Phosphatidylserine and FVa regulate FXa structure

Biochemical Journal

Volumn 459, Issue 1, 2014, Pages 229-239

  Srivasatava, Kinshuk Raj ^a   Majumder, Rinku ^a   Kane, William H ^b   Quinn Allen, Mary Ann ^c   Lentz, Barry R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY HEALTH SYSTEM   (United States)

Author keywords

Conformational regulation; Factor Va; Factor Xa; Fluorescence resonance energy transfer (FRET); Phosphatidylserine; Prothrombinase complex

Indexed keywords

4 CARBOXYGLUTAMIC ACID; BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 5A; EPIDERMAL GROWTH FACTOR; PHOSPHATIDYLSERINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SCINTILLATION COUNTING; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY;

ALLOSTERIC REGULATION; ANIMALS; CELL LINE; CRICETINAE; FACTOR VA; FACTOR XA; HUMANS; PHOSPHATIDYLSERINES; PROTEIN BINDING; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84896121753     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131099     Document Type: Article

References (38)

1. Fenton, 2nd, J. W. (1986) Thrombin. Ann. N.Y. Acad. Sci. 485, 5-15
2. Nesheim, M. E., Kettner, C., Shaw, E. and Mann, K. G. (1981) Cofactor dependence of factor Xa incorporation into the prothrombinase complex. J. Biol. Chem. 256, 6537-6540 (Pubitemid 11010828)
3. Rosing, J., Tans, G., Govers-Riemslag, J., Zwaal, R. and Hemker, H. (1980) The role of phospholipids and factor Va in the prothrombinase complex. J. Biol. Chem. 255, 274-283 (Pubitemid 10146055)
4. Bevers, E. M., Comfurius, P. and Zwaal, R. F. (1983) Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta 736, 57-66 (Pubitemid 14201823)
5. Jones, M. E., Lentz, B. R., Dombrose, F. A. and Sandberg, H. (1985) Comparison of the abilities of synthetic and platelet-derived membranes to enhance thrombin formation. Thromb. Res. 39, 711-724 (Pubitemid 16169731)
6. Kim, S. W., Ortel, T. L., Quinn-Allen, M. A., Yoo, L., Worfolk, L., Zhai, X., Lentz, B. R. and Kane, W. H. (1999) Partial glycosylation at asparagine-2181 of the second C-type domain of human factor V modulates assembly of the prothrombinase complex. Biochemistry 38, 11448-11454
7. Banerjee, M., Drummond, D. C., Srivastava, A., Daleke, D. and Lentz, B. R. (2002) Specificity of soluble phospholipid binding sites on human factor Xa. Biochemistry 41, 7751-7762 (Pubitemid 34627802)
8. Banerjee, M., Majumder, R., Weinreb, G., Wang, J. and Lentz, B. R. (2002) Role of procoagulant lipids in human prothrombin activation. 2. Soluble phosphatidylserine upregulates and directs factor X(a) to appropriate peptide bonds in prothrombin. Biochemistry 41, 950-957 (Pubitemid 34061997)
9. Koppaka, V., Wang, J., Banerjee, M. and Lentz, B. R. (1996) Soluble phospholipids enhance factor Xa-catalyzed prothrombin activation in solution. Biochemistry 35, 7482-7491
10. Majumder, R., Quinn-Allen, M. A., Kane, W. H. and Lentz, B. R. (2008) A phosphatidylserine binding site in factor Va C1 domain regulates both assembly and activity of the prothrombinase complex. Blood 112, 2795-2802
11. Majumder, R., Weinreb, G. and Lentz, B. R. (2005) Efficient thrombin generation requires molecular phosphatidylserine, not a membrane surface. Biochemistry 44, 16998-17006 (Pubitemid 43007228)
12. Srivastava, A., Wang, J., Majumder, R., Rezaie, A. R., Stenflo, J., Esmon, C. T. and Lentz, B. R. (2002) Localization of phosphatidylserine binding sites to structural domains of factor Xa. J. Biol. Chem. 277, 1855-1863 (Pubitemid 34968759)
13. Wu, J. R., Zhou, C., Majumder, R., Powers, D. D., Weinreb, G. and Lentz, B. R. (2002) Role of procoagulant lipids in human prothrombin activation. 1. Prothrombin activation by factor X(a) in the absence of factor V(a) and in the absence and presence of membranes. Biochemistry 41, 935-949 (Pubitemid 34061996)
14. Majumder, R., Wang, J. and Lentz, B. R. (2003) Effects of water soluble phosphotidylserine on bovine factor Xa: functional and structural changes plus dimerization. Biophys. J. 84, 1238-1251 (Pubitemid 36133446)
15. Chen, Q. and Lentz, B. R. (1997) Fluorescence resonance energy transfer study of shape changes in membrane-bound bovine prothrombin and meizothrombin. Biochemistry 36, 4701-4711 (Pubitemid 27180321)
