A mechanism for localized dynamics-driven affinity regulation of the binding of von willebrand factor to platelet glycoprotein Ibα

Journal of Biological Chemistry

Volumn 288, Issue 37, 2013, Pages 26658-26667

  Liu, Guangjian ^a   Fang, Ying ^a   Wu, Jianhua ^a  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAIN-OF FUNCTION; GLYCOPROTEIN IB; N-TERMINALS; STRUCTURAL BASIS; UP-REGULATION; VON WILLEBRAND FACTOR;

BIOCHEMISTRY; BIOLOGY;

GLYCOPROTEINS;

ARGININE; GLYCOPROTEIN IB ALPHA; VON WILLEBRAND FACTOR;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DISEASE ASSOCIATION; GAIN OF FUNCTION MUTATION; HEMOSTASIS; MEMBRANE STABILIZATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SHEAR STRESS; STRUCTURE ANALYSIS; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; UPREGULATION;

BIOPHYSICS; GPIBΑ; MOLECULAR DYNAMICS; PLATELETS; PROTEIN DYNAMICS; STRUCTURAL BIOLOGY; THROMBOSIS; VON WILLEBRAND DISEASE; VON WILLEBRAND FACTOR;

BLOOD PLATELETS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN BONDING; LIGANDS; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTATION; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; THROMBOSIS; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR;

EID: 84884177403     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.453803     Document Type: Article

References (62)

