Allosteric activation of ADAMTS13 by von Willebrand factor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 52, 2014, Pages 18584-18589

  Muia, Joshua ^a   Zhu, Jian ^a   Gupta, Garima ^a   Haberichter, Sandra L ^b   Friedman, Kenneth D ^b   Feys, Hendrik B ^c   Deforche, Louis ^d   Vanhoorelbeke, Karen ^d   Westfield, Lisa A ^a   Roth, Robyn ^a   Tolia, Niraj Harish ^a   Heuser, John E ^a   Sadler, J Evan ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c Transfusion Research Center Belgian Red Cross Flanders   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Allosteric regulation; Hemostasis; Metalloproteases

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COMPLEMENT COMPONENT C1R; COMPLEMENT COMPONENT C1S; CYSTEINE; DISINTEGRIN; ELASTASE; EPIDERMAL GROWTH FACTOR; METALLOPROTEINASE; MONOCLONAL ANTIBODY; PLASMIN; THROMBIN; THROMBOSPONDIN 1; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE; ADAM PROTEIN; ADAMTS13 PROTEIN, HUMAN; PROTEIN BINDING;

ADULT; ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; ENZYME ACTIVATION; HUMAN; MOLECULAR MODEL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SEA URCHIN; SHEAR STRESS; TENSILE STRENGTH; VON WILLEBRAND DISEASE; X RAY CRYSTALLOGRAPHY; BLOOD; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ECHINOIDEA;

ADAM PROTEINS; ALLOSTERIC REGULATION; ENZYME ACTIVATION; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; VON WILLEBRAND FACTOR;

EID: 84924309931     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1413282112     Document Type: Article

References (56)

