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Coronavirus Gene Expression

Genome Organization and Protein Synthesis
  • Willem Luytjes
Chapter
Part of the The Viruses book series (VIRS)

Abstract

Recent studies on coronaviruses have provided detailed insights into the arrangement of open reading frames (ORFs) in the coronavirus genome and the strategies used to translate these ORFs. This chapter will present an updated and detailed overview of coronavirus genomic organization as well as of the coding assignments of the coronavirus ORFs (genes) and their translation strategies (see also the general reviews on coronaviruses by Spaan et al., 1988; Lai, 1990: Holmes, 1991).

Keywords

Infectious Bronchitis Virus Mouse Hepatitis Virus Ribosomal Frameshifting Transmissible Gastroenteritis Virus Murine Hepatitis Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abraham, S., Kienzle, T. E., Lapps, W. E., and Brian, D. A., 1990, Sequence and expression analysis of potential nonstructural proteins of 4.9, 4.8, 12.7, and 9.5 kDa encoded between the spike and membrane protein genes of the bovine coronavirus, Virology 177:488.PubMedCrossRefGoogle Scholar
  2. Baker, S. C., Shieh, C.-K., Soe, L. H., Chang, M. F., Vannier, D. M., and Lai, M. M. C., 1989, Identification of a domain required for autoproteolytic cleavage of murine coronavirus gene A polyprotein, J. Virol. 63:3693.PubMedGoogle Scholar
  3. Baker, S. C., Yokomori, K., Dong, S., Carlisle, R., Gorbalenya, A. E., Koonin, E. V., and Lai, M. M., 1993, Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus, J. Virol 67:6056.PubMedGoogle Scholar
  4. Bonilla, P. J., Gorbalenya, A. E., and Weiss, S. R., 1994, Mouse hepatitis virus strain A59 polymerase gene ORF la: Heterogeneity among MHV strains, Virology 198:736.PubMedCrossRefGoogle Scholar
  5. Boursnell, M. E., Brown, T. D., Foulds, I. J., Green, P. F., Tomley, F. M., and Binns, M. M., 1987, Completion of the sequence of the genome of the coronavirus avian infectious bronchitis virus, J. Gen. Virol. 68:57.PubMedCrossRefGoogle Scholar
  6. Bredenbeek, P. J., Noten, A. F. H., Horzinek, M. C., and Spaan, W. J. M., 1990a, Identification and stability of a 30-kDa non-structural protein encoded by mRNA 2 of mouse hepatitis virus in infected cells, Virology 175:303.PubMedCrossRefGoogle Scholar
  7. Bredenbeek, P. J., Pachuk, C. J., Noten, A. F. H., Charite, J., Luytjes, W., Weiss, S. R., and Spaan, W. J. M., 1990b, The primary structure and expression of the 2nd 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.PubMedCrossRefGoogle Scholar
  8. Bredenbeek, P. J., Snijder, E. J., Noten, F. H., Den Boon, J. A., Schaaper, W M., Horzinek, M. C., and Spaan, W. J., 1990c, The polymerase gene of corona- and toroviruses: Evidence for an evolutionary relationship, Adv. Exp. Med. Biol. 276:307.PubMedCrossRefGoogle Scholar
  9. Bridgen, A., Duarte, M., Tobler, K., Laude, H., and Ackermann, M., 1993, Sequence determination of the nucleocapsid protein gene of the porcine epidemic diarrhoea virus confirms that this virus is a coronavirus related to human coronavirus 229E and porcine transmissible gastroenteritis virus, J. Gen. Virol. 74:1795.PubMedCrossRefGoogle Scholar
  10. Brierley, I., Boursnell, M. E., Binns, M. M., Bilimoria, B., Blok, V. C., Brown, T. D., and Inglis, S. C., 1987, An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV, EMBO J. 6:3779.PubMedGoogle Scholar
