Nuclear magnetic resonance structure shows that the severe acute respiratory syndrome coronavirus-unique domain contains a macrodomain fold

Journal of Virology

Volumn 83, Issue 4, 2009, Pages 1823-1836

  Chatterjee, Amarnath ^a   Johnson, Margaret A ^a   Serrano, Pedro ^a   Pedrini, Bill ^a   Joseph, Jeremiah S ^a   Neuman, Benjamin W ^a,b   Saikatendu, Kumar ^a   Buchmeier, Michael J ^a   Kuhn, Peter ^a   Wüthrich, Kurt ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; AMINO ACID; NONSTRUCTURAL PROTEIN 3; NUCLEOSIDE TRIPHOSPHATE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; SARS CORONAVIRUS; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY;

ELECTROPHORETIC MOBILITY SHIFT ASSAY; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA; RNA REPLICASE; RNA-BINDING PROTEINS; SARS VIRUS; VIRAL NONSTRUCTURAL PROTEINS;

SARS CORONAVIRUS;

EID: 59649087454     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01781-08     Document Type: Article

References (56)

1. Allen, M. D., A. M. Buckle, S. C. Cordell, J. Löwe, and M. Bycroft. 2003. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330:503-511.
2. Brierly, I., and F. J. Dos Ramos. 2006. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res. 119:29-42.
3. Chakravarthy, S., S. K. Gundimella, C. Caron, P. Y. Perche, J. R. Pehrson, S. Khochbin, and K. Luger. 2005. Structural characterization of the histone variant macroH2A. Mol. Cell. Biol. 25:7616-7624.
4. Chatterjee, A., M. A. Johnson, P. Serrano, B. Pedrini, and K. Wüthrich. 2007. NMR assignment of the domain 513-651 from the SARS-CoV nonstructural protein nsp3. Biomol. NMR Assign. 1:191-194.
5. Clamp, M., J. Cuff, S. M. Searle, and G. J. Barton. 2004. The Jalview Java Alignment Editor. Bioinformatics 20:426-427.
6. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, J. Merz, K. M. Ferguson, D. M. Ferguson, D. C. Spellmyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:5179-5197.
7. Egloff, M.-P., H. Malet, A. Putics, M. Heinonen, H. Dutartre, A. Frangeul, A. Gruez, V. Campanacci, C. Cambillau, J. Ziebuhr, T. Ahola, and B. Canard. 2006. Structural and functional basis for ADP-ribose and poly(ADP-ribose) binding by viral macro domains. J. Virol. 80:8493-8502.
8. Enjuanes, L., F. Almazán, I. Sola, and S. Zuñiga. 2006. Biochemical aspects of coronavirus replication and virus-host interaction. Annu. Rev. Microbiol. 60:211-230.
9. Fiorito, F., S. Hiller, G. Wider, and K. Wüthrich. 2006. Automated resonance assignment of proteins: 6D APSY-NMR. J. Biomol. NMR 35:27-37.
10. Güntert, P., C. Mumenthaler, and K. Wüthrich. 1997. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273:283-298.
11. Herrmann, T., P. Güntert, and K. Wüthrich. 2002. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319:209-227.
12. Herrmann, T., P. Güntert, and K. Wüthrich. 2002. Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR 24:171-189.
13. Hiller, S. 2006. NMR methods for studies of folded and unfolded forms of globular proteins. ETH Diss. no. 16729. Ph.D. dissertation. Swiss Federal Institute of Technology, Zurich, Switzerland.
14. Hiller, S., F. Fiorito, K. Wüthrich, and G. Wider. 2005. Automated projection spectroscopy (APSY). Proc. Natl. Acad. Sci. USA 102:10876-10881.
15. Holm, L., and C. Sander. 1993. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:123-138.
16. Holm, L., and C. Sander. 1995. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20:478-480.
17. Koradi, R., M. Billeter, and P. Güntert. 2000. Point-centered domain decomposition for parallel molecular dynamics simulation. Comp. Phys. Commun. 124:139-147.
18. Koradi, R., M. Billeter, and K. Wüthrich. 1996. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14:51-55.
19. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. ClustalW and ClustalX version 2.0. Bioinformatics 23:2947-2948.
20. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
21. Luginbühl, P., P. Güntert, M. Billeter, and K. Wüthrich. 1996. The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules. J. Biomol. NMR 8:136-146.
22. Luginbühl, P., T. Tszyperski, and K. Wüthrich. 1995. Statistical basis for the use of 13C chemical shifts in protein structure determination. J. Magn. Reson. 109:229-233.
23. Marra, M. A., S. J. Jones, C. R. Astell, R. A. Holt, A. Brooks-Wilson, Y. S. Butterfield, J. Khattra, J. K. Asano, S. A. Barber, S. Y. Chan, A. Cloutier, S. M. Coughlin, D. Freeman, N. Girn, O. L. Griffith, S. R. Leach, M. Mayo, H. McDonald, S. B. Montgomery, P. K. Pandoh, A. S. Petrescu, A. G. Robertson, J. E. Schein, A. Siddiqui, D. E. Smailus, J. M. Stott, G. S. Yang, F. Plummer, A. Andonov, H. Artsob, N. Bastien, K. Bernard, T. F. Booth, D. Bowness, M. Czub, M. Drebot, L. Fernando, R. Flick, M. Garbutt, M. Gray, A. Grolla, S. Jones, H. Feldmann, A. Meyers, A. Kabani, Y. Li, S. Normand, U. Stroher, G. A. Tipples, S. Tyler, R. Vogrig, D. Ward, B. Watson, R. C. Brunham, M. Krajden, M. Petric, D. M. Skowronski, C. Upton, and R. L. Roper. 2003. The genome sequence of the SARS-associated coronavirus. Science 300:1399-1404.
24. 2O. J. Magn. Reson. B 102:317-321.
25. Murzin, A. G., S. E. Brenner, T. Hubbard, and C. Chothia. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247:536-540.
26. Navas-Martin, S. R., and S. Weiss. 2004. Coronavirus replication and pathogenesis: implications for the recent outbreak of severe acute respiratory syndrome (SARS), and the challenge for vaccine development. J. Neurovirol. 10:75-85.
27. Neuman, B. W., J. S. Joseph, K. S. Saikatendu, P. Serrano, A. Chatterjee, M. A. Johnson, L. Liao, J. P. Klaus, J. R Yates III, K. Wüthrich, R. C. Stevens, M. J. Buchmeier, and P. Kuhn. 2008. Proteomics analysis unravels the functional repertoire of coronavirus nonstructural protein 3. J. Virol. 82:5279-5294.
28. Oostra, M., M. C. Hagemeijer, M. van Gent, C. P. Bekker, E. G. te Lintelo, P. J. M. Rottier, and C. A. de Haan. 8 October 2008. Topology and membrane anchoring of the coronavirus replication complex: not all of the hydrophobic domains of nsp3 and nsp6 are membrane spanning. J. Virol. doi:10.1128/JVI.01219-08.
29. Prentice, E., J. McAuliffe, X. Lu, K. Subbarao, and M. R. Denison. 2004. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J. Virol. 78:9977-9986.
30. Ratia, K., K. S. Saikatendu, B. D. Santarsiero, N. Barretto, S. C. Baker, R. C. Stevens, and A. D. Mesecar. 2006. Severe acute respiratory syndrome coronavirus papain-like protease: structure of a viral deubiquitinating enzyme. Proc. Natl. Acad. Sci. USA 103:5717-5722.
31. 1H]-NOE experiment. J. Biomol. NMR 23:23-33.
32. Rota, P. A., M. S. Oberste, S. S. Monroe, W. A. Nix, R. Campagnoli, J. P. Icenogle, S. Penaranda, B. Bankamp, K. Maher, M. H. Chen, S. Tong, A. Tamin, L. Lowe, M. Frace, J. L. DeRisi, Q. Chen, D. Wang, D. D. Erdman, T. C. Peret, C. Burns, T. G. Ksiazek, P. E. Rollin, A. Sanchez, S. Liffick, B. Holloway, J. Limor, K. McCaustland, M. Olsen-Rasmussen, R. Fouchier, S. Gunther, A. D. Osterhaus, C. Drosten, M. A. Pallansch, L. J. Anderson, and W. J. Bellini. 2003. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300:1394-1399.
33. Saikatendu, K. S., J. S. Joseph, V. Subramanian, T. Clayton, M. Griffith, K. Moy, J. Velasquez, B. W. Neuman, M. J. Buchmeier, R. C. Stevens, and P. Kuhn. 2005. Structural basis of severe acute respiratory syndrome coronavirus ADP-ribose-1″-phosphate dephosphorylation by a conserved domain of nsP3. Structure 13:1665-1675.
34. Saraste, M., P. R. Sibbald, and A. Wittinghofer. 1990. The P-loop - a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15:430-434.
