Structure and proteolytic properties of ADAMTS13, A metalloprotease involved in the pathogenesis of thrombotic microangiopathies

Progress in Molecular Biology and Translational Science

Volumn 99, Issue C, 2011, Pages 105-144

  Lancellotti, Stefano ^a   De Cristofaro, Raimondo ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

ADAMTS13; Metalloproteases; Shear stress; Thrombotic microangiopathies; von Willebrand factor

Indexed keywords

EID: 78751618413     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-385504-6.00003-8     Document Type: Chapter

References (167)

1. J.L. Moake, C.K. Rudy, J.H. Troll, M.J. Weinstein, N.M. Colannino, and J. Azocar Unusually large plasma factor VIII: von Willebrand factor multimers in chronic relapsing thrombotic thrombocytopenic purpura N Engl J Med 307 1982 1432 1435
2. J.E. Sadler Biochemistry and genetics of von Willebrand factor Annu Rev Biochem 67 1998 395 424
3. Z.M. Ruggeri Von Willebrand factor, platelets and endothelial cell interactions J Thromb Haemost 1 2003 1335 1342
4. M. Furlan, R. Robles, and B. Lamie Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis Blood 87 1996 4223 4234
5. H.M. Tsai Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion Blood 87 1996 4235 4244
6. D.W. Chung, and K. Fujikawa Processing of von Willebrand factor by ADAMTS-13 Biochemistry 41 2002 11065 11070
7. B. Plaimauer, K. Zimmermann, D. Volkel, G. Antoine, R. Kerschbaumer, and P. Jenab Cloning, expression, and functional characterization of the von Willebrand factor-cleaving protease (ADAMTS13) Blood 100 2002 3626 3632
8. G.G. Levy, W.C. Nichols, E.C. Lian, T. Foroud, J.N. McClintick, and B.M. McGee Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura Nature 413 2001 488 494
9. K. Soejima, N. Mimura, M. Hirashima, H. Maeda, T. Hamamoto, and T. Nakagaki A novel human metalloprotease synthesized in the liver and secreted into the blood: possibly, the von Willebrand factor-cleaving protease? J Biochem 130 2001 475 480
10. X. Zheng, D. Chung, T.K. Takayama, E.M. Majerus, J.E. Sadler, and K. Fujikawa Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura J Biol Chem 276 2001 41059 41063
11. H.M. Tsai Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura J Mol Med 80 2002 639 647
12. D.D. Wagner, and V.J. Marder Biosynthesis of von Willebrand protein by human endothelial cells. Identification of a large precursor polypeptide chain J Biol Chem 258 1983 2065 2067
13. R.H. Huang, Y. Wang, R. Roth, X. Yu, A.R. Purvis, and J.E. Heuser Assembly of Weibel-Palade body-like tubules from N-terminal domains of von Willebrand factor Proc Natl Acad Sci USA 105 2008 482 487
14. Z.M. Ruggeri, and T.S. Zimmerman The complex multimeric composition of factor VIII/von Willebrand factor Blood 57 1981 1140 1143
15. H.M. Tsai, R.L. Nagel, V.B. Hatcher, and I.I. Sussman Multimeric composition of endothelial cell-derived von Willebrand factor Blood 73 1989 2074 2076
16. A. Padilla, J.L. Moake, A. Bernardo, C. Ball, Y. Wang, and M. Arya P-selectin anchors newly released ultralarge von Willebrand factor multimers to the endothelial cell surface Blood 103 2004 2150 2156
17. J.E. Sadler von Willebrand factor J Biol Chem 266 1991 22777 22780
18. H.M. Tsai, I.I. Sussman, and R.L. Nagel Shear stress enhances the proteolysis of von Willebrand factor in normal plasma Blood 83 1994 2171 2179
19. J.A. Lopez, and J.F. Dong Cleavage of von Willebrand factor by ADAMTS-13 on endothelial cells Semin Hematol 41 2004 15 23
20. H.M. Tsai, I.I. Sussman, D. Ginsburg, H. Lankhof, J.J. Sixma, and R.L. Nagel Proteolytic cleavage of recombinant type 2A von Willebrand factor mutants R834W and R834Q: inhibition by doxycycline and by monoclonal antibody VP-1 Blood 89 1997 1954 1962
21. M. Furlan, R. Robles, M. Galbusera, G. Remuzzi, P.A. Kyrle, and B. Brenner von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura and the hemolytic-uremic syndrome N Engl J Med 339 1998 1578 1584
22. H.M. Tsai, and E.C. Lian Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura N Engl J Med 339 1998 1585 1594
23. J.J. Hulstein, P.G. de Groot, K. Silence, A. Veyradier, R. Fijnheer, and P.J. Lenting A novel nanobody that detects the gain-of-function phenotype of von Willebrand factor in ADAMTS13 deficiency and von Willebrand disease type 2B Blood 106 2005 3035 3042