  11. Brierley, I., Digard, P., and Inglis, S. C., 1989, Characterization of an efficient coronavirus ribosomal frameshifting signal: Requirement for an RNA pseudoknot, Cell 57:537.PubMedCrossRefGoogle Scholar
  12. Brierley, I., Boursnell, M. E. G., Binns, M. M., Bilimoria, B., Rolley, N. J., Brown, T. D. K., and Inglis, S. C., 1990, Products of the polymerase-encoding region of the coronavirus IBV, Adv. Exp. Med. Biol. 276:275.PubMedCrossRefGoogle Scholar
  13. Brierley, I., Rolley, N. J., Jenner, A. J., and Inglis, S. C., 1991, Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal, J. Mol. Biol. 220:889.PubMedCrossRefGoogle Scholar
  14. Britton, P., Carmenes, R. S., Page, K. W., Garwes, D. J., and Parra, F., 1988, Sequence of the nucleoprotein gene from a virulent British field isolate of transmissible gastroenteritis virus and its expression in Saccharomyces cerevisiae, Mol. Micro. 2:89.CrossRefGoogle Scholar
  15. Britton, P., Lopez Otin, C., Martin Alonso, J., and Parra, F., 1989, Sequence of the coding regions from the 3.0 kb and 3.9 kb mRNA. Subgenomic species from a virulent isolate of transmissible gastroenteritis virus, Arch. Virol. 105:165.PubMedCrossRefGoogle Scholar
  16. Britton, P., Mawditt, K. L., and Page, K. W., 1991, The cloning and sequencing of the virion protein genes from a British isolate of porcine respiratory coronavirus: Comparison with transmissible gastroenteritis virus genes, Virus Res. 21:181.PubMedCrossRefGoogle Scholar
  17. Budzilowicz, C. J., and Weiss, S. R., 1987, In vitro synthesis of two polypeptides from a nonstructural gene of coronavirus mouse hepatitis virus strain A59, Virology 157:509.PubMedCrossRefGoogle Scholar
  18. Cavanagh, D., and Davis, P. J., 1988, Evolution of avian coronavirus IBV: Sequence of the matrix glycoprotein gene and intergenic region of several serotypes, J. Gen. Virol. 69:621.PubMedCrossRefGoogle Scholar
  19. Cavanagh, D., Brian, D. A., Enjuanes, L., Holmes, K. V, Lai, M. M. C., Laude, H., Siddell, S. G., Spaan, W., Taguchi, F., and Talbot, P. J., 1990, Recommendations of the coronavirus study group for the nomenclature of the structural proteins, messenger RNAs, and genes of coronaviruses, Virology 176:306.PubMedCrossRefGoogle Scholar
  20. Cox, G. J., Parker, M. D., and Babiuk, L. A., 1989, The sequence of cDNA of bovine coronavirus 32K nonstructural gene, Nucleic Acids Res. 17:5847.PubMedCrossRefGoogle Scholar
  21. Cox, G. J., Parker, M. D., and Babiuk, L. A., 1991, Bovine coronavirus nonstructural protein ns2 is a phosphoprotein, Virology 185:509.PubMedCrossRefGoogle Scholar
  22. De Groot, R. J., Luytjes, W., Horzinek, M. C., Van der Zeijst, B. A. M., Spaan, W. J., and Lenstra, J. A., 1987, Evidence for a coiled-coil structure in the spike proteins of coronaviruses, J. Mol. Biol. 196:963.PubMedCrossRefGoogle Scholar
  23. De Groot, R. J., Andeweg, A. C., Horzinek, M. C., and Spaan, W. J. M., 1988, Sequence analysis of the 3’ end of the feline coronavirus FIPV 79–1146 genome: Comparison with the genome of porcine coronavirus TGEV reveals large insertions, Virology 167:370.PubMedCrossRefGoogle Scholar
  24. Denison, M. R., and Perlman, S., 1986, Translation and processing of mouse hepatitis virus virion RNA in a cell-free system, J. Virol. 60:12.PubMedGoogle Scholar
  25. Denison, M. R., and Perlman, S., 1987, Identification of putative polymerase gene product in cells infected with murine coronavirus A59, Virology 157:565.PubMedCrossRefGoogle Scholar
