Biophysical characterization of anticoagulant hemextin AB complex from the venom of snake Hemachatus haemachatus

Biophysical Journal

Volumn 93, Issue 11, 2007, Pages 3963-3976

  Banerjee, Yajnavalka ^a,b   Lakshminarayanan, Rajamani ^a,c   Vivekanandan, Subramanian ^a,d   Anand, Ganesh Srinivasan ^a   Valiyaveettil, Suresh ^a   Kini, R Manjunatha ^a,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^e VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT PROTEIN; GLYCEROL; HEMEXTIN AB COMPLEX; SNAKE VENOM; UNCLASSIFIED DRUG;

ANTICOAGULATION; ARTICLE; BETA SHEET; CIRCULAR DICHROISM; COMPLEX FORMATION; ELECTRICITY; ENTHALPY; HEAT; HEMACHATUS HAEMACHATUS; HYDROPHOBICITY; IONIC STRENGTH; MOLECULAR INTERACTION; PROTEIN ANALYSIS; SNAKE;

HEMACHATUS HAEMACHATUS;

EID: 36849015841     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.100164     Document Type: Article

References (57)

1. Davie, E. W., K. Fujikawa, and W. Kisiel. 1991. The coagulation cascade: initiation, maintenance, and regulation. Biochemistry. 30:10363-10370.
2. Davie, E. W. 1995. Biochemical and molecular aspects of the coagulation cascade. Thromb. Haemost. 74:1-6.
3. Nemerson, Y. 1988. Tissue factor and hemostasis. Blood. 71:1-8.
4. Yegneswaran, S., R. M. Mesters, and J. H. Griffin. 2003. Identification of distinct sequences in human blood coagulation factor Xa and prothrombin essential for substrate and cofactor recognition in the prothrombinase complex. J. Biol. Chem. 278:33312-33318.
5. Kumar, R., S. Beguin, and H. C. Hemker. 1995. The effect of fibrin clots and clot-bound thrombin on the development of platelet procoagulant activity. Thromb. Haemost. 74:962-968.
6. Myles, T., T. H. Yun, S. W. Hall, and L. L. Leung. 2001. An extensive interaction interface between thrombin and factor V is required for factor V activation. J. Biol. Chem. 276:25143-25149.
7. Saenko, E. L., D. Scandella, A. V. Yakhyaev, and N. J. Greco. 1998. Activation of factor VIII by thrombin increases its affinity for binding to synthetic phospholipid membranes and activated platelets. J. Biol. Chem. 273:27918-27926.
8. Curtis, J. E., S. L. Helgerson, E. T. Parker, and P. Lollar. 1994. Isolation and characterization of thrombin-activated human factor VIII. J. Biol. Chem. 269:6246-6251.
9. Mann, K. G., S. Butenas, and K. Brummel. 2003. The dynamics of thrombin formation. Arterioscler. Thromb. Vasc. Biol. 23:17-25.
10. Higgins, D. L., S. D. Lewis, and J. A. Shafer. 1983. Steady state kinetic parameters for the thrombin-catalyzed conversion of human fibrinogen to fibrin. J. Biol. Chem. 258:9276-9282.
11. Lewis, S. D., L. Lorand, J. W. Fenton, and J. A. Shafer. 1987. Catalytic competence of human alpha- and gamma-thrombin in the activation of fibrinogen and factor XIII. Biochemistry. 26:7597-7603.
12. Hanessian, S., R. Margarita, A. Hall, S. Johnstone, M. Tremblay, and L. Parlanti. 2002. Total synthesis and structural confirmation of the marine natural product Dysinosin A: a novel inhibitor of thrombin and Factor VIIa. J. Am. Chem. Soc. 124:13342-13343.
13. Carroll, A. R., G. K. Pierens, G. Fechner, L. P. De Almeida, A. Ngo, M. Simpson, E. Hyde, J. N. Hooper, S. L. Bostrom, D. Musil, and R. J. Quinn. 2002. Dysinosin A: a novel inhibitor of Factor VIIa and thrombin from a new genus and species of Australian sponge of the family Dysideidae. J. Am. Chem. Soc. 124:13340-13341.
14. Lindhout, T., J. Franssen, and G. Willems. 1995. Kinetics of the inhibition of tissue factor-factor VIIa by tissue factor pathway inhibitor. Thromb. Haemost. 74:910-915.
15. Salemink, I., J. Franssen, G. M. Willems, H. C. Hemker, and T. Lindhout. 1999. Inhibition of tissue factor-factor VIIa-catalyzed factor X activation by factor Xa-tissue factor pathway inhibitor. A rotating disc study on the effect of phospholipid membrane composition. J. Biol. Chem. 274:28225-28232.