24. K. Kokame, M. Matsumoto, K. Soejima, H. Yagi, H. Ishizashi, and M. Funato Mutations and common polymorphisms in ADAMTS13 gene responsible for von Willebrand factor-cleaving protease activity Proc Natl Acad Sci USA 99 2002 11902 11907
25. D. Shang, X.W. Zheng, M. Niiya, and X.L. Zheng Apical sorting of ADAMTS13 in vascular endothelial cells and Madin-Darby canine kidney cells depends on the CUB domains and their association with lipid rafts Blood 108 2006 2207 2215
26. N. Turner, L. Nolasco, Z. Tao, J.F. Dong, and J. Moake Human endothelial cells synthesize and release ADAMTS-13 J Thromb Haemost 4 2006 1396 1404
27. L. Liu, H. Choi, A. Bernardo, A.L. Bergeron, L. Nolasco, and C. Ruan Platelet-derived VWF-cleaving metalloprotease ADAMTS-13 J Thromb Haemost 3 2005 2536 2544
28. M. Suzuki, M. Murata, Y. Matsubara, T. Uchida, H. Ishihara, and T. Shibano Detection of von Willebrand factor-cleaving protease (ADAMTS-13) in human platelets Biochem Biophys Res Commun 313 2004 212 216
29. K. Soejima, H. Nakamura, M. Hirashima, W. Morikawa, C. Nozaki, and T. Nakagaki Analysis on the molecular species and concentration of circulating ADAMTS13 in blood J Biochem 139 2006 147 154
30. J.T. Crawley, J.K. Lam, J.B. Rance, L.R. Mollica, J.S. O'Donnell, and D.A. Lane Proteolytic inactivation of ADAMTS13 by thrombin and plasmin Blood 105 2005 1085 1093
31. T. Ono, J. Mimuro, S. Madoiwa, K. Soejima, Y. Kashiwakura, and A. Ishiwata Severe secondary deficiency of von Willebrand factor-cleaving protease (ADAMTS13) in patients with sepsis-induced disseminated intravascular coagulation: its correlation with development of renal failure Blood 107 2006 528 534
32. M. Uemura, K. Tatsumi, M. Matsumoto, M. Fujimoto, T. Matsuyama, and M. Ishikawa Localization of ADAMTS13 to the stellate cells of human liver Blood 106 2005 922 924
33. W. Zhou, M. Inada, T.P. Lee, D. Benten, S. Lyubsky, and E.E. Bouhassira ADAMTS13 is expressed in hepatic stellate cells Lab Invest 85 2005 780 788
34. M. Niiya, M. Uemura, X.W. Zheng, E.S. Pollak, M. Dockal, and F. Scheiflinger Increased ADAMTS-13 proteolytic activity in rat hepatic stellate cells upon activation in vitro and in vivo J Thromb Haemost 4 2006 1063 1070
35. S. Cal, A.J. Obaya, M. Llamazares, C. Garabaya, V. Quesada, and C. Lopez-Otin Cloning, expression analysis, and structural characterization of seven novel human ADAMTSs, a family of metalloproteinases with disintegrin and thrombospondin-1 domains Gene 283 2002 49 62
36. P. Bork, and G. Beckmann The CUB domain. A widespread module in developmentally regulated proteins J Mol Biol 231 1993 539 545
37. A. Colige, A.L. Sieron, S.W. Li, U. Schwarze, E. Petty, and W. Wertelecki Human Ehlers-Danlos syndrome type VII C and bovine dermatosparaxis are caused by mutations in the procollagen I N-proteinase gene Am J Hum Genet 65 1999 308 317
38. N. Dagoneau, C. Benoist-Lasselin, C. Huber, L. Faivre, A. Megarbane, and A. Alswaid ADAMTS10 mutations in autosomal recessive Weill-Marchesani syndrome Am J Hum Genet 75 2004 801 806
39. H.C. Dietz, G.R. Cutting, R.E. Pyeritz, C.L. Maslen, L.Y. Sakai, and G.M. Corson Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene Nature 352 1991 337 339
40. T.L. Hurskainen, S. Hirohata, M.F. Seldin, and S.S. Apte ADAM-TS5, ADAM-TS6, and ADAM-TS7, novel members of a new family of zinc metalloproteases. General features and genomic distribution of the ADAM-TS family J Biol Chem 274 1999 25555 25563
41. T. Shindo, H. Kurihara, K. Kuno, H. Yokoyama, T. Wada, and Y. Kurihara ADAMTS-1: a metalloproteinase-disintegrin essential for normal growth, fertility, and organ morphology and function J Clin Invest 105 2000 1345 1352
42. M.D. Tortorella, T.C. Burn, M.A. Pratta, I. Abbaszade, J.M. Hollis, and R. Liu Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins Science 284 1999 1664 1666
43. A.K. Chauhan, J. Kisucka, A. Brill, M.T. Walsh, F. Scheiflinger, and D.D. Wagner ADAMTS13: a new link between thrombosis and inflammation J Exp Med 205 2008 2065 2074
44. M. Akiyama, S. Takeda, K. Kokame, J. Takagi, and T. Miyata Crystal structures of the noncatalytic domains of ADAMTS13 reveal multiple discontinuous exosites for von Willebrand factor Proc Natl Acad Sci USA 106 2009 19274 19279
