A novel calcium-binding site of von Willebrand factor A2 domain regulates its cleavage by ADAMTS13

Blood

Volumn 117, Issue 17, 2011, Pages 4623-4631

  Zhou, Minyun ^a,b   Dong, Xianchi ^a,b   Baldauf, Carsten ^a   Chen, Hua ^c   Zhou, Yanfeng ^d   Springer, Timothy A ^d   Luo, Xinping ^c   Zhong, Chen ^a   Gräter, Frauke ^a,e   Ding, Jianping ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c FUDAN UNIVERSITY   (China)

^d HARVARD MEDICAL SCHOOL   (United States)

^e HEIDELBERG INSTITUTE FOR THEORETICAL STUDIES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; METAL ION; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; VON WILLEBRAND FACTOR A2; VON WILLEBRAND FACTOR CLEAVING PROTEINASE;

ANIMAL CELL; ARTICLE; BINDING SITE; CALCIUM BINDING; CARBOXY TERMINAL SEQUENCE; CHEMICAL ANALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; HEMOSTASIS; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN STABILITY; REGULATORY MECHANISM; WILD TYPE;

EID: 79955977529     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-11-321596     Document Type: Article

References (40)

1. Sadler JE. Biochemistry and genetics of von Willebrand factor. Annu Rev Biochem. 1998;67:395-424. (Pubitemid 28411134)
2. Reininger AJ. Function of von Willebrand factor in haemostasis and thrombosis. Haemophilia. 2008; 14(suppl 5):11-26.
3. Ruggeri ZM. Structure and function of von Willebrand factor. Thromb Haemost. 1999;82(2):576-584.
4. Sadler JE. von Willebrand factor: two sides of a coin. J Thromb Haemost. 2005;3(8):1702-1709.
5. Levy GG, Nichols WC, Lian EC, et al. Mutations in a member of the ADAMTS gene family cause thrombotic thrombocytopenic purpura. Nature. 2001;413(6855):488-494. (Pubitemid 32938741)
6. Batlle J, Lopez-Fernandez MF, Lopez-Borrasca A, et al. Proteolytic degradation of von Willebrand factor after DDAVP administration in normal individuals. Blood. 1987;70(1):173-176. (Pubitemid 17111258)
7. Furlan M, Robles R, Lammle B. Partial purification and characterization of a protease from human plasma cleaving von Willebrand factor to fragments produced by in vivo proteolysis. Blood. 1996;87(10):4223-4234. (Pubitemid 26152266)
8. Sadler JE.Anew name in thrombosis, ADAMTS13. Proc Natl Acad Sci U S A. 2002;99(18):11552-11554.
9. Dent JA, Berkowitz SD, Ware J, Kasper CK, Ruggeri ZM. Identification of a cleavage site directing the immunochemical detection of molecular abnormalities in type IIA von Willebrand factor. Proc Natl Acad Sci U S A. 1990;87(16):6306-6310.
10. Sutherland JJ, O'Brien LA, Lillicrap D, Weaver DF. Molecular modeling of the von Willebrand factor A2 Domain and the effects of associated type 2A von Willebrand disease mutations. J Mol Model. 2004;10(4):259-270. (Pubitemid 39236649)
11. Tsai HM, Sussman II, Nagel RL. Shear stress enhances the proteolysis of von Willebrand factor in normal plasma. Blood. 1994;83(8):2171-2179. (Pubitemid 24112728)
12. Schneider SW, Nuschele S, Wixforth A, et al. Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc Natl Acad Sci U SA. 2007;104(19):7899-7903. (Pubitemid 47185848)
13. Furlan M. Von Willebrand factor: molecular size and functional activity. Ann Hematol. 1996;72(6): 341-348. (Pubitemid 26229974)
14. Tsai HM. Physiologic cleavage of von Willebrand factor by a plasma protease is dependent on its conformation and requires calcium ion. Blood. 1996;87(10):4235-4244.
15. Dong JF, Moake JL, Nolasco L, et al.ADAMTS-13 rapidly cleaves newly secreted ultralarge von Willebrand factor multimers on the endothelial surface under flowing conditions. Blood. 2002; 100(12):4033-4039. (Pubitemid 35396870)
16. Tsai HM. Shear stress and von Willebrand factor in health and disease. Semin Thromb Hemost. 2003;29(5):479-488.
