of an EGF subdomain from human thrombomodulin determined by transferred nuclear Overhauser effects. Biochemistry, 33, 13553-13560.
45. Stearns, D. J., Kurosawa, S. & Esmon, C. T. (1989). Microthrombomodulin. J. Biol. Chem. 264, 3352-3356.
46. Steiner, S. A. & Castellino, F. J. (1982). Kinetic studies of the role of monovelent cations in the amydolytic activity of activated bovine plasma Protein C. Biochemistry, 21, 4609-4614.
47. Stone, S. R. & Hermans, J. M. (1995). Inhibitory mechanism of serpins. Interaction of thrombin with antithrombin and protease nexin 1. Biochemistry, 34, 5164-5172.
48. Stubbs, M., Oschikinat, H., Mayr, I., Huber R., Angliker, H., Stone, S. R. & Bode, W. (1992). The interaction of thrombin with fibrinogen. Eur. J. Biochem. 206, 187-195.
49. Suzuki, K., Hayashi, T., Nishioka, J., Kosaka, Y., Zushi, M., Honda, G. & Yamamoto, S. (1989). A domain composed of epidermal growth factor-like structures of human thrombomodulin is essential for thrombin binding and for Protein C activation. J. Biol. Chem. 264, 4872-4876.
50. Tsiang, M., Lentz, S. R. & Sadler, J. E. (1992). Functional domains of membrane-bound human thrombomodulin. J. Biol. Chem. 267, 6164-6170.
51. Villanueva, G. B. & Perret, V. (1983). Effects of sodium and lithium salts on the conformation of human thrombin. Thromb. Res. 29, 489-498.
52. Walker, F. J., Sexton, P W. & Esmon, C. T. (1979). The inhibition of blood coagulation by activated Protein C through the selective inactivation of Factor V. Biochim. Biophys. Acta, 571, 333-342.
53. +-activated enzyme. Biochemistry, 31, 11721-11730.
54. Workman, E. F. & Lundblad, R. L. (1978). The effect of monovalent cations on the catalytic activity of thrombin. Arch. Biochem. Biophys. 185, 544-548.
55. Wyman, J. (1964). Linked functions and reciprocal effects in hemoglobin: a second look. Advan. Protein Chem. 19, 223-286.
56. Wyman, J. (1984). Linkage graphs: a study in the thermodynamics 3 of macromolecules. Quart. Rev. Biophys. 17, 453-488.
57. Zushi, M., Gomi, K., Yamamoto, S., Maruyama, I., Hayashi, T. & Suzuki, K. (1989). The last three consecutive epidermal growth factor-like structures of human thrombomodulin comprise the minimum functional domain for Protein C-activating cofactor activity and anticoagulant activity. J. Biol. Chem. 264, 10351-10353.