Beta2-glycoprotein I binds thrombin via exosite I and exosite II: Anti-β2-glycoprotein I antibodies potentiate the inhibitory effect of β2-glycoprotein I on thrombin-mediated factor XIa generation

Arthritis and Rheumatism

Volumn 56, Issue 2, 2007, Pages 605-613

  Rahgozar, Soheila ^a   Yang, Qiuxia ^a   Giannakopoulos, Bill ^a   Yan, Xiaokai ^a   Miyakis, Spiros ^a   Krilis, Steven A ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BETA2 GLYCOPROTEIN 1; BETA2 GLYCOPROTEIN 1 ANTIBODY; BLOOD CLOTTING FACTOR 11; BLOOD CLOTTING FACTOR 11A; MONOCLONAL ANTIBODY; MUTANT PROTEIN; OLIGONUCLEOTIDE; THROMBIN; ANION; ANTIBODY; FACTOR IIA; PHOSPHOLIPID ANTIBODY; PROTHROMBIN; UNCLASSIFIED DRUG;

ANTIBODY DETECTION; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; BLOOD CLOTTING; ENZYME SUBSTRATE COMPLEX; EXOSITE I; EXOSITE II; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; BINDING SITE; CHEMISTRY; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

ANIMALS; ANIONS; ANTIBODIES; ANTIBODIES, ANTIPHOSPHOLIPID; ANTIBODIES, MONOCLONAL; ANTIPHOSPHOLIPID SYNDROME; BETA 2-GLYCOPROTEIN I; BINDING SITES; FACTOR XIA; HUMANS; MICE; MUTATION; OLIGONUCLEOTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTHROMBIN; THROMBIN;

EID: 33847055815     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.22367     Document Type: Article

References (47)