1. Savage, B., Saldívar, E., and Ruggeri, Z. M. (1996) Initiation of platelet adhesion by arrest onto fibrinogen or translocation on von Willebrand factor. Cell 84, 289-297
2. Zhou, Z., and Dong, J. F. (2012) Thrombotic thrombocytopenic purpura and anti-thrombotic therapy targeted to von Willebrand factor. Curr. Vasc. Pharmacol. 10, 762-766
3. Ruggeri, Z. M. (2007) von Willebrand factor. Looking back and looking forward. Thromb. Haemost. 98, 55-62
4. Sadler, J. E. (1998) Biochemistry and genetics of von Willebrand factor. Annu. Rev. Biochem. 67, 395-424
5. Emsley, J., Cruz, M., Handin, R., and Liddington, R. (1998) Crystal structure of the von Willebrand factor A1 domain and implications for the binding of platelet glycoprotein Ib. J. Biol. Chem. 273, 10396-10401
6. Huizinga, E. G., Tsuji, S., Romijn, R. A., Schiphorst, M. E., de Groot, P. G., Sixma, J. J., and Gros, P. (2002) Structures of glycoprotein Ibβand its complex with von Willebrand factor A1 domain. Science 297, 1176-1179
7. Martin, C., Morales, L. D., and Cruz, M. A. (2007) Purified A2 domain of von Willebrand factor binds to the active conformation of von Willebrand factor and blocks the interaction with platelet glycoprotein Ibα. J. Thromb. Haemost. 5, 1363-1370
8. Ulrichts, H., Udvardy, M., Lenting, P. J., Pareyn, I., Vandeputte, N., Vanhoorelbeke, K., and Deckmyn, H. (2006) Shielding of the A1 domain by the D′D3 domains of von Willebrand factor modulates its interaction with platelet glycoprotein Ib-IX-V. J. Biol. Chem. 281, 4699-4707
9. Auton, M., Sowa, K. E., Behymer, M., and Cruz, M. A. (2012) The N-terminal flanking region of A1 domain in von Willebrand factor stabilizes structure of A1A2A3 complex and modulates platelet activation under shear stress. J. Biol. Chem. 287, 14579-14585
10. Arya, M., Anvari, B., Romo, G. M., Cruz, M. A., Dong, J. F., McIntire, L. V., Moake, J. L., and López, J. A. (2002) Ultralarge multimers of von Willebrand factor form spontaneous high-strength bonds with the platelet glycoprotein Ib-IX complex. Studies using optical tweezers. Blood 99, 3971-3977
11. Schneider, S. W., Nuschele, S., Wixforth, A., Gorzelanny, C., Alexander- Katz, A., Netz, R. R., and Schneider, M. F. (2007) Shear-induced unfolding triggers adhesion of von Willebrand factor fibers. Proc. Natl. Acad. Sci. U.S.A. 104, 7899-7903
12. Siedlecki, C. A., Lestini, B. J., Kottke-Marchant, K. K., Eppell, S. J., Wilson, D. L., and Marchant, R. E. (1996) Shear-dependent changes in the threedimensional structure of human von Willebrand factor. Blood 88, 2939-2950
13. Kim, J., Zhang, C. Z., Zhang, X., and Springer, T. A. (2010) A mechanically stabilized receptor-ligand flex-bond important in the vasculature. Nature 466, 992-995
14. Springer, T. A. (2011) Biology and physics of von Willebrand factor concatamers. J. Thromb. Haemost. 9, 130-143
15. Yago, T., Lou, J., Wu, T., Yang, J., Miner, J. J., Coburn, L., López, J. A., Cruz, M. A., Dong, J. F., McIntire, L. V., McEver, R. P., and Zhu, C. (2008) Platelet glycoprotein Ibβforms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J. Clin. Invest. 118, 3195-3207
16. Auton, M., Sedlák, E., Marek, J., Wu, T., Zhu, C., and Cruz, M. A. (2009) Changes in thermodynamic stability of von Willebrand factor differentially affect the force-dependent binding to platelet GPIbα. Biophys. J. 97, 618-627
17. Miura, S., Li, C. Q., Cao, Z., Wang, H., Wardell, M. R., and Sadler, J. E. (2000) Interaction of von Willebrand factor domain A1 with platelet glycoprotein Ibα-(1-289). Slow intrinsic binding kinetics mediate rapid platelet adhesion. J. Biol. Chem. 275, 7539-7546
18. Miyata, S., and Ruggeri, Z. M. (1999) Distinct structural attributes regulating von Willebrand factor A1 domain interaction with platelet glycoprotein Ibβunder flow. J. Biol. Chem. 274, 6586-6593
19. Miyata, S., Goto, S., Federici, A. B., Ware, J., and Ruggeri, Z. M. (1996) Conformational changes in the A1 domain of von Willebrand factor modulating the interaction with platelet glycoprotein Ibα. J. Biol. Chem. 271, 9046-9053
20. Dumas, J. J., Kumar, R., McDonagh, T., Sullivan, F., Stahl, M. L., Somers, W. S., and Mosyak, L. (2004) Crystal structure of the wild-type von Willebrand factor A1-glycoprotein Ibβcomplex reveals conformation differences with a complex bearing von Willebrand disease mutations. J. Biol. Chem. 279, 23327-23334
21. Fukuda, K., Doggett, T. A., Bankston, L. A., Cruz, M. A., Diacovo, T. G., and Liddington, R. C. (2002) Structural basis of von Willebrand factor activation by the snake toxin botrocetin. Structure 10, 943-950
22. Celikel, R., Varughese, K. I., Madhusudan, Yoshioka, A., Ware, J., and Ruggeri, Z. M. (1998) Crystal structure of the von Willebrand factor A1 domain in complex with the function blocking NMC-4 Fab. Nat. Struct. Biol. 5, 189-194
23. Celikel, R., Ruggeri, Z. M., and Varughese, K. I. (2000) von Willebrand factor conformation and adhesive function is modulated by an internalized water molecule. Nat. Struct. Biol. 7, 881-884
24. Huang, R. H., Fremont, D. H., Diener, J. L., Schaub, R. G., and Sadler, J. E. (2009) A structural explanation for the antithrombotic activity of ARC1172, a DNA aptamer that binds von Willebrand factor domain A1. Structure 17, 1476-1484
25. Maita, N., Nishio, K., Nishimoto, E., Matsui, T., Shikamoto, Y., Morita, T., Sadler, J. E., and Mizuno, H. (2003) Crystal structure of von Willebrand factor A1 domain complexed with snake venom, bitiscetin. Insight into glycoprotein Ibβbinding mechanism induced by snake venom proteins. J. Biol. Chem. 278, 37777-37781
26. Fukuda, K., Doggett, T., Laurenzi, I. J., Liddington, R. C., and Diacovo, T. G. (2005) The snake venom protein botrocetin acts as a biological brace to promote dysfunctional platelet aggregation. Nat. Struct. Mol. Biol. 12, 152-159
27. Bruice, T. C. (2006) Computational approaches. Reaction trajectories, structures, and atomic motions. Enzyme reactions and proficiency. Chem. Rev. 106, 3119-3139
