Use of a mouse model to elucidate the phenotypic effects of the von Willebrand factor cleavage mutants, Y1605A/M1606A and R1597W

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 5, 2012, Pages 940-950

  Pruss, C M ^a   Golder, M ^a   Bryant, A ^a   Hegadorn, C ^a   Haberichter, S ^b,c   Lillicrap, D ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

ADAMTS13; Cleavage; Hemostasis; Mouse model; Von willebrand disease; Von willebrand factor

Indexed keywords

COMPLEMENTARY DNA; FERRIC CHLORIDE; MUTANT PROTEIN; RECOMBINANT PROTEIN; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HYDRODYNAMICS; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; THROMBOGENESIS; THROMBOSIS;

ANIMALS; BLOOD COAGULATION; BLOTTING, WESTERN; CHLORIDES; DISEASE MODELS, ANIMAL; FERRIC COMPOUNDS; GENE TRANSFER TECHNIQUES; GENOTYPE; HEK293 CELLS; HUMANS; INFUSIONS, INTRAVENOUS; INJECTIONS, INTRAVENOUS; METALLOENDOPEPTIDASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR WEIGHT; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENOTYPE; PLATELET ACTIVATION; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; THROMBOSIS; TIME FACTORS; TRANSFECTION; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR;

EID: 84860454336     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2012.04675.x     Document Type: Article

References (33)

