Three-dimensional domain swapping as a mechanism to lock the active conformation in a super-active octamer of SARS-CoV main protease

Protein and Cell

Volumn 1, Issue 4, 2010, Pages 371-383

  Zhang, Shengnan ^a,b   Zhong, Nan ^a,b   Xue, Fei ^c   Kang, Xue ^a,b   Ren, Xiaobai ^a,b   Chen, Jiaxuan ^a   Jin, Changwen ^a,b   Lou, Zhiyong ^c   Xia, Bin ^a,b  

^a PEKING UNIVERSITY   (China)

^b PEKING UNIVERSITY   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

3D domain swapping; crystal structure; main protease; polyprotein processing; SARS CoV

Indexed keywords

DIMER; MONOMER; PROTEINASE;

AMINO TERMINAL SEQUENCE; ARTICLE; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PROCESSING; SARS CORONAVIRUS; THREE DIMENSIONAL DOMAIN SWAPPING;

SARS CORONAVIRUS;

EID: 77954686917     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-010-0044-8     Document Type: Article

References (55)

1. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L.-W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K., and Terwilliger, T. C. (2002). PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr D 58, 1948-1954.
2. Anand, K., Palm, G. J., Mesters, J. R., Siddell, S. G., Ziebuhr, J., and Hilgenfeld, R. (2002). Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra α-helical domain. EMBO J 21, 3213-3224.
3. Anand, K., Yang, H., Bartlam, M., Rao, Z. & Hilgenfeld, R. (2005). Coronavirus main proteinase: target for antiviral drug therapy. In: Coronaviruses with special emphasis on first insights concerning SARS, A. Schmidt, M. H. Wolff, and O. F. Weber, ed. (Switzerland, Basel; Birkhauser Verlag). pp. 173-199.
4. Anand, K., Ziebuhr, J., Wadhwani, P., Mesters, J. R., and Hilgenfeld, R. (2003). Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300, 1763-1767.
5. Bartlam, M., Yang, H., and Rao, Z. (2005). Structural insights into SARS coronavirus proteins. Curr Opin Struct Biol 15, 664-672.
6. Cattaruzza, S., and Perris, R. (2005). Proteoglycan control of cell movement during wound healing and cancer spreading. Matrix Biol 24, 400-417.
7. Chan, H. L., Tsui, S. K., and Sung, J. J. (2003). Coronavirus in severe acute respiratory syndrome (SARS). Trends Mol Med 9, 323-325.
8. Chen, S., Chen, L., Tan, J., Chen, J., Du, L., Sun, T., Shen, J., Chen, K., Jiang, H., and Shen, X. (2005). Severe acute respiratory syndrome coronavirus 3C-like proteinase N terminus is indispensable for proteolytic activity but not for enzyme dimerization. Biochemical and thermodynamic investigation in conjunction with molecular dynamics simulations. J Biol Chem 280, 164-173.
9. Chen, H., Wei, P., Huang, C., Tan, L., Liu, Y., and Lai, L. (2006). Only one protomer is active in the dimer of SARS 3C-like proteinase. J Biol Chem 281, 13894-13898.
10. Chen, S., Hu, T., Zhang, J., Chen, J., Chen, K., Ding, J., Jiang, H., and Shen, X. (2008). Mutation of Gly11 on the dimer interface results in the complete crystallographic dimer dissociation of SARS-CoV 3CLpro: Crystal structure with molecular dynamics simulations. J Biol Chem 283, 554-564.
11. Chen, S., Jonas, F., Chen, C., and Higenfiled, R. (2010). Liberation of SARS-CoV main protease from the viral polyprotein: N-terminal autocleavage does not depend on the mature dimerization mode. Protein Cell 1, 59-74.
12. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995). NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6, 277-293.
13. Emsley, P., and Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
14. Fan, K., Wei, P., Feng, Q., Chen, S., Huang, C., Ma, L., Lai, B., Pei, J., Liu, Y., Chen, J., et al. (2004). Biosynthesis, purification, and substrate specificity of severe acute respiratory syndrome coronavirus 3C-like proteinase. J Biol Chem 279, 1637-1642.
15. Graziano, V., McGrath, W. J., DeGruccio, A. M., Dunn, J. J., and Mangel, W. F. (2006a). Enzymatic activity of the SARS coronavirus main proteinase dimer. FEBS Lett 580, 2577-2583.