  26. Denison, M. R., Zoltick, P. W., Leibowitz, J. L., Pachuk, C. J., and Weiss, S. R., 1991, Identification of polypeptides encoded in open reading frame-lb of the putative polymerase gene of the murine coronavirus mouse hepatitis virus-A59, J. Virol. 65:3076.PubMedGoogle Scholar
  27. Denison, M. R., Zoltick, P. W., Hughes, S. A., Giangreco, B., Olson, A. L., Perlman, S., Leibowitz, J. L., and Weiss, S. R., 1992, Intracellular processing of the N-terminal ORF la proteins of the coronavirus MHV-A59 requires multiple proteolytic events, Virology 189:274.PubMedCrossRefGoogle Scholar
  28. Duarte, M., Tobler, K., Bridgen, A., Rasschaert, D., Ackermann, M., and Laude, H., 1994, Sequence analysis of the porcine epidemic diarrhea virus genome between the nucleocapsid and spike protein genes reveals a polymorphic ORF, Virology 198:466.PubMedCrossRefGoogle Scholar
  29. Ebner, D., Raabe, T., and Siddell, S. G., 1988, Identification of the coronavirus MHV-JHM mRNA 4 product, J. Gen. Virol. 69:1041.PubMedCrossRefGoogle Scholar
  30. Garwes, D. J., Stewart, F., and Britton, P., 1989, The polypeptide of Mr 14,000 of porcine transmissible gastroenteritis virus: Gene assignment and intracellular location, J. Gen. Virol. 70:2495.PubMedCrossRefGoogle Scholar
  31. Godet, M., L’Haridon, R., Vautherot, J. F., and Laude, H., 1992, TGEV corona virus ORF4 encodes a membrane protein that is incorporated into virions, Virology 188:666.PubMedCrossRefGoogle Scholar
  32. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M., 1989, coronavirus genome: Prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis, Nucleic Acids Res. 17:4847.PubMedCrossRefGoogle Scholar
  33. Gorbalenya, A. E., Koonin, E. V., and Lai, M. M., 1991, Putative papain-related thiol proteases of positive-strand RNA viruses. Identification of rubi- and aphthovirus proteases and delineation of a novel conserved domain associated with proteases of rubi-, alpha- and coronaviruses, FEBS Lett. 288:201.PubMedCrossRefGoogle Scholar
  34. Herold, J., Raabe, T., Schelle-Prinz, B., and Siddell, S. G., 1993, Nucleotide sequence of the human coronavirus 229E RNA polymerase locus, Virology 195:680.PubMedCrossRefGoogle Scholar
  35. Hofmann, M. A., Senanayake, S. D., and Brian, D. A., 1993, A translation-attenuating intraleader open reading frame is selected on coronavirus messenger RNAs during persistent infection, Proc. Natl. Acad. Sci. USA 90:11733.Google Scholar
  36. Holmes, K. V., 1991, Coronaviridae and their replication, in: Fundamental Virology (B. N. Fields and D. M. Knipe, eds.), pp. 471–488, Raven Press, New York.Google Scholar
  37. Hornberger, F. R., 1994, Nucleotide sequence comparison of the membrane protein genes of three enterotropic strains of mouse hepatitis virus, Virus Res. 31:49.CrossRefGoogle Scholar
  38. Horsburgh, B. C., Brierley, I., and Brown, T. D., 1992, Analysis of a 9.6 kb sequence from the 3’ end of canine coronavirus genomic RNA, J. Gen. Virol. 73:2849.PubMedCrossRefGoogle Scholar
  39. Kamahora, T., Soe, L. H., and Lai, M. M. C., 1989, Sequence analysis of nucleocapsid gene and leader RNA of human coronavirus OC43, Virus Res. 12:1.PubMedCrossRefGoogle Scholar
  40. Kapke, P. A., and Brian, D. A., 1986, Sequence analysis of the porcine transmissible gastroenteritis coronavirus nucleocapsid protein gene, Virology 151:41.PubMedCrossRefGoogle Scholar