45. G. Bestetti, A. Stellari, A. Lattuada, M. Corbellino, C. Parravicini, and C. Calzarossa ADAMTS 13 genotype and vWF protease activity in an Italian family with TTP Thromb Haemost 90 2003 955 956
46. E.M. Majerus, P.J. Anderson, and J.E. Sadler Binding of ADAMTS13 to von Willebrand factor J Biol Chem 280 2005 21773 21778
47. H.E. Van Wart, and H. Birkedal-Hansen The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family Proc Natl Acad Sci USA 87 1990 5578 5582
48. C. Klaus, B. Plaimauer, J.D. Studt, F. Dorner, B. Lammle, and P.M. Mannucci Epitope mapping of ADAMTS13 autoantibodies in acquired thrombotic thrombocytopenic purpura Blood 103 2004 4514 4519
49. I. Yiallouros, E. Grosse Berkhoff, and W. Stocker The roles of Glu93 and Tyr149 in astacin-like zinc peptidases FEBS Lett 484 2000 224 228
50. W. Bode, C. Fernandez-Catalan, H. Tschesche, F. Grams, H. Nagase, and K. Maskos Structural properties of matrix metalloproteinases Cell Mol Life Sci 55 1999 639 652
51. W. Bode, F.X. Gomis-Ruth, and W. Stockler Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the 'metzincins' FEBS Lett 331 1993 134 140
52. N.D. Rawlings, and A.J. Barrett Evolutionary families of metallopeptidases Methods Enzymol 248 1995 183 228
53. W. Stocker, F. Grams, U. Baumann, P. Reinemer, F.X. Gomis-Ruth, and D.B. McKay The metzincinstopological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases Protein Sci 4 1995 823 840
54. K. Soejima, M. Matsumoto, K. Kokame, H. Yagi, H. Ishizashi, and H. Maeda ADAMTS-13 cysteine-rich/spacer domains are functionally essential for von Willebrand factor cleavage Blood 102 2003 3232 3237
55. X. Zheng, K. Nishio, E.M. Majerus, and J.E. Sadler Cleavage of von Willebrand factor requires the spacer domain of the metalloprotease ADAMTS13 J Biol Chem 278 2003 30136 30141
56. J. Ai, P. Smith, S. Wang, P. Zhang, and X.L. Zheng The proximal carboxyl-terminal domains of ADAMTS13 determine substrate specificity and are all required for cleavage of von Willebrand factor J Biol Chem 280 2005 29428 29434
57. M.D. Gardner, C.K. Chion, R. de Groot, A. Shah, J.T. Crawley, and D.A. Lane A functional calcium-binding site in the metalloprotease domain of ADAMTS13 Blood 113 2009 1149 1157
58. S. Gerhardt, G. Hassall, P. Hawtin, E. McCall, L. Flavell, and C. Minshull Crystal structures of human ADAMTS-1 reveal a conserved catalytic domain and a disintegrin-like domain with a fold homologous to cysteine-rich domains J Mol Biol 373 2007 891 902
59. E.G. Huizinga, S. Tsuji, R.A. Romijn, M.E. Schiphorst, P.G. de Groot, and J.J. Sixma Structures of glycoprotein Ibalpha and its complex with von Willebrand factor A1 domain Science 297 2002 1176 1179
60. R. Schneppenheim, U. Budde, F. Oyen, D. Angerhaus, V. Aumann, and E. Drewke von Willebrand factor cleaving protease and ADAMTS13 mutations in childhood TTP Blood 101 2003 1845 1850
61. P. Bornstein Thrombospondins: structure and regulation of expression FASEB J 6 1992 3290 3299
62. N.H. Guo, H.C. Krutzsch, E. Negre, V.S. Zabrenetzky, and D.D. Roberts Heparin-binding peptides from the type I repeats of thrombospondin. Structural requirements for heparin binding and promotion of melanoma cell adhesion and chemotaxis J Biol Chem 267 1992 19349 19355
63. D.R. Schultz, P.I. Arnold, W. Jy, P.A. Valant, J. Gruber, and Y.S. Ahn Anti-CD36 autoantibodies in thrombotic thrombocytopenic purpura and other thrombotic disorders: identification of an 85 kD form of CD36 as a target antigen Br J Haematol 103 1998 849 857
64. N.N. Tandon, G. Rock, and G.A. Jamieson Anti-CD36 antibodies in thrombotic thrombocytopenic purpura Br J Haematol 88 1994 816 825
65. P. Bornstein Thrombospondins as matricellular modulators of cell function J Clin Invest 107 2001 929 934
66. M.A. McLane, C. Marcinkiewicz, S. Vijay-Kumar, I. Wierzbicka-Patynowski, and S. Niewiarowski Viper venom disintegrins and related molecules Proc Soc Exp Biol Med 219 1998 109 119
67. W. Gao, P.J. Anderson, E.M. Majerus, E.A. Tuley, and J.E. Sadler Exosite interactions contribute to tension-induced cleavage of von Willebrand factor by the antithrombotic ADAMTS13 metalloprotease Proc Natl Acad Sci USA 103 2006 19099 19104
