A phosphatidylserine binding site in factor Va C1 domain regulates both assembly and activity of the prothrombinase complex

Blood

Volumn 112, Issue 7, 2008, Pages 2795-2802

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

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

^b Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 10A; BLOOD CLOTTING FACTOR 5A; PHOSPHATIDYLSERINE; PROTHROMBIN; THROMBIN; AMINO ACID; BLOOD CLOTTING FACTOR 5; MUTANT PROTEIN; PROTHROMBINASE COMPLEX; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; GENE MUTATION; HEAVY CHAIN; PRIORITY JOURNAL; PROTEIN DOMAIN; STOICHIOMETRY; ANIMAL; BIOLOGICAL MODEL; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SOLUBILITY; STRUCTURE ACTIVITY RELATION;

AMINO ACIDS; ANIMALS; BINDING SITES; CERCOPITHECUS AETHIOPS; COS CELLS; DNA MUTATIONAL ANALYSIS; FACTOR V; FACTOR VA; FACTOR XA; HUMANS; MODELS, BIOLOGICAL; MUTANT PROTEINS; PHOSPHATIDYLSERINES; PROTEIN STRUCTURE, TERTIARY; PROTHROMBIN; RECOMBINANT PROTEINS; SOLUBILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 53449092993     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-02-138941     Document Type: Article

References (51)