1. Zheng X, et al. (2001) Structure of von Willebrand factor-cleaving protease (ADAMTS13), a metalloprotease involved in thrombotic thrombocytopenic purpura. J Biol Chem 276(44):41059-41063.
2. Soejima K, et al. (2001) A novel human metalloprotease synthesized in the liver and secreted into the blood: Possibly, the von Willebrand factor-cleaving protease?J Biochem 130(4):475-480.
3. Levy GG, et al. (2001) Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature 413(6855):488-494.
4. Fujikawa K, Suzuki H, McMullen B, Chung D (2001) Purification of human von Willebrand factor-cleaving protease and its identification as a new member of the metalloproteinase family. Blood 98(6):1662-1666.
5. Gerritsen HE, Robles R, Lämmle B, Furlan M (2001) Partial amino acid sequence of purified von Willebrand factor-cleaving protease. Blood 98(6):1654-1661.
6. Furlan M, et al. (1998) von Willebrand factor-cleaving protease in thrombotic thrombocytopenic purpura and the hemolytic-uremic syndrome. N Engl J Med 339(22):1578-1584.
7. Tsai HM, Lian EC (1998) Antibodies to von Willebrand factor-cleaving protease in acute thrombotic thrombocytopenic purpura. N Engl J Med 339(22):1585-1594.
8. Tsai HM (1996) Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood 87(10):4235-4244.
9. Majerus EM, Anderson PJ, Sadler JE (2005) Binding of ADAMTS13 to von Willebrand factor. J Biol Chem 280(23):21773-21778.
10. Furlan M, Robles R, Lämmle B (1996) Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood 87(10):4223-4234.
11. Zhang Q, et al. (2009) Structural specializations of A2, a force-sensing domain in the ultralarge vascular protein von Willebrand factor. Proc Natl Acad Sci USA 106(23):9226-9231.
12. Gao W, Anderson PJ, Majerus EM, Tuley EA, Sadler JE (2006) Exosite interactions contribute to tension-induced cleavage of von Willebrand factor by the antithrombotic ADAMTS13 metalloprotease. Proc Natl Acad Sci USA 103(50):19099-19104.
13. Gao W, Anderson PJ, Sadler JE (2008) Extensive contacts between ADAMTS13 exosites and von Willebrand factor domain A2 contribute to substrate specificity. Blood 112(5):1713-1719.
14. Zanardelli S, et al. (2006) ADAMTS13 substrate recognition of von Willebrand factor A2 domain. J Biol Chem 281(3):1555-1563.
15. Akiyama M, Takeda S, Kokame K, Takagi J, Miyata T (2009) Crystal structures of the noncatalytic domains of ADAMTS13 reveal multiple discontinuous exosites for von Willebrand factor. Proc Natl Acad Sci USA 106(46):19274-19279.
16. Zhang P, Pan W, Rux AH, Sachais BS, Zheng XL (2007) 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(6):1887-1894.
17. Feys HB, Anderson PJ, Vanhoorelbeke K, Majerus EM, Sadler JE (2009) Multi-step binding of ADAMTS-13 to von Willebrand factor. J Thromb Haemost 7(12):2088-2095.
18. Zanardelli S, et al. (2009) A novel binding site for ADAMTS13 constitutively exposed on the surface of globular VWF. Blood 114(13):2819-2828.
19. Zhou W, Bouhassira EE, Tsai HM (2007) An IAP retrotransposon in themouse ADAMTS13 gene creates ADAMTS13 variant proteins that are less effective in cleaving von Willebrand factor multimers. Blood 110(3):886-893.
20. Banno F, et al. (2009) The distal carboxyl-terminal domains of ADAMTS13 are required for regulation of in vivo thrombus formation. Blood 113(21):5323-5329.
21. Anderson PJ, Kokame K, Sadler JE (2006) Zinc and calcium ions cooperatively modulate ADAMTS13 activity. J Biol Chem 281(2):850-857.
22. Muia J, et al. (2013) An optimized fluorogenic ADAMTS13 assay with increased sensitivity for the investigation of patients with thrombotic thrombocytopenic purpura. J Thromb Haemost 11(8):1511-1518.
23. Kokame K, Nobe Y, Kokubo Y, Okayama A, Miyata T (2005) FRETS-VWF73, a first fluorogenic substrate for ADAMTS13 assay. Br J Haematol 129(1):93-100.
24. Di Stasio E, et al. (2008) Mechanistic studies on ADAMTS13 catalysis. Biophys J 95(5):2450-2461.
25. Wells JA (1990) Additivity of mutational effects in proteins. Biochemistry 29(37):8509-8517.
26. Girma JP, Chopek MW, Titani K, Davie EW (1986) Limited proteolysis of human von Willebrand factor by Staphylococcus aureus V-8 protease: Isolation and partial characterization of a platelet-binding domain. Biochemistry 25(11):3156-3163.
27. Hassenpflug WA, et al. (2006) Impact of mutations in the von Willebrand factor A2 domain on ADAMTS13-dependent proteolysis. Blood 107(6):2339-2345.
28. Svergun DI, Barberato C, Koch MHJ (1995) CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J Appl Cryst 28:768-773.
29. Crawley JT, et al. (2005) Proteolytic inactivation of ADAMTS13 by thrombin and plasmin. Blood 105(3):1085-1093.
30. Hiura H, et al. (2010) Proteolytic fragmentation and sugar chains of plasma ADAMTS13 purified by a conformation-dependent monoclonal antibody. J Biochem 148(4):403-411.
31. Banno F, Kaminaka K, Soejima K, Kokame K, Miyata T (2004) Identification of strain-specific variants of mouse Adamts13 gene encoding von Willebrand factor-cleaving protease. J Biol Chem 279(29):30896-30903.
32. Crawley JT, Lane DA, Woodward M, Rumley A, Lowe GD (2008) Evidence that high von Willebrand factor and low ADAMTS-13 levels independently increase the risk of a non-fatal heart attack. J Thromb Haemost 6(4):583-588.
33. Bongers TN, et al. (2009) Lower levels of ADAMTS13 are associated with cardiovascular disease in young patients. Atherosclerosis 207(1):250-254.
34. Andersson HM, et al. (2012) High VWF, low ADAMTS13, and oral contraceptives increase the risk of ischemic stroke and myocardial infarction in young women. Blood 119(6):1555-1560.
35. Gandhi C, Khan MM, Lentz SR, Chauhan AK (2012) ADAMTS13 reduces vascular inflammation and the development of early atherosclerosis in mice. Blood 119(10):2385-2391.
36. Ginsburg D, Bowie EJW (1992) Molecular genetics of von Willebrand disease. Blood 79(10):2507-2519.
37. Nichols WL, et al. (2008) von Willebrand disease (VWD): Evidence-based diagnosis and management guidelines, the National Heart, Lung, and Blood Institute (NHLBI) Expert Panel report (USA). Haemophilia 14(2):171-232.
38. Suarez J, et al. (2011) Mechanisms of bleeding and approach to patients with axial-flow left ventricular assist devices. Circ Heart Fail 4(6):779-784.
39. Rauch A, et al. (2014) Antibody-based prevention of von Willebrand factor degradation mediated by circulatory assist devices. Thromb Haemost 112(5):1014-1023.
40. Apte SS (2009) A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms. J Biol Chem 284(46):31493-31497.
41. Le Goff C, Cormier-Daire V (2011) The ADAMTS(L) family and human genetic disorders. Hum Mol Genet 20(R2):R163-R167.
42. Shi M, et al. (2011) Latent TGF-β structure and activation. Nature 474(7351):343-349.
43. Hubmacher D, Apte SS (2011) Genetic and functional linkage between ADAMTS superfamily proteins and fibrillin-1: A novel mechanism influencing microfibril assembly and function. Cell Mol Life Sci 68(19):3137-3148.
44. Feys HB, et al. (2006) ADAMTS-13 plasma level determination uncovers antigen absence in acquired thrombotic thrombocytopenic purpura and ethnic differences. J Thromb Haemost 4(5):955-962.
45. Feys HB, et al. (2010) Thrombotic thrombocytopenic purpura directly linked with ADAMTS13 inhibition in the baboon (Papio ursinus). Blood 116(12):2005-2010.
46. Mosyak L, et al. (2008) Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci 17(1):16-21.
47. Söding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33(Web Server issue):W244-8.
48. Heuser JE, et al. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol 81(2):275-300.
49. Heuser JE (1983) Procedure for freeze-drying molecules adsorbed to mica flakes. J Mol Biol 169(1):155-195.
50. Heuser J (1989) Protocol for 3-D visualization of molecules on mica via the quickfreeze, deep-etch technique. J Electron Microsc Tech 13(3):244-263.
51. Hura GL, et al. (2009) Robust, high-throughput solution structural analyses by small angle X-ray scattering (SAXS). Nat Methods 6(8):606-612.
52. Svergun DI (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 25(4):495-503.
53. Bohne-Lang A, von der Lieth CW (2005) GlyProt: In silico glycosylation of proteins. Nucleic Acids Res 33(Web Server issue):W214-9.
54. Svergun DI (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys J 76(6):2879-2886.
55. Volkov VV, Svergun DI (2003) Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 36(3-1):860-864.
56. Kozin MB, Svergun DI (2001) Automated matching of high- and low-resolution structural models. J Appl Cryst 34(1):33-41.