A novel mechanism of thrombosis in antiphospholipid antibody syndrome

Journal of Autoimmunity

Volumn 35, Issue 3, 2010, Pages 248-255

  Vlachoyiannopoulos, Panayiotis G ^a   Routsias, John G ^b  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

Author keywords

2 GPI; Antiphospholipid syndrome; Autoantibodies; HITT; Platelet factor 4

Indexed keywords

ACTIVATED PROTEIN C; ANTICOAGULANT AGENT; BETA2 GLYCOPROTEIN 1; BETA2 GLYCOPROTEIN 1 ANTIBODY; CHLORPROMAZINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HEPARIN; LUPUS ANTICOAGULANT; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHOLIPID ANTIBODY; PROCAINAMIDE; PROTEIN C; PROTHROMBIN; THROMBOCYTE FACTOR 4; THROMBOMODULIN; THROMBOXANE B2; VASCULAR CELL ADHESION MOLECULE 1;

ANTIBODY PRODUCTION; ANTIPHOSPHOLIPID ANTIBODY SYNDROME; ARTICLE; AUTOIMMUNE DISEASE; DIMERIZATION; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; FIBRINOLYSIS; HEPARIN INDUCED THROMBOCYTOPENIA AND THROMBOSIS SYNDROME; HUMAN; INNATE IMMUNITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTE ACTIVATION; THROMBOCYTE MEMBRANE; THROMBOPHILIA; THROMBOSIS;

ANTIPHOSPHOLIPID SYNDROME; AUTOANTIBODIES; BETA 2-GLYCOPROTEIN I; FIBRINOLYSIS; HUMANS; MULTIPROTEIN COMPLEXES; PLATELET ACTIVATION; PLATELET FACTOR 4; PROTEIN MULTIMERIZATION; THROMBOCYTOPENIA; THROMBOPHILIA; THROMBOSIS;

EID: 77957778469     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2010.06.015     Document Type: Article

References (66)

