New insights into the regulation of the blood clotting cascade derived from the X-ray crystal structure of bovine meizothrombin des F1 in complex with PPACK

Structure

Volumn 5, Issue 12, 1997, Pages 1681-1693

  Martin, Philip D ^a   Malkowski, Michael G ^a   Box, Jeffrey ^b   Esmon, Charles T ^b   Edwards, Brian F P ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

Crystal structure heparin binding site; Kringle domain; Meizothrombin; Thrombin

Indexed keywords

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 0031574020     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00314-6     Document Type: Article

References (70)

1. Degen, S.J., MacGillivray, R.T. & Davie, E.W. (1983). Characterization of the complementary deoxyribonucleic acid and gene coding for human prothrombin. Biochemistry 22, 2087-2097.
2. MacGillivray, R.T.A. & Davie, E.W. (1984). Characterization of bovine prothrombin mRNA and its translation product. Biochemistry 23, 1626-1634.
3. Seegers, W.A. & Walz, D.A. (1986). Prothrombin and other Vitamin K Proteins Vol. 1. CRC Press, Boca Raton, FL.
4. Mann, K.G. (1987). The assembly of blood clotting complexes on membranes. Trends Biochem. Sci. 12, 229-233.
5. Davie, E.W., Fujikawa, K. & Kisiel, W. (1991). The coagulation cascade: initiation, maintenance and regulation. Biochemistry 30, 10363-10370.
6. Berliner, J. (1992). Thrombin: Structure and Function. Plenum Press, New York, NY.
7. Mann, K.G., Nesheim, M.E., Hibbard, L.S. & Tracy, P.B. (1981). The role of factor V in the assembly of the prothrombinase complex. Ann. NY Acad. Sci. 370, 378-397.
8. Owen, W.G., Esmon, C.T. & Jackson, C.M. (1974). The conversion of prothrombin to thrombin. I. Characterization of the reaction products formed during the activation of bovine prothrombin. J. Biol. Chem. 249, 594-605.
9. Doyle, M.F. & Mann, K.G. (1990). Multiple active forms of thrombin. IV. Relative activities of meizothrombins. J. Biol. Chem. 265, 10693-10701.
10. Krishnaswamy, S., Mann, K.G. & Nesheim, M.E. (1986). The prothrombinase-catalyzed activation of prothrombin proceeds through the intermediate meizothrombin in an ordered, sequential reaction. J. Biol. Chem. 261, 8977-8984.
11. Rosing, J. & Tans, G. (1988). Meizothrombin, a major product of factor Xa-catalyzed prothrombin activation. Thromb. Haemost. 60, 355-360.
12. Boskovic, D.S., Giles, A.R. & Nesheim, M.E. (1990). Studies of the role of factor Va in the factor Xa-catalyzed activation of prothrombin, fragment 1.2-prethrombin-2, and dansyl-L-glutamyl-glycyl-L-arginine-meizothrombin in the absence of phospholipid. J. Biol. Chem. 265, 10497-10505.
13. Tans, G., et al., & Rosing, J. (1994). Activation of human factor V by meizothrombin. J. Biol. Chem. 269, 15969-15972.
14. Sadler, J.E., Lentz, S.R., Sheehan, J.P., Tsiang, M. & Wu, Q. (1993). Structure-function relationships of the thrombin-thrombomodulin interaction. Haemostasis 23, Supplement 1, 183-193.
15. Bevers, E.M., Comfurius, P. & Zwaal, R.F.A. (1983). Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta 736, 57-66.
16. Sheehan, J.P., Wu, Q., Tollefsen, D.M. & Sadler, J.E. (1993). Mutagenesis of thrombin selectively modulates inhibition by serpins heparin cofactor II and antithrombin III. J. Biol. Chem. 268, 3639-3645.
17. Gan, Z.-R., Li, Y., Chen, Z., Lewis, S.D. & Shafer, J.A. (1994). Identification of basic amino acid residues in thrombin essential for heparin-catalyzed inactivation by antithrombin III. J. Biol. Chem. 269, 1301-1305.
18. Ye, J., Rezaie, A.R. & Esmon, C.T. (1994). Glycosaminoglycan contributions to both protein C activation and thrombin inhibition involve a common arginine-rich site in thrombin that includes residues arginine 93, 97, and 101. J. Biol. Chem. 269, 17965-17970.
19. Pei, G., Laue, T.M., Aulabaugh, A., Fowlkes, D.M. & Lentz, B.R. (1992). Structural comparisons of meizothrombin and its precursor prothrombin in the presence or absence of procoagulant membranes. Biochemistry 31, 6990-6996.
20. Doyle, M.F. & Haley, P.E. (1993). Meizothrombin: active intermediate formed during prothrombin-catalyzed activation of prothrombin. Methods Enzymol. 222, 299-313.