1. McNeil HP, Chesterman CN, Krilis S. Immunology and clinical importance of antiphospholipid antibodies. In: Dixon FJ. editor. Advances in immunology. San Diego: Academic Press; 1991. p. 193-280.
2. Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006;4:295-306.
3. Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, et al, for the Euro-Phospholipid Project Group. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum 2002;46:1019-27.
4. McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. Antiphospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: β2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci U S A 1990;87:4120-4.
5. Matsuura E, Igarashi Y, Fujimoto M. Ichikawa K, Koike T. Anticardiolipin cofactor(s) and differential diagnosis of autoimmune disease. Lancet 1990;336:177-8.
6. Galli M, Comfurius P, Maassen C, Hemker HC, de Baets MH, van Breda-Vriesman PJ, et al. Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet 1990;335:1544-7.
7. Jankowski M, Vreys I, Wittevrongel C, Boon D, Vermylen J, Hoylaerts MF, et al. Thrombogenicity of β2-glycoprotein I-dependent antiphospholipid antibodies in a photochemically induced thrombosis model in the hamster. Blood 2003;101:157-62.
8. Fischetti F, Durigutto P, Pellis V, Debeus A. Macor P, Bulla R, et al. Thrombus formation induced by antibodies to β2-glycoprotein I is complement dependent and requires a priming factor. Blood 2005;106:2340-6.
9. Miyakis S, Giannakopoulos B, Krilis SA. β2 glycoprotein I-function in health and disease. Thromb Res 2004;114:335-46.
10. Reddel S, Krilis S. The anti-phospholipid syndrome. In: Bona C, editor. The molecular pathology of autoimmune diseases. New York: Taylor & Francis; 2002. p. 325-52.
11. Hunt JE, Simpson RJ, Krilis SA. Identification of a region of β 2-glycoprotein I critical for lipid binding and anti-cardiolipin antibody cofactor activity. Proc Natl Acad Sci U S A 1993;90:2141-5.
12. Shi T, Giannakopoulos B, Iverson GM, Cockerill KA, Linnik MD, Krilis SA. Domain V of β 2 glycoprotein I binds factor XI/XIa and is cleaved at Lys317-Thr318. J Biol Chem 2005;280:907-12.
13. Ohkura N, Hagihara Y, Yoshimura T, Goto Y, Kato H. Plasmin can reduce the function of human β2 glycoprotein I by cleaving domain V into a nicked form. Blood 1998;91:4173-9.
14. Schousboe I. β2-Glycoprotein 1: a plasma inhibitor of the contact activation of the intrinsic blood coagulation pathway. Blood 1985;66:1086-91.
15. Shi T, Iverson GM, Qi JC, Cockerill KA, Linnik MD, Konecny P, et al. β2-Glycoprotein I binds factor XI and inhibits its activation by thrombin and factor XIIa: loss of inhibition by clipped β2-glycoprotein I. Proc Natl Acad Sci U S A 2004;101:3939-44.
16. Lane DA, Philippou H, Huntington JA. Directing thrombin. Blood 2005;106:2605-12.
17. Miesbach W, Matthias T, Scharrer I. Identification of thrombin antibodies in patients with antiphospholipid syndrome. Ann N Y Acad Sci 2005;1050:250-6.
18. Hwang KK, Grossman JM, Visvanathan S, Chukwuocha RU, Woods VL Jr, Le DT, et al. Identification of anti-thrombin antibodies in the antiphospholipid syndrome that interfere with the inactivation of thrombin by antithrombin. J Immunol 2001;167:7192-8.
19. Reddel SW, Wang YX, Sheng YH, Krilis SA. Epitope studies with anti-β2-glycoprotein I antibodies from autoantibody and immunized sources. J Autoimmun 2000;15:91-6.
20. Guerin J, Sheng Y, Reddel S, Iverson GM, Chapman MG, Krilis SA. Heparin inhibits the binding of β2-glycoprotein I to phospholipids and promotes the plasmin-mediated inactivation of this blood protein. J Biol Chem 2002;277:2644-9.
21. 2-glycoprotein I and prothrombin. Clin Exp Immunol 2001;124:502-8.
22. Sheng Y, Sali A, Herzog H, Lahnstein J, Krilis SA. Site-directed mutagenesis of recombinant human β2-glycoprotein I identifies a cluster of lysine residues that are critical for phospholipid binding and anti-cardiolipin antibody activity. J Immunol 1996;157:3744-51.
23. Lutters BC, Derksen RH, Tekelenburg WL, Lenting PJ, Arnout J, de Groot PG. Dimers of β2-glycoprotein I increase platelet deposition to collagen via interaction with phospholipids and the apolipoprotein E receptor 2′. J Biol Chem 2003;278:33831-8.
