A novel flow-based assay reveals discrepancies in ADAMTS- 13 inhibitor assessment as compared with a conventional clinical static assay

Journal of Thrombosis and Haemostasis

Volumn 12, Issue 9, 2014, Pages 1523-1532

  Grillberger, R ^a   Gruber, B ^a   Skalicky, S ^a   Schrenk, G ^a   Knol P ^a   Plaimauer, B ^a   Turecek, P L ^a   Scheiflinger, F ^a   Rottensteiner, H ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

ADAMTS13 protein, human; Autoantibodies; Mechanical stress; Thrombotic thrombocytopenic purpura; Von Willebrand factor

Indexed keywords

ADAMTS 13 AUTOANTIBODY; AUTOANTIBODY; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; PROTEIN G; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN; CYTOSKELETON PROTEIN; LIM PROTEIN; PROTEIN BINDING; TES PROTEIN, HUMAN;

ARTICLE; ASSAY; BLOOD VESSEL WALL; CELL SUSPENSION; CHROMATOGRAPHY; CLINICAL ARTICLE; COLLAGEN FIBER; ERYTHROCYTE; EXTRACELLULAR MATRIX; FLOW BASED ASSAY; HUMAN; PREDICTION; SHEAR RATE; THROMBOCYTE; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; THROMBOTIC THROMBOCYTOPENIC PURPURA; BLOOD; BLOOD CLOTTING TEST; BLOOD EXAMINATION; CHEMISTRY; COMPARATIVE STUDY; DEVICES; FLUORESCENCE RESONANCE ENERGY TRANSFER; IMMUNOLOGY; MECHANICAL STRESS; PROCEDURES; PURPURA, THROMBOTIC THROMBOCYTOPENIC; SHEAR STRENGTH;

ADAM PROTEINS; AUTOANTIBODIES; BLOOD COAGULATION TESTS; CYTOSKELETAL PROTEINS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEMATOLOGIC TESTS; HUMANS; IMMUNOGLOBULIN G; LIM DOMAIN PROTEINS; PLATELET AGGREGATION; PROTEIN BINDING; PURPURA, THROMBOTIC THROMBOCYTOPENIC; SHEAR STRENGTH; STRESS, MECHANICAL; VON WILLEBRAND FACTOR;

EID: 84908547819     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12653     Document Type: Article

References (38)