16. Moons, A. H., R. J. Peters, N. R. Bijsterveld, J. J. Piek, M. H. Prins, G. P. Vlasuk, W. E. Rote, and H. R. Buller. 2003. Recombinant nematode anticoagulant protein c2, an inhibitor of the tissue factor/factor VIIa complex, in patients undergoing elective coronary angioplasty. J. Am. Coll. Cardiol. 41:2147-2153.
17. Lee, A. Y., and G. P. Vlasuk. 2003. Recombinant nematode anticoagulant protein c2 and other inhibitors targeting blood coagulation factor VIIa/tissue factor. J. Intern. Med. 254:313-321.
18. Baugh, R. J., G. J. Broze, Jr., and S. Krishnaswamy. 1998. Regulation of extrinsic pathway factor Xa formation by tissue factor pathway inhibitor. J. Biol. Chem. 273:4378-4386.
19. Broze, G. J. Jr., and J. P. Miletich. 1987. Characterization of the inhibition of tissue factor in serum. Blood. 69:150-155.
20. Sanders, N. L., S. P. Bajaj, A. Zivelin, and S. I. Rapaport. 1985. Inhibition of tissue factor/factor VIIa activity in plasma requires factor X and an additional plasma component. Blood. 66:204-212.
21. Buddai, S. K., L. Toulokhonova, P. W. Bergum, G. P. Vlasuk, and S. Krishnaswamy. 2002. Nematode anticoagulant protein c2 reveals a site on factor Xa that is important for macromolecular substrate binding to human prothrombinase. J. Biol. Chem. 277:26689-26698.
22. Kini, R. M. 2006. Anticoagulant proteins from snake venoms: structure, function and mechanism. Biochem. J. 397:377-387.
23. Kini, R. M. 2005. Serine proteases affecting blood coagulation and fibrinolysis from snake venoms. Pathophysiol. Haemost. Thromb. 34:200-204.
24. Banerjee, Y., J. Mizuguchi, S. Iwanaga, and R. M. Kini. 2005. Hemextin AB complex, a unique anticoagulant protein complex from Hemachatus haemachatus (African Ringhals cobra) venom that inhibits clot initiation and factor VIIa activity. J. Biol. Chem. 280:42601-42611.
25. Banerjee, Y., J. Mizuguchi, S. Iwanaga, and R. M. Kini. 2005. Hemextin AB complex - a snake venom anticoagulant protein complex that inhibits factor VIIa activity. Pathophysiol. Haemost. Thromb. 34:184-187.
26. Wang, R., R. M. Kini, and M. C. Chung. 1999. Rhodocetin, a novel platelet aggregation inhibitor from the venom of Calloselasma rhodostoma (Malayan pit viper): synergistic and noncovalent interaction between its subunits. Biochemistry. 38:7584-7593.
27. Paaventhan, P., C. Kong, J. S. Joseph, M. C. Chung, and P. R. Kolatkar. 2005. Structure of rhodocetin reveals noncovalently bound heterodimer interface. Protein Sci. 14:169-175.
28. Rao, V. S., and R. M. Kini. 2002. Pseutarin C, a prothrombin activator from Pseudonaja textilis venom: its structural and functional similarity to mammalian coagulation factor Xa-Va complex. Thromb. Haemost. 88:611-619.
29. Rao, V. S., S. Swarup, and R. M. Kini. 2003. The nonenzymatic subunit of pseutarin C, a prothrombin activator from eastern brown snake (Pseudonaja textilis) venom, shows structural similarity to mammalian coagulation factor V. Blood. 102:1347-1354.
30. Knutson, E. O., and K. T. Whitby. 1975. Aerosol classification by electric mobility: apparatus, theory, and applications. J. Aerosol Sci. 6:443-451.
31. Provencher, S. W. 1976. A Fourier method for the analysis of exponential decay curves. Biophys. J. 16:27-41.
32. Levenberg, K. 1944. A method for the solution of certain problems in least squares. Q. Appl. Math. 2:164-168.
33. Marquardt, D. 1963. An algorithm for least-squares estimation of nonlinear parameters. SIAM J. Appl. Math. 11:431-441.
34. Lakshminarayanan, R., E. O. Chi-Jin, X. J. Loh, R. M. Kini, and S. Valiyaveettil. 2005. Purification and characterization of a vaterite-inducing peptide, pelovaterin, from the eggshells of Pelodiscus sinensis (Chinese soft-shelled turtle). Biomacromolecules. 6:1429-1437.