24. Yasuda S, Atsumi T, Ieko M, Matsuura E, Kobayashi K. Inagaki J, et al. Nicked β2-glycoprotein I: a marker of cerebral infarct and a novel role in the negative feedback pathway of extrinsic fibrinolysis. Blood 2004;103:3766-72.
25. Mann KG, Butenas S, Brummel K. The dynamics of thrombin formation. Arterioscler Thromb Vasc Biol 2003;23:17-25.
26. Lisman T, Weeterings C, de Groot PG. Platelet aggregation: involvement of thrombin and fibrin(ogen). Front Biosci 2005;10:2504-17.
27. Esmon CT. Regulation of blood coagulation. Biochim Biophys Acta 2000;1477:349-60.
28. Huntington JA. Molecular recognition mechanisms of thrombin. J Thromb Haemost 2005;3:1861-72.
29. Enrico DC. Thrombin interactions. Chest 2003;124:11-7S.
30. Celikel R, McClintock RA, Roberts JR, Mendolicchio GL, Ware J, Varughese KI, et al. Modulation of α-thrombin function by distinct interactions with platelet glycoprotein Ibα. Science 2003;301:218-21.
31. Ye J, Liu LW, Esmon CT, Johnson AE. The fifth and sixth growth factor-like domains of thrombomodulin bind to the anion-binding exosite of thrombin and alter its specificity. J Biol Chem 1992;267:11023-8.
32. 2+ dependence of protein C activation. J Biol Chem 1994;269:11807-12.
33. Walsh PN. Platelets and factor XI bypass the contact system of blood coagulation. Thromb Haemost 1999;82:234-42.
34. Baglia FA, Badellino KO, Li CQ, Lopez JA, Walsh PN. Factor XI binding to the platelet glycoprotein Ib-IX-V complex promotes factor XI activation by thrombin. J Biol Chem 2002;277:1662-8.
35. Baglia FA, Shrimpton CN, Emsley J, Kitagawa K, Ruggeri ZM, Lopez JA, et al. Factor XI interacts with the leucine-rich repeats of glycoprotein Ibα on the activated platelet. J Biol Chem 2004;279:49323-9.
36. Shi T, Giannakopoulos B, Yan X, Yu P, Berndt MC, Andrews RC, et al. Anti-β2-glycoprotein I antibodies in complex with β2-glycoprotein I can activate platelets in a dysregulated manner via glycoprotein Ib-IX-V. Arthritis Rheum 2006;54:2558-67.
37. Pennings MT, Derksen RH, van Lummel M, Adelmeijer J, Lisman T, de Groot PG. Platelet adhesion to dimeric β2-glycoprotein-I under conditions of flow is mediated by glycoprotein Ibα [abstract]. J Thromb Haemost 2005;3 Suppl 1:Abstract OR256.
38. Yun TH, Baglia FA, Myles T, Navaneetham D, Lopez JA, Walsh PN, et al. Thrombin activation of factor XI on activated platelets requires the interaction of factor XI and platelet glycoprotein Ib α with thrombin anion-binding exosites I and II. respectively. J Biol Chem 2003;278:48112-9.
39. Stricker RB, Lane PK, Leffert PD, Rodger GM, Shuman MA, Corash L. Development of antithrombin antibodies following surgery in patients with prosthetic cardiac valves. Blood 1988;72:1375-80.
40. Zehnder JL, Leung LL. Development of antibodies to thrombin and factor V with recurrent bleeding in a patient exposed to topical bovine thrombin. Blood 1990;76:2011-6.
41. De Laat B, Derksen RH, Urbanus RT, de Groot PG. IgG antibodies that recognize epitope Gly40-Arg43 in domain I of β2-glycoprotein I cause LAC, and their presence correlates strongly with thrombosis. Blood 2005;105:1540-5.
42. Iverson GM, Reddel S, Victoria EJ, Cockerill KA, Wang YX, Marti-Renom MA, et al. Use of single point mutations in domain I of β2-glycoprotein I to determine fine antigenic specificity of antiphospholipid autoantibodies. J Immunol 2002;169:7097-103.
43. 2-glycoprotein I antibodies in children with atopic dermatitis. Int Immunol 2002;14:823-30.
44. Arvieux J, Renaudineau Y, Mane I, Perraut R, Krilis SA, Youinou P. Distinguishing features of anti-β2 glycoprotein I antibodies between patients with leprosy and the antiphospholipid syndrome. Thromb Haemost 2002;87:599-605.
45. Sheng Y, Kandiah DA, Krilis SA. Anti-β 2-glycoprotein I autoantibodies from patients with the "antiphospholipid" syndrome bind to β2-glycoprotein I with low affinity: dimerization of β2-glycoprotein I induces a significant increase in anti-β2- glycoprotein I antibody affinity. J Immunol 1998;161:2038-43.
46. Bas de Laat H, Derksen RH, de Groot PG. β2-glycoprotein I, the playmaker of the antiphospholipid syndrome. Clin Immunol 2004;112:161-8.
47. Urbanus RT, de Laat HB, de Groot PG, Derksen RH. Prolonged bleeding time and lupus anticoagulant: a second paradox in the antiphospholipid syndrome. Arthritis Rheum 2004;50:3605-9.