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Thromb Haemost 1997; 78(01): 420-426
DOI: 10.1055/s-0038-1657563
PLENARY LECTURE – Sol Sherry Lecture
Schattauer GmbH Stuttgart

Antibody-Mediated Thrombosis

J Vermylen
Center for Molecular and Vascular Biology, University of Leuven, Leuven, Belgium
,
M F Hoylaerts
Center for Molecular and Vascular Biology, University of Leuven, Leuven, Belgium
,
J Arnout
Center for Molecular and Vascular Biology, University of Leuven, Leuven, Belgium
› Author Affiliations
Further Information

Publication History

Publication Date:
12 July 2018 (online)

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  • References

  • 1 Vermylen J, Blockmans D, Spitz B, Deckmyn H. Thrombosis and immune disorders. Clin Haematol 1986; 15: 393-412
    PubMedSearch in Google Scholar
  • 2 Carreras LO. Thrombosis and thrombocytopenia induced by heparin. Scand J Haematol 1980; (Suppl. 36) 64-80
    PubMedSearch in Google Scholar
  • 3 Rhodes GR, Dixon RH, Silver D. Heparin induced thrombocytopenia with thrombotic and hemorrhagic manifestations. Surg Gynecol Obstet 1973; 136: 409-416
    Search in Google Scholar
  • 4 Towne JB, Bernhard VM, Hussey C, Garancis JC. White-clot syndrome peripheral vascular complications of heparin therapy. Arch Surg 1979; 114: 372-377
    CrossrefPubMedSearch in Google Scholar
  • 5 Chong BH, Pitney WR, Castaldi PA. Heparin-induced thrombocytopenia: association of thrombotic complications with heparin-dependent IgG antibody that induces thromboxane synthesis and platelet aggregation. Lancet 02 1982; 1246-1249
    PubMedSearch in Google Scholar
  • 6 Kappa JR, Fisher CA, Addonizio Jr VP. Heparin-induced platelet activation: the role of thromboxane A2 synthesis and the extent of platelet granule release in two patients. J Vase Surg 09 1989; 574-579
    PubMedSearch in Google Scholar
  • 7 Sheridan D, Carter C, Kelton JG. A diagnostic test for heparin- induced thrombocytopenia. Blood 1986; 67: 27-30
    CrossrefPubMedSearch in Google Scholar
  • 8 Warkentin TE, Hayward CP, Boshkov LK, Santos AV, Sheppard JA, Bode AP, Kelton JG. Sera from patients with heparin-induced thrombocytopenia generate platelet-derived microparticles with procoagulant activity: an explanation for the thrombotic complications of heparin-induced thrombocytopenia. Blood 1994; 84: 3691-3699
    PubMedSearch in Google Scholar
  • 9 Kelton JG, Sheridan D, Santos A, Smith J, Steeves K, Smith C, Brown C, Murphy WG. Heparin-induced thrombocytopenia: laboratory studies. Blood 1988; 72: 925-930
    PubMedSearch in Google Scholar
  • 10 Chong BH, Castaldi PA, Berndt MC. Heparin-induced thrombocytopenia: effects of rabbit IgG, and its Fab and Fc fragments on antibody-heparin-platelet interaction. Thromb Res 1989; 55: 291-295
    CrossrefPubMedSearch in Google Scholar
  • 11 De ReysS, Blom C, Lepoudre B, Declerck PJ, De LeyM, Vermylen J, Deckmyn H. Human platelet aggregation by murine monoclonal antiplatelet antibodies is subtype-dependent. Blood 1993; 81: 1792-1800
    PubMedSearch in Google Scholar
  • 12 Warmerdam PAM, van deWinkel JGJ, Vlug A, Westerdaal NAC, Capel PJA. A single amino acid in the second Ig-like domain of the Fcg receptor II is critical for human IgG2 binding. J Immunol 1991; 147: 1338-1343
    PubMedSearch in Google Scholar
  • 13 Brandt JT, Isenhart CE, Osborne JM, Ahmed A, Anderson CL. On the role of platelet FcgRIIa phenotype in heparin-induced thrombocytopenia. Thromb Haemost 1995; 74: 1564-1572
    Thieme ConnectPubMedSearch in Google Scholar