28. Wang, Y., and McCammon, J. A. (2012) Introduction to molecular dynamics. Theory and applications in biomolecular modeling, in Computational Modeling of Biological Systems, pp. 3-30, Springer US, New York.
29. Auton, M., Zhu, C., and Cruz, M. A. (2010) The mechanism of VWFmediated platelet GPIbβbinding. Biophys. J. 99, 1192-1201
30. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD. Visual molecular dynamics. J. Mol. Graph. 14, 33-38, 27-38
31. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb- Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723
32. Matsushita, T., and Sadler, J. E. (1995) Identification of amino acid residues essential for von Willebrand factor binding to platelet glycoprotein Ib. Charged-to-alanine scanning mutagenesis of the A1 domain of human von Willebrand factor. J. Biol. Chem. 270, 13406-13414
33. Randi, A. M., Jorieux, S., Tuley, E. A., Mazurier, C., and Sadler, J. E. (1992) Recombinant von Willebrand factor Arg578 3 Gln. A type IIB von Willebrand disease mutation affects binding to glycoprotein Ib but not to collagen or heparin. J. Biol. Chem. 267, 21187-21192
34. Casaña, P., Martínez, F., Espinós, C., Haya, S., Lorenzo, J. I., and Aznar, J. A. (1998) Search for mutations in a segment of the exon 28 of the human von Willebrand factor gene. New mutations, R1315C and R1341W, associated with type 2M and 2B variants. Am. J. Hematol. 59, 57-63
35. Hilbert, L., Gaucher, C., Abgrall, J. F., Parquet, A., Trzeciak, C., and Mazurier, C. (1998) Identification of new type 2B von Willebrand disease mutations. Arg543Gln, Arg545Pro and Arg578Leu. Br. J. Haematol. 103, 877-884
36. Bas, D. C., Rogers, D. M., and Jensen, J. H. (2008) Very fast prediction and rationalization of pKa values for protein-ligand complexes. Proteins 73, 765-783
37. Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., and Schulten, K. (2005) Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802
38. MacKerell, A. D., Jr., Bashford, D., Bellott, M., Dunbrack, R. L., Jr., Evanseck, J., Field, M., Fischer, S., Gao, J., Guo, H., and Ha, S. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616
39. Romijn, R. A. (2002) Structural studies on the von Willebrand factor A1 and A3 domains. Ph.D. thesis, Universiteit Utrecht
40. Auton, M., Cruz, M. A., and Moake, J. (2007) Conformational stability and domain unfolding of the Von Willebrand factor A domains. J. Mol. Biol. 366, 986-1000
41. Cooney, K. A., and Ginsburg, D. (1996) Comparative analysis of type 2b von Willebrand disease mutations. Implications for the mechanism of von Willebrand factor binding to platelets. Blood 87, 2322-2328
42. Springer, T. A. (2006) Complement and the multifaceted functions of VWA and integrin I domains. Structure 14, 1611-1616
43. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796
44. Whitley, M. J., and Lee, A. L. (2009) Frameworks for understanding longrange intra-protein communication. Curr. Protein Pept. Sci. 10, 116-127
45. Auton, M., Sowa, K. E., Smith, S. M., Sedlák, E., Vijayan, K. V., and Cruz, M. A. (2010) Destabilization of the A1 domain in von Willebrand factor dissociates the A1A2A3 tri-domain and provokes spontaneous binding to glycoprotein Ibβand platelet activation under shear stress. J. Biol. Chem. 285, 22831-22839
46. Ma, B., Tsai, C. J., Haliloglu, T., and Nussinov, R. (2011) Dynamic allostery. Linkers are not merely flexible. Structure 19, 907-917
47. Henzler-Wildman, K. A., Lei, M., Thai, V., Kerns, S. J., Karplus, M., and Kern, D. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450, 913-916
48. Tzeng, S. R., and Kalodimos, C. G. (2009) Dynamic activation of an allosteric regulatory protein. Nature 462, 368-372
49. Popovych, N., Sun, S., Ebright, R. H., and Kalodimos, C. G. (2006) Dynamically driven protein allostery. Nat. Struct. Mol. Biol. 13, 831-838
50. Smock, R. G., and Gierasch, L. M. (2009) Sending signals dynamically. Science's STKE 324, 198-203
51. Wallnoefer, H. G., Lingott, T., Gutiérrez, J. M., Merfort, I., and Liedl, K. R. (2010) Backbone flexibility controls the activity and specificity of a protein- protein interface. Specificity in snake venom metalloproteases. J. Am. Chem. Soc. 132, 10330-10337
52. Ishikawa, H., Kwak, K., Chung, J. K., Kim, S., and Fayer, M. D. (2008) Direct observation of fast protein conformational switching. Proc. Natl. Acad. Sci. U.S.A. 105, 8619-8624
53. Whitten, S. T., García-Moreno, E. B., and Hilser, V. J. (2005) Local conformational fluctuations can modulate the coupling between proton binding and global structural transitions in proteins. Proc. Natl. Acad. Sci. U.S.A. 102, 4282-4287
54. Csermely, P., Palotai, R., and Nussinov, R. (2010) Induced fit, conformational selection and independent dynamic segments. An extended view of binding events. Trends Biochem. Sci. 35, 539-546
55. Cooper, A., and Dryden, D. (1984) Allostery without conformational change. Eur. Biophys. J. 11, 103-109
56. Fuentes, E. J., Der, C. J., and Lee, A. L. (2004) Ligand-dependent dynamics and intramolecular signaling in a PDZ domain. J. Mol. Biol. 335, 1105-1115
57. Chaplin, M. (2006) Do we underestimate the importance of water in cell biology? Nat. Rev. Mol. Cell Biol. 7, 861-866
58. Zhang, H., Zhang, T., Chen, K., Shen, S., Ruan, J., and Kurgan, L. (2009)On the relation between residue flexibility and local solvent accessibility in proteins. Proteins 76, 617-636
59. Fu, X., Chen, J., Gallagher, R., Zheng, Y., Chung, D. W., and López, J. A. (2011) Shear stress-induced unfolding of VWF accelerates oxidation of key methionine residues in the A1A2A3 region. Blood 118, 5283-5291
60. Wayman, A. M., Chen, W., McEver, R. P., and Zhu, C. (2010) Triphasic force dependence of E-selectin/ligand dissociation governs cell rolling under flow. Biophys. J. 99, 1166-1174
61. Li, Q., Fang, Y., Ding, X., and Wu, J. (2012) Force-dependent bond dissociation govern rolling of HL-60 cells through E-selectin. Exp. Cell Res. 318, 1649-1658
62. Interlandi, G., and Thomas, W. (2010) The catch bond mechanism between von Willebrand factor and platelet surface receptors investigated by molecular dynamics simulations. Proteins 78, 2506-2522