1. Vlachoyiannopoulos P.G., Samarkos M., Sikara M., Tsiligros P. Antiphospholipid antibodies: laboratory and pathogenetic aspects. Crit Rev Clin Lab Sci 2007, 44:271-338.
2. McNeil H.P., Simpson R.J., Chesterman C.N., Krilis S.A. Anti-phospholipid antibodies are directed against a complex antigen that includes a lipid-binding inhibitor of coagulation: beta 2-glycoprotein I (apolipoprotein H). Proc Natl Acad Sci U S A 1990, 87:4120-4124.
3. Bevers E.M., Galli M., Barbui T., Comfurius P., Zwaal R.F. Lupus anticoagulant IgG's (LA) are not directed to phospholipids only, but to a complex of lipid-bound human prothrombin. Thromb Haemost 1991, 66:629-632.
4. Arnout J. Antiphospholipid syndrome: diagnostic aspects of lupus anticoagulants. Thromb Haemost 2001, 86:83-91.
5. Von A.Wafssermann, Neisser A., Bruck C. Eine serodiagnostische Reaktion bei Syphilis. Deutsch Med Wochenschr 1906, 32:745-746.
6. Pangborn M. A new serologically active phospholipid from beef heart. Proc Soc Exp Biol Med 1941, 48:484-486.
7. Moore J., Mohr C. Biologically false-positive tests for syphilis. JAMA 1952, 150:463-473.
8. Conley M., Hartmann R. A hemorrhagic disorder caused by circulating anticoagulant in patients with disseminated lupus erythematosus. J Lab Clin Invest 1952, 31:621-622.
9. Bowie E.J., Thompson J.H., Pascuzzi C.A., Owen C.A. Thrombosis in systemic lupus erythematosus despite circulating anticoagulants. J Lab Clin Med 1963, 62:416-430.
10. Feinstein D.I., Rapaport S.I. Acquired inhibitors of blood coagulation. Prog Hemost Thromb 1972, 1:75-95.
11. Lechner K. Acquired inhibitors in nonhemophilic patients. Haemostasis 1974, 3:65-93.
12. Nilsson I.M., Astedt B., Hedner U., Berezin D. Intrauterine death and circulating anticoagulant (" antithromboplastin" ). Acta Med Scand 1975, 197:153-159.
13. Loizou S., McCrea J.D., Rudge A.C., Reynolds R., Boyle C.C., Harris E.N. Measurement of anti-cardiolipin antibodies by an enzyme-linked immunosorbent assay (ELISA): standardization and quantitation of results. Clin Exp Immunol 1985, 62:738-745.
14. Asherson R.A., Khamashta M.A., Ordi-Ros J., Derksen R.H., Machin S.J., Barquinero J., et al. The "primary" antiphospholipid syndrome: major clinical and serological features. Medicine (Baltimore) 1989, 68:366-374.
15. McNeil H.P., Chesterman C.N., Krilis S.A. Anticardiolipin antibodies and lupus anticoagulants comprise separate antibody subgroups with different phospholipid binding characteristics. Br J Haematol 1989, 73:506-513.
16. Oosting J.D., Derksen R.H., Entjes H.T., Bouma B.N., de Groot P.G. Lupus anticoagulant activity is frequently dependent on the presence of beta 2-glycoprotein I. Thromb Haemost 1992, 67:499-502.
17. Izumi T., Pound M.L., Su Z., Iverson G.M., Ortel T.L. Anti-beta(2)-glycoprotein I antibody-mediated inhibition of activated protein C requires binding of beta(2)-glycoprotein I to phospholipids. Thromb Haemost 2002, 88:620-626.
18. Galli M., Willems G.M., Rosing J., Janssen R.M., Govers-Riemslag J.W., Comfurius P., et al. Anti-prothrombin IgG from patients with anti-phospholipid antibodies inhibits the inactivation of factor Va by activated protein C. Br J Haematol 2005, 129:240-247.
19. Takeuchi R., Atsumi T., Ieko M., Amasaki Y., Ichikawa K., Koike T. Suppressed intrinsic fibrinolytic activity by monoclonal anti-beta-2 glycoprotein I autoantibodies: possible mechanism for thrombosis in patients with antiphospholipid syndrome. Br J Haematol 2002, 119:781-788.
20. Ieko M., Ichikawa K., Atsumi T., Takeuchi R., Sawada K.I., Yasukouchi T., et al. Effects of beta2-glycoprotein I and monoclonal anticardiolipin antibodies on extrinsic fibrinolysis. Semin Thromb Hemost 2000, 26:85-90.
21. Yang C.D., Hwang K.K., Yan W., Gallagher K., FitzGerald J., Grossman J.M., et al. Identification of anti-plasmin antibodies in the antiphospholipid syndrome that inhibit degradation of fibrin. J Immunol 2004, 172:5765-5773.
22. Kolev K., Gombas J., Varadi B., Skopal J., Mede K., Pitlik E., et al. Immunoglobulin G from patients with antiphospholipid syndrome impairs the fibrin dissolution with plasmin. Thromb Haemost 2002, 87:502-508.
23. Atsumi T., Khamashta M.A., Andujar C., Leandro M.J., Amengual O., Ames P.R., et al. Elevated plasma lipoprotein(a) level and its association with impaired fibrinolysis in patients with antiphospholipid syndrome. J Rheumatol 1998, 25:69-73.
24. Del Papa N., Guidali L., Spatola L., Bonara P., Borghi M.O., Tincani A., et al. Relationship between anti-phospholipid and anti-endothelial cell antibodies III: beta 2 glycoprotein I mediates the antibody binding to endothelial membranes and induces the expression of adhesion molecules. Clin Exp Rheumatol 1995, 13:179-185.
