Modeling zymogen protein C

Biophysical Journal

Volumn 79, Issue 6, 2000, Pages 2925-2943

  Perera, Lalith ^a   Foley, Charles ^a   Darden, Thomas A ^b   Stafford, Darrel ^c   Mather, Timothy ^d   Esmon, Charles T ^d   Pedersen, Lee G ^a,b  

^a University of North Carolina at Chapel Hill   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; ENZYME PRECURSOR; EPIDERMAL GROWTH FACTOR; PROTEIN C; SERINE PROTEINASE; THROMBIN; VITAMIN K GROUP;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; MOLECULAR DYNAMICS; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

SUIDAE;

EID: 0033635315     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76530-1     Document Type: Article

References (86)

1. Banner, D. W., A. D'Arcy, C. Chene, F. Vilbois, W. H. Konigsberg, A. Guha, Y. Nemerson, and D. Kirchhofer. 1995. The crystal structure of the complex of human factor Vila with human soluble tissue factor. Thromb. Haemost. 73:1183-1183.
2. Banner, D. W., A. D'Arcy, C. Chene, F. K. Winkler, A. Guha, W. H. Konigsberg, Y. Nemerson, and D. Kirchhofer. 1996. The crystal structure of the complex of blood coagulation factor Vila with soluble tissue factor. Nature. 380:41-46.
3. Blow, D. M., and T. A. Steitz. 1970. X-ray diffraction studies of enzymes. Annu. Rev. Biochem. 39:63-100.
4. Bode, W., and P. Schwager. 1975. The refined crystal structure of bovine beta-trypsin at 1.8 A resolution. II. Crystallographic refinement, calcium binding site, benzamidine binding site and active site at pH 7.0. J. Mol. Biol. 98:693-717.
5. Brandstetter, H., M. Bauer, R. Huber, P. Lollar, and W. Bode. 1995. X-ray structure of clotting factor IXa: active site and module structure related to Xase activity and hemophilia B. Proc. Natl. Acad. Sci. USA. 92: 9796-9800.
6. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E. III, Ross, W. S., Simmerling, C. L., Darden, T. A., Merz, K. M., Stanton, R. V., Cheng, A. L., Vincent, J. J., Crowley, M., Ferguson, D. M., Radmer, R. J., Siebel, G. L., Singh, U. C., and Kollman, P. A. AMBER 5. 1997. University of California, San Francisco.
7. Cheatham, T. E. III, J. L. Miller, T. Fox, T. Darden, and P. A. Kollman. 1995. Molecular dynamics simulations on solvated biomolecular systems: the particle mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins. J. Am. Chem. Soc. 117:4193-4194.
8. Cheng, C. H., J. P. Geng, and F. J. Castellino. 1997. The functions of the first epidermal growth factor homology region of human protein C as revealed by a charge-to-alanine scanning mutagenesis investigation. Biol. Chem. 378:1491-1500.
9. Christiansen, W. T., and F. J. Castellino. 1994. Properties of recombinant chimeric human protein C and activated protein C containing the gamma-carboxyglutamic acid and trailing helical stack domains of protein C replaced by those of human coagulation factor IX. Biochemistry. 33: 5901-5911.
10. Christiansen, W. T., J. P. Geng, and F. J. Castellino. 1995b. Structure-function assessment of the role of the helical stack domain in the properties of human recombinant protein C and activated protein C. Biochemistry. 34:8082-8090.
11. Christiansen, W. T., L. R. Jalbert, R. M. Robertson, A. Jhingan, M. Prorok, and F. J. Castellino. 1995a. Hydrophobic amino acid residues of human anticoagulation protein C that contribute to its functional binding to phospholipid Vesicles. Biochemistry 34:10376-10382.
12. Christiansen, W. T., A. Tulinsky, and F. J. Castellino. 1994. Functions of individual gamma-carboxyglutamic acid (Gla) residues of human protein c. Determination of functionally nonessential Gla residues and correlations with their mode of binding to calcium. Biochemistry. 33: 14993-15000.
