Analysis of murine hepatitis virus strain A59 temperature-sensitive mutant TS-LA6 suggests that nsp10 plays a critical role in polyprotein processing

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 7086-7098

  Donaldson, Eric F ^a   Graham, Rachel L ^c,d   Sims, Amy C ^b   Denison, Mark R ^c,d   Baric, Ralph S ^a,b  

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

^b University of North Carolina at Chapel Hill   (United States)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYPROTEIN; PROTEIN NSP10; PROTEIN NSP11; PROTEIN NSP4; PROTEINASE; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RNA;

ANIMAL CELL; ARTICLE; CELL STRAIN BHK; CISTRON; CONTROLLED STUDY; MURINE HEPATITIS CORONAVIRUS; MURINE HEPATITIS VIRUS A59; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; RNA STRUCTURE; RNA SYNTHESIS; TEMPERATURE SENSITIVE MUTANT; TS LA6 VIRUS; VIRUS GENOME; VIRUS MUTANT; VIRUS REPLICATION; VIRUS STRAIN;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CRICETINAE; CYSTEINE ENDOPEPTIDASES; GENES; GENOME, VIRAL; HEAT; MURINE HEPATITIS VIRUS; MUTATION, MISSENSE; POLYPROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

MURINE HEPATITIS VIRUS; RNA VIRUSES;

EID: 34250846350     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00049-07     Document Type: Article

References (62)

