Role of the γ-carboxyglutamic acid domain of activated factor X in the presence of calcium during inhibition by antithrombin-heparin

Journal of Thrombosis and Haemostasis

Volumn 2, Issue 7, 2004, Pages 1127-1134

  Whinna, Herbert C ^a   Lesesky, E B ^a   Monroe, D M ^a   High, K A ^b   Larson, P J ^b,c   Church, F C ^a  

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

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c BAYER CORPORATION   (United States)

Author keywords

Antithrombin; Calcium heparin; Factor Xa; Serpin

Indexed keywords

4 CARBOXYGLUTAMIC ACID; ANTITHROMBIN; ASPARTIC ACID; BLOOD CLOTTING FACTOR 10A; CALCIUM; EDETIC ACID; HEPARIN;

ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; GENE MUTATION; HUMAN; INHIBITION KINETICS; MEMBRANE BINDING; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; THEORY; WILD TYPE;

1-CARBOXYGLUTAMIC ACID; AMINO ACID SUBSTITUTION; ANTITHROMBINS; BINDING SITES; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR XA; HEPARIN; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

EID: 13244251027     PISSN: 15387933     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2004.00796.x     Document Type: Article

References (50)

1. Dählback B. Blood coagulation. Lancet 2000; 355 1627-32.
2. Whiteman T, Hassouna HL Hypercoagulable states. Hemat Oncol Clin N Am 2000; 14: 355-77.
3. Esmon CT. Protein C anticoagulant pathway and its role in controlling microvascular thrombosis and inflammation. Crit Care Med 2001; 29 (7 Suppl.): S48-S52.
4. Monroe DM, Hoffman M, Roberts HR. Platelets and thrombin generation. Arterioscler Thromb Vasc Biol 2002; 22: 1381-9.
5. Mann KG, Butenas S, Brummel K. The dynamics of thrombin formation. Arterioscler Thromb Vasc Biol 2003; 23: 17-25.
6. Mann KG, Nesheim ME, Church WR, Haley P, Krishnaswamy S. Surface-dependent reactions of the vitamin K-dependent enzyme complexes. Blood 1990; 76: 1-16.
7. Sunnerhagen M, Olah GA, Stenflo J, Forsen S, Drakenberg T, Trewhella J. The relative orientation of Gla and EGF domains in coagulation factor X is altered by Ca2+ binding to the first EGF domain. A combined NMR-small angle X-ray scattering study. Biochemistry 1996; 35: 11547-59.
8. Sunnerhagen M, Forsen S, Hoffren AM, Drakenberg T, Teleman O, Stenflo J. Structure of the Ca(2 +)-free Gla domain sheds fight on membrane binding of blood coagulation proteins. Nat Struct Biol 1995; 2: 504-9.
9. Mizuno H, Fujimoto Z, Atoda H, Morita T. Crystal structure of an anticoagulant protein in complex with the Gla domain of factor X. Proc Natl Acad Sci USA 2001; 98: 7230-4.
10. Gettins P, Petston PA, Austin TX, Olson ST. Serpins: Structure, Function and Biology, 1st edn. Landes, R.G. Publishers, Austin, TX, 1996: 202.
11. Chemistry and biology of serpins. In: Church FC, Cunningham DD, Ginsburg D, Hoffman M, Stone SR, Tollefsen DME, eds. Advances in Experimental Medical Biology. New York: Plenum Press, 1997: 358.
12. Rezaie AR. Calcium enhances heparin catalysis of the antithrombin factor Xa reaction by a template mechanism. Evidence that calcium alleviates Gla domain antagonism of heparin binding to factor Xa. J Biol Chem 1998; 273: 16824-7.
13. Rezaie AR, Olson ST. Calcium enhances heparin catalysis of the antithrombin-factor Xa reaction by promoting the assembly of an intermediate heparin-antithrombin-factor Xa bridging complex. Demonstration by rapid kinetics studies. Biochemistry 2000; 39 12083-90.
14. Rezaie AR, Yang L. Probing the molecular basis of factor Xa specificity by mutagenesis of the serpin, antithrombin. Biochim Biophys Acta 2001; 1528: 167-76.