68. E. Di Stasio, S. Lancellotti, F. Peyvandi, R. Palla, P.M. Mannucci, and R. De Cristofaro Mechanistic studies on ADAMTS13 catalysis Biophys J 95 2008 2450 2461
69. Z. Zhou, H. Jing, Z. Tao, H. Choi, K. Aboulfatova, and J. Moake Effects of naturally occurring mutations in CUB-1 domain on synthesis, stability, and activity of ADAMTS-13 Thromb Res 124 2009 323 327
70. Z. Tao, Y. Wang, H. Choi, A. Bernardo, K. Nishio, and J.E. Sadler Cleavage of ultralarge multimers of von Willebrand factor by C-terminal-truncated mutants of ADAMTS-13 under flow Blood 106 2005 141 143
71. J.E. Pimanda, A. Maekawa, T. Wind, J. Paxton, C.N. Chesterman, and P.J. Hogg Congenital thrombotic thrombocytopenic purpura in association with a mutation in the second CUB domain of ADAMTS13 Blood 103 2004 627 629
72. S.G. Shelat, J. Ai, and X.L. Zheng Molecular biology of ADAMTS13 and diagnostic utility of ADAMTS13 proteolytic activity and inhibitor assays Semin Thromb Hemost 31 2005 659 672
73. Z. Tao, Y. Peng, L. Nolasco, S. Cal, C. Lopez-Otin, and R. Li Recombinant CUB-1 domain polypeptide inhibits the cleavage of ULVWF strings by ADAMTS13 under flow conditions Blood 106 2005 4139 4145
74. P. Zhang, W. Pan, A.H. Rux, B.S. Sachais, and X.L. Zheng The cooperative activity between the carboxyl-terminal TSP1 repeats and the CUB domains of ADAMTS13 is crucial for recognition of von Willebrand factor under flow Blood 110 2007 1887 1894
75. H.M. Tsai Shear stress and von Willebrand factor in health and disease Semin Thromb Hemost 29 2003 479 488
76. R. De Cristofaro, F. Peyvandi, R. Palla, S. Lavoretano, R. Lombardi, and G. Merati Role of chloride ions in modulation of the interaction between von Willebrand factor and ADAMTS-13 J Biol Chem 280 2005 23295 23302
77. J.F. Dong, J.L. Moake, L. Nolasco, A. Bernardo, W. Arceneaux, and C.N. Shrimpton ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions Blood 100 2002 4033 4039
78. J.F. Dong Cleavage of ultra-large von Willebrand factor by ADAMTS-13 under flow conditions J Thromb Haemost 3 2005 1710 1716
79. M. Auton, M.A. Cruz, and J. Moake Conformational stability and domain unfolding of the Von Willebrand factor A domains J Mol Biol 366 2007 986 1000
80. R.T. McGrath, E. McRae, O.P. Smith, and J.S. O'Donnell Platelet von Willebrand factor - structure, function and biological importance Br J Haematol 148 2010 834 843
81. J.L. Moake Thrombotic microangiopathies N Engl J Med 347 2002 589 600
82. W.A. Hassenpflug, U. Budde, T. Obser, D. Angerhaus, E. Drewke, and S. Schneppenheim Impact of mutations in the von Willebrand factor A2 domain on ADAMTS13-dependent proteolysis Blood 107 2006 2339 2345
83. J.J. Sutherland, L.A. O'Brien, D. Lillicrap, and D.F. Weaver Molecular modeling of the von Willebrand factor A2 Domain and the effects of associated type 2A von Willebrand disease mutations J Mol Model 10 2004 259 270
84. Q. Zhang, Y.F. Zhou, C.Z. Zhang, X. Zhang, C. Lu, and T.A. Springer Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor Proc Natl Acad Sci USA 106 2009 9226 9231
85. H. Shankaran, and S. Neelamegham Hydrodynamic forces applied on intercellular bonds, soluble molecules, and cell-surface receptors Biophys J 86 2004 576 588
86. K. Nishio, P.J. Anderson, X.L. Zheng, and J.E. Sadler Binding of platelet glycoprotein Ibalpha to von Willebrand factor domain A1 stimulates the cleavage of the adjacent domain A2 by ADAMTS13 Proc Natl Acad Sci USA 101 2004 10578 10583
87. A. Bernardo, C. Ball, L. Nolasco, J.F. Moake, and J.F. Dong Effects of inflammatory cytokines on the release and cleavage of the endothelial cell-derived ultralarge von Willebrand factor multimers under flow Blood 104 2004 100 106
88. J.K. Lam, C.K. Chion, S. Zanardelli, D.A. Lane, and J.T. Crawley Further characterization of ADAMTS-13 inactivation by thrombin J Thromb Haemost 5 2007 1010 1018
89. J.N. George Clinical practice. Thrombotic thrombocytopenic purpura N Engl J Med 354 2006 1927 1935
90. A. Silverstein Thrombotic thrombocytopenic purpura. The initial neurologic manifestations Arch Neurol 18 1968 358 362
91. P. Ruggenenti, and G. Remuzzi Thrombotic microangiopathies Crit Rev Oncol Hematol 11 1991 243 265