25. Meroni P.L., Papa N.D., Beltrami B., Tincani A., Balestrieri G., Krilis S.A. Modulation of endothelial cell function by antiphospholipid antibodies. Lupus 1996, 5:448-450.
26. Pierangeli S.S., Liu X.W., Barker J.H., Anderson G., Harris E.N. Induction of thrombosis in a mouse model by IgG, IgM and IgA immunoglobulins from patients with the antiphospholipid syndrome. Thromb Haemost 1995, 74:1361-1367.
27. Cho C.S., Cho M.L., Chen P.P., Min S.Y., Hwang S.Y., Park K.S., et al. Antiphospholipid antibodies induce monocyte chemoattractant protein-1 in endothelial cells. J Immunol 2002, 168:4209-4215.
28. Lopez-Lira F., Rosales-Leon L., Martinez V.M., Ruiz Ordaz B.H. The role of beta2-glycoprotein I (beta2GPI) in the activation of plasminogen. Biochim Biophys Acta 2006, 1764:815-823.
29. Dunoyer-Geindre S., de Moerloose P., Galve-de Rochemonteix B., Reber G., Kruithof E.K. NFkappaB is an essential intermediate in the activation of endothelial cells by anti-beta(2)-glycoprotein 1 antibodies. Thromb Haemost 2002, 88:851-857.
30. Raschi E., Testoni C., Bosisio D., Borghi M.O., Koike T., Mantovani A., et al. Role of the MyD88 transduction signaling pathway in endothelial activation by antiphospholipid antibodies. Blood 2003, 101:3495-3500.
31. Espinola R.G., Liu X., Colden-Stanfield M., Hall J., Harris E.N., Pierangeli S.S. E-Selectin mediates pathogenic effects of antiphospholipid antibodies. J Thromb Haemost 2003, 1:843-848.
32. Rand J.H., Wu X.X., Quinn A.S., Chen P.P., McCrae K.R., Bovill E.G., et al. Human monoclonal antiphospholipid antibodies disrupt the annexin A5 anticoagulant crystal shield on phospholipid bilayers: evidence from atomic force microscopy and functional assay. Am J Pathol 2003, 163:1193-1200.
33. Chen Q., Stone P.R., Woon S.T., Ching L.M., Hung S., McCowan L.M., et al. Antiphospholipid antibodies bind to activated but not resting endothelial cells: is an independent triggering event required to induce antiphospholipid antibody-mediated disease?. Thromb Res 2004, 114:101-111.
34. Hasselaar P., Derksen R.H., Oosting J.D., Blokzijl L., de Groot P.G. Synergistic effect of low doses of tumor necrosis factor and sera from patients with systemic lupus erythematosus on the expression of procoagulant activity by cultured endothelial cells. Thromb Haemost 1989, 62:654-660.
35. Bouma B., de Groot P.G., van den Elsen J.M., Ravelli R.B., Schouten A., Simmelink M.J., et al. Adhesion mechanism of human beta(2)-glycoprotein I to phospholipids based on its crystal structure. EMBO J 1999, 18:5166-5174.
36. Guerin J., Sheng Y., Reddel S., Iverson G.M., Chapman M.G., Krilis S.A. Heparin inhibits the binding of beta 2-glycoprotein I to phospholipids and promotes the plasmin-mediated inactivation of this blood protein. Elucidation of the consequences of the two biological events in patients with the anti-phospholipid syndrome. J Biol Chem 2002, 277:2644-2649.
37. Hanly J.G., Hong C., Issekutz A. Beta 2-glycoprotein I and anticardiolipin antibody binding to resting and activated cultured human endothelial cells. J Rheumatol 1996, 23:1543-1549.
38. Kotowicz K., Dixon G.L., Klein N.J., Peters M.J., Callard R.E. Biological function of CD40 on human endothelial cells: costimulation with CD40 ligand and interleukin-4 selectively induces expression of vascular cell adhesion molecule-1 and P-selectin resulting in preferential adhesion of lymphocytes. Immunology 2000, 100:441-448.
39. Vega-Ostertag M., Harris E.N., Pierangeli S.S. Intracellular events in platelet activation induced by antiphospholipid antibodies in the presence of low doses of thrombin. Arthritis Rheum 2004, 50:2911-2919.
40. Lutters B.C., Derksen R.H., Tekelenburg W.L., Lenting P.J., Arnout J., de Groot P.G. Dimers of beta 2-glycoprotein I increase platelet deposition to collagen via interaction with phospholipids and the apolipoprotein E receptor 2'. J Biol Chem 2003, 278:33831-33838.
41. Shi T., Giannakopoulos B., Yan X., Yu P., Berndt M.C., Andrews R.K., et al. Anti-beta2-glycoprotein I antibodies in complex with beta2-glycoprotein I can activate platelets in a dysregulated manner via glycoprotein Ib-IX-V. Arthritis Rheum 2006, 54:2558-2567.
42. Sikara M.P., Routsias J.G., Samiotaki M., Panayotou G., Moutsopoulos H.M., Vlachoyiannopoulos P.G. {beta}2 Glycoprotein I ({beta}2GPI) binds platelet factor 4 (PF4): implications for the pathogenesis of antiphospholipid syndrome. Blood 2010, 115:713-723.
43. Zucker M.B., Katz I.R. Platelet factor 4: production, structure, and physiologic and immunologic action. Proc Soc Exp Biol Med 1991, 198:693-702.
