Characterization of bafinivirus main protease autoprocessing activities

Journal of Virology

Volumn 85, Issue 3, 2011, Pages 1348-1359

  Ulferts, Rachel ^a   Mettenleiter, Thomas C ^b   Ziebuhr, John ^a,c  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^c JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ASPARTIC ACID; GLYCINE; HISTIDINE; PROTEINASE; SERINE; THREONINE; VIRUS ENZYME;

ARTICLE; BAFINIVIRUS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONSENSUS SEQUENCE; CORONAVIRUS; DNA FLANKING REGION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME SUBSTRATE; EPITHELIUM TUMOR; GENE EXPRESSION SYSTEM; HETEROLOGOUS EXPRESSION; MUTAGENESIS; NIDOVIRALES; NONHUMAN; PHYLOGENY; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; SEQUENCE ANALYSIS; WHITE BREAM VIRUS;

BINDING SITES; CATALYTIC DOMAIN; CORONAVIRIDAE; DNA MUTATIONAL ANALYSIS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SERINE PROTEASES; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); CORONAVIRIDAE; EPITHELIOMA PAPULOSUM; HYPEROGLYPHE POROSA; NIDOVIRALES; PICORNAVIRIDAE;

EID: 78651386377     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01716-10     Document Type: Article

References (64)

