A novel mutation in murine hepatitis virus nsp5, the viral 3C-like proteinase, causes temperature-sensitive defects in viral growth and protein processing

Journal of Virology

Volumn 82, Issue 12, 2008, Pages 5999-6008

  Sparks, Jennifer S ^a,b   Donaldson, Eric F ^c   Lu, Xiaotao ^a,b   Baric, Ralph S ^c,d   Denison, Mark R ^a,b,e  

^a Department of Microbiology and Immunology ^*

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d IL   (United States)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; GENOMICS; MURINE HEPATITIS CORONAVIRUS; MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PROCESSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TEMPERATURE SENSITIVITY; VIROGENESIS; VIRUS ISOLATION;

ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CONSERVED SEQUENCE; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MURINE HEPATITIS VIRUS; MUTATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; TEMPERATURE; VIRAL PROTEINS;

MURINE HEPATITIS VIRUS;

EID: 44949216764     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00203-08     Document Type: Article

References (45)

1. 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.
2. Anand, K., J. Ziebuhr, P. Wadhwani, J. R. Mesters, and R. Hilgenfeld. 2003. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767.
3. Bacha, U., J. Barrila, A. Velazquez-Campoy, S. A. Leavitt, and E. Freire. 2004. Identification of novel inhibitors of the SARS coronavirus main protease 3CLpro. Biochemistry 43:4906-4912.
4. Baker, S. C., K. Yokomori, S. Dong, R. Carlisle, A. E. Gorbalenya, E. V. Koonin, and M. M. C. Lai. 1993. Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus. J. Virol. 67:6056-6063.
5. Bates, P. A., L. A. Kelley, R. M. MaeCallum, and M. J. Sternberg. 2001. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins 45(Suppl. 5): 39-46.
6. Bates, P. A., and M. J. Sternberg. 1999. Model building by comparison at CASP3: using expert knowledge and computer automation. Proteins 37(Suppl. 3):47-54.
7. Bonilla, P. J., A. E. Gorbalenya, and S. R. Weiss. 1994. Mouse hepatitis virus strain A59 RNA polymerase gene ORF 1a: heterogeneity among MHV strains. Virology 198:736-740.
8. Bost, A. G., E. Prentice, and M. R. Denison. 2001. Mouse hepatitis virus replicase protein complexes are translocated to sites of M protein accumulation in the ERGIC at late times of infection. Virology 285:21-29.
9. Bredenbeek, P. J., C. J. Pachuk, A. F. H. Noten, J. Charite, W. Luytjes, S. R. Weiss, and W. J. M. Spaan. 1990. The primary structure and expression of the second open reading frame of the polymerase gene of the coronavirus MHV-A59; a highly conserved polymerase is expressed by an efficient ribosomal frameshifting mechanism. Nucleic Acids Res. 18:1825-1832.
10. Brockway, S. M., X. T. Lu, T. R. Peters, T. S. Dermody, and M. R. Denison. 2004. Intracellular localization and protein interactions of the gene 1 protein p28 during mouse hepatitis virus replication. J. Virol. 78:11551-11562.
11. Chen, W., and R. S. Baric. 1996. Molecular anatomy of mouse hepatitis virus persistence: coevolution of increased host cell resistance and virus virulence. J. Virol. 70:3947-3960.
12. Chen, W., V. J. Madden, C. J. Bagnell, and R. S. Baric. 1997. Host-derived intracellular immunization against mouse hepatitis virus infection. Virology 228:318-332.
13. Cheng, V. C., S. K. Lau, P. C. Woo, and K. Y. Yuen. 2007. Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clin. Microbiol. Rev. 20:660-694.
14. Contreras-Moreira, B., and P. A. Bates. 2002. Domain fishing: a first step in protein comparative modelling. Bioinformatics 18:1141-1142.
15. Denison, M. R., B. Yount, S. M. Brockway, R. L. Graham, A. C. Sims, X. Lu, and R. S. Baric. 2004. Cleavage between replicase proteins p28 and p65 of mouse hepatitis virus is not required for virus replication. J. Virol. 78:5957-5965.
16. Denison, M. R., P. W. Zoltick, S. A. Hughes, B. Giangreco, A. L. Olson, S. Perlman, J. L. Leibowitz, and S. R. Weiss. 1992. Intracellular processing of the N-terminal ORF 1a proteins of the coronavirus MHV-A59 requires multiple proteolytic events. Virology 189:274-284.
17. Donaldson, E. F., A. C. Sims, R. L. Graham, M. R. Denison, and R. S. Baric. 2007. Murine hepatitis virus replicase protein nsp10 is a critical regulator of viral RNA synthesis. J. Virol. 81:6356-6368.
18. Drosten, C., S. Gunther, W. Preiser, S. van der Werf, H. R. Brodt, S. Becker, H. Rabenau, M. Panning, L. Kolesnikova, R. A. Fouchier, A. Berger, A. M. Burguiere, J. Cinatl, M. Eickmann, N. Escriou, K. Grywna, S. Kramme, J. C. Manuguerra, S. Muller, V. Rickerts, M. Sturmer, S. Vieth, H. D. Klenk, A. D. Osterhaus, H. Schmitz, and H. W. Doerr. 2003. Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348:1967-1976.