13. Colpitts, T. L., M. Prorok, and F. J. Castellino. 1995. Binding of calcium to individual γ-carboxyglutamic acid residues of human protein C. Biochemistry. 34:2424-2430.
14. Comp, P. C., and C. T. Esmon. 1981. Generation of fibrinolytic activity by infusion of activated protein C in dogs. J. Clin. Invest. 68:1221-1228.
15. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, Jr., D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 117:5179-5197.
16. Dahlback, B. 1997. Factor V and protein S as cofactors to activated protein C. Haematologica. 82:91-95.
17. Dahlback, B., and B. Hildebrand. 1994. Inherited resistance to activated protein C is corrected by anticoagulant cofactor activity found to be a property of factor V. Proc. Natl. Acad. Sci. USA. 91:1396-1400.
18. Davie, E. W. 1995. Biochemical and molecular aspects of the coagulation cascade. Thromb. Haemost. 74:1-6.
19. De Fouw, N. J., R. M. Bertina, and F. Haverkate. 1988. Activated protein C and fibrinolys. In Protein C and related proteins. R.M. Bertina, editor. Longman Group UK, Churchill Livingstone. 71-90.
20. Drakenberg, T., P. Fernlund, P. Roepstorff, and J. Stenflo. 1983. beta-Hydroxyaspartic acid in vitamin K-dependent protein C. Proc. Natl. Acad. Sci. USA. 80:1802-1806.
21. Esmon, C. T. 1989. The roles of protein C and thrombomodulin in the regulation of blood coagulation. J. Biol. Chem. 264:4743-4746.
22. Esmon, C. T. 1995b. Inflammation and thrombosis: the impact of inflammation on the protein C anticoagulant pathway. Haematologica. 80: 49-56.
23. Esmon, C. T. 1995a. Inflammation: they're not just for clots anymore. Curr. Biol. 5:743-746.
24. Esmon, C. T., and N. L. Esmon. 1984. Protein C activation. Semin. Thromb. Hemost. 10:122-130.
25. Esmon, C. T., N. L. Esmon, B. B. Le, and A. E. Johnson. 1993. Protein C activation. Methods Enzymol. 222:359-85:359-385.
26. Esmon, C. T., F. B. J. Taylor, and T. R. Snow. 1991. Inflammation and coagulation: linked processes potentially regulated through a common pathway mediated by protein C. Thromb. Haemost. 66:160-165.
27. Essmann, U., L. Perera, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen. 1995. A smooth particle mesh Ewald method. J. Chem. Phys. 103:8577-8593.
28. Fay, P. J., T. M. Smudzin, and F. J. Walker. 1991. Activated protein C-catalyzed inactivation of human factor VIII and factor Villa. Identification of cleavage sites and correlation of proteolysis with cofactor activity. J. Biol. Chem. 266:20139-20145.
29. Fernlund, P., and J. Stenflo. 1982. Amino acid sequence of the light chain of bovine protein C. J. Biol. Chem. 257:12170-12179.
30. Fernlund, P., and J. Stenflo. 1983. Beta-hydroxyaspartic acid in vitamin K-dependent proteins. J. Biol. Chem. 258:12509-12512.
31. Fisher, C. L., J. S. Greengard, and J. H. Griffin. 1994. Models of the serine protease domain of the human antithrombotic plasma factor activated protein c and its zymogen. Prat. Sci. 3:588-599.
32. Foster, D., and E. W. Davie. 1984. Characterization of a cDNA coding for human protein C. Proc. Natl. Acad. Sci. USA. 81:4766-4770.
33. Foster, D. C., M. S. Rudinski, B. G. Schach, K. L. Berkner, A. A. Kumar, F. S. Hagen, C. A. Sprecher, M. Y. Insley, and E. W. Davie. 1987. Propeptide of human protein C is necessary for gamma-carboxylation. Biochemistry. 26:7003-7011.
34. Foster, D. C., C. A. Sprecher, R. D. Holly, J. E. Gambee, K. M. Walker, and A. A. Kumar. 1990. Endoproteolytic processing of the dibasic cleavage site in the human protein C precursor in transfected mammalian cells: effects of sequence alterations on efficiency of cleavage. Biochemistry. 29:347-354.