1. Adams, M. J., J. F. Antoniw, and F. Beaudoin. 2005. Overview and analysis of the polyprotein cleavage sites in the family Potyviridae. Mol. Plant Pathol. 6:471-487.
2. Allaire, M., M. M. Chernaia, B. A. Malcolm, and M. N. James. 1994. Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature 369:72-76.
3. Anand, K., G. J. Palm, J. R. Mesters, S. G. Siddell, J. Ziebuhr, and R. Hilgenfeld. 2002. Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra alpha-helical domain. EMBO J. 21:3213-3224.
4. pro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767.
5. Ash, E. L., J. L. Sudmeier, E. C. De Fabo, and W. W. Bachovchin. 1997. A low-barrier hydrogen bond in the catalytic triad of serine proteases? Theory versus experiment. Science 278:1128-1132.
6. Bachovchin, W. W. 1986. 15N NMR spectroscopy of hydrogen-bonding interactions in the active site of serine proteases: evidence for a moving histidine mechanism. Biochemistry 25:7751-7759.
7. Barrette-Ng, I. H., K. K. Ng, B. L. Mark, D. Van Aken, M. M. Cherney, C. Garen, Y. Kolodenko, A. E. Gorbalenya, E. J. Snijder, and M. N. James. 2002. Structure of arterivirus nsp4: the smallest chymotrypsin-like proteinase with an alpha/beta C-terminal extension and alternate conformations of the oxyanion hole. J. Biol. Chem. 277:39960-39966.
8. Blair, W. S., J. H. Nguyen, T. B. Parsley, and B. L. Semler. 1996. Mutations in the poliovirus 3CD proteinase S1-specificity pocket affect substrate recognition and RNA binding. Virology 218:1-13.
9. Cole, C., J. D. Barber, and G. J. Barton. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36:W197-W201.
10. Craik, C. S., S. Roczniak, C. Largman, and W. J. Rutter. 1987. The catalytic role of the active site aspartic acid in serine proteases. Science 237:909-913.
11. Deming, D. J., R. L. Graham, M. R. Denison, and R. S. Baric. 2007. Processing of open reading frame 1a replicase proteins nsp7 to nsp10 in murine hepatitis virus strain A59 replication. J. Virol. 81:10280-10291.
12. Donaldson, E. F., R. L. Graham, A. C. Sims, M. R. Denison, and R. S. Baric. 2007. Analysis of murine hepatitis virus strain A59 temperature-sensitive mutant TS-LA6 suggests that nsp10 plays a critical role in polyprotein processing. J. Virol. 81:7086-7098.
13. Enjuanes, L., A. E. Gorbalenya, R. J. de Groot, J. A. Cowley, J. Ziebuhr, and E. J. Snijder. 2008. Nidovirales, p. 419-430. In B. W. J. Mahy and M. H. V. van Regenmortel (ed.), Encyclopedia of virology, 3rd ed., vol. 3. Elsevier, Oxford, England.
14. Fang, S., H. Shen, J. Wang, F. P. Tay, and D. X. Liu. 2010. Functional and genetic studies of the substrate specificity of coronavirus infectious bronchitis virus 3C-like proteinase. J. Virol. 84:7325-7336.
15. Fodor, K., V. Harmat, R. Neutze, L. Szilagyi, L. Graf, and G. Katona. 2006. Enzyme:substrate hydrogen bond shortening during the acylation phase of serine protease catalysis. Biochemistry 45:2114-2121.
16. Frey, P. A., S. A. Whitt, and J. B. Tobin. 1994. A low-barrier hydrogen bond in the catalytic triad of serine proteases. Science 264:1927-1930.
17. Gayathri, P., P. S. Satheshkumar, K. Prasad, S. Nair, H. S. Savithri, and M. R. Murthy. 2006. Crystal structure of the serine protease domain of Sesbania mosaic virus polyprotein and mutational analysis of residues forming the S1-binding pocket. Virology 346:440-451.
18. Gorbalenya, A. E. 2008. Genomics and evolution of the Nidovirales, p. 15-28. In S. Perlman, T. Gallagher, and E. J. Snijder (ed.), Nidoviruses. ASM Press, Washington, DC.
19. Gorbalenya, A. E., A. P. Donchenko, V. M. Blinov, and E. V. Koonin. 1989. Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold. FEBS Lett. 243:103-114.
20. Gorbalenya, A. E., L. Enjuanes, J. Ziebuhr, and E. J. Snijder. 2006. Nidovirales: evolving the largest RNA virus genome. Virus Res. 117:17-37.
21. Gorbalenya, A. E., E. V. Koonin, A. P. Donchenko, and V. M. Blinov. 1989. Coronavirus genome: prediction of putative functional domains in the nonstructural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res. 17:4847-4861.
