The fragment 1 region of prothrombin facilitates the favored binding of fragment 12 to zymogen and enforces zymogen-like character in the proteinase

Journal of Biological Chemistry

Volumn 291, Issue 21, 2016, Pages 11114-11123

  Bradford, Harlan N ^a   Krishnaswamy, Sriram ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; GLYCOPROTEINS;

CATALYTIC DOMAINS; COVALENT LINKAGE; HIGH AFFINITY; N-TERMINALS; PROTEOLYTIC ACTIVATION; PROTHROMBIN ACTIVATION; THERMODYNAMIC CONSTANTS;

BINS;

4 CARBOXYGLUTAMIC ACID; CALCIUM; ENZYME PRECURSOR; MEIZOTHROMBIN; PROTEINASE; PROTHROMBIN; THROMBIN; PEPTIDE FRAGMENT; PROTEIN BINDING; PROTEIN PRECURSOR; PROTHROMBIN FRAGMENT 1; PROTHROMBIN FRAGMENT 1.2;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COVALENT BOND; HUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; THERMODYNAMICS; CHEMISTRY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; IN VITRO STUDY; KINETICS; KRINGLE DOMAIN; METABOLISM; MOLECULAR MODEL;

CATALYTIC DOMAIN; ENZYME ACTIVATION; ENZYME PRECURSORS; HUMANS; IN VITRO TECHNIQUES; KINETICS; KRINGLES; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTHROMBIN; THERMODYNAMICS;

EID: 84971236575     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.723072     Document Type: Article

References (40)