1. Zheng X, Chung D, Takayama TK, Majerus EM, Sadler JE, Fujikawa K. Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J Biol Chem 2001; 276: 41059-63.
2. Levy GG, Nichols WC, Lian EC, Foroud T, McClintick JN, McGee BM, Yang AY, Siemieniak DR, Stark KR, Gruppo R, Sarode R, Shurin SB, Chandrasekaran V, Stabler SP, Sabio H, Bouhassira EE, Upshaw JD Jr, Ginsburg D, Tsai HM. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 2001; 413: 488-94.
3. Soejima K, Mimura N, Hirashima M, Maeda H, Hamamoto T, Nakagaki T, Nozaki C. A novel human metalloprotease synthesized in the liver and secreted into the blood: possibly, the von Willebrand factor-cleaving protease? J Biochem 2001; 130: 475-80.
4. Dong JF, Moake JL, Nolasco L, Bernardo A, Arceneaux W, Shrimpton CN, Schade AJ, McIntire LV, Fujikawa K, Lopez JA. ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood 2002; 100: 4033-9.
5. Donadelli R, Orje JN, Capoferri C, Remuzzi G, Ruggeri ZM. Size regulation of von Willebrand factor-mediated platelet thrombi by ADAMTS13 in flowing blood. Blood 2006; 107:1943-50.
6. Moake JL. Thrombotic microangiopathies. N Engl J Med 2002; 347: 589-600.
7. Rieger M, Mannucci PM, Kremer Hovinga JA, Herzog A, Gerstenbauer G, Konetschny C, Zimmermann K, Scharrer I, Peyvandi F, Galbusera M, Remuzzi G, B€ohm M, Plaimauer B, L€ammle B, Scheiflinger F. ADAMTS13 autoantibodies in patients with thrombotic microangiopathies and other immunomediated diseases. Blood 2005; 106: 1262-7.
8. Ferrari S, Scheiflinger F, Rieger M, Mudde G, Wolf M, Coppo P, Girma JP, Azoulay E, Brun-Buisson C, Fakhouri F, Mira JP, Oksenhendler E, Poullin P, Rondeau E, Schleinitz N, Schlemmer B, Teboul JL, Vanhille P, Vernant JP, Meyer D, et al. Prognostic value of anti-ADAMTS 13 antibody features (Ig isotype, titer, and inhibitory effect) in a cohort of 35 adult French patients undergoing a first episode of thrombotic microangiopathy with undetectable ADAMTS 13 activity. Blood 2007; 109: 2815-22.
9. Pos W, Sorvillo N, Fijnheer R, Feys HB, Kaijen PH, Vidarsson G, Voorberg J. Residues Arg568 and Phe592 contribute to an antigenic surface for anti-ADAMTS13 antibodies in the spacer domain. Haematologica 2011; 96: 1670-7.
10. Ferrari S, Mudde GC, Rieger M, Veyradier A, Kremer Hovinga JA, Scheiflinger F. IgG subclass distribution of anti-ADAMTS13 antibodies in patients with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost 2009; 7: 1703-10.
11. Klaus C, Plaimauer B, Studt JD, Dorner F, Lammle B, Mannucci PM, Scheiflinger F. Epitope mapping of ADAMTS13 autoantibodies in acquired thrombotic thrombocytopenic purpura. Blood 2004; 103: 4514-19.
12. Zheng XL, Wu HM, Shang D, Falls E, Skipwith CG, Cataland SR, Bennett CL, Kwaan HC. Multiple domains of ADAMTS13 are targeted by autoantibodies against ADAMTS13 in patients with acquired idiopathic thrombotic thrombocytopenic purpura. Haematologica 2010; 95: 1555-62.
13. Luken BM, Turenhout EA, Kaijen PH, Greuter MJ, Pos W, van Mourik JA, Fijnheer R, Voorberg J. Amino acid regions 572-579 and 657-666 of the spacer domain of ADAMTS13 provide a common antigenic core required for binding of antibodies in patients with acquired TTP. Thromb Haemost 2006; 96: 295-301.
14. Pos W, Crawley JT, Fijnheer R, Voorberg J, Lane DA, Luken BM. An autoantibody epitope comprising residues R660, Y661, and Y665 in the ADAMTS13 spacer domain identifies a binding site for the A2 domain of VWF. Blood 2010; 115: 1640-9.
15. Yamaguchi Y, Moriki T, Igari A, Nakagawa T, Wada H, Matsumoto M, Fujimura Y, Murata M. Epitope analysis of autoantibodies to ADAMTS13 in patients with acquired thrombotic thrombocytopenic purpura. Thromb Res 2011; 128:169-73.
16. Luken BM, Kaijen PH, Turenhout EA, Kremer Hovinga JA, van Mourik JA, Fijnheer R, Voorberg J. Multiple B-cell clones producing antibodies directed to the spacer and disintegrin/thrombospondin type-1 repeat 1 (TSP1) of ADAMTS13 in a patient with acquired thrombotic thrombocytopenic purpura. J Thromb Haemost 2006; 4: 2355-64.
17. Grillberger R, Casina VC, Turecek PL, Zheng XL, Rottensteiner H, Scheiflinger F. Anti-ADAMTS13 IgG autoantibodies present in healthy individuals share linear epitopes with those in patients with thrombotic thrombocytopenic purpura. Haematologica 2014; 99: e58-60.
18. Kokame K, Nobe Y, Kokubo Y, Okayama A, Miyata T. FRETS-VWF73, a first fluorogenic substrate for ADAMTS13 assay. Br J Haematol 2005; 129: 93-100.