35. Foster, D. C., S. Yoshitake, and E. W. Davie. 1985. The nucleotide sequence of the gene for human protein C. Proc. Natl. Acad. Sci. USA. 82:4673-4677.
36. Fuentes-Prior, P., Y. Iwanaga, R. Huber, R. Pagila, G. Rumennik, M. Seto, J. Morser, D. R. Light, and W. Bode. 2000. Structural basis for the anticoagulant activity of the thrombin-thrombomodulin complex. Nature. 404:518-525.
37. Geng, J. P., and F. J. Castellino. 1997. Properties of a recombinant chimeric protein in which the gamma- carboxyglutamic acid and helical stack domains of human anticoagulant protein C are replaced by those of human coagulation factor VII. Thromb. Haemost. 77:926-933.
38. Geng, J. P., C. H. Cheng, and F. J. Castellino. 1996. Functional consequences of mutations in amino acid residues that stabilize calcium binding to the first epidermal growth factor homology domain of human protein C. Thromb. Haemost. 76:720-728.
39. Gerlitz, B., and B. W. Grinnell. 1996. Mutation of protease domain residues Lys37-39 in human protein C inhibits activation by the thrombomodulin-thrombin complex without affecting activation by free thrombin. J. Biol. Chem. 271:22285-22288.
40. Gomis-Ruth, F. X., M. Gomez, W. Bode, R. Huber, and F. X. Aviles. 1995. The three-dimensional structure of the native ternary complex of bovine pancreatic procarboxypeptidase A with proproteinase E and chymotrypsinogen C. EMBO J. 14:4387-4394.
41. Grinnell, B. W., J. D. Walls, and B. Gerlitz. 1991. Glycosylation of human protein C affects its secretion, processing, functional activities, and activation by thrombin. J. Biol. Chem. 266:9778-9785.
42. Hamaguchi, N., P. Charifson, T. Darden, L. Xiao, K. Padmanabhan, A. Tulinsky, R. Hiskey, and L. Pedersen. 1992. Molecular dynamics simulation of bovine prothrombin fragment 1 in the presence of calcium ions. Biochemistry: 31:8840-8848.
43. Harvey, S. C., R. K. Z. Tan, and T. E. Cheatham III. 1998. The flying ice cube: velocity rescaling in molecular dynamics leads to violation of energy equipartition. J. Compulat. Chem. 18:726.
44. He, X., and A. R. Rezaie. 1999. Identification and characterization of the sodium-binding site of activated protein C. J. Biol. Chem. 274: 4970-4976.
45. Hogg, P. J., A. K. Ohlin, and J. Stenflo. 1992. Identification of structural domains in protein C involved in its interaction with thrombin-thrombomodulin on the surface of endothelial cells. J. Biol. Chem. 267:703-706.
46. Jalbert, L. R., J. C. Chan, W. T. Christiansen, and F. J. Castellino. 1996. The hydrophobia nature of residue-5 of human protein C is a major determinant of its functional interactions with acidic phospholipid vesicles. Biochemistry. 35:7093-7099.
47. Jane, S. M., L. Hau, and H. H. Salem. 1991. Regulation of activated protein C by factor Xa. Blood Coagul. Fibrinolysis. 2:723-729.
48. Kalafatis, M., M. D. Rand, and K. G. Mann. 1994. The mechanism of inactivation of human factor V and human factor Va by activated protein C. J. Biol. Chem. 269:31869-31880.
49. Kisiel, W., L. H. Ericsson, and E. W. Davie. 1976. Proteolytic activation of protein C from bovine plasma. Biochemistry. 15:4893-4900.
50. Knobe, K. E., A. Berntsdotter, L. Shen, J. Morser, B. Dahlback, and B. O. Villoutreix. 1999. Probing the activation of protein C by the thrombin-thrombomodulin complex using structural analysis, site-directed mutagenesis, and computer modeling. Proteins. 35:218-234.
51. Kraulis, P. J. 1991. MOLSCRIPT: A program to produce both detailed and Schematic plots of protein structure. J. Appl. Crystallogr. 24:946-950.