16. Di Scipio, R. G., Hermodson, M. A., Yates, S. G. and Davie, E. W. (1977) A comparison of human prothrombin, factor IX (Christmas factor), factor X (Stuart factor), and protein S. Biochemistry 16, 698-706 (Pubitemid 8047809)
17. Venkateswarlu, D., Perera, L., Darden, T. and Pedersen, L. G. (2002) Structure and dynamics of zymogen human blood coagulation factor X. Biophys. J. 82, 1190-1206 (Pubitemid 34204743)
18. Husten, E. J., Esmon, C. T. and Johnson, A. E. (1987) The active site of blood coagulation factor Xa: its distance from the phospholipid surface and its conformational sensitivity to components of the prothrombinase complex. J. Biol. Chem. 262, 12953-12961 (Pubitemid 18001238)
19. Mutucumarana, V. P., Duffy, E. J., Lollar, P. and Johnson, A. E. (1992) The active site of factor IXa is located far above the membrane surface and its conformation is altered upon association with factor VIIIa: a fluorescence study. J. Biol. Chem. 267, 17012-17021
20. Qureshi, S. H., Yang, L., Yegneswaran, S. and Rezaie, A. R. (2007) FRET studies with factor X mutants provide insight into the topography of the membrane-bound factor X/Xa. Biochem. J. 407, 427-433 (Pubitemid 350058476)
21. Lee, C. J., Lin, P., Chandrasekaran, V., Duke, R. E., Everse, S. J., Perera, L. and Pedersen, L. G. (2008) Proposed structural models of human factor Va and prothrombinase. J. Thromb. Haemost. 6, 83-89
22. Huang, M., Rigby, A. C., Morelli, X., Grant, M. A., Huang, G., Furie, B., Seaton, B. and Furie, B. C. (2003) Structural basis of membrane binding by Gla domains of vitamin K-dependent proteins. Nat. Struct. Biol. 10, 751-756 (Pubitemid 37052415)
23. Chattopadhyay, R., Iacob, R., Sen, S., Majumder, R., Tomer, K. B. and Lentz, B. R. (2009) Functional and structural characterization of factor Xa dimer in solution. Biophys. J. 96, 974-986
24. 2Cl. Biochemistry 27, 6633-6639
25. Chen, P. S., Toribara, T. Y. and Huber, W. (1956) Microdetermination of phosphorus. Anal. Chem. 28, 1756-1758
26. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy (2nd edn), Kluwer Academic/Plenum Publishers, New York
27. Prazeres, T. J., Fedorov, A., Barbosa, S. P., Martinho, J. M. and Berberan-Santos, M. N. (2008) Accurate determination of the limiting anisotropy of rhodamine 101: implications for its use as a fluorescence polarization standard. J. Phys. Chem. A 112, 5034-5039
28. Zorrilla, S., Rivas, G., Acuna, A. U. and Lillo, M. P. (2004) Protein self-association in crowded protein solutions: a time-resolved fluorescence polarization study. Protein Sci. 13, 2960-2969 (Pubitemid 39431258)
29. Dale, R. E., Eisinger, J. and Blumberg, W. E. (1979) The orientational freedom of molecular probes: the orientation factor in intramolecular energy transfer. Biophys. J. 26, 161-193
30. Majumder, R., Weinreb, G., Zhai, X. and Lentz, B. R. (2002) Soluble phosphatidylserine triggers assembly in solution of a prothrombin-activating complex in the absence of a membrane surface. J. Biol. Chem. 277, 29765-29773
31. Koklic, T., Majumder, R., Weinreb, G. E. and Lentz, B. R. (2009) Factor Xa binding to phosphatidylserine-containing membranes produces an inactive membrane-bound dimer. Biophys. J. 97, 2232-2241
32. Majumder, R., Koklic, T., Rezaie, A. R. and Lentz, B. R. (2013) Phosphatidylserine-induced factor Xa dimerization and binding to factor Va are competing processes in solution. Biochemistry 52, 143-151
33. Nesheim, M. E. and Mann, K. G. (1983) The kinetics and cofactor dependence of the two cleavages involved in prothrombin activation. J. Biol. Chem. 258, 5386-5391 (Pubitemid 13096462)
34. Boskovic, D. S., Bajzar, L. S. and Nesheim, M. E. (2001) Channeling during prothrombin activation. J. Biol. Chem. 276, 28686-28693
35. Weinreb, G. E., Mukhopadhyay, K., Majumder, R. and Lentz, B. R. (2003) Cooperative roles of factor V(a) and phosphatidylserine-containing membranes as cofactors in prothrombin activation. J. Biol. Chem. 278, 5679-5684 (Pubitemid 36800811)
36. Wood, J. P., Silveira, J. R., Maille, N. M., Haynes, L. M. and Tracy, P. B. (2011) Prothrombin activation on the activated platelet surface optimizes expression of procoagulant activity. Blood 117, 1710-1718
37. Boskovic, D. S., Giles, A. R. and 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
38. 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