22. Gouet, P., E. Courcelle, D. I. Stuart, and F. Metoz. 1999. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305-308.
23. Granzow, H., F. Weiland, D. Fichtner, H. Schütze, A. Karger, E. Mundt, B. Dresenkamp, P. Martin, and T. C. Mettenleiter. 2001. Identification and ultrastructural characterization of a novel virus from fish. J. Gen. Virol. 82:2849-2859.
24. Hedstrom, L. 2002. Serine protease mechanism and specificity. Chem. Rev. 102:4501-4524.
25. Hegyi, A., A. Friebe, A. E. Gorbalenya, and J. Ziebuhr. 2002. Mutational analysis of the active centre of coronavirus 3C-like proteases. J. Gen. Virol. 83:581-593.
26. Hegyi, A., and J. Ziebuhr. 2002. Conservation of substrate specificities among coronavirus main proteases. J. Gen. Virol. 83:595-599.
27. Ivanoff, L. A., T. Towatari, J. Ray, B. D. Korant, and S. R. Petteway, Jr. 1986. Expression and site-specific mutagenesis of the poliovirus 3C protease in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 83:5392-5396.
28. Jones, D. H., and B. H. Howard. 1991. A rapid method for recombination and site-specific mutagenesis by placing homologous ends on DNA using polymerase chain reaction. Biotechniques 10:62-66.
29. Kiang, D., and S. M. Matsui. 2002. Proteolytic processing of a human astrovirus nonstructural protein. J. Gen. Virol. 83:25-34.
30. 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. CLUSTAL W and CLUSTAL X version 2.0. Bioinformatics 23:2947-2948.
31. Matthews, D. A., W. W. Smith, R. A. Ferre, B. Condon, G. Budahazi, W. Sisson, J. E. Villafranca, C. A. Janson, H. E. McElroy, C. L. Gribskov, and S. Worland. 1994. Structure of human rhinovirus 3C protease reveals a trypsin-like polypeptide fold, RNA-binding site, and means for cleaving precursor polyprotein. Cell 77:761-771.
32. Mosimann, S. C., M. M. Cherney, S. Sia, S. Plotch, and M. N. James. 1997. Refined X-ray crystallographic structure of the poliovirus 3C gene product. J. Mol. Biol. 273:1032-1047.
33. Phan, J., A. Zdanov, A. G. Evdokimov, J. E. Tropea, H. K. Peters III, R. B. Kapust, M. Li, A. Wlodawer, and D. S. Waugh. 2002. Structural basis for the substrate specificity of tobacco etch virus protease. J. Biol. Chem. 277:50564-50572.
34. Rost, B., G. Yachdav, and J. Liu. 2004. The PredictProtein server. Nucleic Acids Res. 32:W321-W326.
35. Roy, A., A. Kucukural, and Y. Zhang. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5:725-738.
36. Ryan, M. D., and M. Flint. 1997. Virus-encoded proteinases of the picornavirus supergroup. J. Gen. Virol. 78:699-723.
37. Schechter, I., and A. Berger. 1967. On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27:157-162.
38. Schütze, H., R. Ulferts, B. Schelle, S. Bayer, H. Granzow, B. Hoffmann, T. C. Mettenleiter, and J. Ziebuhr. 2006. Characterization of White bream virus reveals a novel genetic cluster of nidoviruses. J. Virol. 80:11598-11609.
39. Smits, S. L., E. J. Snijder, and R. J. de Groot. 2006. Characterization of a torovirus main proteinase. J. Virol. 80:4157-4167.
40. 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.
41. Snijder, E. J., A. L. Wassenaar, L. C. van Dinten, W. J. Spaan, and A. E. Gorbalenya. 1996. The arterivirus nsp4 protease is the prototype of a novel group of chymotrypsin-like enzymes, the 3C-like serine proteases. J. Biol. Chem. 271:4864-4871.
42. Speroni, S., J. Rohayem, S. Nenci, D. Bonivento, I. Robel, J. Barthel, V. B. Luzhkov, B. Coutard, B. Canard, and A. Mattevi. 2009. Structural and biochemical analysis of human pathogenic astrovirus serine protease at 2.0 Å resolution. J. Mol. Biol. 387:1137-1152.
43. Sprang, S., T. Standing, R. J. Fletterick, R. M. Stroud, J. Finer-Moore, N. H. Xuong, R. Hamlin, W. J. Rutter, and C. S. Craik. 1987. The three-dimensional structure of Asn102 mutant of trypsin: role of Asp102 in serine protease catalysis. Science 237:905-909.
44. Tautz, N., A. Kaiser, and H. J. Thiel. 2000. NS3 serine protease of bovine viral diarrhea virus: characterization of active site residues, NS4A cofactor domain, and protease-cofactor interactions. Virology 273:351-363.