92. B.C. McLeod Thrombotic microangiopathies in bone marrow and organ transplant patients J Clin Apher 17 2002 118 123
93. F. Peyvandi, S. Ferrari, S. Lavoretano, M.T. Canciani, and P.M. Mannucci von Willebrand factor cleaving protease (ADAMTS-13) and ADAMTS-13 neutralizing autoantibodies in 100 patients with thrombotic thrombocytopenic purpura Br J Haematol 127 2004 433 439
94. Y. Asada, A. Sumiyoshi, T. Hayashi, J. Suzumiya, and K. Kaketani Immunohistochemistry of vascular lesion in thrombotic thrombocytopenic purpura, with special reference to factor VIII related antigen Thromb Res 38 1985 469 479
95. H.M. Tsai, W.L. Chandler, R. Sarode, R. Hoffman, S. Jelacic, and R.L. Habeeb von Willebrand factor and von Willebrand factor-cleaving metalloprotease activity in Escherichia coli O157:H7-associated hemolytic uremic syndrome Pediatr Res 49 2001 653 659
96. G.A. Hosler, A.M. Cusumano, and G.M. Hutchins Thrombotic thrombocytopenic purpura and hemolytic uremic syndrome are distinct pathologic entities. A review of 56 autopsy cases Arch Pathol Lab Med 127 2003 834 839
97. R.S. Camilleri, H. Cohen, I.J. Mackie, M. Scully, R.D. Starke, and J.T. Crawley Prevalence of the ADAMTS-13 missense mutation R1060W in late onset adult thrombotic thrombocytopenic purpura J Thromb Haemost 6 2008 331 338
98. R. Mahdian, J. Rayes, J.P. Girma, A. Houllier, B. Obert, and D. Meyer Comparison of FRETS-VWF73 to full-length VWF as a substrate for ADAMTS13 activity measurement in human plasma samples Thromb Haemost 95 2006 1049 1051
99. K. Kentouche, U. Budde, M. Furlan, V. Scharfe, R. Schneppenheim, and F. Zintl Remission of thrombotic thrombocytopenic purpura in a patient with compound heterozygous deficiency of von Willebrand factor-cleaving protease by infusion of solvent/detergent plasma Acta Paediatr 91 2002 1056 1059
100. K. Assink, R. Schiphorst, S. Allford, D. Karpman, A. Etzioni, and B. Brichard Mutation analysis and clinical implications of von Willebrand factor-cleaving protease deficiency Kidney Int 63 2003 1995 1999
101. R. Schneppenheim, J.A. Kremer Hovinga, T. Becker, U. Budde, D. Karpman, and W. Brockhaus A common origin of the 4143insA ADAMTS13 mutation Thromb Haemost 96 2006 3 6
102. S. Savasan, S.K. Lee, D. Ginsburg, and H.M. Tsai ADAMTS13 gene mutation in congenital thrombotic thrombocytopenic purpura with previously reported normal VWF cleaving protease activity Blood 101 2003 4449 4451
103. M. Matsumoto, K. Kokame, K. Soejima, M. Miura, S. Hayashi, and Y. Fujii Molecular characterization of ADAMTS13 gene mutations in Japanese patients with Upshaw-Schulman syndrome Blood 103 2004 1305 1310
104. T. Uchida, H. Wada, M. Mizutani, M. Iwashita, H. Ishihara, and T. Shibano Identification of novel mutations in ADAMTS13 in an adult patient with congenital thrombotic thrombocytopenic purpura Blood 104 2004 2081 2083
105. C. Licht, L. Stapenhorst, T. Simon, U. Budde, R. Schneppenheim, and B. Hoppe Two novel ADAMTS13 gene mutations in thrombotic thrombocytopenic purpura/hemolytic-uremic syndrome (TTP/HUS) Kidney Int 66 2004 955 958
106. C.E. Snider, J.C. Moore, T.E. Warkentin, C.N. Finch, C.P. Hayward, and J.G. Kelton Dissociation between the level of von Willebrand factor-cleaving protease activity and disease in a patient with congenital thrombotic thrombocytopenic purpura Am J Hematol 77 2004 387 390
107. M. Noris, S. Bucchioni, M. Galbusera, R. Donadelli, E. Bresin, and F. Castelletti Complement factor H mutation in familial thrombotic thrombocytopenic purpura with ADAMTS13 deficiency and renal involvement J Am Soc Nephrol 16 2005 1177 1183
108. F. Liu, J. Jin, N.Z. Dong, Y.G. Wang, and C.G. Ruan Identification of two novel mutations in ADAMTS13 gene in a patient with hereditary thrombotic thrombocytopenic purpura Zhonghua Xue Ye Xue Za Zhi 26 2005 521 524
109. R. Donadelli, F. Banterla, M. Galbusera, C. Capoferri, S. Bucchioni, and S. Gastoldi In-vitro and in-vivo consequences of mutations in the von Willebrand factor cleaving protease ADAMTS13 in thrombotic thrombocytopenic purpura Thromb Haemost 96 2006 454 464
110. F. Peyvandi, S. Lavoretano, R. Palla, C. Valsecchi, G. Merati, and R. De Cristofaro Mechanisms of the interaction between two ADAMTS13 gene mutations leading to severe deficiency of enzymatic activity Hum Mutat 27 2006 330 336