52. Le Bonniec, B. F., and C. T. Esmon. 1991. Glu-192 - Gln substitution in thrombin mimics the catalytic switch induced by thrombomodulin. Proc. Natl. Acad. Sci. USA. 88:7371-7375.
53. Le Bonniec, B. F., R. T. MacGillivray, and C. T. Esmon. 1991. Thrombin Glu-39 restricts the P'3 specificity to nonacidic residues. J. Biol. Chem. 266:13796-13803.
54. Li, L., T. Darden, R. Hiskey, and L. G. Pedersen. 1996. Computational studies of human prothrombin fragment 1, the Gla domain of factor IX and several biological interesting mutants. Haemostasis 26:54-59.
55. Li, L. P., T. A. Darden, S. J. Freedman, B. C. Furie, B. Furie, J. D. Baleja, H. Smith, R. G. Hiskey, and L. G. Pedersen. 1997. Refinement of the NMR solution structure of the gamma-carobxyglutamic acid domain of coagulation factor IX using molecular dynamics simulation with initial Ca2+ postions determined by a genetic algorithm. Biochem. 36: 2132-2138.
56. Mammen, E. F., W. R. Thomas, and W. H. Seegers. 1960. Activation of purified prothrombin to autoprothrombin or autoprothrombin II (platelet cofactor II) autoprothrombin II-a. Thromb. Diath. Haemorrh. 5:218-249.
57. Mather, T., V. Oganessyan, P. Hof, R. Huber, S. Foundling, C. Esmon, and W. Bode. 1996. The 2.8 A crystal structure of Gla-domainless activated protein C. EMBO J. 15:6822-6831.
58. McClure, D. B., J. D. Walls, and B. W. Grinnell. 1992. Post-translational processing events in the secretion pathway of human protein C, a complex vitamin K-dependent antithrombotic factor. J. Biol. Chem. 267:19710-19717.
59. McDonald, J. F., T. C. J. Evans, D. B. Emeagwali, M. Hariharan, N. M. Allewell, M. L. Pusey, A. M. Shah, and G. L. Nelsestuen. 1997a. Ionic properties of membrane association by vitamin K-dependent proteins: the case for univalency. Biochemistry. 36:15589-15598.
60. McDonald, J. F., A. M. Shah, R. A. Schwalbe, W. Kisiel, B. Dahlback, and G. L. Nelsestuen. 1997b. Comparison of naturally occurring vitamin K-dependent proteins: correlation of amino acid sequences and membrane binding properties suggests a membrane contact site. Biochemistry. 36:5120-5127.
61. Nesheim, M. E., W. M. Canfield, W. Kisiel, and K. G. Mann. 1982. Studies of the capacity of factor Xa to protect factor Va from inactivation by activated protein C. J. Biol. Chem. 257:1443-1447.
62. Nicholls, A., K. A. Sharp, and B. Honig. 1991. GRASP: graphical representation and analysis of surface properties. Proteins. 11:281-296.
63. Nishioka, J., M. Ido, T. Hayashi, and K. Suzuki. 1996. The Gla26 residue of protein C is required for the binding of protein C to thrombomodulin and endothelial cell protein C receptor, but not to protein S and factor Va. Thromb. Haemost. 75:275-282.
64. Perera, L., T. A. Darden, and L. G. Pedersen. 1999. Probing the structural changes in the light chain of human coagulation factor Vila due to tissue factor association. Biophys. J. 77:99-113.
65. Perera, L., L. Li, T. Darden, D. M. Monroe, and L. G. Pedersen. 1997. Prediction of solution structures of the Ca2+-bound gamma- carboxy-glutamic acid domains of protein S and homolog growth arrest specific protein 6: use of the particle mesh Ewald method. Biophys. J. 73: 1847-1856.
66. Reitsma, P. H. 1997. Protein C deficiency: from gene defects to disease. Thromb. Haemost. 78:344-350.
67. Rezaie, A. R., and C. T. Esmon. 1992. The function of calcium in protein C activation by thrombin and the thrombin-thrombomodulin complex can be distinguished by mutational analysis of protein C derivatives. J. Biol. Chem. 267:26104-26109.