1. Sadler JE. Biochemistry and genetics of von willebrand factor. Annu Rev Biochem 1998; 67: 395-424.
2. Plaimauer B, Zimmermann K, Volkel D, Antoine G, Kerschbaumer R, Jenab P, Furlan M, Gerritsen H, Lammle B, Schwarz HP, Scheiflinger F. Cloning, expression, and functional characterization of the von willebrand factor-cleaving protease (ADAMTS13). Blood 2002; 100: 3626-32.
3. Hassenpflug WA, Budde U, Obser T, Angerhaus D, Drewke E, Schneppenheim S, Schneppenheim R. Impact of mutations in the von willebrand factor A2 domain on ADAMTS13-dependent proteolysis. Blood 2006; 107: 2339-45.
4. Baronciani L, Federici AB, Cozzi G, Canciani MT, Mannucci PM. von willebrand factor collagen binding assay in von willebrand disease type 2A, 2B, and 2M. J Thromb Haemost 2006; 4: 2088-90.
5. Moake JL. von willebrand factor, ADAMTS-13, and thrombotic thrombocytopenic purpura. Semin Hematol 2004; 41: 4-14.
6. von willebrand disease international database [homepage on the Internet]. Accessed 12 May 2011.
7. Zhang Q, Zhou YF, Zhang CZ, Zhang X, Lu C, Springer TA. Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von willebrand factor. Proc Natl Acad Sci USA 2009; 106: 9226-31.
8. Pruss CM, Notley CR, Hegadorn CA, O'Brien LA, Lillicrap D. ADAMTS13 cleavage efficiency is altered by mutagenic and, to a lesser extent, polymorphic sequence changes in the A1 and A2 domains of von willebrand factor. Br J Haematol 2008; 143: 552-8.
9. Zanardelli S, Crawley JT, Chion CK, Lam JK, Preston RJ, Lane DA. ADAMTS13 substrate recognition of von willebrand factor A2 domain. J Biol Chem 2006; 281: 1555-63.
10. Lyons SE, Bruck ME, Bowie EJ, Ginsburg D. Impaired intracellular transport produced by a subset of type IIA von willebrand disease mutations. J Biol Chem 1992; 267: 4424-30.
11. de Groot R, Lane DA, Crawley JT. The ADAMTS13 metalloprotease domain: roles of subsites in enzyme activity and specificity. Blood 2010; 116: 3064-72.
12. Motto DG, Chauhan AK, Zhu G, Homeister J, Lamb CB, Desch KC, Zhang W, Tsai HM, Wagner DD, Ginsburg D. Shigatoxin triggers thrombotic thrombocytopenic purpura in genetically susceptible ADAMTS13-deficient mice. J Clin Invest 2005; 115: 2752-61.
13. Banno F, Kokame K, Okuda T, Honda S, Miyata S, Kato H, Tomiyama Y, Miyata T. Complete deficiency in ADAMTS13 is prothrombotic, but it alone is not sufficient to cause thrombotic thrombocytopenic purpura. Blood 2006; 107: 3161-6.
14. Marx I, Christophe OD, Lenting PJ, Rupin A, Vallez MO, Verbeuren TJ, Denis CV. Altered thrombus formation in von willebrand factor-deficient mice expressing von willebrand factor variants with defective binding to collagen or GPIIbIIIa. Blood 2008; 112: 603-9.
15. Pruss CM, Golder M, Bryant A, Hegadorn CA, Burnett E, Laverty K, Sponagle K, Dhala A, Notley C, Haberichter S, Lillicrap D. Pathologic mechanisms of type 1 von willebrand disease mutations R1205H and Y1584C through in vitro and in vivo mouse models. Blood 2011; 117: 4358-66.
16. Golder M, Pruss CM, Hegadorn C, Mewburn J, Laverty K, Sponagle K, Lillicrap D. Mutation-specific hemostatic variability in mice expressing common type 2B von willebrand disease substitutions. Blood 2010; 115: 4862-9.
17. Rayes J, Hollestelle MJ, Legendre P, Marx I, de Groot PG, Christophe OD, Lenting PJ, Denis CV. Mutation & ADAMTS13-dependent modulation of disease severity in a mouse model for von willebrand disease type 2B. Blood 2010; 115: 4870-7.
18. Kokame K, Matsumoto M, Fujimura Y, Miyata T. VWF73, a region from D1596 to R1668 of von willebrand factor, provides a minimal substrate for ADAMTS-13. Blood 2004; 103: 607-12.
19. Kato S, Matsumoto M, Matsuyama T, Isonishi A, Hiura H, Fujimura Y. Novel monoclonal antibody-based enzyme immunoassay for determining plasma levels of ADAMTS13 activity. Transfusion 2006; 46: 1444-52.
20. Bruno K, Volkel D, Plaimauer B, Antoine G, Pable S, Motto DG, Lemmerhirt HL, Dorner F, Zimmermann K, Scheiflinger F. Cloning, expression and functional characterization of the full-length murine ADAMTS13. J Thromb Haemost 2005; 3: 1064-73.
21. Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, Wagner DD. A mouse model of severe von willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci USA 1998; 95: 9524-9.
22. Varadi K, Rottensteiner H, Vejda S, Weber A, Muchitsch EM, Turecek PL, Ehrlich HJ, Scheiflinger F, Schwarz HP. Species-dependent variability of ADAMTS13-mediated proteolysis of human recombinant von willebrand factor. J Thromb Haemost 2009; 7: 1134-42.
23. Chitta MS, Duhe RJ, Kermode JC. Cloning of the cDNA for murine von willebrand factor and identification of orthologous genes reveals the extent of conservation among diverse species. Platelets 2007; 18: 182-98.
24. Banno F, Kaminaka K, Soejima K, Kokame K, Miyata T. Identification of strain-specific variants of mouse Adamts13 gene encoding von willebrand factor-cleaving protease. J Biol Chem 2004; 279: 30896-903.
25. Zhang P, Pan W, Rux AH, Sachais BS, Zheng XL. 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 2007; 110: 1887-94.
26. Banno F, Chauhan AK, Kokame K, Yang J, Miyata S, Wagner DD, Miyata T. The distal carboxyl-terminal domains of ADAMTS13 are required for regulation of in vivo thrombus formation. Blood 2009; 113: 5323-9.
27. Sebestyen MG, Budker VG, Budker T, Subbotin VM, Zhang G, Monahan SD, Lewis DL, Wong SC, Hagstrom JE, Wolff JA. Mechanism of plasmid delivery by hydrodynamic tail vein injection. I. hepatocyte uptake of various molecules. J Gene Med 2006; 8: 852-73.
28. Lenting PJ, Westein E, Terraube V, Ribba AS, Huizinga EG, Meyer D, de Groot PG, Denis CV. An experimental model to study the in vivo survival of von willebrand factor. basic aspects and application to the R1205H mutation. J Biol Chem 2004; 279: 12102-9.
29. Haberichter SL, Castaman G, James PD, Christopherson PA, Roheghiero F, Lillicrap D, Montgomery RR. Clearance of von Willebrand Factor (VWF) in type 2 von Willebrand Disease (VWD): the implications of VWF propeptide (VWFpp) and VWF:Ag levels. J Thromb Haemost 2009; 7(Suppl. 2): 10.
30. Bonnefoy A, Hoylaerts MF. Thrombospondin-1 in von willebrand factor function. Curr Drug Targets 2008; 9: 822-32.
31. Raife TJ, Cao W, Atkinson BS, Bedell B, Montgomery RR, Lentz SR, Johnson GF, Zheng XL. Leukocyte proteases cleave von willebrand factor at or near the ADAMTS13 cleavage site. Blood 2009; 114: 1666-74.
32. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA. Mechanoenzymatic cleavage of the ultralarge vascular protein von willebrand factor. Science 2009; 324: 1330-4.
33. Auton M, Cruz MA, Moake J. Conformational stability and domain unfolding of the von willebrand factor A domains. J Mol Biol 2007; 366: 986-1000.