1. Kane WH, Davie EW. Blood coagulation factors V and VIII: structural and functional similarities and their relationship to hemorrhagic and thrombotic disorders. Blood. 1988;71:539-555.
2. Mann KG, Kalafatis M. Factor V: Acombination of Dr. Jekyll and Mr. Hyde. Blood. 2003;101: 20-30.
3. Dahlback B. Human coagulation factor V purification and thrombin-catalyzed activation. J Clin Invest. 1980;66:583-591.
4. Nesheim ME, Taswell JB, Mann KG. The contribution of bovine Factor V and Factor Va to the activity of prothrombinase. J Biol Chem. 1979; 254:10952-10962.
5. Jenny RJ, Pittman DD, Toole JJ, et al. Gomplete cDNAand derived amino acid sequence of human factor V. Proc Natl Acad Sci U S A. 1987;84: 4846-4850.
6. Kane WH, Davie EW. Cloning of a cDNA coding for human factor V. a blood coagulation factor homologous to factor VIII and ceruloplasmin. Proc Natl Acad Sci U S A. 1986;83:6800-6804.
7. Kane WH, Majerus PW. Purification and characterization of human coagulation factor V. J Biol Chem. 1981;256:1002-1007.
8. Monkovic DD, Tracy PB. Activation of human factor V by factor Xa and thrombin. Biochemistry. 1990;29:1118-1128.
9. Esmon GT. The subunit structure of thrombinactivated factor V: isolation of activated factor V, separation of subunits, and reconstitution of biological activity. J Biol Chem. 1979;254:964-973.
10. Orte lTL. Quinn-Allen MA, Keller FG, Peterson JA, Larocca D, Kane WH. Localization of functionally important epitopes within the second City pe domain of coagulation factor V using recombinant chimeras. J Biol Chem. 1994;269:15898-15905.
11. Kim SW, Ortel TL, Quinn-Allen MA, et al. Partial glycosylation at asparagine-2181 of the second C-type domain of human factor V modulates assembly of the prothrombinase complex. Biochemistry. 1999;38:11448-11454.
12. Nicolaes GA, Villoutreix BO, Dahlback B. Partial glycosylation of Asn2181 in human factor V as a cause of molecular and functional heterogeneity: modulation of glycosylation efficiency by mutagenesis of the consensus sequence for N-linked glycosylation. Biochemistry. 1999;38: 13584-13591.
13. Koppaka V, Talbot WF, Zhai X, Lentz BR. Roles of factor Va heavy and light chains in protein and lipid rearrangements associated with the formation of a bovine factor Vamembrane complex. Biophys J. 1997;73:2638-2652.
14. Majumder R, Weinreb G, Zhai X, Lentz BR. Soluble phosphatidylserine triggers assembly in solution of a prothrombin-activating complex in the absence of a membrane surface. J Biol Chem. 2002;277:29765-29773.
15. Rosing J, Bakker HM, Thomassen MC, Hemker HC, Tans G. Characterization of two forms of human factor Va with different cofactor activities. J Biol Chem. 1993;268:21130-21136.
16. Majumder R, Weinreb GE, Lentz BR. Efficient thrombin generation requires molecular phosphatidylserine. not a membrane surface. Biochemistry. 2005;44:16998-17006.
17. Srivastava A, Quinn-Allen MA, Kim SW, Kane WH, Lentz BR. Soluble phosphatidylserine binds to a single identified site in the C2 domain of human factor Va. Biochemistry. 2001;40:8246-8255.
18. Kim SW, Quinn-Allen MA, Camp JT, et al. Identification of functionally important amino acid residues within the C2 domain of human factor V using alanine-scanning mutagenesis. Biochemistry. 2000;39:1951-1958.
19. Nicolaes GA, Villoutreix BO, Dahlback B. Mutations in a potential phospholipid binding loop in the C2 domain of factor V affecting the assembly of the prothrombinase complex. Blood Coagul Fibrinolysis. 2000;11:89-100.
20. 2064 in the factor Va C2 domain are required for high-affinity binding to phospholipid membranes but not for assembly of the prothrombinase complex. Biochemistry. 2004; 43:4385-4393.
21. Majumder R, Quinn-Allen MA, Kane WH, Lentz BR. The phosphatidylserine binding site of the factor Va C2 domain accounts for membrane binding but does not contribute to the assembly or activity of a human factor Xa-factor Va complex. Biochemistry. 2005;44:711-718.
22. Zhai X, Srivastava A, Drummond DC, Daleke D. Lentz BR. Phosphatidylserine binding alters the conformation and specifically enhances the cofactor activity of bovine factor V(a). Biochemistry. 2002;41:5675-5684.
23. Saleh M, Peng W, Quinn-Allen MA, et al. The factor V C1 domain is involved in membrane binding: identification of functionally important amino acid residues within the C1 domain of factor V using alanine scanning mutagenesis. Thromb Haemost. 2004;91:16-27.
24. Comfurius P. Zwaal R. The enzymatic synthesis of phosphatidylserine and purification by CM-cellulose column chromatography. Biochim Biophys Acta,. 1977;488:36-42.
25. Peng W, Quinn-Allen MA, Kane W. Mutation of hydrophobic residues in the factor Va C1 and C2 domains blocks membrane-dependent prothrombin activation. J Thromb Haemost. 2005;3:351-354.
26. Boskovic DS, Giles AR, Nesheim ME. 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. 1990;265:10497-10505.