  • 14 Arepally G, Poncz M, McKenzie SE, Cines D. Characterization of antibody subclass specificity and antigenic determinants in heparin-associated thrombocytopenia. Blood 1994; 84: 189 a
    PubMedSearch in Google Scholar
  • 15 McCree KR, Shattil SJ, Cines DB. Platelet activation induces increased Fc gamma receptor expression. J Immunol 1990; 144: 3920-3927
    PubMedSearch in Google Scholar
  • 16 Chong BH, Pilgrim RL, Cooley MA, Chesterman CN. Increased expression of platelet IgG Fc receptors in immune heparin-induced thrombocytopenia. Blood 1993; 81: 988-993
    PubMedSearch in Google Scholar
  • 17 Green D, Harris K, Reynolds N, Roberts M, Patterson R. Heparin immune thrombocytopenia: evidence for a heparin- platelet complex as the antigenic determinant. J Lab Clin Med 1978; 91: 167-175
    PubMedSearch in Google Scholar
  • 18 Greinacher A, Michels I, Mueller-Eckhardt C. Heparin-associated thrombocytopenia: the antibody is not heparin specific. Thromb Haemost 1992; 67: 545-549
    Thieme ConnectPubMedSearch in Google Scholar
  • 19 Amiral J, Bridey F, Dreyfus M, Vissoc AM, Fressinand E, Wolf M, Meyer D. Platelet factor 4 complexed to heparin is the target for antibodies generated in heparin-induced thrombocytopenia. Thromb Haemost 1992; 68: 95-96
    Thieme ConnectPubMedSearch in Google Scholar
  • 20 Kelton JG, Smith JW, Warkentin TE, Hayward CP, Denomme GA, Horsewood P. Immunoglobulin G from patients with heparin-induced thrombocytopenia binds to a complex of heparin and platelet factor 4. Blood 1994; 83: 3232-3239
    Search in Google Scholar
  • 21 Greinacher A, Pötzsch B, Amiral J, Dummel V, Eichner A, Mueller-Eckhardt C. Heparin-associated thrombocytopenia: isolation of the antibody and characterization of a multimolecular PF4-heparin complex as the major antigen. Thromb Haemost 1994; 71: 247-251
    PubMedSearch in Google Scholar
  • 22 Brandt JT. Platelet aggregation in heparin-induced thrombocytopenia is dependent on complement activation. Blood 1996; 88: 517 a
    PubMedSearch in Google Scholar
  • 23 Visentin GP, Ford SE, Scott JP, Aster RH. Antibodies from patients with heparin-induced thrombocytopenia/thrombosis are specific for platelet factor 4 complexed with heparin or bound to endothelial cells. J Clin Invest 1994; 93: 81-88
    CrossrefPubMedSearch in Google Scholar
  • 24 Cines DB, Tomaski A, Tannenbaum S. Immune endothelialcell injury in heparin-associated thrombocytopenia. N Engl J Med 1987; 316: 581-589
    CrossrefPubMedSearch in Google Scholar
  • 25 Ikeda K, Nagasawa K, Hiriuchi T, Tsuru T, Nishizaka H, Niho Y. C5a induces tissue factor activity on endothelial cells. Thromb Haemost 1997; 77: 394-398
    Thieme ConnectPubMedSearch in Google Scholar
  • 26 Boshkov LKWarkentin TE, Hayward CP, Andrew M, Kelton JG. Heparin-induced thrombocytopenia and thrombosis: clinical and laboratory studies. Br J Haematol 1993; 84: 322-328
    CrossrefPubMedSearch in Google Scholar
  • 27 Feinstein PG, Rapaport SI. Acquired inhibitors of blood coagulation. Prog Hemost Thromb 1972; 01: 75-95
    PubMedSearch in Google Scholar
  • 28 Frick PG. Acquired circulating anticoagulants in systemic “collagen disease”. Auto-immune thromboplastin deficiency. Blood 1995; 10: 691-706
    PubMedSearch in Google Scholar
  • 29 Harris EN, Gharavi AE, Boey ML, Patel BM, Mackworth-Young CG, Loizou S, Hughes GR. Anticoardiolipin antibodies: detection by radioimmunoassay and association with thrombosis in systemic lupus erythematosus. Lancet 1983; 02: 1211-1244
    PubMedSearch in Google Scholar