  41. Kapke, P. A., Tung, F. Y. T., Hogue, B. G., Brian, D. A., Woods, R. D., and Wesley, R., 1988, The amino-terminal signal peptide on the porcine transmissible gastroenteritis coronavirus matrix protein is not an absolute requirement for membrane translocation and glycosylation, Virology 165:367.PubMedCrossRefGoogle Scholar
  42. Kienzle, T. E., Abraham, S., Hogue, B. G., and Brian, D. A., 1990, Structure and orientation of expressed bovine coronavirus hemagglutinin-esterase protein, J. Virol. 64:1834.PubMedGoogle Scholar
  43. Kozak, M., 1987, An analysis of 5’-noncoding sequences from 699 vertebrate messenger RNAs, Nucleic Acids Res. 15:8125.PubMedCrossRefGoogle Scholar
  44. Kozak, M., 1989, The scanning model for translation: An update, J. Cell Biol. 108:229.PubMedCrossRefGoogle Scholar
  45. Kunita, S., Mori, M., and Terada, E., 1993, Sequence analysis of the nucleocapsid protein gene of rat coronavirus SDAV-681, Virology 193:520.PubMedCrossRefGoogle Scholar
  46. Lai, M. M.C., 1990, coronavirus—organization, replication and expression of genome, Annu. Rev. Microbiol. 44:303.PubMedCrossRefGoogle Scholar
  47. La Monica, N., Banner, L. R., Morris, V. L., and Lai, M. M., 1991, Localization of extensive deletions in the structural genes of two neurotropic variants of murine coronavirus JHM, Virology 182:883.PubMedCrossRefGoogle Scholar
  48. Lapps, W., Hogue, B. G., and Brian, D. A., 1987, Sequence analysis of the bovine coronavirus nucleocapsid and matrix protein genes, Virology 157:47.PubMedCrossRefGoogle Scholar
  49. Le, S-Y., Sonenberg, N., and Maizel, J. V., Jr., 1994, Distinct structural elements and internal entry of ribosomes in mRNA3 encoded by infectious bronchitis virus, Virology 198:405.PubMedCrossRefGoogle Scholar
  50. Lee, H. J., Shieh, C. K., Gorbalenya, A. E., Koonin, E. V., Lamonica, N., Tuler, J., Bagdzhadzhyan, A., and Lai, M. M. C., 1991, The complete sequence (22 kilobases) of murine coronavirus gene-1 encoding the putative proteases and RNA polymerase, Virology 180:567.PubMedCrossRefGoogle Scholar
  51. Leibowitz, J. L., Weiss, S. R., Paavola, E., and Bond, C. W., 1982, Cell-free translation of murine coronavirus RNA, J. Virol. 43:905.PubMedGoogle Scholar
  52. Leibowitz, J. L., Perlman, S., Weinstock, G. M., De Vries, J. R., Budzilowicz, C. J., Weissemann, J. M., and Weiss, S. R., 1988, Detection of a murine coronavirus nonstructural protein encoded in a downstream open reading frame, Virology 164:156.PubMedCrossRefGoogle Scholar
  53. Liu, D. X., and Inglis, S. C., 1991, Association of the infectious bronchitis virus 3c protein with the virion envelope, Virology 185:911.PubMedCrossRefGoogle Scholar
  54. Liu, D. X., and Inglis, S. C., 1992a, Identification of two new polypeptides encoded by mRNA5 of the coronavirus infectious bronchitis virus, Virology 186:342.PubMedCrossRefGoogle Scholar
  55. Liu, D. X., and Inglis, S. C., 1992b, Internal entry of ribosomes on a tricistronic mRNA encoded by infectious bronchitis virus [published erratum appears in J. Virol. 1992 66(11):6840], J. Virol. 66:6143.PubMedGoogle Scholar
  56. Liu, D. X., Cavanagh, D., Green, P., and Inglis, S. C., 1991, A polycistronic mRNA specified by the coronavirus infectious bronchitis virus, Virology 184:531.PubMedCrossRefGoogle Scholar
  57. Luytjes, W., Sturman, L. S., Bredenbeek, P. J., Charite, J., Van der Zeijst, B. A. M., Horzinek, M. C., and Spaan, W. J., 1987, Primary structure of the glycoprotein E2 of coronavirus MHV-A59 and identification of the trypsin cleavage site, Virology 161:479.PubMedCrossRefGoogle Scholar