16. Graziano, V., McGrath, W. J., Yang, L., and Mangel, W. F. (2006b). SARS CoV main proteinase: The monomer-dimer equilibrium dissociation constant. Biochemistry 45, 14632-14641.
17. Gronenborn, A. M. (2009). Protein acrobatics in pairs-dimerization via domain swapping. Curr Opin Struct Biol 19, 39-49.
18. Hsu, W. C., Chang, H. C., Chou, C. Y., Tsai, P. J., Lin, P. I., and Chang, G. G. (2005). Critical assessment of important regions in the subunit association and catalytic action of the severe acute respiratory syndrome coronavirus main protease. J Biol Chem 280, 22741-22748.
19. Hu, T., Zhang, Y., Li, L., Wang, K., Chen, S., Chen, J., Ding, J., Jiang, H., and Shen, X. (2009). Two adjacent mutations on the dimer interface of SARS coronavirus 3C-like protease cause different conformational changes in crystal structure. Virology 388, 324-334.
20. Ivanov, D., Tsodikov, O. V., Kasanov, J., Ellenberger, T., Wagner, G., and Collins, T. (2007). Domain-swapped dimerization of the HIV-1 capsid C-terminal domain. Proc Natl Acad Sci U S A 104, 4353-4358.
21. Johnson, B. A., and Blevins, R. A. (1994). NMR View: A computer program for the visualization and analysis of NMR data. J Biomol NMR 4, 603-614.
22. Koradi, R., Billeter, M., and Wuthrich, K. (1996). MOLMOL: a program for display and analysis of macromolecular structures. Journal of molecular graphics 14, 51-55.
23. Kuiken, T., Fouchier, R. A., Schutten, M., Rimmelzwaan, G. F., van Amerongen, G., van Riel, D., Laman, J. D., de Jong, T., van Doornum, G., Lim, W., et al. (2003). Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362, 263-270.
24. Kuo, C.-J., Chi, Y.-H., Hsu, J. T.-A., and Liang, P.-H. (2004). Characterization of SARS main protease and inhibitor assay using a fluorogenic substrate. Biochem Biophys Res Commun 318, 862-867.
25. Laskowski, R., MacArthur, M., Moss, D., and Thornton, J. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26, 283-291.
26. Lee, T. W., Cherney, M. M., Huitema, C., Liu, J., James, K. E., Powers, J. C., Eltis, L. D., and James, M. N. (2005). Crystal structures of the main peptidase from the SARS coronavirus inhibited by a substrate-like aza-peptide epoxide. J Mol Biol 353, 1137-1151.
27. Leng, Q., and Bentwich, Z. (2003). A novel coronavirus and SARS. N Engl J Med 349, 709.
28. Libonati, M., Gotte, G., and Vottariello, F. (2008). A novel biological actions acquired by ribonuclease through oligomerization. Curr Pharm Biotechnol 9, 200-209.
29. Lin, P. Y., Chou, C. Y., Chang, H. C., Hsu, W. C., and Chang, G. G. (2008). Correlation between dissociation and catalysis of SARSCoV main protease. Arch Biochem Biophys 472, 34-42.
30. Liu, Y., and Eisenberg, D. (2002). 3D domain swapping: as domains continue to swap. Protein Sci 11, 1285-1299.
31. Mammen, M., Choi, S.-K., and Whitesides, G. M. (1998). Polyvalent interactions in biological systems: implications for design and use of multivalent ligands and inhibitors. Angew Chem Int Ed 37, 2754-2794.
32. Marley, J., Lu, M., and Bracken, C. (2001). A method for efficient isotopic labeling of recombinant proteins. J Biomol NMR 20, 71-75.
33. Matthews, B. W. (1968). Solvent content of protein crystals. J Mol Biol 33, 491-497.
34. McCoy, A., Grosse-Kunstleve, R., Adams, P., Winn, M., Storoni, L., and Read, R. (2007). Phaser crystallographic software. J Appl Cryst 40, 658-674.
35. Minor, K. H., and Peterson, C. B. (2002). Plasminogen activator inhibitor type 1 promotes the self-association of vitronectin into complexes exhibiting altered incorporation into the extracellular matrix. J Biol Chem 277, 10337-10345.
36. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D 53, 240-255.
37. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Macromolecular Crystallography, part A, C. W. Carter Jr., and R. M. Sweet, eds. (Academic Press), pp. 307-326.
38. Po-Huang, L. (2006). Characterization and inhibition of SARScoronavirus main protease. Curr Top Med Chem 6, 361-176.