35. Sattler, M., J. Schleucher, and C. Griesinger. 1999. Heteronuclear multidimensional NMR experiments for the structure determination of proteins in solution employing pulsed field gradients. Prog. Nucl. Magnet. Reson. Spectrosc. 34:93-158.
36. Schmid, S. R., and P. Linder. 1992. D-E-A-D protein family of putative RNA helicases. Mol. Microbiol. 6:283-291.
37. Serrano, P., M. A. Johnson, M. S. Almeida, R. Horst, T. Herrmann, J. S. Joseph, B. W. Neuman, V. Subramanian, K. S. Saikatendu, M. J. Buchmeier, R. C. Stevens, P. Kuhn, and K. Wüthrich. 2007. Nuclear magnetic resonance structure of the N-terminal domain of nonstructural protein 3 from the severe acute respiratory syndrome coronavirus. J. Virol. 81:12049-12060.
38. Snijder, E. J., P. J. Bredenbeek, J. C. Dobbe, V. Thiel, J. Ziebuhr, L. L. Poon, Y. Guan, M. Rozanov, W. J. Spaan, and A. E. Gorbalenya. 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.
39. 13C nuclear magnetic resonance chemical shifts. J. Am. Chem. Soc. 113:5490-5492.
40. Stephen, F. A., L. M. Thomas, A. S. Alejandro, Z. Jinghui, Z. Zheng, M. Webb, and J. L. David. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res. 25:3389-3402.
41. Talluri, S., and G. Wagner. 1996. An optimized 3D NOESY-HSQC. J. Magn. Reson. B 112:200-205.
42. Tan, J., Y. Kusov, D. Mutschall, S. Tech, K. Nagarajan, R. Hilgenfeld, and C. L. Schmidt. 2007. The "SARS-unique domain" (SUD) of SARS coronavirus is an oligo(G)-binding protein. Biochem. Biophys. Res. Commun. 364:877-882.
43. Thiel, V., J. Herold, B. Schelle, and S. G. Siddell. 2001. Viral replicase gene products suffice for coronavirus discontinuous transcription. J. Virol. 75:6676-6681.
44. Thiel, V., K. A. Ivanov, A. Putics, T. Hertzig, B. Schelle, S. Bayer, B. Weissbrich, E. J. Snijder, H. Rabenau, H. W. Doerr, A. E. Gorbalenya, and J. Ziebuhr. 2003. Mechanisms and enzymes involved in SARS coronavirus genome expression. J. Gen. Virol. 84:2305-2315.
45. Volk, J., T. Herrmann, and K. Wüthrich. 2008. Automated sequence-specific protein NMR assignment using the memetic algorithm MATCH. J. Biomol. NMR 41:127-138.
46. Walker, J. E., M. Saraste, M. J. Runswick, and N. J. Gay. 1982. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:945-951.
47. Webb, M. R. 1992. A continuous spectrophotometric assay for inorganic phosphate and for measuring phosphate release kinetics in biological systems. Proc. Natl. Acad. Sci. USA 89:4884-4887.
48. Weiss, S. R., and S. Navas-Martin. 2005. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol. Mol. Biol. Rev. 69:635-664.
49. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 6:135-140.
50. Woo, P. C., S. K. Lau, C. C. Yip, Y. Huang, H. W. Tsoi, K. H. Chan, and K. Y. Yuen. 2006. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J. Virol. 80:7136-7145.
51. Woo, P. C., M. Wang, S. K. Lau, H. Xu, R. W. Poon, R. Guo, Wong, B. H., K. Gao, H. W. Tsoi, Y. Huang, K. S. Li, C. S. Lam, K. H. Chan, B. J. Zheng, and K. Y. Yuen. 2007. Comparative analysis of twelve genomes of three novel group 2c and group 2d coronaviruses reveals unique group and subgroup features. J. Virol. 81:1574-1585.
52. Wüthrich, K. 1986. NMR of proteins and nucleic acids. Wiley, New York, NY.
53. Yao, N., T. Hesson, M. Cable, Z. Hong, A. D. Kwong, H. V. Le, and P. C. Weber. 1997. Structure of the hepatitis C virus RNA helicase domain. Nat. Struct. Biol. 4:463-467.
54. Zhu, G., Y. Xia, L. K. Nicholson, and K. H. Sze. 2000. Protein dynamics measurements by TROSY-based NMR experiments. J. Magn. Reson. 143:423-426.
55. Ziebuhr, J. 2004. Molecular biology of severe acute respiratory syndrome coronavirus. Curr. Opin. Microbiol. 7:412-419.
56. Zuñiga, S., I. Sola, S. Alonso, and L. Enjuanes. 2004. Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J. Virol. 78:980-994.