  58. Luytjes, W., Bredenbeek, P. J., Noten, A. F. H., Horzinek, M. C., and Spaan, W. J. M., 1988, Sequence of mouse hepatitis virus A59 mRNA2: Indications for RNA-recombination between coronaviruses and influenza C virus, Virology 166:415.PubMedCrossRefGoogle Scholar
  59. Mounir, S., and Talbot, P. J., 1993, Human coronavirus OC43 RNA 4 lacks two open reading frames located downstream of the S gene of bovine coronavirus, Virology 192:355.PubMedCrossRefGoogle Scholar
  60. Page, K. W., Mawditt, K. L., and Britton, P., 1991, Sequence comparison of the 5’ end of messenger RNA 3 from transmissible gastroenteritis virus and porcine respiratory coronavirus, J. Gen. Virol. 72:579.PubMedCrossRefGoogle Scholar
  61. Parker, M. M., and Masters, P. S, 1990, Sequence comparison of the N genes of five strains of the coronavirus mouse hepatitis virus suggests a three domain structure for the nucleocapsid protein, Virology 179:463.PubMedCrossRefGoogle Scholar
  62. Parker, M. D., Cox, G. J., Deregt, D., Fitzpatrick, D. R., and Babiuk, L. A., 1989a, Cloning and in vitro expression of the gene for the E3 haemagglutinin glycoprotein of bovine coronavirus, J. Gen. Virol. 70:155.PubMedCrossRefGoogle Scholar
  63. Parker, S. E., Gallagher, T. M., and Buchmeier, M. J., 1989b, Sequence analysis reveals extensive polymorphism and evidence of deletions within the E2 glycoprotein gene of several strains of murine hepatitis virus, Virology 173:664.PubMedCrossRefGoogle Scholar
  64. Raabe, T., and Siddell, S., 1989, Nucleotide sequence of the human coronavirus HCV 229E mRNA 4 and mRNA 5 unique regions, Nucleic Acids Res. 17:6387.PubMedCrossRefGoogle Scholar
  65. Raabe, T., Schelleprinz, B., and Siddell, S. G., 1990, Nucleotide sequence of the gene encoding the spike glycoprotein of human coronavirus HCV-229E, J. Gen. Virol. 71:1065.PubMedCrossRefGoogle Scholar
  66. Rasschaert, D., Gelfi, J., and Laude, H., 1987, Enteric coronavirus TGEV: Partial sequence of the genomic RNA, its organization and expression, Biochimie 69:591.PubMedCrossRefGoogle Scholar
  67. Rasschaert, D., Duarte, M., and Laude, H., 1990, Porcine respiratory coronavirus differs from transmissible gastroenteritis virus by a few genomic deletions, J. Gen. Virol. 71:2599.PubMedCrossRefGoogle Scholar
  68. Rottier, P. J. M., Spaan, W. J. M., Horzinek, M. C., and van der Zeijst, B. A. M., 1981, Translation of three mouse hepatitis virus strain A59 subgenomic RNAs in Xenopus laevis oocytes, J. Virol. 38:20.PubMedGoogle Scholar
  69. Schaad, M. C., and Baric, R. S., 1993, Evidence for new transcriptional units encoded at the 3’ end of the mouse hepatitis virus genome, Virology 196:190.PubMedCrossRefGoogle Scholar
  70. Schmidt, I., Skinner, M., and Siddell, S., 1987, Nucleotide sequence of the gene encoding the surface projection glycoprotein of coronavirus MHV-JHM, J. Gen. Virol. 68:47.PubMedCrossRefGoogle Scholar
  71. Schreiber, S. S., Kamahora, T., and Lai, M. M. C., 1989, Sequence analysis of the nucleocapsid protein gene of human coronavirus 229E, Virology 169:142.PubMedCrossRefGoogle Scholar
  72. Schwarz, B., Routledge, E., and Siddell, S. G., 1990, Murine coronavirus nonstructural protein NS2 is not essential for virus replication in transformed cells, J. Virol. 64:4784.PubMedGoogle Scholar