44. Levine S.P., Wohl H. Human platelet factor 4: purification and characterization by affinity chromatography. Purification of human platelet factor 4. J Biol Chem 1976, 251:324-328.
45. Galazka M., Keil L.B., Kohles J.D., Li J., Kelty S.P., Petersheim M., et al. A stable, multi-subunit complex of beta2glycoprotein I. Thromb Res 1998, 90:131-137.
46. Kamboh M.I., Sanghera D.K., Mehdi H., Nestlerode C.S., Chen Q., Khalifa O., et al. Single nucleotide polymorphisms in the coding region of the apolipoprotein H (beta2-glycoprotein I) gene and their correlation with the protein polymorphism, anti-beta2glycoprotein I antibodies and cardiolipin binding: description of novel haplotypes and their evolution. Ann Hum Genet 2004, 68:285-299.
47. Chen Q., Kamboh M.I. Complete DNA sequence variation in the apolipoprotein H (beta-glycoprotein I) gene and identification of informative SNPs. Ann Hum Genet 2006, 70:1-11.
48. Yasuda S., Atsumi T., Matsuura E., Kaihara K., Yamamoto D., Ichikawa K., et al. Significance of valine/leucine247 polymorphism of beta2-glycoprotein I in antiphospholipid syndrome: increased reactivity of anti-beta2-glycoprotein I autoantibodies to the valine247 beta2-glycoprotein I variant. Arthritis Rheum 2005, 52:212-218.
49. von Scheven E., Elder M.E. Association between beta2-glycoprotein I gene polymorphisms and pediatric SLE and antiphospholipid antibodies. Lupus 2005, 14:440-444.
50. Prieto G.A., Cabral A.R., Zapata-Zuniga M., Simon A.J., Villa A.R., Alarcon-Segovia D., et al. Valine/valine genotype at position 247 of the beta2-glycoprotein I gene in Mexican patients with primary antiphospholipid syndrome: association with anti-beta2-glycoprotein I antibodies. Arthritis Rheum 2003, 48:471-474.
51. Terashi H., Hashimoto S., Uchiyama S. Brain Nerve 2008, 60:1333-1338.
52. Pernambuco-Climaco J.M., Brochado M.J., Freitas M.V., Roselino A.M., Louzada-Junior P. Val/Leu247 polymorphism of beta2-glycoprotein I in Brazilian patients with antiphospholipid syndrome - a genetic risk factor?. Ann N Y Acad Sci 2009, 1173:509-514.
53. Fernandez-Recio J., Totrov M., Abagyan R. Soft protein-protein docking in internal coordinates. Protein Sci 2002, 11:280-291.
54. Lane D.A., Denton J., Flynn A.M., Thunberg L., Lindahl U. Anticoagulant activities of heparin oligosaccharides and their neutralization by platelet factor 4. Biochem J 1984, 218:725-732.
55. Eslin D.E., Zhang C., Samuels K.J., Rauova L., Zhai L., Niewiarowski S., et al. Transgenic mice studies demonstrate a role for platelet factor 4 in thrombosis: dissociation between anticoagulant and antithrombotic effect of heparin. Blood 2004, 104:3173-3180.
56. Slungaard A., Fernandez J.A., Griffin J.H., Key N.S., Long J.R., Piegors D.J., et al. Platelet factor 4 enhances generation of activated protein C in vitro and in vivo. Blood 2003, 102:146-151.
57. Reilly M.P., Taylor S.M., Hartman N.K., Arepally G.M., Sachais B.S., Cines D.B., et al. Heparin-induced thrombocytopenia/thrombosis in a transgenic mouse model requires human platelet factor 4 and platelet activation through FcgammaRIIA. Blood 2001, 98:2442-2447.
58. Pervushina O., Scheuerer B., Reiling N., Behnke L., Schroder J.M., Kasper B., et al. Platelet factor 4/CXCL4 induces phagocytosis and the generation of reactive oxygen metabolites in mononuclear phagocytes independently of Gi protein activation or intracellular calcium transients. J Immunol 2004, 173:2060-2067.
59. Lasagni L., Grepin R., Mazzinghi B., Lazzeri E., Meini C., Sagrinati C., et al. PF-4/CXCL4 and CXCL4L1 exhibit distinct subcellular localization and a differentially regulated mechanism of secretion. Blood 2007, 109:4127-4134.
60. Schaffner A., Rhyn P., Schoedon G., Schaer D.J. Regulated expression of platelet factor 4 in human monocytes - role of PARs as a quantitatively important monocyte activation pathway. J Leukoc Biol 2005, 78:202-209.
61. Maier M., Wutzler S., Bauer M., Trendafilov P., Henrich D., Marzi I. Altered gene expression patterns in dendritic cells after severe trauma: implications for systemic inflammation and organ injury. Shock 2008, 30:344-351.
62. Asherson R.A. The catastrophic antiphospholipid (Asherson's) syndrome. Autoimmun Rev 2006, 6:64-67.
63. Ansari A.A., Gershwin M.E. Navigating the passage between Charybdis and Scylla: recognizing the achievements of Noel Rose. J Autoimmun 2009, 33:165-169.
64. Whittingham S., Rowley M.J., Gershwin M.E. A tribute to an outstanding immunologist - Ian Reay Mackay. J Autoimmun 2008, 31:197-200.
65. Gershwin M.E. Bone marrow transplantation, refractory autoimmunity and the contributions of Susumu Ikehara. J Autoimmun 2008, 30:105-107.
66. Gershwin M.E. The mosaic of autoimmunity. Autoimmun Rev 2008, 7:161-163.