  • 30 Loizou S, McCrea JD, Rudge AC, Reynolds R, Boyle CC, Harris EN. Measurement of anticardiolipin antibodies by enzyme- linked immunosorbent assay: standardization and quantitation of results. Clin Exp Immunol 1985; 62: 738-744
    PubMedSearch in Google Scholar
  • 31 Bowie EJW, Thompson Jr JH, Pascuzzi CA, Owen Jr CA. Thrombosis in systemic lupus erythematosus despite circulating anticoagulants. J Lab Clin Med 1963; 62: 416-430
    PubMedSearch in Google Scholar
  • 32 Nilsson IM, Astedt B, Hedner U, Berezin D. Intrauterine death and circulating anticoagulant (antithromboplastin). Acta Med Scand 1975; 197: 153-159
    PubMedSearch in Google Scholar
  • 33 Soulier JP, Boffa MC. Avortements à répétitition, thromboses et anticoagulant circulant antithromboplastin. Trois observations. Nouv Press Médicale 1980; 09: 859-864
    PubMedSearch in Google Scholar
  • 34 De Wolf F, Carreras LO, Moerman PH, Vermylen J, Van Assche A, Renaer M. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss and a lupus anticoagulant. Am J Obstet Gynecol 1982; 142: 829-834
    CrossrefPubMedSearch in Google Scholar
  • 35 Harris EN, Baguley E, Asherson RA, Hughes GRV. Clinical and neurological features of the antiphospholipid syndrome (APS). Br J Rheumatol 1987; 26: 19
    PubMedSearch in Google Scholar
  • 36 Asherson RA. A “primary” antiphospholipid syndrome ?. J Rheumatol 1988; 15: 1742-1746
    PubMedSearch in Google Scholar
  • 37 Carreras LO, Defreyn G, Machin SJ, Vermylen J, Deman R, Spitz B, Van Assche A. Arterial thrombosis, intrauterine death and “lupus” anticoagulant: detection of immunoglobulin interfering with prostacyclin formation. Lancet 1981; 01: 244-246
    PubMedSearch in Google Scholar
  • 38 Comp PC, De Bault LE, Esmon NL, Esmon CT. Human thrombomodulin is inhibited by IgG from two patients with non-specific anticoagulants. Blood 1983; 62 (Suppl. 01) 299
    PubMedSearch in Google Scholar
  • 39 McNeil HP, Simpson RJ, Chesterman CN, Krilis SA. 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 USA 1990; 87: 4120-4124
    CrossrefPubMedSearch in Google Scholar
  • 40 Galli M, Comfurius P, Maassen C, Hemker HC, de Baets MH, van Breda-Vriesman PJ, Barbui T, Zwaal RF, Bevers EM. Anticardiolipin antibodies (ACA) directed not to cardiolipin but to a plasma protein cofactor. Lancet 1990; 335: 1544-1547
    CrossrefPubMedSearch in Google Scholar
  • 41 Bevers EM, Galli M, Barbui T, Comfurius P, Zwaal RF. 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 42 Oosting JD, Derksen RH, Entjes HT, Bouma BN, de Groot PG. Lupus anticoagulant activity is frequently dependent on the presence of beta 2-glycoprotein I. Thromb Haemost 1992; 67: 499-502
    Thieme ConnectPubMedSearch in Google Scholar
  • 43 Roubey RA, Pratt CW, Buyon JP, Winfield JB. Lupus anticoagulant activity of autoimmune antiphospholipid antibodies is dependent upon beta 2-glycoprotein I. J Clin Invest 1992; 90: 1100-1104
    CrossrefPubMedSearch in Google Scholar
  • 44 Galli M, Comfurius P, Barbui T, Zwaal RF, Bevers EM. Anticoagulant activity of beta 2-glycoprotein I is potentiated by a distinct subgroup of anticardiolipin antibodies. Thromb Haemost 1992; 68: 297-300
    Thieme ConnectPubMedSearch in Google Scholar
  • 45 Matsuura E, Igarashi Y, Yasuda T, Triplett DA, Koike T. Anticardiolipin antibodies recognize b 2-Glycoprotein I structure altered by interaction with an oxygen modified solid phase surface. J Exp Med 1994; 179: 457-462
    CrossrefPubMedSearch in Google Scholar
  • 46 Ichikawa Y, Takamatsu K, Shimizu H, Uchiyama M, Moriuchi J, Takaya M, Kobayashi N, Kawada T, Arimori S. Serum apolipoprotein H levels in systemic lupus erythematosus are not influenced by antiphospholipid antibodies. Lupus 1992; 01: 145-149