19. Ghosh, A. K., K. Xi, V. Grum-Tokars, X. Xu, K. Ratia, W. Fu, K. V. Houser, S. C. Baker, M. E. Johnson, and A. D. Mesecar. 2007. Structure-based design, synthesis, and biological evaluation of peptidomimetic SARS-CoV 3CLpro inhibitors. Bioorg. Med. Chem. Lett. 17:5876-5880.
20. Ghosh, A. K., K. Xi, K. Ratia, B. D. Santarsiero, W. Fu, B. H. Harcourt, P. A. Rota, S. C. Baker, M. E. Johnson, and A. D. Mesecar. 2005. Design and synthesis of peptidomimetic severe acute respiratory syndrome chymotrypsin-like protease inhibitors. J. Med. Chem. 48:6767-6771.
21. Goetz, D. H., Y. Choe, E. Hansell, Y. T. Chen, M. McDowell, C. B. Jonsson, W. R. Roush, J. McKerrow, and C. S. Craik. 2007. Substrate specificity profiling and identification of a new class of inhibitor for the major protease of the SARS coronavirus. Biochemistry 46:8744-8752.
22. Gosert, R., A. Kanjanahaluethai, D. Egger, K. Bienz, and S. C. Baker. 2002. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 76:3697-3708.
23. Hirano, N., K. Fujiwara, and M. Matumoto. 1976. Mouse hepatitis virus (MHV-2). Plaque assay and propagation in mouse cell line DBT cells. Jpn. J. Microbiol. 20:219-225.
24. Hooft, R. W., C. Sander, and G. Vriend. 1996. Positioning hydrogen atoms by optimizing hydrogen-bond networks in protein structures. Proteins 26:363-376.
25. Kanjanahaluethai, A., and S. C. Baker. 2000. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J. Virol. 74:7911-7921.
26. Kanjanahaluethai, A., and S. C. Baker. 2001. Processing of the replicase of murine coronavirus: papain-like proteinase 2 (PLP2) acts to generate p150 and p44. Adv. Exp. Med. Biol. 494:267-273.
27. Kanjanahaluethai, A., D. Jukneliene, and S. C. Baker. 2003. Identification of the murine coronavirus MP1 cleavage site recognized by papain-like proteinase 2. J. Virol. 77:7376-7382.
28. Kim, J. C., R. A. Spence, P. F. Currier, X. Lu, and M. R. Denison. 1995. Coronavirus protein processing and RNA synthesis is inhibited by the cysteine proteinase inhibitor E64d. Virology 208:1-8.
29. Lee, H.-J., C.-K., Shieh, A. E. Gorbalenya, E. V. Koonin, N. LaMonica, J. Tuler, A. Bagdzhadhzyan, and M. M. C. Lai. 1991. The complete sequence (22 kilobases) of murine coronavirus gene 1 encoding the putative proteases and RNA polymerase. Virology 180:567-582.
30. Liu, Y., and B. Kuhlman. 2006. RosettaDesign server for protein design. Nucleic Acids Res. 34:W235-W238.
31. Lu, X., Y. Lu, and M. R. Denison. 1996. Intracellular and in vitro-translated 27-kDa proteins contain the 3C-like proteinase activity of the coronavirus MHV-A59. Virology 222:375-382.
32. Lu, Y., and M. R. Denison. 1997. Determinants of mouse hepatitis virus 3C-like proteinase activity. Virology 230:335-342.
33. Lu, Y., X. Lu, and M. R. Denison. 1995. Identification and characterization of a serine-like proteinase of the murine coronavirus MHV-A59. J. Virol. 69:3554-3559.
34. Paehuk, C. J., P. J. Bredenbeek, P. W. Zoltiek, W. J. Spaan, and S. R. Weiss. 1989. Molecular cloning of the gene encoding the putative polymerase of mouse hepatitis coronavirus, strain A59. Virology 171:141-148.
35. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
36. Poon, L. L., K. H. Chan, O. K. Wong, T. K. Cheung, I. Ng, B. Zheng, W. H. Seto, K. Y. Yuen, Y. Guan, and J. S. Peiris. 2004. Detection of SARS coronavirus in patients with severe acute respiratory syndrome by conventional and real-time quantitative reverse transcription-PCR assays. Clin. Chem. 50:67-72.
37. Poon, L. L. M., D. K. W. Chu, K. H. Chan, O. K. Wong, T. M. Ellis, Y. H. C. Leung, S. K. P. Lau, P. C. Y. Woo, K. Y. Suen, K. Y. Yuen, Y. Guan, and J. S. M. Peiris. 2005. Identification of a novel coronavirus in bats. J. Virol. 79:2001-2009.
38. Sawieki, S. G., and D. L. Sawieki. 1986. Coronavirus minus-strand RNA synthesis and effect of cycloheximide on coronavirus RNA synthesis. J. Virol. 57:328-334.
39. Sawieki, S. G., D. L. Sawieki, D. Younker, Y. Meyer, V. Thiel, H. Stokes, and S. G. Siddell. 2005. Functional and genetic analysis of coronavirus replicase-transcriptase proteins. PLoS Pathog. 1:e39.
40. Sperry, S. M., L. Kazi, R. L. Graham, R. S. Baric, S. R. Weiss, and M. R. Denison. 2005. Single-amino-acid substitutions in open reading frame (ORF) 1b-nsp14 and ORF 2a proteins of the coronavirus nouse hepatitis virus are attenuating in mice. J. Virol. 79:3391-3400.
41. Sturman, L. S., C. Eastwood, M. F. Frana, C. Duchala, F. Baker, C. S. Ricard, S. G. Sawieki, and K. V. Holmes. 1987. Temperature-sensitive mutants of MHV-A59. Adv. Exp. Med. Biol. 218:159-168.
42. 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.
43. 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. USA 100: 13190-13195.
44. Yount, B., M. R. Denison, S. R. Weiss, and R. S. Baric. 2102. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
45. Ziebuhr, J. 2005. The coronavirus replicase. Curr. Top. Microbiol. Immunol. 287:57-94.