Beta2-glycoprotein I protects thrombin from inhibition by heparin cofactor II: Potentiation of this effect in the presence of anti-β2-glycoprotein I autoantibodies

Arthritis and Rheumatism

Volumn 58, Issue 4, 2008, Pages 1146-1155

  Rahgozar, Soheila ^a   Giannakopoulos, Bill ^a   Yan, Xiaokai ^a   Wei, Jiewei ^a   Jian, Cheng Qi ^a   Gemmell, Rosalie ^b   Krilis, Steven A ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b ST GEORGE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; BETA2 GLYCOPROTEIN 1; BETA2 GLYCOPROTEIN 1 ANTIBODY; CHROMOGENIC SUBSTRATE; HEPARIN; HEPARIN COFACTOR II; IMMUNOGLOBULIN G; LYSINE; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; THREONINE; THROMBIN; ANTICOAGULANT AGENT;

ANIMAL CELL; ANTIPHOSPHOLIPID SYNDROME; ARTICLE; BLOOD CLOTTING; CONTROLLED STUDY; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTECTION; PROTEIN DEGRADATION; REGULATORY MECHANISM; THROMBOCYTE FUNCTION; THROMBOGENICITY; THROMBOSIS; ADULT; BLOOD; FEMALE; IMMUNOLOGY; MALE; PHYSIOLOGY;

ADULT; ANTICOAGULANTS; AUTOANTIBODIES; BETA 2-GLYCOPROTEIN I; BLOOD COAGULATION; FEMALE; HEPARIN; HEPARIN COFACTOR II; HUMANS; MALE; THROMBIN;

EID: 42449145853     PISSN: 00043591     EISSN: None     Source Type: Journal    
DOI: 10.1002/art.23387     Document Type: Article

References (50)