45. 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.
46. Tian, X., G. Lu, F. Gao, H. Peng, Y. Feng, G. Ma, M. Bartlam, K. Tian, J. Yan, R. Hilgenfeld, and G. F. Gao. 2009. Structure and cleavage specificity of the chymotrypsin-like serine protease (3CLSP/nsp4) of porcine reproductive and respiratory syndrome virus (PRRSV). J. Mol. Biol. 392:977-993.
47. Ulferts, R., I. Imbert, B. Canard, and J. Ziebuhr. 2010. Expression and functions of SARS coronavirus replicative proteins, p. 75-98. In S. K. Lal (ed.), Molecular biology of the SARS-coronavirus. Springer, Berlin, Germany.
48. van Vliet, A. L., S. L. Smits, P. J. Rottier, and R. J. de Groot. 2002. Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J. 21:6571-6580. (Pubitemid 35448434)
49. Verschueren, K. H., K. Pumpor, S. Anemuller, S. Chen, J. R. Mesters, and R. Hilgenfeld. 2008. A structural view of the inactivation of the SARS coronavirus main proteinase by benzotriazole esters. Chem. Biol. 15:597-606.
50. Woo, P. C., Y. Huang, S. K. Lau, H. W. Tsoi, and K. Y. Yuen. 2005. In silico analysis of ORF1ab in coronavirus HKU1 genome reveals a unique putative cleavage site of coronavirus HKU1 3C-like protease. Microbiol. Immunol. 49:899-908.
51. Xue, X., H. Yang, W. Shen, Q. Zhao, J. Li, K. Yang, C. Chen, Y. Jin, M. Bartlam, and Z. Rao. 2007. Production of authentic SARS-CoV M(pro) with enhanced activity: application as a novel tag-cleavage endopeptidase for protein overproduction. J. Mol. Biol. 366:965-975.
52. Xue, X., H. Yu, H. Yang, F. Xue, Z. Wu, W. Shen, J. Li, Z. Zhou, Y. Ding, Q. Zhao, X. C. Zhang, M. Liao, M. Bartlam, and Z. Rao. 2008. Structures of two coronavirus main proteases: implications for substrate binding and antiviral drug design. J. Virol. 82:2515-2527.
53. Yang, H., W. Xie, X. Xue, K. Yang, J. Ma, W. Liang, Q. Zhao, Z. Zhou, D. Pei, J. Ziebuhr, R. Hilgenfeld, K. Y. Yuen, L. Wong, G. Gao, S. Chen, Z. Chen, D. Ma, M. Bartlam, and Z. Rao. 2005. Design of wide-spectrum inhibitors targeting coronavirus main proteases. PLoS Biol. 3:e324.
54. Yang, H., M. Yang, Y. Ding, Y. Liu, Z. Lou, Z. Zhou, L. Sun, L. Mo, S. Ye, H. Pang, G. F. Gao, K. Anand, M. Bartlam, R. Hilgenfeld, and Z. Rao. 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.
55. Yao, Z., D. H. Jones, and C. Grose. 1992. Site-directed mutagenesis of herpesvirus glycoprotein phosphorylation sites by recombination polymerase chain reaction. PCR Methods Appl. 1:205-207.
56. Zhang, Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. (Pubitemid 351267364)
57. Zhao, Q., S. Li, F. Xue, Y. Zou, C. Chen, M. Bartlam, and Z. Rao. 2008. Structure of the main protease from a global infectious human coronavirus, HCoV-HKU1. J. Virol. 82:8647-8655.
58. Ziebuhr, J. 2008. Coronavirus replicative proteins, p. 65-81. In S. Perlman, T. Gallagher, and E. J. Snijder (ed.), Nidoviruses. ASM Press, Washington, DC.
59. Ziebuhr, J. 2005. The coronavirus replicase. Curr. Top. Microbiol. Immunol. 287:57-94.
60. Ziebuhr, J., S. Bayer, J. A. Cowley, and A. E. Gorbalenya. 2003. The 3C-like proteinase of an invertebrate nidovirus links coronavirus and potyvirus homologs. J. Virol. 77:1415-1426.
61. Ziebuhr, J., G. Heusipp, and S. G. Siddell. 1997. Biosynthesis, purification, and characterization of the human coronavirus 229E 3C-like proteinase. J. Virol. 71:3992-3997.
62. Ziebuhr, J., and S. G. Siddell. 1999. Processing of the human coronavirus 229E replicase polyproteins by the virus-encoded 3C-like proteinase: identification of proteolytic products and cleavage sites common to pp1a and pp1ab. J. Virol. 73:177-185.
63. Ziebuhr, J., E. J. Snijder, and A. E. Gorbalenya. 2000. Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol. 81:853-879.
64. Zunszain, P. A., S. R. Knox, T. R. Sweeney, J. Yang, N. Roque-Rosell, G. J. Belsham, R. J. Leatherbarrow, and S. Curry. 2010. Insights into cleavage specificity from the crystal structure of foot-and-mouth disease virus 3C protease complexed with a peptide substrate. J. Mol. Biol. 395:375-389.