21. Côté, H.C., Stevens, W.K., Bajzar, L., Banfield, D.K., Nesheim, M.E. & MacGillivray, R.T. (1994). Characterization of a stable form of human meizothrombin derived from recombinant prothrombin (R155A, R271A, and R284A). J. Biol. Chem. 269, 11374-11380.
22. Côté, H.C.F., et al., & Nesheim, M. (1997). Functional characterization of recombinant human meizothrombin and meizothrombin (desF1). J. Biol. Chem. 272, 6194-6200.
23. Wu, Q., Picard, V., Aiach, M. & Sadler, J.E. (1994). Activation-induced exposure of the thrombin anion-binding exosite. Interactions of recombinant mutant prothrombins with thrombomodulin and a thrombin exosite-specific antibody. J. Biol. Chem. 269, 3725-3730.
24. Boxrud, P.D. & Berliner, L.J. (1996). A comparison of the active site conformations of bovine alpha-thrombin and meizothrombin(desF1) by electron spin resonance. J. Prot. Chem. 15, 231-242.
25. Schoen, P. & Lindhout, T. (1987). The in situ inhibition of prothrombinase-formed human alpha-thrombin and meizothrombin (Des FI) by antithrombin III and heparin. J. Biol. Chem. 262, 11268-11274.
26. Patthy, L. (1985). Evolution of the proteases of blood coagulation and fibrinolysis by assembly from modules. Cell 41, 657-663.
27. Padmanabhan, K., Wu, T.P., Ravichandran, K.G. & Tulinsky, A. (1994). Kringle-kringle interactions in multimer kringle structures. Protein Sci. 3, 898-910.
28. 2+ ion and membrane binding structure of the Gla domain of Ca-prothrombin fragment 1. Biochemistry 31, 2554-2566.
29. Ami, R.K., Padmanabhan, K., Padmanabhan, K.P., Wu, T.-P. & Tulinsky, A. (1993). Structure of the noncovalent complexes of human and bovine prothrombin fragment 2 with human PPACK-thrombin. Biochemistry. 32, 4727-4737.
30. Van de Locht, A., Stubbs, M., Bauer, M. & Bode, W. (1996). Crystallographic evidence that the F2 kringle catalytic domain linker of prothrombin does not cover the fibrinogen recognition exosite. J. Biol. Chem. 271, 3413-3416.
31. Park, C.H. & Tulinsky, A. (1986). Three-dimensional structure of the kringle sequence: structure of prothrombin fragment 1. Biochemistry 25, 3977-3982.
32. Cohen, G.H., Silverton, E.W. & Davies, D.R. (1981). Refined crystal structure of gamma-chymotrypsin at 1.9 A resolution. Comparison with other pancreatic serine proteases. J. Mol. Biol. 148, 449-479.
33. Church, F.C., et al., & Meade, J.B. (1989). Structural and functional properties of human alpha-thrombin, phosphopyridoxylated alpha-thrombin, and gamma T-thrombin. Identification of lysyl residues in alpha-thrombin that are critical for heparin and fibrin(ogen) interactions. J. Biol. Chem. 264, 18419-18425.
34. Bode, W., Turk, D. & Karshikov, A. (1992). The refined 1.9-Å X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human alpha-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci. 1, 426-471.
35. Karshikov, A., Bode, W., Tulinsky, A. & Stone, S.R. (1992). Electrostatic interactions in the association of proteins: an analysis of the thrombin-hirudin complex. Protein Sci. 1, 727-735.
36. Lentz, B.R., Zhou, C.-M. & Wu, J.R. (1994). Phosphatidylserine-containing membranes alter the thermal stability of prothrombin's catalytic domain: a differential scanning calorimetric study. Biochemistry 33, 5460-5468.
37. Koppaka, V., Wang, J., Banerjee, M. & Lentz, B. (1996). Soluble phospholipids are allosteric effectors of factor Xa catalyzed prothrombin activation in solution. Biochemistry 35, 7482-7491.
38. Rossmann, M.G. & Argos, P. (1975). A comparison of the heme binding pocket in globins and cytochrome b5. J. Biol. Chem. 250, 7525-7532.
39. Martin, P.D., Robertson, W., Turk, D., Huber, R., Bode, W. & Edwards, B.F.P. (1992). The structure of residues 7-16 of the Aα-chain of human fibrinogen bound to bovine thrombin at 2.3 Å resolution. J. Biol. Chem. 267, 7911-7920.
40. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S.R. & Hofsteenge, J. (1989). The refined 1.9 Å crystal structure of human alpha-thrombin: interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475.
41. Luzatti, P.V. (1952). Traitement statistique des erreurs dans la determination des structures crystallines. Acta Cryst. 5, 802-810.
42. 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 a thrombin. J. Mol. Biol. 221, 1379-1393.