35. Piotto, M., V. Saudek, and V. Sklenar. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR. 2:661-665.
36. Wilkins, D. K., S. B. Grimshaw, V. Receveur, C. M. Dobson, J. A. Jones, and L. J. Smith. 1999. Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques. Biochemistry. 38:16424-16431.
37. Lu, H., B. Isralewitz, A. Krammer, V. Vogel, and K. Schulten. 1998. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation. Biophys. J. 75:662-671.
38. Longhi, S., V. Receveur-Brechot, D. Karlin, K. Johansson, H. Darbon, D. Bhella, R. Yeo, S. Finet, and B. Canard. 2003. The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278:18638-18648.
39. Perozzo, R., G. Folkers, and L. Scapozza. 2004. Thermodynamics of protein-ligand interactions: history, presence, and future aspects. J. Recept. Signal Transduct. Res. 24:1-52.
40. Velazquez-Campoy, A., S. A. Leavitt, and E. Freire. 2004. Characterization of protein-protein interactions by isothermal titration calorimetry. Methods Mol. Biol. 261:35-54.
41. Weber, P. C., and F. R. Salemme. 2003. Applications of calorimetric methods to drug discovery and the study of protein interactions. Curr. Opin. Struct. Biol. 13:115-121.
42. Katragadda, M., D. Morikis, and J. D. Lambris. 2004. Thermodynamic studies on the interaction of the third complement component and its inhibitor, compstatin. J. Biol. Chem. 279:54987-54995.
43. Tidor, B., and M. Karplus. 1994. The contribution of vibrational entropy to molecular association. The dimerization of insulin. J. Mol. Biol. 238:405-414.
44. Stites, W. E. 1997. Protein-protein interactions: interface structure, binding thermodynamics, and mutational analysis. Chem. Rev. 97:1233-1250.
45. Murphy, K. P., and S. J. Gill. 1991. Solid model compounds and the thermodynamics of protein unfolding. J. Mol. Biol. 222:699-709.
46. Murphy, K. P., and E. Freire. 1992. Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43:313-361.
47. Cooper, A. 1999. Thermodynamic analysis of biomolecular interactions. Curr. Opin. Chem. Biol. 3:557-563.
48. Dunitz, J. D. 1995. Win some, lose some: enthalpy-entropy compensation in weak intermolecular interactions. Chem. Biol. 2:709-712.
49. Lumry, R. 2003. Uses of enthalpy-entropy compensation in protein research. Biophys. Chem. 105:545-557.
50. Spolar, R. S., and M. T. Record, Jr. 1994. Coupling of local folding to site-specific binding of proteins to DNA. Science. 263:777-784.
51. von Hippel, P. H. 1994. Protein-DNA recognition: new perspectives and underlying themes. Science. 263:769-770.
52. Finkelstein, A. V., and J. Janin. 1989. The price of lost freedom: entropy of bimolecular complex formation. Protein Eng. 3:1-3.
53. Janin, J., and C. Chothia. 1978. Role of hydrophobicity in the binding of coenzymes. Appendix. Translational and rotational contribution to the free energy of dissociation. Biochemistry. 17:2943-2948.
54. Hilpert, K., H. Wessner, J. Schneider-Mergener, K. Welfle, R. Misselwitz, H. Welfle, A. C. Hocke, S. Hippenstiel, and W. Hohne. 2003. Design and characterization of a hybrid miniprotein that specifically inhibits porcine pancreatic elastase. J. Biol. Chem. 278:24986-24993.
55. Liu, W., D. Bratko, J. M. Prausnitz, and H. W. Blanch. 2004. Effect of alcohols on aqueous lysozyme-lysozyme interactions from static light-scattering measurements. Biophys. Chem. 107:289-298.
56. Livingstone, J. R., R. S. Spolar, and M. T. Record, Jr. 1991. Contribution to the thermodynamics of protein folding from the reduction in water-accessible nonpolar surface area. Biochemistry. 30:4237-4244.
57. Kini, R. M. 2002. Molecular moulds with multiple missions: functional sites in three-finger toxins. Clin. Exp. Pharmacol. Physiol. 29:815-822.