1. 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.
2. 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.
3. Matsuura E, Igarashi Y, Fujimoto M, Ichikawa K, Koike T. Anticardiolipin cofactor(s) and differential diagnosis of auto-immune disease. Lancet 1990;336:177-8.
4. 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.
5. Giannakopoulos B, Passam F, Rahgozar S, Krilis SA. Current concepts on the pathogenesis of the antiphospholipid syndrome. Blood 2007;109:422-30.
6. Danowski A, Kickler TS, Petri M. Anti-β2-glycoprotein I: prevalence, clinical correlations, and importance of persistent positivity in patients with antiphospholipid syndrome and systemic lupus erythematosus. J Rheumatol 2006;33:1775-9.
7. 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.
8. Kato H, Enjyoji K. Amino acid sequence and location of the disulfide bonds in bovine β2 glycoprotein I: the presence of five Sushi domains. Biochemistry 1991;30:11687-94.
9. 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.
10. Mehdi H, Naqvi A, Kamboh MI. A hydrophobic sequence at position 313-316 (Leu-Ala-Phe-Trp) in the fifth domain of apolipoprotein H (β2-glycoprotein I) is crucial for cardiolipin binding. Eur J Biochem 2000;267:1770-6.
11. Hunt JE, Simpson RJ, Krilis SA. Identification of a region of β2-glycoprotein I critical for lipid binding and anti-cardiolipin antibody cofactor activity. Proc Natl Acad Sci U S A 1993;90:2141-5.
12. 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.
13. Shi T, Giannakopoulos B, Iverson GM, Cockerill KA, Linnik MD, Krilis SA. Domain V of β2-glycoprotein I binds factor XI/XIa and is cleaved at Lys317-Thr318. J Biol Chem 2005;280:907-12.
14. 2-glycoprotein I on thrombin-mediated factor XIa generation. Arthritis Rheum 2007;56:605-13.
15. 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.
16. 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.
17. 2-glycoprotein I can activate platelets in a dysregulated manner via glycoprotein Ib-IX-V. Arthritis Rheum 2006;54:2558-67.
18. 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:OR256.
19. 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.
20. Bancsi LF, van der Linden IK, Bertina RM. Beta 2-glycoprotein I deficiency and the risk of thrombosis. Thromb Haemost 1992;67:649-53.
21. Yasuda S, Tsutsumi A, Chiba H, Yanai H, Miyoshi Y, Takeuchi R, et al. Beta(2)-glycoprotein I deficiency: prevalence, genetic background and effects on plasma lipoprotein metabolism and hemostasis. Atherosclerosis 2000;152:337-46.
22. Nimpf J, Wurm H, Kostner GM. Interaction of β2-glycoprotein-I with human blood platelets: influence upon the ADP-induced aggregation. Thromb Haemost 1985;54:397-401.
23. Shi T, Iverson GM, Qi JC, Cockerill KA, Linnik MD, Konecny P, et al. Beta 2-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.
24. Mori T, Takeya H, Nishioka J, Gabazza EC, Suzuki K. Beta 2-glycoprotein I modulates the anticoagulant activity of activated protein C on the phospholipid surface. Thromb Haemost 1996;75:49-55.
25. Wolberg AS. Thrombin generation and fibrin clot structure. Blood Rev 2007;21:131-42.
26. Esmon CT. The protein C pathway. Chest 2003;124 (3 Suppl): 26S-32S.
27. Huntington JA. Mechanisms of glycosaminoglycan activation of the serpins in hemostasis. J Thromb Haemost 2003;1:1535-49.
28. He L, Vicente CP, Westrick RJ, Eitzman DT, Tollefsen DM. Heparin cofactor II inhibits arterial thrombosis after endothelial injury. J Clin Invest 2002;109:213-9.
29. Tollefsen DM. Heparin cofactor II deficiency. Arch Pathol Lab Med 2002;126:1394-400.
30. Aihara K, Azuma H, Takamori N, Kanagawa Y, Akaike M, Fujimura M, et al. Heparin cofactor II is a novel protective factor against carotid atherosclerosis in elderly individuals. Circulation 2004;109:2761-5.
31. Takamori N, Azuma H, Kato M, Hashizume S, Aihara K, Akaike M, et al. High plasma heparin cofactor II activity is associated with reduced incidence of in-stent restenosis after percutaneous coronary intervention. Circulation 2004;109:481-6.
32. Kanagawa Y, Shigekiyo T, Aihara K, Akaike M, Azuma H, Matsumoto T. Molecular mechanism of type I congenital heparin cofactor (HC) II deficiency caused by a missense mutation at reactive P2 site: HC II Tokushima. Thromb Haemost 2001;85:101-7.
33. Aihara K, Azuma H, Akaike M, Ikeda Y, Sata M, Takamori N, et al. Strain-dependent embryonic lethality and exaggerated vascular remodeling in heparin cofactor II-deficient mice. J Clin Invest 2007;117:1514-26.
34. 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.
35. Sheng Y, Hanly JG, Reddel SW, Kouts S, Guerin J, Koike T, et al. Detection of 'antiphospholipid' antibodies: a single chromogenic assay of thrombin generation sensitively detects lupus anticoagulants, anticardiolipin antibodies, plus antibodies binding β(2)-glycoprotein I and prothrombin. Clin Exp Immunol 2001;124:502-8.
36. Sheng Y, Kandiah DA, Krilis SA. Anti-β2-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.
37. Costa JM, Fiessinger JN, Capron L, Aiach M. Partial characterization of an autoantibody recognizing the secondary binding site(s) of thrombin in a patient with recurrent spontaneous arterial thrombosis. Thromb Haemost 1992;67:193-9.
38. Giri TK, Tollefsen DM. Placental dermatan sulfate: isolation, anticoagulant activity, and association with heparin cofactor II. Blood 2006;107:2753-8.
39. Kitazato K, Kitazato KT, Sasaki E, Minamiguchi K, Nagase H. Prolonged bleeding time induced by anticoagulant glycosaminoglycans in dogs is associated with the inhibition of thrombin-induced platelet aggregation. Thromb Res 2003;112:83-91.
40. Sie P, Fernandes F, Caranobe C, Gabaig AM, Boneu B. Inhibition of thrombin-induced platelet aggregation and serotonin release by antithrombin III and heparin cofactor II in the presence of standard heparin, dermatan sulfate and pentosan polysulfate. Thromb Res 1984;35:231-6.
41. Liaw PC, Becker DL, Stafford AR, Fredenburgh JC, Weitz JI. Molecular basis for the susceptibility of fibrin-bound thrombin to inactivation by heparin cofactor ii in the presence of dermatan sulfate but not heparin. J Biol Chem 2001;276:20959-65.
42. Becker DL, Fredenburgh JC, Stafford AR, Weitz JI. Exosites 1 and 2 are essential for protection of fibrin-bound thrombin from heparin-catalyzed inhibition by antithrombin and heparin cofactor II. J Biol Chem 1999;274:6226-33.
43. Pike RN, Buckle AM, le Bonniec BF, Church FC. Control of the coagulation system by serpins: getting by with a little help from glycosaminoglycans. FEBS J 2005;272:4842-51.
44. Lane DA, Philippou H, Huntington JA. Directing thrombin. Blood 2005;106:2605-12.
45. Tollefsen DM. Heparin cofactor II modulates the response to vascular injury. Arterioscler Thromb Vasc Biol 2007;27:454-60.
46. Shirk RA, Parthasarathy N, San Antonio JD, Church FC, Wagner WD. Altered dermatan sulfate structure and reduced heparin cofactor II-stimulating activity of biglycan and decorin from human atherosclerotic plaque. J Biol Chem 2000;275:18085-92.
47. Rose MJ, Page C. Glycosaminoglycans and the regulation of allergic inflammation. Curr Drug Targets Inflamm Allergy 2004;3:221-5.
48. Libby P, Shi GP. Mast cells as mediators and modulators of atherogenesis. Circulation 2007;115:2471-3.
49. George J, Harats D, Gilburd B, Afek A, Levy Y, Schneiderman J, et al. Immunolocalization of β2-glycoprotein I (apolipoprotein H) to human atherosclerotic plaques: potential implications for lesion progression. Circulation 1999;99:2227-30.
50. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation 2005;111:3481-8.