Crystal structure and enzymatic activity of an ADAMTS-13 mutant with the East Asian-specific P475S polymorphism

Journal of Thrombosis and Haemostasis

Volumn 11, Issue 7, 2013, Pages 1399-1406

  Akiyama, M ^a   Nakayama, D ^a   Takeda, S ^a   Kokame, K ^a   Takagi, J ^b   Miyata, T ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

ADAMTS 13; Crystallography; Genetic polymorphism; Human; Proteins; Thrombotic thrombocytopenic purpura; Von Willebrand factor

Indexed keywords

MUTANT PROTEIN; PROLINE; SERINE; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

AMINO ACID SUBSTITUTION; ARTICLE; ASIAN; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DENATURATION; ENZYME ACTIVITY; HIGH TEMPERATURE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REACTION TIME; SINGLE NUCLEOTIDE POLYMORPHISM; THROMBOTIC THROMBOCYTOPENIC PURPURA; WILD TYPE;

ADAMTS-13; CRYSTALLOGRAPHY; GENETIC POLYMORPHISM; HUMAN; PROTEINS; THROMBOTIC THROMBOCYTOPENIC PURPURA; VON WILLEBRAND FACTOR;

ADAM PROTEINS; ANIMALS; ASIAN CONTINENTAL ANCESTRY GROUP; CHO CELLS; CRICETINAE; CRICETULUS; ENZYME STABILITY; GENETIC PREDISPOSITION TO DISEASE; HUMANS; KINETICS; MODELS, MOLECULAR; PHENOTYPE; POLYMORPHISM, GENETIC; PROTEIN CONFORMATION; PROTEIN DENATURATION; PURPURA, THROMBOTIC THROMBOCYTOPENIC; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE; TRANSFECTION; VON WILLEBRAND FACTOR;

EID: 84880412052     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12279     Document Type: Article

References (39)