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. 2003. Coronavirus main proteinase (3CLpro) structure: basis for design of anti-SARS drugs. Science 300:1763-1767.
3. Baker, S. C. 2004. Coronaviruses: from common colds to severe acute respiratory syndrome. Pediatr. Infect. Dis. J. 23:1049-1050.
4. Baker, S. C., H. Gao, and R. S. Baric. 1993. Altered proteolytic processing of the polymerase polyprotein in RNA (-) temperature sensitive mutants of murine coronavirus. Adv. Exp. Med. Biol. 342:215-219.
5. Baric, R. S., and B. Yount. 2000. Subgenomic negative-strand RNA function during mouse hepatitis virus infection. J. Virol. 74:4039-4046.
6. Bost, A. G., R. H. Carnahan, X. T. Lu, and M. R. Denison. 2000. Four proteins processed from the replicase gene polyprotein of mouse hepatitis virus colocalize in the cell periphery and adjacent to sites of virion assembly. J. Virol. 74:3379-3387.
7. Bredenbeek, P. J., C. J. Pachuk, A. F. Noten, J. Charite, W. Luytjes, S. R. Weiss, and W. J. 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.
8. Brierley, I., and F. J. Dos Ramos. 2006. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res. 119:29-42.
9. Brockway, S. M., and M. R. Denison. 2005. Mutagenesis of the murine hepatitis virus nsp1-coding region identifies residues important for protein processing, viral RNA synthesis, and viral replication. Virology 340:209-223.
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. Broughan, J. H., V. B. Randolph, and J. M. Tatem. 1997. Biochemical characterizations of two temperature-sensitive and attenuated strains of respiratory syncytial virus subgroup B. J. Virol. 71:4962-4970.
12. Cavanagh, D. 2005. Coronaviruses in poultry and other birds. Avian Pathol. 34:439-448.
13. Chambers, T. J., D. A. Droll, Y. Tang, Y. Liang, V. K. Ganesh, K. H. Murthy, and M. Nickells. 2005. Yellow fever virus NS2B-NS3 protease: characterization of charged-to-alanine mutant and revertant viruses and analysis of polyprotein cleavage activities. J. Gen. Virol. 86:1403-1413.
14. Diamond, S. E., and K. Kirkegaard. 1994. Clustered charged-to-alanine mutagenesis of poliovirus RNA-dependent RNA polymerase yields multiple temperature-sensitive mutants defective in RNA synthesis. J. Virol. 68:863-876.
15. 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.
16. Enjuanes, L., F. Almazan, I. Sola, and S. Zuniga. 2006. Biochemical aspects of coronavirus replication and virus-host interaction. Annu. Rev. Microbiol. 60:211-230.
17. Enjuanes, L., D. Cavanaugh, K. Holmes, M. Lai, H. Laude, P. Masters, P. Rottier, S. Siddell, W. Spaan, F. Taguchi, and P. Talbot. 2000. Coronaviridae, p. 835-859. In M. H. V. Van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carstens, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle, and R. B. Wickner (ed.), Virus taxonomy: classification and nomenclature of viruses. Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, San Diego, CA.
18. Fiser, A., R. K. Do, and A. Sali. 2000. Modeling of loops in protein structures. Protein Sci. 9:1753-1773.
19. Fournier, J. G., O. Robain, I. Cerutti, I. Tardivel, F. Chany-Fournier, and C. Chany. 1988. Detection of vesicular stomatitis virus (VSV) RNA in the central nervous system of infected mice by in situ hybridization. Acta Neuropathol. (Berlin) 75:554-556.
20. Gadkari, D. A., and C. R. Pringle. 1980. Temperature-sensitive mutants of Chandipura virus. II. Phenotypic characteristics of the six complementation groups. J. Virol. 33:107-114.
21. Gosert, R., G. Dollenmaier, and M. Weitz. 1997. Identification of active-site residues in protease 3C of hepatitis A virus by site-directed mutagenesis. J. Virol. 71:3062-3068.
22. Graham, R. L., A. C. Sims, S. M. Brockway, R. S. Baric, and M. R. Denison. 2005. The nsp2 replicase proteins of murine hepatitis virus and severe acute respiratory syndrome coronavirus are dispensable for viral replication. J. Virol. 79:13399-13411.
23. Harcourt, B. H., D. Jukneliene, A. Kanjanahaluethai, J. Bechill, K. M. Severson, C. M. Smith, P. A. Rota, and S. C. Baker. 2004. Identification of severe acute respiratory syndrome coronavirus replicase products and characterization of papain-like protease activity. J. Virol. 78:13600-13612.
24. Joseph, J. S., K. S. Saikatendu, V. Subramanian, B. W. Neuman, A. Brooun, M. Griffith, K. Moy, M. K. Yadav, J. Velasquez, M. J. Buchmeier, R. C. Stevens, and P. Kuhn. 2006. Crystal structure of nonstructural protein 10 from the severe acute respiratory syndrome coronavirus reveals a novel fold with two zinc-binding motifs. J. Virol. 80:7894-7901.
25. Kanjanahaluethai, A., and S. C. Baker. 2000. Identification of mouse hepatitis virus papain-like proteinase 2 activity. J. Virol. 74:7911-7921.
26. Kao, C. C., R. Quadt, R. P. Hershberger, and P. Ahlquist. 1992. Brome mosaic virus RNA replication proteins 1a and 2a form a complex in vitro. J. Virol. 66:6322-6329.
27. Kennedy-Morrow, J., and J. A. Lesnaw. 1984. Structural and functional characterization of the RNA-positive complementation groups, C and D, of the New lersey serotype of vesicular stomatitis virus: assignment of the M gene to the C complementation group. Virology 132:38-52.
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. Kroner, P., D. Richards, P. Traynor, and P. Ahlquist. 1989. Defined mutations in a small region of the brome mosaic virus 2 gene cause diverse temperature-sensitive RNA replication phenotypes. J. Virol. 63:5302-5309.
30. Kroner, P. A., B. M. Young, and P. Ahlquist. 1990. Analysis of the role of brome mosaic virus 1a protein domains in RNA replication, using linker insertion mutagenesis. J. Virol. 64:6110-6120.