17. Sadler JE. New concepts in von Willebrand disease. Annu Rev Med. 2005;56:173-191. (Pubitemid 40299779)
18. Hassenpflug WA, Budde U, Obser T, et al. Impact of mutations in the von Willebrand factor A2 domain on ADAMTS13-dependent proteolysis. Blood. 2006;107(6):2339-2345. (Pubitemid 43345553)
19. Zhang X, Halvorsen K, Zhang CZ, Wong WP, Springer TA. Mechanoenzymatic cleavage of the ultralarge vascular protein von Willebrand factor. Science. 2009;324(5932):1330-1334.
20. Baldauf C, Schneppenheim R, Stacklies W, et al. Shear-induced unfolding activates von Willebrand factor A2 domain for proteolysis. J Thromb Haemost. 2009;7(12):2096-2105.
21. 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 U SA. 2009;106(23):9226-9231.
22. 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(2):607-612. (Pubitemid 38140094)
23. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. In: Abelson JN, Simon MI, Carter CW Jr, Sweet RM, eds. Methods in Enzymology, Volume 276: Macromolecular Crystallography, Part A. San Diego: Academic Press; 1997:307-326. (Pubitemid 27085611)
24. McCoy AJ. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr. 2007; 63(pt 1):32-41.
25. Huizinga EG, Martijn van der Plas R, Kroon J, Sixma JJ, Gros P. Crystal structure of the A3 domain of human von Willebrand factor: implications for collagen binding. Structure. 1997;5(9): 1147-1156.
26. Brünger AT, Adams PD, Clore GM, et al. Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr. 1998;54(pt 5):905-921.
27. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60(pt 12):2126-2132. (Pubitemid 41742764)
28. Murshudov GN, Vagin AA, Dodson EJ. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr. 1997;53(pt 3):240-255. (Pubitemid 27235885)
29. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ. GROMACS: fast, flexible, and free. J Comput Chem. 2005;26(16): 1701-1718. (Pubitemid 43076182)
30. Jorgensen WL, Ulmschneider JP, Tirado-Rives J. Free energies of hydration from a generalized Born model and an ALL-atom force field. J Phys Chem B. 2004;108:16264-16270.
31. Lawrence CP, Skinner JL. Flexible TIP4P model for molecular dynamics simulation of liquid water. Chem Phys Lett. 2003;372(5-6):842-847. (Pubitemid 36535688)
32. Harding MM. Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr. 2001;57(pt 3):401-411. (Pubitemid 32203174)
33. Tsai HM, Sussman II, Ginsburg D, Lankhof H, Sixma JJ, Nagel RL. Proteolytic cleavage of recombinant type 2A von Willebrand factor mutants R834W and R834Q: inhibition by doxycycline and by monoclonal antibody VP-1. Blood. 1997;89(6): 1954-1962. (Pubitemid 27132110)
34. Anderson PJ, Kokame K, Sadler JE. Zinc and calcium ions cooperatively modulate ADAMTS13 activity. J Biol Chem. 2006;281(2):850-857.
35. Gao W, Anderson PJ, Sadler JE. Extensive contacts between ADAMTS13 exosites and von Willebrand factor domain A2 contribute to substrate specificity. Blood. 2008;112(5):1713-1719.
36. Emsley J, Cruz M, Handin R, Liddington R. Crystal structure of the von Willebrand Factor A1 domain and implications for the binding of platelet glycoprotein Ib. J Biol Chem. 1998;273(17): 10396-10401. (Pubitemid 28227648)
37. Springer TA. Complement and the multifaceted functions of VWA and integrin I domains. Structure. 2006;14(11):1611-1616.
38. Harding MM. Metal-ligand geometry relevant to proteins and in proteins: sodium and potassium. Acta Crystallogr D Biol Crystallogr. 2002;58(pt 5):872-874. (Pubitemid 34557307)
39. McKinnon TA, Chion AC, Millington AJ, Lane DA, Laffan MA. N-linked glycosylation of VWF modulates its interaction with ADAMTS13. Blood. 2008; 111(6):3042-3049.
40. Mosyak L, Georgiadis K, Shane T, et al. Crystal structures of the two major aggrecan degrading enzymes, ADAMTS4 and ADAMTS5. Protein Sci. 2008;17(1):16-21.