111. R. Palla, S. Lavoretano, R. Lombardi, I. Garagiola, M. Karimi, and A. Afrasiabi The first deletion mutation in the TSP1-6 repeat domain of ADAMTS13 in a family with inherited thrombotic thrombocytopenic purpura Haematologica 94 2009 289 293
112. B. Plaimauer, J. Fuhrmann, G. Mohr, W. Wernhart, K. Bruno, and S. Ferrari Modulation of ADAMTS13 secretion and specific activity by a combination of common amino acid polymorphisms and a missense mutation Blood 107 2006 118 125
113. Y. Shibagaki, M. Matsumoto, K. Kokame, S. Ohba, T. Miyata, and Y. Fujimura Novel compound heterozygote mutations (H234Q/R1206X) of the ADAMTS13 gene in an adult patient with Upshaw-Schulman syndrome showing predominant episodes of repeated acute renal failure Nephrol Dial Transplant 21 2006 1289 1292
114. Z. Tao, K. Anthony, Y. Peng, H. Choi, L. Nolasco, and L. Rice Novel ADAMTS-13 mutations in an adult with delayed onset thrombotic thrombocytopenic purpura J Thromb Haemost 4 2006 1931 1935
115. A. Hommais, J. Rayes, A. Houllier, B. Obert, P. Legendre, and A. Veyradier Molecular characterization of four ADAMTS13 mutations responsible for congenital thrombotic thrombocytopenic purpura (Upshaw-Schulman syndrome) Thromb Haemost 98 2007 593 599
116. S.C. Meyer, R. Jeddi, B. Meddeb, E. Gouider, B. Lammle, and J.A. Kremer Hovinga A first case of congenital TTP on the African continent due to a new homozygous mutation in the catalytic domain of ADAMTS13 Ann Hematol 87 2008 663 666
117. K. Kokame, Y. Aoyama, M. Matsumoto, Y. Fujimura, and T. Miyata Inherited and de novo mutations of ADAMTS13 in a patient with Upshaw-Schulman syndrome J Thromb Haemost 6 2008 213 215
118. I. Garagiola, C. Valsecchi, S. Lavoretano, H. Oren, M. Bohm, and F. Peyvandi Nonsense-mediated mRNA decay in the ADAMTS13 gene caused by a 29-nucleotide deletion Haematologica 93 2008 1678 1685
119. Y. Fujimura, M. Matsumoto, K. Kokame, A. Isonishi, K. Soejima, and N. Akiyama Pregnancy-induced thrombocytopenia and TTP, and the risk of fetal death, in Upshaw-Schulman syndrome: a series of 15 pregnancies in 9 genotyped patients Br J Haematol 144 2009 742 754
120. M. Manea, A. Kristoffersson, H.M. Tsai, W. Zhou, I. Winqvist, and G. Oldaeus ADAMTS13 phenotype in plasma from normal individuals and patients with thrombotic thrombocytopenic purpura Eur J Pediatr 166 2007 249 257
121. D.G. Motto, A.K. Chauhan, G. Zhu, J. Homeister, C.B. Lamb, and K.C. Desch Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice J Clin Invest 115 2005 2752 2761
122. F. Banno, K. Kokame, T. Okuda, S. Honda, S. Miyata, and H. Kato Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura Blood 107 2006 3161 3166
123. L.H. Nolasco, N.A. Turner, A. Bernardo, Z. Tao, T.G. Cleary, and J.F. Dong Hemolytic uremic syndrome-associated Shiga toxins promote endothelial-cell secretion and impair ADAMTS13 cleavage of unusually large von Willebrand factor multimers Blood 106 2005 4199 4209
124. H.M. Tsai Pathophysiology of thrombotic thrombocytopenic purpura Int J Hematol 91 2010 1 19
125. M.J. Jang, N.K. Kim, S.Y. Chong, H.J. Kim, S.J. Lee, and M.S. Kang Frequency of Pro475Ser polymorphism of ADAMTS13 gene and its association with ADAMTS-13 activity in the Korean population Yonsei Med J 49 2008 405 408
126. M. Akiyama, K. Kokame, and T. Miyata ADAMTS13 P475S polymorphism causes a lowered enzymatic activity and urea lability in vitro J Thromb Haemost 6 2008 1830 1832
127. J.E. Sadler, J.L. Moake, T. Miyata, and J.N. George Recent advances in thrombotic thrombocytopenic purpura Hematology Am Soc Hematol Educ Program 2004 407 423
128. P. Coppo, D. Bengoufa, A. Veyradier, M. Wolf, A. Bussel, and G.A. Millot Severe ADAMTS13 deficiency in adult idiopathic thrombotic microangiopathies defines a subset of patients characterized by various autoimmune manifestations, lower platelet count, and mild renal involvement Medicine (Baltimore) 83 2004 233 244
129. X.L. Zheng, R.M. Kaufman, L.T. Goodnough, and J.E. Sadler Effect of plasma exchange on plasma ADAMTS13 metalloprotease activity, inhibitor level, and clinical outcome in patients with idiopathic and nonidiopathic thrombotic thrombocytopenic purpura Blood 103 2004 4043 4049