31. Lai, M. M., and D. Cavanagh. 1997. The molecular biology of coronaviruses. Adv. Virus Res. 48:1-100.
32. Lau, S. K., P. C. Woo, C. C. Yip, H. Tse, H. W. Tsoi, V. C. Cheng, P. Lee, B. S. Tang, C. H. Cheung, R. A. Lee, L. Y. So, Y. L. Lau, K. H. Chan, and K. Y. Yuen. 2006. Coronavirus HKU1 and other coronavirus infections in Hong Kong. J. Clin. Microbiol. 44:2063-2071.
33. Marti-Renom, M. A., A. C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali. 2000. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29:291-325.
34. Masters, P. S. 2006. The molecular biology of coronaviruses. Adv. Virus Res. 66:193-292.
35. McIntosh, K. 1974. Coronaviruses: a comparative review. Curr. Top. Microbiol. Immunol. 1974:85-129.
36. Misura, K. M., D. Chivian, C. A. Rohl, D. E. Kim, and D. Baker. 2006. Physically realistic homology models built with ROSETTA can be more accurate than their templates. Proc. Natl. Acad. Sci. USA 103:5361-5366.
37. Ng, L. F., and D. X. Liu. 2002. Membrane association and dimerization of a cysteine-rich, 16-kilodalton polypeptide released from the C-terminal region of the coronavirus infectious bronchitis virus 1a polyprotein. J. Virol. 76: 6257-6267.
38. Pasternak, A. O., W. J. Spaan, and E. J. Snijder. 2006. Nidovirus transcription: how to make sense? J. Gen. Virol. 87:1403-1421.
39. Perlman, S. 1998. Pathogenesis of coronavirus-induced infections. Review of pathological and immunological aspects. Adv. Exp. Med. Biol. 440:503-513.
40. 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.
41. Pinon, J. D., R. R. Mayreddy, J. D. Turner, F. S. Khan, P. J. Bonilla, and S. R. Weiss. 1997. Efficient autoproteolytic processing of the MHV-A59 3C-like proteinase from the flanking hydrophobic domains requires membranes. Virology 230:309-322.
42. Racaniello, V. R., and C. Meriam. 1986. Poliovirus temperature-sensitive mutant containing a single nucleotide deletion in the 5′-noncoding region of the viral RNA. Virology 155:498-507.
43. Sawicki, D., D. B. Barkhimer, S. G. Sawicki, C. M. Rice, and S. Schlesinger. 1990. Temperature sensitive shut-off of alphavirus minus strand RNA synthesis maps to a nonstructural protein, nsP4. Virology 174:43-52.
44. Sawicki, D. L., and S. G. Sawicki. 1994. Alphavirus positive and negative strand RNA synthesis and the role of polyproteins in formation of viral replication complexes. Arch. Virol. Suppl. 9:393-405.
45. Sawicki, D. L., and S. G. Sawicki. 1993. A second nonstructural protein functions in the regulation of alphavirus negative-strand RNA synthesis. J. Virol. 67:3605-3610.
46. Sawicki, S. G., and D. L. Sawicki. 1986. Coronavirus minus-strand RNA synthesis and effect of cycloheximide on coronavirus RNA synthesis. J. Virol. 57:328-334.
47. Sawicki, S. G., and D. L. Sawicki. 2005. Coronavirus transcription: a perspective. Curr. Top. Microbiol. Immunol. 287:31-55.
48. Sawicki, S. G., D. L. Sawicki, 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.
49. Schaad, M. C., and R. S. Baric. 1994. Genetics of mouse hepatitis virus transcription: evidence that subgenomic negative strands are functional templates. J. Virol. 68:8169-8179.
50. Schaad, M. C., S. A. Stohlman, J. Egbert, K. Lum, K. Fu, T. Wei, Jr., and R. S. Baric. 1990. Genetics of mouse hepatitis virus transcription: identification of cistrons which may function in positive and negative strand RNA synthesis. Virology 177:634-645.
51. Schiller, J. J., A. Kanjanahaluethai, and S. C. Baker. 1998. Processing of the coronavirus MHV-JHM polymerase polyprotein: identification of precursors and proteolytic products spanning 400 kilodaltons of ORF1a. Virology 242: 288-302.
52. Siddell, S., D. Sawicki, Y. Meyer, V. Thiel, and S. Sawicki. 2001. Identification of the mutations responsible for the phenotype of three MHV RNA-negative ts mutants. Adv. Exp. Med. Biol. 494:453-458.
53. Stadler, K., V. Masignani, M. Eickmann, S. Becker, S. Abrignani, H. D. Klenk, and R. Rappuoli. 2003. SARS - beginning to understand a new virus. Nat. Rev. Microbiol. 1:209-218.
54. Stalcup, R. P., R. S. Baric, and J. L. Leibowitz. 1998. Genetic complementation among three panels of mouse hepatitis virus gene 1 mutants. Virology 241:112-121.
55. Tan, J., K. H. G. Verschueren, K. Anand, J. Shen, M. Yang, Y. Xu, Z. Rao, J. Bigalke, B. Heisen, and J. R. Mesters. 2005. pH-dependent conformational flexibility of the SARS-CoV main proteinase (Mpro) dimer: molecular dynamics simulations and multiple X-ray structure analyses. J. Mol. Biol. 354:25-40.
56. Tarr, G. C., and A. S. Lubiniecki. 1976. Chemically-induced temperature sensitive mutants of dengue virus type 2. I. Isolation and partial characterization. Arch. Virol. 50:223-235.
57. Tibble, K. W., I. Brierley, D. Cavanaugh, and T. D. Brown. 1996. Characterization in vitro of an autocatalytic processing activity associated with the predicted 3C-like proteinase domain of the coronavirus avian infectious bronchitis virus. J. Virol. 70:1923-1930.
58. van der Hoek, L., K. Pyrc, and B. Berkhout. 2006. Human coronavirus NL63, a new respiratory virus. FEMS Microbiol. Rev. 30:760-773.
59. 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.
60. Younker, D. R., and S. G. Sawicki. 1998. Negative strand RNA synthesis by temperature-sensitive mutants of mouse hepatitis virus. Adv. Exp. Med. Biol. 440:221-226.
61. Yount, B., M. R. Denison, S. R. Weiss, and R. S. Baric. 2002. Systematic assembly of a full-length infectious cDNA of mouse hepatitis virus strain A59. J. Virol. 76:11065-11078.
62. Ziebuhr, J. 2006. The coronavirus replicase: insights into a sophisticated enzyme machinery. Adv. Exp. Med. Biol. 581:3-11.