    PubMedSearch in Google Scholar
  • 47 Bancsi LF, van der Linden IK, Bertina RM. b2-glycoprotein I deficiency and the risk of thrombosis. Thromb Haemost 1992; 67: 649-653
    Thieme ConnectPubMedSearch in Google Scholar
  • 48 Galli M, Bevers EM. Inhibition of phospholipid-dependent coagulation reactions by “antiphospholipid antibodies:l possible modes of action. Lupus 1994; 03: 223-238
    CrossrefPubMedSearch in Google Scholar
  • 49 Lechner K, Pabinger-Fasching I. Lupus anticoagulants and thrombosis A study of 25 cases and review of the literature. Haemostasis, 1985; 15: 154-162
    PubMedSearch in Google Scholar
  • 50 Branch DW, Dudley DJ, Mitchell MD, Creighton KA, Abbott TM, Hammond EH, Daynes RA. Immunoglobulin G fractions from patients with antiphospholipid antibodies cause fetal death in BALB/c mice: a model for autoimmune fetal loss. Am J Obstet Gynecol 1990; 163: 210-216
    CrossrefPubMedSearch in Google Scholar
  • 51 Blank M, Cohen J, Toder V, Shoenfeld Y. Induction of anti-phospholipid syndrome in naive mice with mouse lupus monoclonal and human polyclonal anti-cardiolipin antibodies. Proc Natl Acad Sci USA 1991; 88: 3069-3073
    CrossrefPubMedSearch in Google Scholar
  • 52 Blank M, Faden D, Tincani A, Kopolovic J, Goldberg I, Gilburd B, Allegri F, Balestrieri G, Valesini G, Shoenfeld Y. Immunization with anticardiolipin cofactor (beta-2-glycoprotein I) induces experimental antiphospholipid syndrome in naive mice. J Autoimmun 1994; 07: 441-455
    CrossrefPubMedSearch in Google Scholar
  • 53 Arvieux J, Pouzol P, Roussel B, Jacob MC, Colomb MG. Lupus-like anticoagulant properties of murine monoclonal antibodies to b 2-glycoprotein I. Br J Haematol 1992; 81: 568-573
    CrossrefPubMedSearch in Google Scholar
  • 54 Arvieux J, Roussel B, Pouzol P, Colomb MG. Platelet activating properties of murine monoclonal antibodies to beta 2-glycoprotein I. Thromb Haemost 1993; 70: 336-341
    Thieme ConnectPubMedSearch in Google Scholar
  • 55 Arvieux J, Jacob MC, Roussel B, Bensa JC, Colomb MG. Neutrophil activation by anti-b2glycoprotein I monoclonal antibodies via Fcg receptor II. J Leukoc Biol 1995; 57: 387-394
    CrossrefPubMedSearch in Google Scholar
  • 56 Arnout J. The pathogenesis of the antiphospholipid syndrome: a hypothesis based on parallelisms with heparin-induced thrombocytopenia. Thromb Haemost 1996; 75: 536-541
    Thieme ConnectPubMedSearch in Google Scholar
  • 57 Simantov R, Gharavi A, Casali P, Lo SK, Salmon JE, Sammaritano LR, Silverstein RL. Activation of vascular endothelial cells by murine and human monoclonal anticoardiolipin antibodies. Blood 1996; 88 (Suppl. 01) 510 a
    PubMedSearch in Google Scholar
  • 58 Olee T, Pierangeli SS, Handley HH, Le DT, Wei X, Lai CJ, En J, Novotny W, Harris EN, Woods Jr VL, Chen PP. A monoclonal IgG anticardiolipin antibody from a patient with the antiphospholipid syndrome is thrombogenic in mice. Proc Natl Acad Sci USA 1996; 93: 8606-8611
    CrossrefPubMedSearch in Google Scholar
  • 59 Rosove MH, Brewer PM. Antiphospholipid thrombosis: Clinical course after the first thrombotic event in 70 patients. Ann Intern Med 1992; 117: 303-308
    CrossrefPubMedSearch in Google Scholar
  • 60 Khamashta MA, Cuadrado MJ, Mujic F, Taub NA, Hunt BJ, Hughes GR. The management of thrombosis in the antiphospholipid-antibody syndrome. N Engl J Med 1995; 332: 993-997
    CrossrefPubMedSearch in Google Scholar
