Inherited ADAMTS13 deficiency (Upshaw-Schulman syndrome): A short review

Thrombosis Research

Volumn 134, Issue 6, 2014, Pages 1171-1175

  Pérez Rodríguez, Almudena ^a   Lourés, Esther ^a   Rodríguez Trillo, Ángela ^a   Costa Pinto, Joana ^a   García Rivero, Aránzazu ^b   Batlle López, Ana ^c,d   Batlle, Javier ^a   López Fernández, María Fernanda ^a  

^a HOSPITAL JUAN CANALEJO   (Spain)

^b Centro Oncologico de Galicia   (Spain)

^c HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^d UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

ADAMTS13; Mutation; Thrombotic thrombocytopenic purpura; Upshaw Schulman syndrome

Indexed keywords

FRESH FROZEN PLASMA; METHYLPREDNISOLONE; RECOMBINANT ENZYME; RITUXIMAB; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN;

AUTOIMMUNE HEMOLYTIC ANEMIA; BLOOD CLOTTING; CARBOXY TERMINAL SEQUENCE; CHILDHOOD; DISEASE COURSE; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME STRUCTURE; EXON; FEVER; GENE MUTATION; GENETIC HETEROGENEITY; GENOTYPE; HEMOLYTIC ANEMIA; HEMOLYTIC UREMIC SYNDROME; HOMOZYGOSITY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFANCY; NEONATAL THROMBOCYTOPENIA; NEUROLOGIC DISEASE; NONHUMAN; PATHOGENESIS; PHENOTYPE; PLASMA TRANSFUSION; PLASMAPHERESIS; PREVALENCE; PROPHYLAXIS; PROTEIN DEGRADATION; PROTEIN SECRETION; REVIEW; SHEAR STRESS; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOCYTE COUNT; THROMBOCYTOPENIA; THROMBOTIC THROMBOCYTOPENIC PURPURA; UPSHAW SCHULMAN SYNDROME; VON WILLEBRAND FACTOR CLEAVING PROTEINASE DEFICIENCY; DEFICIENCY; GENETIC PREDISPOSITION; GENETIC SCREENING; GENETICS; PLASMA; PROCEDURES; PURPURA, THROMBOTIC THROMBOCYTOPENIC;

ADAM PROTEINS; GENETIC PREDISPOSITION TO DISEASE; GENETIC TESTING; HUMANS; PLASMA; POLYMORPHISM, SINGLE NUCLEOTIDE; PURPURA, THROMBOTIC THROMBOCYTOPENIC;

EID: 84915805225     PISSN: 00493848     EISSN: 18792472     Source Type: Journal    
DOI: 10.1016/j.thromres.2014.09.004     Document Type: Review

References (80)