  73. Senanayake, S. D., Hofmann, M. A., Maki, J. L., and Brian, D. A., 1992, The nucleocapsid protein gene of bovine coronavirus is bicistronic, J. Virol. 66:5277.PubMedGoogle Scholar
  74. Shieh, C. K., Lee, H. J., Yokomori, K., La Monica, N., Makino, S., and Lai, M. M., 1989, Identification of a new transcriptional initiation site and the corresponding functional gene 2b in the murine coronavirus RNA genome, J. Virol. 63:3729.PubMedGoogle Scholar
  75. Siddell, S., 1983, Coronavirus JHM: Coding assignments of subgenomic mRNAs, J. Gen. Virol. 64:113.PubMedCrossRefGoogle Scholar
  76. Smith, A. R., Boursnell, M. E. G., Binns, M. M., Brown, T. D. K., and Inglis, S. C., 1990, Identification of a new membrane-associated polypeptide specified by the coronavirus infectious bronchitis virus, J. Gen. Virol. 71:3.PubMedCrossRefGoogle Scholar
  77. Soe, L. H., Shieh, C. K., Baker, S. C., Chang, M. F., and Lai, M. M., 1987, Sequence and translation of the murine coronavirus 5’-end genomic RNA reveals the N-terminal structure of the putative RNA polymerase, J. Virol. 61:3968.PubMedGoogle Scholar
  78. Spaan, W., Cavanagh, D., and Horzinek, M. C., 1988, coronaviruses: Structure and genome expression, J. Gen. Virol. 69:2939.PubMedCrossRefGoogle Scholar
  79. Taguchi, F., Ikeda, T., Makino, S., and Yoshikura, H., 1994, A murine coronavirus MHV-S isolate from persistently infected cells has a leader and two consensus sequences between the M and N genes, Virology 198:355.CrossRefGoogle Scholar
  80. Tahara, S. M., Dietlin, T. A., Bergmann, C. C., Nelson, G. W., Kyuwa, S., Anthony, R. P., and Stohlman, S. A., 1994, coronavirus translational regulation: Leader affects mRNA efficiency, Virology 202:621.PubMedCrossRefGoogle Scholar
  81. Thiel, V., and Siddell, S. G., 1994, An internal ribosome entry site in the coding region of murine hepatitis virus mRNA 5, J. Gen. Virol. 75:3041.PubMedCrossRefGoogle Scholar
  82. Tung, F. Y. T., Abraham, S., Sethna, M., Hung, S.-L., Sethna, P., Hogue, B., and Brian, D. A., 1992, The 9-kDa hydrophobic protein encoded at the 3’ end of the porcine transmissible gastroenteritis virus genome is membrane-associated, Virology 186:676.PubMedCrossRefGoogle Scholar
  83. Vennema, H., 1991, The Proteins of Feline Infectious Peritonitis coronavirus: Their Biosynthesis and Involvement in Pathogenesis, thesis, State University of Utrecht.Google Scholar
  84. Vennema, H., Heijnen, L., Rottier, P. J., Horzinek, M. C., and Spaan, W. J., 1992a, A novel glycoprotein of feline infectious peritonitis coronavirus contains a KDEL-like endoplasmic reticulum retention signal, J. Virol. 66:4951.PubMedGoogle Scholar
  85. Vennema, H., Rossen, J. W., Wesseling, J., Horzinek, M. C., and Rottier, P. J., 1992b, Genomic organization and expression of the 3’ end of the canine and feline enteric coronaviruses, Virology 191:134.PubMedCrossRefGoogle Scholar
  86. Verbeek, A., and Tijssen, P., 1991, Sequence analysis of the turkey enteric coronavirus nucleocapsid and membrane protein genes: A close genomic relationship with bovine coronavirus, J. Gen. Virol. 72:1659.PubMedCrossRefGoogle Scholar
  87. Vlasak, R., Luytjes, W., Leider, J., Spaan, W., and Palese, P., 1988a, The E3 protein of bovine coronavirus is a receptor-destroying enzyme with acetylesterase activity, J. Virol. 62:4686.PubMedGoogle Scholar
  88. Vlasak, R., Luytjes, W., Spaan, W., and Palese, P., 1988b, Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses, Proc. Natl. Acad. Sci. USA 85: 4526.PubMedCrossRefGoogle Scholar