130. M. Rieger, P.M. Mannucci, J.A. Kremer Hovinga, A. Herzog, G. Gerstenbauer, and C. Konetschny ADAMTS13 autoantibodies in patients with thrombotic microangiopathies and other immunomediated diseases Blood 106 2005 1262 1267
131. P.M. Mannucci Thrombotic thromboytopenic purpura: another example of immunomediated thrombosis Pathophysiol Haemost Thromb 35 2006 89 97
132. P.M. Mannucci, M. Bohm, I. Scharrer, and F. Scheiflinger Patterns of changes of anti-ADAMTS13 after plasma exchange J Thromb Haemost 4 2006 1405 1406
133. B. Waters, M. Qadura, E. Burnett, R. Chegeni, A. Labelle, and P. Thompson Anti-CD3 prevents factor VIII inhibitor development in hemophilia A mice by a regulatory CD4+CD25+-dependent mechanism and by shifting cytokine production to favor a Th1 response Blood 113 2009 193 203
134. D.R. Terrell, L.A. Williams, S.K. Vesely, B. Lammle, J.A. Hovinga, and J.N. George The incidence of thrombotic thrombocytopenic purpura-hemolytic uremic syndrome: all patients, idiopathic patients, and patients with severe ADAMTS-13 deficiency J Thromb Haemost 3 2005 1432 1436
135. S. Ferrari, G.C. Mudde, M. Rieger, A. Veyradier, J.A. Kremer Hovinga, and F. Scheiflinger IgG subclass distribution of anti-ADAMTS13 antibodies in patients with acquired thrombotic thrombocytopenic purpura J Thromb Haemost 7 2009 1703 1710
136. L. Dong, V. Chandrasekaran, W. Zhou, and H.M. Tsai Evolution of ADAMTS13 antibodies in a fatal case of thrombotic thrombocytopenic purpura Am J Hematol 83 2008 815 817
137. W. Zhou, L. Dong, D. Ginsburg, E.E. Bouhassira, and H.M. Tsai Enzymatically active ADAMTS13 variants are not inhibited by anti-ADAMTS13 autoantibodies: a novel therapeutic strategy? J Biol Chem 280 2005 39934 39941
138. B.M. Luken, E.A. Turenhout, J.J. Hulstein, J.A. Van Mourik, R. Fijnheer, and J. Voorberg The spacer domain of ADAMTS13 contains a major binding site for antibodies in patients with thrombotic thrombocytopenic purpura Thromb Haemost 93 2005 267 274
139. B.M. Luken, P.H. Kaijen, E.A. Turenhout, J.A. Kremer Hovinga, J.A. van Mourik, and R. Fijnheer 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 4 2006 2355 2364
140. B.M. Luken, E.A. Turenhout, P.H. Kaijen, M.J. Greuter, W. Pos, and J.A. van Mourik 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 96 2006 295 301
141. H.M. Tsai, A. Li, and G. Rock Inhibitors of von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura Clin Lab 47 2001 387 392
142. E.J. Favaloro, R. Bonar, G. Kershaw, E. Duncan, J. Sioufi, and K. Marsden Investigations from external quality assurance programs reveal a high degree of variation in the laboratory identification of coagulation factor inhibitors Semin Thromb Hemost 35 2009 794 805
143. R. Yomtovian, W. Niklinski, B. Silver, R. Sarode, and H.M. Tsai Rituximab for chronic recurring thrombotic thrombocytopenic purpura: a case report and review of the literature Br J Haematol 124 2004 787 795
144. M.P. Ruiz-Torres, F. Casiraghi, M. Galbusera, D. Macconi, S. Gastoldi, and M. Todeschini Complement activation: the missing link between ADAMTS-13 deficiency and microvascular thrombosis of thrombotic microangiopathies Thromb Haemost 93 2005 443 452
145. P.M. Mannucci, M. Vanoli, I. Forza, M.T. Canciani, and R. Scorza Von Willebrand factor cleaving protease (ADAMTS-13) in 123 patients with connective tissue diseases (systemic lupus erythematosus and systemic sclerosis) Haematologica 88 2003 914 918
146. M. Uemura, T. Matsuyama, M. Ishikawa, M. Fujimoto, H. Kojima, and S. Sakurai Decreased activity of plasma ADAMTS13 may contribute to the development of liver disturbance and multiorgan failure in patients with alcoholic hepatitis Alcohol Clin Exp Res 29 2005 264S 271S
147. K. Martin, D. Borgel, N. Lerolle, H.B. Feys, L. Trinquart, and K. Vanhoorelbeke Decreased ADAMTS-13 (A disintegrin-like and metalloprotease with thrombospondin type 1 repeats) is associated with a poor prognosis in sepsis-induced organ failure Crit Care Med 35 2007 2375 2382
148. D. Larkin, B. de Laat, P.V. Jenkins, J. Bunn, A.G. Craig, and V. Terraube Severe Plasmodium falciparum malaria is associated with circulating ultra-large von Willebrand multimers and ADAMTS13 inhibition PLoS Pathog 5 2009 e1000349