1. Springer TA. Biology and physics of von Willebrand factor concatamers. J Thromb Haemost 2011; 9(Suppl. 1): 130-43.
2. Dent JA, Galbusera M, Ruggeri ZM. Heterogeneity of plasma von Willebrand factor multimers resulting from proteolysis of the constituent subunit. J Clin Invest 1991; 88: 774-82.
3. Tsai HM, Sussman II, Nagel RL. Shear stress enhances the proteolysis of von Willebrand factor in normal plasma. Blood 1994; 83: 2171-9.
4. Sadler JE, Moake JL, Miyata T, George JN. Recent advances in thrombotic thrombocytopenic purpura. Hematology Am Soc Hematol Educ Program 2004; 2004: 407-23.
5. 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.
6. 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.
7. 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.
8. Kokame K, Matsumoto M, Soejima K, Yagi H, Ishizashi H, Funato M, Tamai H, Konno M, Kamide K, Kawano Y, Miyata T, Fujimura Y. Mutations and common polymorphisms in ADAMTS13 gene responsible for von Willebrand factor-cleaving protease activity. Proc Natl Acad Sci USA 2002; 99: 11902-7.
9. Lotta LA, Garagiola I, Palla R, Cairo A, Peyvandi F. ADAMTS13 mutations and polymorphisms in congenital thrombotic thrombocytopenic purpura. Hum Mutat 2010; 31: 11-19.
10. Kokame K, Kokubo Y, Miyata T. Polymorphisms and mutations of ADAMTS13 in the Japanese population and estimation of the number of patients with Upshaw-Schulman syndrome. J Thromb Haemost 2011; 9: 1654-6.
11. Jang MJ, Kim NK, Chong SY, Kim HJ, Lee SJ, Kang MS, Oh D. Frequency of Pro475Ser polymorphism of ADAMTS13 gene and its association with ADAMTS-13 activity in the Korean population. Yonsei Med J 2008; 49: 405-8.
12. Gao W, Ruan C, Dai L, Su J, Wang Z. The frequency of P475S polymorphism in von Willebrand factor-cleaving protease in the Chinese population and its relevance to arterial thrombotic disorders. Thromb Haemost 2004; 91: 1257-8.
13. Bongers TN, De Maat MP, Dippel DW, Uitterlinden AG, Leebeek FW. Absence of Pro475Ser polymorphism in ADAMTS-13 in Caucasians. J Thromb Haemost 2005; 3: 805.
14. Kokame K, Miyata T. Genetic defects leading to hereditary thrombotic thrombocytopenic purpura. Semin Hematol 2004; 41: 34-40.
15. Akiyama M, Kokame K, Miyata T. ADAMTS13 P475S polymorphism causes a lowered enzymatic activity and urea lability in vitro. J Thromb Haemost 2008; 6: 1830-2.
16. Soejima K, Matsumoto M, Kokame K, Yagi H, Ishizashi H, Maeda H, Nozaki C, Miyata T, Fujimura Y, Nakagaki T. ADAMTS-13 cysteine-rich/spacer domains are functionally essential for von Willebrand factor cleavage. Blood 2003; 102: 3232-7.
17. Zheng X, Nishio K, Majerus EM, Sadler JE. Cleavage of von Willebrand factor requires the spacer domain of the metalloprotease ADAMTS13. J Biol Chem 2003; 278: 30136-41.
18. Akiyama M, Takeda S, Kokame K, Takagi J, Miyata T. Crystal structures of the noncatalytic domains of ADAMTS13 reveal multiple discontinuous exosites for von Willebrand factor. Proc Natl Acad Sci USA 2009; 106: 19274-9.
19. Crawley JT, de Groot R, Xiang Y, Luken BM, Lane DA. Unraveling the scissile bond: how ADAMTS13 recognizes and cleaves von Willebrand factor. Blood 2011; 118: 3212-21.
20. Wu JJ, Fujikawa K, McMullen BA, Chung DW. Characterization of a core binding site for ADAMTS-13 in the A2 domain of von Willebrand factor. Proc Natl Acad Sci USA 2006; 103: 18470-4.
21. Jin SY, Skipwith CG, Zheng XL. Amino acid residues Arg(659), Arg(660), and Tyr(661) in the spacer domain of ADAMTS13 are critical for cleavage of von Willebrand factor. Blood 2010; 115: 2300-10.
22. 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.
23. Akiyama M, Takeda S, Kokame K, Takagi J, Miyata T. Production, crystallization and preliminary crystallographic analysis of an exosite-containing fragment of human von Willebrand factor-cleaving proteinase ADAMTS13. Acta Crystallogr F Struct Biol Crystallogr Commun 2009; 65: 739-42.
24. Reeves PJ, Callewaert N, Contreras R, Khorana HG. Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible N-acetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc Natl Acad Sci USA 2002; 99: 13419-24.
25. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 2011; 67: 235-42.
26. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 2010; 66: 486-501.
27. Brunger AT. Version 1.2 of the crystallography and NMR system. Nat Protoc 2007; 2: 2728-33.
28. 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.
29. Anderson PJ, Kokame K, Sadler JE. Zinc and calcium ions cooperatively modulate ADAMTS13 activity. J Biol Chem 2006; 281: 850-7.
30. 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.
31. De Marco L, Shapiro SS. Properties of human asialo-factor VIII. A ristocetin-independent platelet-aggregating agent. J Clin Invest 1981; 68: 321-8.
32. Gonzalez de Peredo A, Klein D, Macek B, Hess D, Peter-Katalinic J, Hofsteenge J. C-mannosylation and O-fucosylation of thrombospondin type 1 repeats. Mol Cell Proteomics 2002; 1: 11-18.
33. Wang LW, Leonhard-Melief C, Haltiwanger RS, Apte SS. Post-translational modification of thrombospondin type-1 repeats in ADAMTS-like 1/punctin-1 by C-mannosylation of tryptophan. J Biol Chem 2009; 284: 30004-15.
34. 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.
35. 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.
36. Zakai NA, McClure LA. Racial differences in venous thromboembolism. J Thromb Haemost 2011; 9: 1877-82.
37. Miyata T, Hamasaki N, Wada H, Kojima T. More on: racial differences in venous thromboembolism. J Thromb Haemost 2012; 10: 319-20.
38. Zhou W, Bouhassira EE, Tsai HM. An IAP retrotransposon in the mouse ADAMTS13 gene creates ADAMTS13 variant proteins that are less effective in cleaving von Willebrand factor multimers. Blood 2007; 110: 886-93.
39. 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.