1. E. Moschcowitz Hyalin thrombosis of the terminal arterioles and capillaries: A hitherto underscribed disease Proc N Y Pathol Soc 24 1924 21 24
2. 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
3. J.L. Moake Thrombotic microangiopathies N Engl J Med 347 2002 589 600
4. J.N. George Clinical practice. Thrombotic thrombocytopenic purpura N Engl J Med 354 2006 1927 1935
5. K.R. McCrae Thrombocytopenia in pregnancy Hematol Am Soc Hematol Educ Program 2010 2010 397 402
6. J.E. Sadler Von Willebrand factor, ADAMTS13, and thrombotic thrombocytopenic purpura Blood 112 1 2008 11 18
7. H.M. Tsai Pathophysiology of thrombotic thrombocytopenic purpura Int J Hematol 91 1 2010 1 19
8. 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
9. L.A. Sporn, V.J. Marder, and D.D. Wagner Inducible secretion of large, biologically potent von Willebrand factor multimers Cell 46 1986 185 190
10. 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
11. J.A. Dent, M. Galbusera, and Z.M. Ruggeri Heterogeneity of plasma von Willebrand factor multimers resulting from proteolysis of the constituent subunit J Clin Invest 88 1991 774 782
12. M. Furlan, R. Robles, D. Affolter, D. Meyer, P. Baillod, and B. Lämmle Triplet structure of von Willebrand factor reflects proteolytic degradation of high molecular weight multimers Proc Natl Acad Sci U S A 90 1993 7503 7507
13. 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
14. K. Fujikawa, H. Suzuki, B. McMullen, and D. Chung Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family Blood 98 2001 1662 1666
15. H.E. Gerritsen, R. Robles, B. Lämmle, and M. Furlan Partial amino acid sequence of purified von Willebrand factor-cleaving protease Blood 98 2001 1654 1661
16. 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
17. 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
18. 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
19. 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 [Erratum in: J Biochem (Tokyo) 2001;130:719]
20. 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
21. 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
22. 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
23. M. Furlan, R. Robles, and B. Lämmle 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
24. 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
25. F. Scheiflinger, P. Knöbl, B. Trattner, B. Plaimauer, G. Mohr, and M. Dockal Nonneutralizing IgM and IgG antibodies to von Willebrand factor-cleaving protease (ADAMTS-13) in a patient with thrombotic thrombocytopenic purpura Blood 102 2003 3241 3243
26. 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
27. 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
28. 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
29. K. Kokame, and T. Miyata Genetic defects leading to hereditary thrombotic thrombocytopenic purpura Semin Hematol 41 2004 34 40
30. 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
31. 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
32. A. Veyradier, J.M. Lavergne, A.S. Ribba, B. Obert, C. Loirat, and D. Meyer Ten candidate ADAMTS13 mutations in six French families with congenital thrombotic thrombocytopenic purpura (Upshaw-Schulman syndrome) J Thromb Haemost 2 2004 424 429
33. I. Schulman, M. Pierce, A. Lukens, and Z. Currimbhoy Studies on thrombopoiesis, I: a factor in normal human plasma required for platelet production; chronic thrombocytopenia due to its deficiency Blood 16 1960 943 957
34. J.D. Upshaw Jr. Congenital deficiency of a factor in normal plasma that reverses microangiopathic hemolysis and thrombocytopenia N Engl J Med 298 1978 1350 1352
35. M. Furlan, and B. Lämmle Aetiology and pathogenesis of thrombotic thrombocytopenic purpura and haemolytic uraemic syndrome: the role of von Willebrand factor-cleaving protease Best Pract Res Clin Haematol 14 2001 437 454
36. L.A. Lotta, H.M. Wu, I.J. Mackie, M. Noris, A. Veyradier, and M.A. Scully Residual plasmatic activity of ADAMTS13 is correlated with phenotype severity in congenital thrombotic thrombocytopenic purpura Blood 120 2012 440 448
37. W.A. Hassenpflug, U. Budde, S. Schneppenheim, and R. Schneppenheim Inherited thrombotic thrombocytopenic purpura in children Semin Thromb Hemost 40 2014 487 492
38. A. Veyradier, B. Obert, E. Haddad, S. Cloarec, H. Nivet, and M. Foulard Severe deficiency of the specific von Willebrand factor-cleaving protease (ADAMTS 13) activity in a subgroup of children with atypical hemolytic uremic syndrome J Pediatr 142 2003 310 317 [Erratum in: J Pediatr. 2003;142:616. Loriat, C [corrected to Loirat, C]]
39. J.A. Kremer Hovinga, J.D. Studt, and B. Lämmle The von Willebrand factor-cleaving protease (ADAMTS-13) and the diagnosis of thrombotic thrombocytopenic purpura (TTP) Pathophysiol Haemost Thromb 33 2003 417 421
40. 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
41. 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
42. 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
43. 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
44. 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 U S A 99 2002 11902 11907