39. Ruthenburg, A. J., Li, H., Patel, D. J., and Allis, C. D. (2007). Multivalent engagement of chromatin modifications by linked binding modules. Nat Rev Mol Cell Biol 8, 983-994.
40. Shi, J., and Song, J. (2006). The catalysis of the SARS 3C-like protease is under extensive regulation by its extra domain. FEBS J 273, 1035-1045.
41. Shi, J., Wei, Z., and Song, J. (2004). Dissection study on the severe acute respiratory syndrome 3C-like protease reveals the critical role of the extra domain in dimerization of the enzyme: defining the extra domain as a new target for design of highly specific protease inhibitors. J Biol Chem 279, 24765-24773.
42. Shi, J., Sivaraman, J., and Song, J. (2008). Mechanism for controlling the dimer-monomer switch and coupling dimerization to catalysis of the severe acute respiratory syndrome coronavirus 3C-like protease. J Virol 82, 4620-4629.
43. Snijder, E. J., Bredenbeek, P. J., Dobbe, J. C., Thiel, V., Ziebuhr, J., Poon, L. L., Guan, Y., Rozanov, M., Spaan, W. J., and Gorbalenya, A. E. (2003). Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol 331, 991-1004.
44. Tan, J., Verschueren, K. H., Anand, K., Shen, J., Yang, M., Xu, Y., Rao, Z., Bigalke, J., Heisen, B., Mesters, J. R., et al. (2005). pH-dependent conformational flexibility of the SARS-CoV main proteinase (M(pro)) dimer: molecular dynamics simulations and multiple X-ray structure analyses. J Mol Biol 354, 25-40.
45. Verschueren, K. H. G., Pumpor, K., Anemüller, S., Chen, S., Mesters, J. R., Hilgenfeld, R., (2008). A structural view of the inactivation of the SARS coronavirus main proteinase by benzotriazole esters. Chem Biol 15, 597-606.
46. Wei, P., Fan, K., Chen, H., Ma, L., Huang, C., Tan, L., Xi, D., Li, C., Liu, Y., Cao, A., et al. (2006). The N-terminal octapeptide acts as a dimerization inhibitor of SARS coronavirus 3C-like proteinase. Biochem Biophys Res Commun 339, 865-872.
47. Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfield, E., Markley, J. L., and Sykes, B. D. (1995). 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6, 135-140.
48. Xu, T., Ooi, A., Lee, H. C., Wilmouth, R., Liu, D. X., and Lescar, J. (2005). Structure of the SARS coronavirus main proteinase as an active C2 crystallographic dimer. Acta Crystallogr Sect F Struct Biol Cryst Commun 61, 964-966.
49. Xue, X., Yang, H., Shen, W., Zhao, Q., Li, J., Yang, K., Chen, C., Jin, Y., Bartlam, M., and Rao, Z. (2007). Production of authentic SARSCoV M(pro) with enhanced activity: application as a novel tagcleavage endopeptidase for protein overproduction. J Mol Biol 366, 965-975.
50. Yamasaki, M., Li, W., Johnson, D. J., and Huntington, J. A. (2008). Crystal structure of a stable dimer reveals the molecular basis of serpin polymerization. Nature 455, 1255-1258.
51. Yang, H., Yang, M., Ding, Y., Liu, Y., Lou, Z., Zhou, Z., Sun, L., Mo, L., Ye, S., Pang, H., et al. (2003). The crystal structures of severe acute respiratory syndrome virus main protease and its complex with an inhibitor. Proc Natl Acad Sci U S A 100, 13190-13195.
52. Yang, H., Xie, W., Xue, X., Yang, K., Ma, J., Liang, W., Zhao, Q., Zhou, Z., Pei, D., Ziebuhr, J., et al. (2005). Design of wide-spectrum inhibitors targeting coronavirus main proteases. PLoS Biol 3, e324.
53. Yang, H., Bartlam, M., and Rao, Z. (2006). Drug design targeting the main protease, the Achilles' heel of coronaviruses. Curr Pharm Des 12, 4573-4590.
54. Zhong, N., Zhang, S., Zou, P., Chen, J., Kang, X., Li, Z., Liang, C., Jin, C., and Xia, B. (2008). Without its N-finger, SARS-CoV main protease can form a novel dimer through its C-terminal domain. J Virol 82, 4227-4234.
55. Zhong, N., Zhang, S., Xue, F., Kang, X., Zou, P., Chen, J., Liang, C., Rao, Z., Jin, C., Lou, Z., et al. (2009). C-terminal domain of SARSCoV main protease can form a 3D domain-swapped dimer. Protein Sci 18, 839-844.