43. Qiu, X., et al., & Fenton, I.J. (1992). Structure of the hirulog-3 thrombin complex and nature of the S' subsites of substrates and inhibitors. Biochemistry 31, 11689-11697.
44. Qiu, X., Yin, M., Padmanabhan, K.P., Krystenansky, J.L. & Tulinsky, A. (1993). Structures of thrombin complexes with a designed and a natural exosite peptide inhibitor. J. Biol. Chem. 268, 20318-20326.
45. Rydel, T.J., Tulinsky, A., Bode, W. & Huber, R. (1991). Refined structure of the hirudin-thrombin complex. J. Mol. Biol. 221, 583-601.
46. Mathews, I., et al., & Fenton, J.W.n. (1994). Crystal log raphic structures of thrombin complexed with thrombin receptor peptides: existence of expected and novel binding modes. Biochemistry 33, 3266-3279.
47. Liu, L.-W, Vu, T.K.H., Esmon, C.T. & Coughlin, S.R. (1991). The region of the thrombin receptor resembling hirudin binds to thrombin and alters enzyme specificity. J. Biol. Chem. 266, 16977-16980.
48. Loll, P.J. & Lattman, E.E. (1990). Active site mutant Glu-43 to Asp in staphylococcal nuclease displays nonlocal structural changes. Biochemistry 29, 6866-6873.
49. 7-19: geometry of the catalytic triad and interactions of the P′, P′2, and P′3 substrate residue. Biochemistry 35, 13030-13039.
50. Stubbs, M.T. & Bode, W. (1993). A player of many parts: the spotlight falls on thrombin's structure. Thromb. Res. 69, 1-58.
51. Schechter, J. & Berger, A. (1967). On the size of the active site in proteases I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
52. 10 Biochemistry 22, 4170-4174.
53. 2+ dependence of protein C activation. J. Biol. Chem. 269, 11807-11812.
54. Jakubowski, H.V., Kline, M.D. & Owen, W.G. (1986). The effect of thrombomodulin on the specificity of bovine thrombin. J. Biol. Chem. 261, 3876-3882.
55. Ami, R.K., Padmanabhan, K., Padmanabhan, K.P., Wu, T.P. equation presented Tulinsky, A. (1994). Structure of the non-covalent complex of prothrombin kringle 2 with PPACK-thrombin. Chemistry & Physics of Lipids 67/68, 59-66.
56. 56 and catalytic activity. J. Biol. Chem. 271, 9-17.
57. Seshadri, T.P., Tulinsky, A., Skrzypczak-Jankun, E. & Park, C.H. (1991). Structure of bovine prothrombin fragment 1 refined at 2.25 Å resolution. J. Mol. Biol. 220, 481-494.
58. Chambers, J.L., Ortega, R.B. & Campana, C.F. (1992). In American Crystallographic Association, 50th Annual Meeting, Vol. 20. pp. 87-87, American Crystallographic Association, USA.
59. Howard, A.J., Gilliland, G.L., Finzel, B.C., Poulos, T.L., Ohlendorf, D.H. & Salemme, F.R. (1987). The use of an imaging proportional counter in macromolecular crystallography. J. Appl. Cryst. 20, 383-387.
60. Rossmann, M.G. & Blow, D.M. (1962). The detection of subunits within the crystallographic asymmetric unit. Acta Cryst. 15, 24-31.
61. Brünger, A.T. (1988). Crystallographic refinement by simulated annealing: application to a 2.8 Å resolution structure of aspartate aminotransferase. J. Mol. Biol. 203, 803-816.
62. Brünger, A.T. (1990). Extension of molecular replacement: a new search strategy based on Patterson correlation refinement. Acta Cryst. A 46, 46-57.
63. Wang, B.-C. (1985). Resolution of phase ambiguity in macromolecular crystallography. Methods Enzymol. 115, 90-112.
64. Jones, T.A. (1985). Interactive computer graphics: FRODO. Methods Enzymol. 115, 157-171.
65. Cambillau, C. & Horjales, E. (1987). TOM: a FRODO subpackage for protein-ligand fitting with interactive energy minimization. J. Mol. Graph. 5, 174-177.
66. Matthews, B.W. (1985). Determination of protein molecular weight, hydration, and packing from crystal density. Methods Enzymol. 114, 176-187.
67. Quiocho, F.A. & Richards, F.M. (1964). Intermolecular cross linking of a protein in the crystalline state: carboxypeptidase-A. Proc. Natl. Acad. Sci. USA 52, 833-839.
68. Harpaz, Y., Gerstein, M. & Chothia, C. (1994). Volume changes on protein folding. Structure 2, 641-649.
69. Nilsson, B., Horne, M.K., III. & Gralnick, H.R. (1983). The carbohydrate of human thrombin: structural analysis of glycoprotein oligosaccharides by mass spectrometry. Arch. Biochem. Biophys. 224, 127-133.
70. Zhang, K.Y.J. (1993). SQUASH-combining constraints for macromolecular phase refinement and extension. Acta Cryst. D 49, 213-222.