1. Mann, K. G., Jenny, R. J., and Krishnaswamy, S. (1988) Cofactor proteins in the assembly and expression of blood clotting enzyme complexes. Annu. Rev. Biochem. 57, 915-956
2. Mann, K. G., Nesheim, M. E., Church, W. R., Haley, P., and Krishnaswamy, S. (1990) Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 76, 1-16
3. Mann, K. G. (2003) Thrombin formation. Chest 124, 4S-10S
4. Jenny, N. S., Lundblad, R. L., and Mann, K. G. (2006) Thrombin. In Hemostasis and Thrombosis. Basic Principles and Clinical Practice (Colman, R. W., Marder, V. J., Clowes, A. J., George, J. N., and Goldhaber, S. Z., eds.) pp 193-213, Lippincott Williams & Wilkins, Philadelphia
5. Esmon, C. T. (2003) The protein C pathway. Chest 124, 26S-32S
6. Lane, D. A., Philippou, H., and Huntington, J. A. (2005) Directing thrombin. Blood 106, 2605-2612
7. Bock, P. E., Panizzi, P., and Verhamme, I. M. (2007) Exosites in the substrate specificity of blood coagulation reactions. J. Thromb. Haemost. 5, 81-94
8. Huntington, J. A. (2005) Molecular recognition mechanisms of thrombin. J. Thromb. Haemost. 3, 1861-1872
9. Arni, R. K., Padmanabhan, K., Padmanabhan, K. P., Wu, T. P., and Tulinsky, A. (1993) Structures of the noncovalent complexes of human and bovine prothrombin fragment 2 with human PPACK-thrombin. Biochemistry 32, 4727-4737
10. Adams, T. E., and Huntington, J. A. (2016) Structural transitions during prothrombin activation: on the importance of fragment 2. Biochimie 122, 235-242
11. Pozzi, N., Chen, Z., Pelc, L. A., Shropshire, D. B., and Di Cera, E. (2014) The linker connecting the two kringles plays a key role in prothrombin activation. Proc. Natl. Acad. Sci. U.S.A. 111, 7630-7635
12. Pozzi, N., Chen, Z., and Di Cera, E. (2016) How the Linker Connecting the two kringles influences activation and conformational plasticity of prothrombin. J. Biol. Chem. 291, 6071-6082
13. Kamath, P., and Krishnaswamy, S. (2008) Fate of membrane-bound reactants and products during the activation of human prothrombin by prothrombinase. J. Biol. Chem. 283, 30164-30173
14. Kamath, P., Huntington, J. A., and Krishnaswamy, S. (2010) Ligand binding shuttles thrombin along a continuum of zymogen- and proteinase-like states. J. Biol. Chem. 285, 28651-28658
15. Bradford, H. N., and Krishnaswamy, S. (2012) Meizothrombin is an unexpectedly zymogen-like variant of thrombin. J. Biol. Chem. 287, 30414-30425
16. Krishnaswamy, S. (2013) The transition of prothrombin to thrombin J. Thromb. Haemost. 11, 265-276
17. Bloom, J. W., and Mann, K. G. (1979) Prothrombin domains: circular dichroic evidence for a lack of cooperativity. Biochemistry 18, 1957-1961
18. Armstrong, S. A., Husten, E. J., Esmon, C. T., and Johnson, A. E. (1990) The active site of membrane-bound meizothrombin. A fluorescence determination of its distance from the phospholipid surface and its conformational sensitivity to calcium and factor Va. J. Biol. Chem. 265, 6210-6218
19. Doyle, M. F., and Mann, K. G. (1990) Multiple active forms of thrombin. IV. Relative activities of meizothrombins. J. Biol. Chem. 265, 10693-10701
20. Côté, H. C., Stevens, W. K., Bajzar, L., Banfield, D. K., Nesheim, M. E., and 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
21. Baugh, R. J., and Krishnaswamy, S. (1996) Role of the activation peptide domain in human factor X activation by the extrinsic Xase complex. J. Biol. Chem. 271, 16126-16134
22. Orcutt, S. J., Pietropaolo, C., and Krishnaswamy, S. (2002) Extended interactions with prothrombinase enforce affinity and specificity for its macromolecular substrate. J. Biol. Chem. 277, 46191-46196
23. Bradford, H. N., Orcutt, S. J., and Krishnaswamy, S. (2013) Membrane binding by prothrombin mediates its constrained presentation to prothrombinase for cleavage. J. Biol. Chem. 288, 27789-27800
24. Price, P. A. (1983) Analysis for γ-carboxyglutamic acid. Methods Enzymol. 91, 13-17
25. Mann, K. G., Elion, J., Butkowski, R. J., Downing, M., and Nesheim, M. E. (1981) Prothrombin. Methods Enzymol. 80, 286-302
26. Pollock, J. S., Shepard, A. J., Weber, D. J., Olson, D. L., Klapper, D. G., Pedersen, L. G., and Hiskey, R. G. (1988) Phospholipid binding properties of bovine prothrombin peptide residues 1-45. J. Biol. Chem. 263, 14216-14223
27. Lundblad, R. L., Kingdon, H. S., and Mann, K. G. (1976) Thrombin. Methods Enzymol. 45, 156-176
28. Keller, S., Vargas, C., Zhao, H., Piszczek, G., Brautigam, C. A., and Schuck, P. (2012) High-precision isothermal titration calorimetry with automated peak shape analysis. Anal. Chem. 84, 5066-5073
29. Houtman, J. C., Brown, P. H., Bowden, B., Yamaguchi, H., Appella, E., Samelson, L. E., and Schuck, P. (2007) Studying multisite binary and ternary protein interactions by global analysis of isothermal titration calorimetry data in SEDPHAT: application to adaptor protein complexes in cell signaling. Protein Sci. 16, 30-42
30. Bevington, P. R., and Robinson, K. D. (1992) Data Reduction and Error Analysis for the Physical Sciences, pp. 161-167, 2nd Ed., McGraw-Hill, New York
31. Chen, Z., Pelc, L. A., and Di Cera, E. (2010) Crystal structure of prethrombin-1. Proc. Natl. Acad. Sci. U.S.A. 107, 19278-19283
32. Doyle, M. F., and Haley, P. E. (1993) Meizothrombin: active intermediate formed during prothrombinase-catalyzed activation of prothrombin. Methods Enzymol. 222, 299-312
33. Krishnaswamy, S., Church, W. R., Nesheim, M. E., and Mann, K. G. (1987) Activation of human prothrombin by human prothrombinase: influence of factor Va on the reaction mechanism. J. Biol. Chem. 262, 3291-3299
34. Lu, G., Chhum, S., and Krishnaswamy, S. (2005) The affinity of protein C for the thrombin•thrombomodulin complex is determined in a primary way by active site-dependent interactions. J. Biol. Chem. 280, 15471-15478
35. Nesheim, M. E., Prendergast, F. G., and Mann, K. G. (1979) Interactions of a fluorescent active-site-directed inhibitor of thrombin: dansylarginine N-(3-ethyl-1,5-pentanediyl)amide. Biochemistry 18, 996-1003
36. Lechtenberg, B. C., Murray-Rust, T. A., Johnson, D. J., Adams, T. E., Krishnaswamy, S., Camire, R. M., and Huntington, J. A. (2013) Crystal structure of the prothrombinase complex from the venom of Pseudonaja textilis. Blood 122, 2777-2783
37. Bianchini, E. P., Orcutt, S. J., Panizzi, P., Bock, P. E., and Krishnaswamy, S. (2005) Ratcheting of the substrate from the zymogen to proteinase conformations directs the sequential cleavage of prothrombin by prothrombinase. Proc. Natl. Acad. Sci. U.S.A. 102, 10099-10104
38. Tans, G., Nicolaes, G. A., Thomassen, M. C., Hemker, H. C., van Zonnenveld, A.-J., Pannekoek, H., and Rosing, J. (1994) Activation of human factor V by meizothrombin. J. Biol. Chem. 269, 15969-15972
39. Matafonov, A., Sarilla, S., Sun, M. F., Sheehan, J. P., Serebrov, V., Verhamme, I. M., and Gailani, D. (2011) Activation of factor XI by products of prothrombin activation. Blood 118, 437-445
40. Orfeo, T., Brufatto, N., Nesheim, M. E., Xu, H., Butenas, S., and Mann, K. G. (2004) The factor V activation paradox. J. Biol. Chem. 279, 19580-19591