27. Husten EJ, Esmon CT, Johnson AE. 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. 1987;262:12953-12961.
28. Haque ME, Das AR, Moulik SP. Behaviors of sodium deoxycholate (Nadc) and polyoxyethylene tert-octylphenyl ether (Triton X-100) at the air/water interface and in the bulk. J Phys Chem. 1995;99:14032-14038.
29. Weinreb GE, Mukhopadhyay K, Majumder R, Lentz BR. Cooperative roles of factor Va and phosphatidylserine-containing membranes as cofactors in prothrombin activation. J Biol Chem. 2003;278:5679-5684.
30. Krishnaswamy S, Church WR, Nesheim ME, Mann KG. Activation of human prothrombin by human prothrombinase: influence of factor Va on the reaction mechanism. J Biol Chem. 1987;262: 3291-3299.
31. Koppaka V, Wang J, Banerjee M, Lentz BR. Soluble phospholipids enhance factor Xacatalyzed prothrombin activation in solution. Biochemistry. 1996;35:7482-7491.
32. Banerjee M, Drummond DC, Srivastava A, Daleke D, Lentz BR. Specificity of the phospholipid regulatory sites on human Factor Xa. Biochemistry. 2002;41:7751-7762.
33. Banerjee M, Majumder R, Weinreb G, Wang J, Lentz BR. Role of procoagulant lipids in human prothrombin activation: 2. Soluble phosphatidylserine upregulates and directs factor X (a) to appropriate peptide bonds in prothrombin. Biochemistry. 2002;41:950-957.
34. Haque ME, Das AR, Moulik SP. Mixed micelles of sodium deoxycholate and polyoxyethylene sorbitan monooleate (Tween 80). J Colloid Interface Sci. 1999;217:1-7.
35. Majumder R, Wang J, Lentz BR. Effects of water soluble phosphotidylserine on bovine factor X (a): functional and structural changes plus dimerization. Biophys J. 2003;84:1238-1251.
36. Macedo-Ribeiro S, Bode W, Huber R, et al. Crystal structures of the membrane-binding C2 domain of human coagulation factor V Nature. 1999;402:434-439.
37. Lee CJ, Lin P, Chandrasekaran V, et al. Proposed structural models of human factor Va and prothrombinase. J Thromb Haemost. 2008;6:83-89.
38. Adams TE, Hockin MF, Mann KG, Everse SJ. The crystal structure of activated protein C-inactivated bovine factor Va: implications for cofactor function. Proc Natl Acad Sci U S A. 2004;101:8918-8923.
39. Wu JR, Zhou C, Majumder R, Powers DD, Weinreb G, Lentz BR. Role of procoagulant lipids in human prothrombin activation: 1. Prothrombin activation by factor X (a) in the absence of factor V 39 (a) and in the absence and presence of membranes. Biochemistry. 2002;41:935-949.
40. Cutsforth GA, Whitaker RN, Hermans J, Lentz BR. A new model to describe extrinsic protein binding to phospholipid membranes of varying composition: application to human coagulation proteins. Biochemistry. 1989;28:7453-7461.
41. Cutsforth GA, Koppaka V, Krishnaswamy S, Wu JR, Mann KG, Lentz BR. Insights into the complex association of bovine factor Va with acidiclipid-containing synthetic membranes. Biophys J. 1996;70:2938-2949.
42. Rand MD, Lock JB, van't Veer C, Gaffney DP, Mann KG. Blood clotting in minimally altered whole blood. Blood. 1996;88:3432-3445.
43. Kalafatis M, Beck DO. Identification of a binding site for blood coagulation factor Xa on the heavy chain of factor Va. amino acid residues 323-331 of factor V represent an interactive site for activated factor X. Biochemistry. 2002;41:12715-12728.
44. Kojima Y, Heeb MJ, Gale AJ, Hackeng TM, Griffin JH. Binding site for blood coagulation factor Xa involving residues 311-325 in factor Va. J Biol Chem. 1998;273:14900-14905.
45. Gale AJ, Yegneswaran S, Xu X, Pellequer J-L, Griffin JH. Characterization of factor Xa binding site on factor Va near the Arg-506 activated protein C cleavage site. J Biol Chem. 2007;282: 21848-21855.
46. Bakker HM, Tans G, Thomassen MC, et al. Functional properties of human factor Va lacking the Asp683-Arg709 domain of the heavy chain. J Biol Chem. 1994;269:20662-20667.
47. Steen M, Villoutreix BO, Norstrom EA, Yamazaki T, Dahlback B. Defining the factor Xa-binding site on factor Va by site-directed glycosylation. J Biol Chem. 2002;277:50022-50029.
48. Marcus A. Multicellular eicosanoid and other metabolic interactions of platelets and other cells. In: Colman RW, Hirsh J, MarderVJ, Salzman EW, eds. Hemostasis and Thrombosis: Basic Principles and Clinical Practice. 3rd ed. Philadelphia: Lippincott: 1994.
49. Sandberg H, BodeAP, Dombrose FA, Hoechli M, Lentz BR. Expression of coagulant activity in human platelets: release of membranous vesicles providing platelet factor 1 and platelet factor 3. Thromb Res. 1985;39:63-79.
50. Hamilton KK, Hattori R, Esmon CT, Sims PJ. Complement proteins C5b-9 induce vesiculation of the endothelial plasma membrane and expose catalytic surface for assembly of the prothrombinase enzyme complex. J Biol Chem. 1990;265:3809-3814.
51. Wang Y, Geer LY, Chappey C, Kans JA, Bryant SH. Cn3D: sequence and structure views for Entrez. Trends Biochem Sci. 2000;25:300-302.