  • 61 Hasselaar P, Derksen RH, Oosting JD, Blokzijl L, de GrootPG. 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
    Thieme ConnectPubMedSearch in Google Scholar
  • 62 Shi W, Chong BH, Chesterman CN. Beta 2-glycoprotein I is a requirement for anticardiolipin antibodies binding to activated platelets: differences with lupus anticoagulants. Blood 1993; 81: 1255-1262
    PubMedSearch in Google Scholar
  • 63 Willems GM, Janssen MP, Pelsers MMAL, Confurius P, Galli M, Zwaal RFA, Bevers EM. Role of divalency in the high-affin- ity binding of anticardiolipin antibody-b2-glycprotein I complexes to lipid membranes. Biochemistry 1996; 35: 13833-13842
    CrossrefPubMedSearch in Google Scholar
  • 64 Chamley LW, Pattison NS, McKay EJ. Elution of anticardiolipin antibodies and their cofactor b 2-glycoprotein I from placentae of patients with a poor obsteric history. J Reprod Immunol 1993; 25: 209-220
    CrossrefPubMedSearch in Google Scholar
  • 65 La RosaL, Meroni PL, Tincani A, Balestrieri G, Faden D, Lojacono A, Morassi L, Brocchi E, Del PapaN, Gharavi A, Sammaritano L, Lockshin M. b 2 glycoprotein I and placental anticoagulant protein I in placentae from patients with antiphospholipid syndrome. J Rheumatol 1994; 21: 1684-1693
    PubMedSearch in Google Scholar
  • 66 Nomura S, Yanabu M, Miyake T, Miyazaki Y, Kido H, Kagawa H, Fukuhara S, Komiyama Y, Matsuura E, Koike T. Relationship of microparticles with b 2-glycoprotein I and P-selectin positivity to anticardiolipin antibodies in immune thrombocytopenic purpura. Ann Hematol 1995; 70: 25-30
    CrossrefPubMedSearch in Google Scholar
  • 67 Horbach DA, van Oort E, Donders RCJM, Derksen RHWM, de Groot PG. Lupus anticoagulant is the strongest risk factor for both venous and arterial thrombosis in patients with systemic lupus erythematosus. Comparison between different assays for the detection of antiphospholipid antibodies. Thromb Haemost 1996; 76: 916-924
    Thieme ConnectPubMedSearch in Google Scholar
  • 68 Arvieux J, Roussel B, Ponard D, Colomb MG. IgG2 subclass restriction of anti-b2glycoprotein I antibodies in autoimmune patients. Clin Exp Immunol 1994; 95: 310-315
    PubMedSearch in Google Scholar
  • 69 Reverter JC, Tassies D, Font J, Monteagudo J, Escolar G, Ingelmo M, Ordinas A. Hypercoagulable state in patients with antiphospholipid syndrome is related to high induced tissue factor expression on monocytes and to low free protein S. Arterioscl Thromb Vase Biol 1996; 16: 1319-1326
    PubMedSearch in Google Scholar
  • 70 Muhlfelder TW, Niemetz J, Kreutzer D, Beebe D, Ward PA, Rosenfeld SI. C5 chemotactic fragment induces leukocyte production of tissue factor activity: a link between complement and coagulation. J Clin Invest 1979; 63: 147-150
    CrossrefPubMedSearch in Google Scholar
  • 71 Hoylaerts MF, Arnout J, Thys C, Vermylen J. Auto-antibodies induce von Willebrand factor mediated platelet activation via immune complex formation in a patients with recurrent thrombosis. Thromb Haemost. 1997. 78. suppl 01 abstract this congress
    Search in Google Scholar
  • 72 Tornai I, Arnout J, Deckmyn H, Peerlinck K, Vermylen J. A monoclonal antibody recognizes a von Willebrand factor domain within the amino-terminal portion of the subunit that modulates the function of the glycoprotein Ib - and IIb/IIIa- binding domains. J Clin Invest 1993; 91: 273-282
    CrossrefPubMedSearch in Google Scholar
  • 73 Vermylen J, Arnout J. Is the antiphospholipid syndrome caused by antibodies directed against physiologically relevant phos-pholipid-protein complexes. J Lab Clin Med 1992; 120: 10-12
    PubMedSearch in Google Scholar