15. Rezaie AR. Insight into the molecular basis of coagulation proteinase specificity by mutagenesis of the serpin antithrombin. Biochemistry 2002; 41: 12179-85.
16. Desai UR, Petitou M, Bjork I, Olson ST. Mechanism of heparin activation of antirhrombin: evidence for an induced-fit model of allosteric activation involving two inteaction sites. Biochemsitry 1998; 37: 13033-41.
17. Gettins PGW, Fan B, Crews BC, Turko IV, Olson ST, Streusand VJ. Transmission of conformational change from the heparin binding site to the reactive center of antithrombin. Biochemistry 1993; 32 8385-9.
18. Olson ST, Srinivasan KR, Bjork I, Shore JD. Binding of high affinity heparin to antithrombin-III. J Biol Chem 1981; 256: 11073-9.
19. Olson ST. Heparin and ionic strength-dependent conversion of antithrombin III from an inhibitor to a substrate of a-thrombin. J Biol Chem 1984; 260: 10153-60.
20. Olson ST, Shore JD. Transient kinetics of heparin-catalyzed protease inactivation by antithrombin III. The reaction step limiting heparin turnover in thrombin neutralization. J Biol Chem 1986; 261: 13151-9.
21. Olson ST. Transient kinetics of heparin-catalyzed protease inactivation by antithrombin III. Linkage of protease-inhibitor heparin interactions in the reaction with thrombin. J Biol Chem 1988; 263: 1698-708.
22. Olson ST, Bjork I, Sheffer R, Craig PA, Shore JD, Choay J. Role of the antithrombin-binding pentasaccharide in heparin acceleration of antithrombin protemase reactions. Resolution of the antithrombin conformational change contribution to heparin rate enhancement. J Biol Chem 1992; 267: 12528-38.
23. Rezaie AR. Identification of basic residues in the heparin-binding exosite of factor Xa critical for heparin and factor Va binding. J Biol Chem 2000; 275: 3320-7.
24. Larson PJ, Camire RM, Wong D, Fasano NC, Monroe DM, Tracy PB, High KA. Structure/function analyses of recombinant variants of human factor Xa: factor Xa incorporation into prothrombinase on the thrombin-activated platelet surface is not mimicked by synthetic phospholipid vesicles. Biochemistry 1998; 37: 5029-38.
25. Griffith MJ, Noyes CM, Church FC. Reactive site peptide structural similarity between heparin cofactor II and antithrombin III. J Biol Chem 1985; 260: 2218-25.
26. Rudolph AE, Mullane MP, Porche-Sorbet R, Milefich JP. Expression, purification, and characterization of recombinant human factor X. Protein Expr Purif 1997; 10: 373-8.
27. Ciaccia AV, Willemze AJ, Church FC. Heparin promotes proteolytic inactivation by thrombin of a reactive site mutant (L444R) of recombinant heparin cofactor II. J Biol Chem 1997; 272: 888-93.
28. Bauman SJ, Church FC. Enhancement of heparin cofactor II anti-coagulant activity. J Biol Chem 1999; 274: 34556-65.
29. Mitchell JW, Church FC. Aspartic acid residues 72 and 75 and tyrosine-sulfate 73 of heparin cofactor II promote intramolecular interactions during glycosaminoglycan binding and thrombin inhibition. J Biol Chem 2002; 277: 19823-30.
30. Mather T, Oganessyan V, Hof P, Huber R, Foundling S, Esmon C, Bode W. The 2.8 A crystal structure of Gla-domainless activated protein C. EMBO J 1996; 15: 6822-31.
31. Banner DW, D'Arcy A, Chene C, Winkler FK, Guha A, Konigsberg WH, Nemerson Y, Kirchhofer D. The crystal structure of the complex of blood coagulation factor VIIa with soluble tissue factor. Nature 1996; 380: 41-6.
32. Brandstetter H, Bauer M, Huber R, Lollar P, Bode W. X-ray structure of clotting factor Ixa: active site and module structure related to Xase activity and hemophilia B. Proc Natl Acad Sci USA 1995; 92: 9796-800.