149. M. Uemura, Y. Fujimura, M. Matsumoto, H. Ishizashi, S. Kato, and T. Matsuyama Comprehensive analysis of ADAMTS13 in patients with liver cirrhosis Thromb Haemost 99 2008 1019 1029
150. D.J. Bridges, J. Bunn, J.A. van Mourik, G. Grau, R.J. Preston, and M. Molyneux Rapid activation of endothelial cells enables Plasmodium falciparum adhesion to platelet-decorated von Willebrand factor strings Blood 115 2010 1472 1474
151. E.C. Lowenberg, P. Charunwatthana, S. Cohen, B.J. van den Born, J.C. Meijers, and E.B. Yunus Severe malaria is associated with a deficiency of von Willebrand factor cleaving protease, ADAMTS13 Thromb Haemost 103 2010 181 187
152. V. Bianchi, R. Robles, L. Alberio, M. Furlan, and B. Lammle Von Willebrand factor-cleaving protease (ADAMTS13) in thrombocytopenic disorders: a severely deficient activity is specific for thrombotic thrombocytopenic purpura Blood 100 2002 710 713
153. A. Sanchez-Luceros, C.E. Farias, M.M. Amaral, A.C. Kempfer, R. Votta, and C. Marchese von Willebrand factor-cleaving protease (ADAMTS13) activity in normal non-pregnant women, pregnant and post-delivery women Thromb Haemost 92 2004 1320 1326
154. A. Lattuada, E. Rossi, C. Calzarossa, R. Candolfi, and P.M. Mannucci Mild to moderate reduction of a von Willebrand factor cleaving protease (ADAMTS-13) in pregnant women with HELLP microangiopathic syndrome Haematologica 88 2003 1029 1034
155. J.N. George The association of pregnancy with thrombotic thrombocytopenic purpura-hemolytic uremic syndrome Curr Opin Hematol 10 2003 339 344
156. A. Bonnefoy, K. Daenens, H.B. Feys, R. De Vos, P. Vandervoort, and J. Vermylen Thrombospondin-1 controls vascular platelet recruitment and thrombus adherence in mice by protecting (sub)endothelial VWF from cleavage by ADAMTS13 Blood 107 2006 955 964
157. C.M. Eckmann, R.T. De Laaf, J.M. Van Keulen, J.A. Van Mourik, and B. De Laat Bilirubin oxidase as a solution for the interference of hyperbilirubinemia with ADAMTS-13 activity measurement by FRETS-VWF73 assay J Thromb Haemost 5 2007 1330 1331
158. J. Chen, X. Fu, Y. Wang, M. Ling, B. McMullen, and J. Kulman Oxidative
159. S. Lancellotti, V. De Filippis, N. Pozzi, F. Peyvandi, R. Palla, and B. Rocca Formation of methionine sulfoxide by peroxynitrite at position 1606 of von Willebrand factor inhibits its cleavage by ADAMTS-13: a new prothrombotic mechanism in diseases associated with oxidative stress Free Radic Biol Med 48 2010 446 456
160. S.C. Meyer, I. Sulzer, B. Lammle, and J.A. Kremer Hovinga Hyperbilirubinemia interferes with ADAMTS-13 activity measurement by FRETS-VWF73 assay: diagnostic relevance in patients suffering from acute thrombotic microangiopathies J Thromb Haemost 5 2007 866 867
161. T.J. Raife, W. Cao, B.S. Atkinson, B. Bedell, R.R. Montgomery, and S.R. Lentz Leukocyte proteases cleave von Willebrand factor at or near the ADAMTS13 cleavage site Blood 114 2009 1666 1674
162. J.A. Hovinga, S.K. Vesely, D.R. Terrell, B. Lammle, and J.N. George Survival and relapse in patients with thrombotic thrombocytopenic purpura Blood 115 2010 1500 1511 quiz 1662
163. A. Tripodi, V. Chantarangkul, M. Bohm, U. Budde, J.F. Dong, and K.D. Friedman Measurement of von Willebrand factor cleaving protease (ADAMTS-13): results of an international collaborative study involving 11 methods testing the same set of coded plasmas J Thromb Haemost 2 2004 1601 1609
164. A. Tripodi, F. Peyvandi, V. Chantarangkul, R. Palla, A. Afrasiabi, and M.T. Canciani Second international collaborative study evaluating performance characteristics of methods measuring the von Willebrand factor cleaving protease (ADAMTS-13) J Thromb Haemost 6 2008 1534 1541
165. H. Wada, T. Kaneko, M. Ohiwa, M. Tanigawa, S. Tamaki, and N. Minami Plasma cytokine levels in thrombotic thrombocytopenic purpura Am J Hematol 40 1992 167 170
166. A. Klukowska, E. Niewiadomska, U. Budde, F. Oyen, and R. Schneppenheim Difficulties in diagnosing congenital thrombotic thrombocytopenic purpura J Pediatr Hematol Oncol 32 2010 103 107
167. H.W. Park, D. Oh, N. Kim, H.Y. Cho, K.C. Moon, and J.H. Chae Congenital thrombotic thrombocytopenic purpura associated with unilateral moyamoya disease Pediatr Nephrol 23 2008 1555 1558