45. G. Antoine, K. Zimmermann, B. Plaimauer, M. Grillowitzer, J.D. Studt, and B. Lämmle ADAMTS13 gene defects in two brothers with constitutional thrombotic thrombocytopenic purpura and normalization of von Willebrand factor-cleaving protease activity by recombinant human ADAMTS13 Br J Haematol 120 2003 821 824
46. 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
47. 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
48. 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
49. F. Peyvandi, S. Ferrari, S. Lavoretano, M.T. Canciani, and P.M. von Mannucci 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
50. 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
51. S.C. Meyer, R. Jeddi, B. Meddeb, E. Gouider, B. Lämmle, 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
52. S.H. Lee, J.H. Park, S.K. Park, E.H. Lee, J.I. Choi, and G.P. Visentin A novel homozygous missense ADAMTS13 mutation Y658C in a patient with recurrent thrombotic thrombocytopenic purpura Ann Clin Lab Sci 41 2011 273 276
53. A. Borgi, M. Khemiri, A. Veyradier, K. Kazdaghli, and S. Barsaoui Congenital thrombotic thrombocytopenic purpura: Atypical presentation and new ADAMTS 13 mutation in a Tunisian child Mediterr J Hematol Infect Dis 3 5 2013 e2013041
54. M. Mansouri Taleghani, A.S. von Krogh, Y. Fujimura, J.N. George, I. Hrachovinová, and P.N. Knöbl Hereditary thrombotic thrombocytopenic purpura and the hereditary TTP registry Hamostaseologie 33 2013 138 143
55. R.S. Camilleri, M. Scully, M. Thomas, I.J. Mackie, R. Liesner, and W.J. Chen A phenotype-genotype correlation of ADAMTS13 mutations in congenital thrombotic thrombocytopenic purpura patients treated in the United Kingdom J Thromb Haemost 10 2012 1792 1801
56. 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
57. 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
58. 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
59. M. Noris, S. Bucchioni, M. Galbusera, R. Donadelli, E. Bresin, and F. Castelletti International Registry of Recurrent and Familial HUS/TTP. Complement factor H mutation in familial thrombotic thrombocytopenic purpura with ADAMTS13 deficiency and renal involvement J Am Soc Nephrol 16 2005 1177 1183
60. K.C. Desch, and D.G. Motto Thrombotic thrombocytopenic purpura in humans and mice Arterioscler Thromb Vasc Biol 27 2007 1901 1908
61. L.A. Lotta, H.M. Wu, K.M. Musallam, and F. Peyvandi The emerging concept of residual ADAMTS13 activity in ADAMTS13-deficient thrombotic thrombocytopenic purpura Blood Rev 27 2013 71 76
62. K. Vanhoorelbeke, and S.F. De Meyer Animal models for thrombotic thrombocytopenic purpura J Thromb Haemost 11 Suppl. 1 2013 2 10
63. 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
64. 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
65. A. Pérez-Rodríguez, A. Batlle-López, R. Blanco, I. Varela, J. León, and M.D. Delgado A novel mutation in the ADAMTS13 of a child with Upshaw-Schulman Syndrome Thromb Haemost 112 2014 (ahead of print)
66. M. Moatti-Cohen, C. Garrec, M. Wolf, P. Boisseau, L. Galicier, and E. Azoulay Unexpected frequency of Upshaw-Schulman syndrome in pregnancy-onset thrombotic thrombocytopenic purpura Blood 119 2012 5888 5897
67. 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
68. 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
69. 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
70. 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
71. L.A. Lotta, I. Garagiola, R. Palla, A. Cairo, and F. Peyvandi ADAMTS13 mutations and polymorphisms in congenital thrombotic thrombocytopenic purpura Hum Mutat 31 2010 11 19
72. M. Furlan, R. Robles, B. Morselli, P. Sandoz, and B. Lämmle Recovery and half-life of von Willebrand factor-cleaving protease after plasma therapy in patients with thrombotic thrombocytopenic purpura Thromb Haemost 81 1999 8 13
73. J. Barbot, E. Costa, M. Guerra, M.S. Barreirinho, P. Isvarlal, and R. Robles Ten years of prophylactic treatment with fresh-frozen plasma in a child with chronic relapsing thrombotic thrombocytopenic purpura as a result of a congenital deficiency of von Willebrand factor-cleaving protease Br J Haematol 113 2001 649 651
74. J.N. George How I treat patients with thrombotic thrombocytopenic purpura: 2010 Blood 116 20 2010 Nov 18 4060-9 10.1182/blood-2010-07-271445 [Epub 2010 Aug 4. Erratum in: Blood. 2011;117:5551]
75. Y. Fujimura, M. Matsumoto, A. Isonishi, H. Yagi, K. Kokame, and K. Soejima Natural history of Upshaw-Schulman syndrome based on ADAMTS13 gene analysis in Japan J Thromb Haemost 9 Suppl. 1 2011 283 301
76. P. Blombery, and M. Scully Management of thrombotic thrombocytopenic purpura: current perspectives J Blood Med 5 2014 15 23
77. M. Scully, and T. Goodship How I treat thrombotic thrombocytopenic purpura and atypical haemolytic uraemic syndrome Br J Haematol 164 2014 759 766
78. C. Loirat, P. Coppo, and A. Veyradier Thrombotic thrombocytopenic purpura in children Curr Opin Pediatr 25 2013 216 224
79. B. Plaimauer, K. Zimmermann, D. Völkel, 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
80. A. Schiviz, K. Wuersch, C. Piskernik, B. Dietrich, W. Hoellriegl, and H. Rottensteiner A new mouse model mimicking thrombotic thrombocytopenic purpura: correction of symptoms by recombinant human ADAMTS13 Blood 119 2012 6128 6135