33. Pike AC, Brzozowski AM, Roberts SM, Olsen OH, Persson E. Structure of human factor VIIa and its implications for the triggering of blood coagulation. Proc Natl Acad Sci USA 1999; 96: 8925-30.
34. Kamata K, Kawamoto H, Honma T, Iwama T, Kim SH. Structural basis for chemical inhibition of human blood coagulation factor Xa. Proc Natl Acad Sci USA 1998; 95: 6630-5.
35. Wang SX, Hur E, Sousa CA, Brinen L, Shvka EJ, Fletterick RJ. The extended interactions and Gla domain of blood coagulation factor Xa. Biochemistry 2003; 42: 7959-66.
36. Valcarce C, Selander-Sunnerhagen M, Tamlitz AM, Drakenberg T, Bjork I, Stenflo J. Calcium affinity of the NH2-terminal epidermal growth factor-like module of factor X. Effect of the gamma-carboxyglutamic acid-containing module. J Biol Chem 1993; 268: 26673-8.
37. Colpitts TL, Prorok M, Castellino FJ. Binding of calcium to individual gamma-carboxyglutamic acid residues of human protein C. Biochemistry 1995; 34: 2424-30.
38. Christiansen WT, Tulinsky A, Castellino FJ. Functions of individual gamma-carboxyglutamic acid (Gla) residues of human protein c. Determination of functionally nonessential Gla residues and correlations with their mode of binding to calcium. Biochemistry 1994; 33: 14993-5000.
39. Pinotti M, Marchetti G, Baroni M, Cinotti F, Morfini M, Bernardi F. Reduced activation of the Gla19Ala FX variant via the extrinsic coagulation pathway results in symptomatic CRMred FX deficiency. Thromb Haemost 2002; 88: 236-41.
40. Hirsh J, Lee AY. How we diagnose and treat deep vein thrombosis. Blood 2002; 99: 3102-10.
41. Thomas DP, Roberts HR. Hypercoagulability in venous and arterial thrombosis. Ann Intern Med 1997; 126: 639-44.
42. Weitz JI. Low-molecular-weight heparins. N Engl J Med 1997; 337: 688-98.
43. Ellis V, Scully MF, Kakkar W. The acceleration of the inhibition of platelet prothrombinase complex by heparin. Biochem J 1986; 233: 161-5.
44. Ellis V, Scully MF, Kakkar W. The relative molecular mass dependence of the anti-factor Xa properties of heparin. Biochem J 1986; 238: 329-33.
45. Koopman MM, Prandoni P, Piovella F, Ockelford PA, Brandjes DP, van der Meer J, Gallus AS, Simonneau G, Chesterman CH, Prins MH. Treatment of venous thrombosis with intravenous unfractionated heparin administered in the hospital as compared with subcutaneous low-molecular-weight heparin administered at home. The Tasman Study Group. N Engl J Med 1996; 334: 682-7.
46. Lee AY, Hirsh J. Diagnosis and treatment of venous thromboembolism. Annu Rev Med 2002; 53: 15-33.
47. Ockefford PA, Carter CJ, Mitchell L, Hirsh J. Discordance between the anti-Xa activity and the antithrombotic activity in an ultra-low molecular weight heparin fraction. Thromb Res 1982; 28 401-9.
48. Owen BA, Owen WG. Interaction of factor Xa with heparin does not contribute to the inhibition of factor Xa by antithrombin III-heparin. Biochemistry 1990; 29: 9412-7.
49. Ridker PM, Goldhaber SZ, Danielson E, Rosenberg Y, Eby CS, Deitcher SR, Cushman M, Moll S, Kessler CM, Elliot CG, Paulson R, Wong T, Bauer KA, Schawartz BA, Miletich JP, Bounameaux H, Glynn RJ. Long-term, low-intensity warfarin therapy for the prevention of recurrent venous thromboembolism. N Engl J Med 2003; 348: 1425-34.
50. Kovacs MJ, Rodger M, Anderson DR, Morrow B, Kells G, Kovacs J, Boyle E, Wells PS. Comparison of 10-mg and 5-mg warfarin initiation nomograms together with low-molecular-weight heparin for outpatient treatment of acute venous thromboembolism. A randomized, double-blind, controlled trial. Ann Intern Med 2003; 138: 714-9.