19. Tsai HM, Lian EC. Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med 1998; 339: 1585-94.
20. Furlan M, Robles R, Galbusera M, Remuzzi G, Kyrle PA, Brenner B, Krause M, Scharrer I, Aumann V, Mittler U, Solenthaler M, Lammle B. von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura and the hemolytic-uremic syndrome. N Engl J Med 1998; 339: 1578-84.
21. Mancini I, Valsecchi C, Palla R, Lotta LA, Peyvandi F. Measurement of anti-ADAMTS13 neutralizing autoantibodies: a comparison between CBA and FRET assays. J Thromb Haemost 2012; 10: 1439-42.
22. Shenkman B, Inbal A, Tamarin I, Lubetsky A, Savion N, Varon D. Diagnosis of thrombotic thrombocytopenic purpura based on modulation by patient plasma of normal platelet adhesion under flow condition. Br J Haematol 2003; 120: 597-604.
23. Shim K, Anderson PJ, Tuley EA, Wiswall E, Sadler JE. Platelet-VWF complexes are preferred substrates of ADAMTS13 under fluid shear stress. Blood 2008; 111: 651-7.
24. Han Y, Xiao J, Falls E, Zheng XL. A shear-based assay for assessing plasma ADAMTS13 activity and inhibitors in patients with thrombotic thrombocytopenic purpura. Transfusion 2011; 51: 1580-91.
25. Froehlich-Zahnd R, George JN, Vesely SK, Terrell DR, Aboulfatova K, Dong JF, Luken BM, Voorberg J, Budde U, Sulzer I, Lammle B, Kremer Hovinga JA. Evidence for a role of anti-ADAMTS13 autoantibodies despite normal ADAMTS13 activity in recurrent thrombotic thrombocytopenic purpura. Haematologica 2012; 97: 297-303.
26. Kinoshita S, Yoshioka A, Park YD, Ishizashi H, Konno M, Funato M, Matsui T, Titani K, Yagi H, Matsumoto M, Fujimura Y. Upshaw-Schulman syndrome revisited: a concept of congenital thrombotic thrombocytopenic purpura. Int J Hematol 2001; 74: 101-8.
27. Li Y, Choi H, Zhou Z, Nolasco L, Pownall HJ, Voorberg J, Moake JL, Dong JF. Covalent regulation of ULVWF string formation and elongation on endothelial cells under flow conditions. J Thromb Haemost 2008; 6: 1135-43.
28. Nieswandt B, Watson SP. Platelet-collagen interaction: is GPVI the central receptor? Blood 2003; 102: 449-61.
29. Dong JF, Whitelock J, Bernardo A, Ball C, Cruz MA. Variations among normal individuals in the cleavage of endothelialderived ultra-large von Willebrand factor under flow. J Thromb Haemost 2004; 2: 1460-6.
30. Turner NA, Nolasco L, Ruggeri ZM, Moake JL. Endothelial cell ADAMTS-13 and VWF: production, release, and VWF string cleavage. Blood 2009; 114: 5102-11.
31. Plaimauer B, Kremer Hovinga JA, Juno C, Wolfsegger MJ, Skalicky S, Schmidt M, Grillberger L, Hasslacher M, Knobl P, Ehrlich H, Scheiflinger F. Recombinant ADAMTS13 normalizes von Willebrand factor-cleaving activity in plasma of acquired TTP patients by overriding inhibitory antibodies. J Thromb Haemost 2011; 9: 936-44.
32. Tao Z, Peng Y, Nolasco L, Cal S, Lopez-Otin C, Li R, Moake JL, Lopez JA, Dong JF. Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions. Blood 2005; 106: 4139-45.
33. Tao Z, Wang Y, Choi H, Bernardo A, Nishio K, Sadler JE, Lopez JA, Dong JF. Cleavage of ultralarge multimers of von Willebrand factor by C-terminal-truncated mutants of ADAMTS-13 under flow. Blood 2005; 106: 141-3.
34. De Maeyer B, De Meyer SF, Feys HB, Pareyn I, Vandeputte N, Deckmyn H, Vanhoorelbeke K. The distal carboxyterminal domains of murine ADAMTS13 influence proteolysis of plateletdecorated VWF strings in vivo. J Thromb Haemost 2010; 8: 2305-12.
35. Muia J, Gao W, Haberichter SL, Dolatshahi L, Zhu J, Westfield LA, Covill SC, Friedman KD, Sadler JE. An optimized fluorogenic ADAMTS13 assay with increased sensitivity for the investigation of patients with thrombotic thrombocytopenic purpura. J Thromb Haemost 2013; 11: 1511-18.
36. Gawryl MS, Hoyer LW. Inactivation of factor VIII coagulant activity by two different types of human antibodies. Blood 1982; 60: 1103-9.
37. Rieger M, Ferrari S, Kremer Hovinga JA, Konetschny C, Herzog A, Koller L, Weber A, Remuzzi G, Dockal M, Plaimauer B, Scheiflinger F. Relation between ADAMTS13 activity and ADAMTS13 antigen levels in healthy donors and patients with thrombotic microangiopathies (TMA). Thromb Haemost 2006; 95: 212-20.
38. Ferrari S, Palavra K, Gruber B, Kremer Hovinga JA, Knobl P, Caron C, Cromwell C, Aledort L, Plaimauer B, Turecek PL, Rottensteiner H, Scheiflinger F. Persistence of circulating ADAMTS13- specific immune complexes in patients with acquired thrombotic thrombocytopenic purpura. Haematologica 2014; 99:779-87.