  89. Weiss, S. R., Zoltick, P. W., and Leibowitz, J. L., 1993, The ns 4 gene of mouse hepatitis virus (MHV), strain A 59 contains two ORFs and thus differs from ns 4 of the JHM and S strains, Arch. Virol. 129:301.PubMedCrossRefGoogle Scholar
  90. Weiss, S. R., Hughes, S. A., Bonilla, P. J., Turner, J. D., Leibowitz, J. L., and Denison, M.R 1994, coronavirus polyprotein processing, Arch. Virol. Suppl. 9:349.PubMedGoogle Scholar
  91. Wesley, R. D., Cheung, A. K., Michael, D. D., and Woods, R. D., 1989, Nucleotide sequence of coronavirus TGEV genomic RNA: Evidence for 3 mRNA species between the peplomer and matrix protein genes, Virus Res. 13:87.PubMedCrossRefGoogle Scholar
  92. Wesley, R. D., Woods, R. D., and Cheung, A. K., 1990, Genetic basis for the pathogenesis of transmissible gastroenteritis virus, J. Virol. 64:4761.PubMedGoogle Scholar
  93. Wesley, R. D., Woods, R. D., and Cheung, A. K., 1991, Genetic analysis of porcine respiratory coronavirus, an attenuated variant of transmissible gastroenteritis virus, J. Virol. 65:3369.PubMedGoogle Scholar
  94. Woloszyn, N., Boireau, P., and Laporte, J., 1990, Nucleotide sequence of the bovine enteric coronavirus BECV F15 mRNA5 and mRNA 6 unique regions, Nucleic Acids Res. 18:1303.PubMedCrossRefGoogle Scholar
  95. Yokomori, K., and Lai, M. M., 1991, Mouse hepatitis virus S RNA sequence reveals that nonstructural proteins ns4 and ns5a are not essential for murine coronavirus replication, J. Virol. 65:5605.PubMedGoogle Scholar
  96. Yokomori, K., Banner, L. R., and Lai, M. M. C., 1991, Heterogeneity of gene expression of the hemagglutinin-esterase (HE) protein of murine coronaviruses, Virology 183:647.PubMedCrossRefGoogle Scholar
  97. Yokomori, K., Stohlman, S. A., and Lai, M. M., 1993, The detection and characterization of multiple hemagglutinin-esterase (HE)-defective viruses in the mouse brain during subacute demyelina-tion induced by mouse hepatitis virus, Virology 192:170.PubMedCrossRefGoogle Scholar
  98. Yu, X., Bi, W., Weiss, S. R., and Leibowitz, J. L., 1994, Mouse hepatitis virus gene 5b protein is a new virion envelope protein, Virology 202:1018.PubMedCrossRefGoogle Scholar
  99. Zhang, X. M., Kousoulas, K. G., and Storz, J., 1991a, Comparison of the nucleotide and deduced amino acid sequences of the S-genes specified by virulent and avirulent strains of bovine coronaviruses, Virology 183:397.PubMedCrossRefGoogle Scholar
  100. Zhang, X. M., Kousoulas, K. G., and Storz, J., 1991b, The hemagglutinin/esterase glycoprotein of bovine coronaviruses: Sequence and functional comparisons between virulent and avirulent strains, Virology 185:847.PubMedCrossRefGoogle Scholar
  101. Zhang, X., Kousoulas, K. G., and Storz, J., 1992, The hemagglutinin/esterase gene of human coronavirus strain OC43: Phylogenetic relationships to bovine and murine coronaviruses and influenza C virus, Virology 186:318.PubMedCrossRefGoogle Scholar
  102. Zoltick, R W., Leibowitz, J. L., Oleszak, E. L., and Weiss, S. R., 1990, Mouse hepatitis virus ORF-2A is expressed in the cytosol of infected mouse fibroblasts, Virology 174:605.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Willem Luytjes
    • 1
  1. 1.Department of Virology, Institute of Medical MicrobiologyLeiden UniversityLeidenThe Netherlands

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