68. Rezaie, A. R., and C. T. Esmon. 1993. Conversion of glutamic acid 192 to glutamine in activated protein C changes the substrate specificity and increases reactivity toward macromolecular inhibitors. J. Biol. Chem. 268:19943-19948.
69. Rezaie, A. R., and C. T. Esmon. 1995. Tryptophans 231 and 234 in protein C report the Ca(2+)-dependent conformational change required for activation by the thrombin- thrombomodulin complex. Biochemistry. 34:12221-12226.
70. Rezaie, A. R., N. L. Esmon, and C. T. Esmon. 1992. The high affinity calcium-binding site involved in protein C activation is outside the first epidermal growth factor homology domain. J. Biol. Chem. 267: 11701-11704.
71. Rezaie, A. R., T. Mather, F. Sussman, and C. T. Esmon. 1994. Mutation of Glu-80->Lys results in a protein C mutant that no longer requires Ca2+ for rapid activation by the thrombin-thrombomodulin complex. J. Biol. Chem. 269:3151-3154.
72. Shen, L., and B. Dahlback. 1994. Factor V and protein S as synergistic cofactors to activated protein C in degradation of factor Villa. J. Biol. Chem. 269:18735-18738.
73. Shen, L., X. He, and B. Dahlback. 1997a. Synergistic cofactor function of factor V and protein S to activated protein C in the inactivation of the factor VIIIa - factor IXa complex: species specific interactions of components of the protein C anticoagulant system. Thromb. Haemost. 78: 1030-1036.
74. Shen, L., A. M. Shah, B. Dahlback, and G. L. Nelsestuen. 1997b. Enhancing the activity of protein C by mutagenesis to improve the membrane-binding site: studies related to proline-10. Biochemistry. 36: 16025-16031.
75. Shen, L., A. M. Shah, B. Dahlback, and G. L. Nelsestuen. 1998. Enhancement of human protein C function by site-directed mutagenesis of the gamma-carboxyglutamic acid domain. J. Biol. Chem. 273: 31086-31091.
76. Stenflo, J. 1976. A new vitamin K-dependent protein. J. Biol. Chem. 251:355-363.
77. Stenflo, J., and P. Fernlund. 1982. Amino acid sequence of the heavy chain of bovine protein C. J. Biol. Chem. 257:12180-12190.
78. Stryer, I. 1988. Biochemistry. W. H. Freeman and Co., New York.
79. Suzuki, K. 1995. Protein C. In Molecular basis of thrombosis and hemostasis. K. A. High and H. R. Roberts, editors. Marcel Dekker, New York. 393-424.
80. Tanabe, S., T. Sugo, and M. Matsuda. 1991. Synthesis of protein C in human umbilical vein endothelial cells. J. Biochem. (Tokyo). 109: 924-928.
81. Tuddenham, E. G. D., and D. N. Cooper. 1994. The Molecular Genetics of Haemostasis and its Inherited Disorder. Oxford University Press, New York.
82. Vijayalakshmi, J., K. P. Padmanabhan, K. G. Mann, and A. Tulinsky. 1994. The isomorphous structures of prethrombin2, hirugen-, and PPACK-thrombin: changes accompanying activation and exosite binding to thrombin. Protein Sci. 3:2254-2271.
83. Wang, D., W. Bode, and R. Huber. 1985. Bovine chymotrypsinogen A X-ray crystal structure analysis and refinement of a new crystal form at 1.8 A resolution. J. Mol. Biol. 185:595-624.
84. Yegneswaran, S., G. M. Wood, C. T. Esmon, and A. E. Johnson. 1997. Protein S alters the active site location of activated protein C above the membrane surface. A fluorescence resonance energy transfer study of topography. J. Biol. Chem. 272:25013-25021.
85. York, D. M., A. Wlodawer, L. G. Pedersen, and T. Darden. 1994. Atomic-level accuracy in simulations of large protein crystals. Proc. Natl. Acad. Sci. USA. 91:8715-8718.
86. Zolton, R. P., and W. H. Seegers. 1973. Autoprothrombin II-A: thrombin removal and mechanism of induction of fibrinolysis. Thromb. Res. 3:23-33.