The Coronaviruslike Superfamily

  • Eric J. Snijder
  • Willy J. M. Spaan
Part of the The Viruses book series (VIRS)


Until recently, the Coronaviridae was classified as a monogeneric family of closely related viruses. However, in the past four years, it has become evident that similarities in the genome organization, replication strategies, and nucleotide sequences of coronaviruses, toroviruses, and arteriviruses, require a revision of this taxonomy. The “superfamily” concept (Strauss and Strauss, 1988; Goldbach and Wellink, 1988), which is based on evolution and phylogeny and which has already closed the gaps between other virus groups (e.g., the alpha-viruslike and picornaviruslike superfamilies), can now also be applied to a group of “coronaviruslike viruses.”


Infectious Bronchitis Virus Virus Group Mouse Hepatitis Virus Equine Arteritis Virus Replicase Gene 
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.


  1. Baker, S. C., Yokomori, K., Dong, S., Carlisle, R., Gorbalenya, A. E., Koonin, E. V., and Lai, M. M. C., 1993, Identification of the catalytic sites of a papain-like cysteine proteinase of murine coronavirus, J. Virol. 67:6056.PubMedGoogle Scholar
  2. Baric, R. S., Stohlman, S. A., and Lai, M. M. C., 1983, Characterization of replicative intermediate RNA of mouse hepatitis virus: Presence of leader RNA sequences on nascent chains, J. Virol. 48:633.PubMedGoogle Scholar
  3. Baric, R. S., Fu, K., Schaad, M. C., and Stohlman, S. A., 1990, Establishing a genetic recombination map for murine Coronavirus strain A59 complementation groups, Virology 177:646.PubMedCrossRefGoogle Scholar
  4. Bazan, J. F., and Fletterick, R. J., 1988, Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: Structural and functional implications, Proc. Natl. Acad. Sei. USA 85:7872.CrossRefGoogle Scholar
  5. Bazan, J. F., and Fletterick, R. J., 1990, Structural and catalytic models of trypsin-like viral proteases, Semin. Virol. 1:311.Google Scholar
  6. Boursnell, M. E. G., Brown, T. D. K., 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
  7. Bredenbeek, P. J., Pachuk, C. J., Noten, J. F. H., Charité, J., Luytjes, W., Weiss, S. R., and Spaan, W. J. M., 1990, The primary structure and expression of the second open reading frame of the polymerase gene of the Coronavirus MHV-A59, Nucleic Acids Res. 18:1825.PubMedCrossRefGoogle Scholar
  8. Brierley, I., Diggard, P., and Inglis, S., 1989, Characterization of an efficient Coronavirus ribosomal frameshifting signal: Requirement for an RNA pseudoknot, Cell 57:537.PubMedCrossRefGoogle Scholar
  9. Cavanagh, D., Brian, D. A., Brinton, M., Enjuanes, L., Holmes, K. V., Horzinek, M. C., Lai, M. M. C., Laude, H., Plagemann, P. G. W., Siddell, S., Spaan, W. J. M., Taguchi, F., and Talbot, P. J., 1994, Revision of the taxonomy of the Coronavirus, Torovirus and Arterivirus genera, Archives Virology 135:227.CrossRefGoogle Scholar
  10. Chen, Z., Kuo, L., Rowland, R. R. R., Even, C., Faaberg, K. S., and Plagemann, P. G. W., 1993, Sequence of 3′-end of genome and 5′-end of ORF la of lactate dehydrogenase-elevating virus (LDV) and common junction motifs between 5′-leader and bodies of seven subgenomic mRNAs, J. Gen. Virol. 74:643.PubMedCrossRefGoogle Scholar
  11. de Groot, R. J., Hardy, W. R., Shirako, Y., and Strauss, J. H., 1990, Cleavage-site preferences of Sindbis virus polyproteins containing the non-structural proteinase. Evidence for temporal regulation of polyprotein processing in vivo, EMBO J. 9:2631.PubMedGoogle Scholar
  12. Den Boon, J. A., Snijder, E. J., Krijnse Locker, J., Horzinek, M. C., and Rottier, P. J. M., 1991a, Another triple-spanning envelope protein among intracellularly budding RNA viruses: The torovirus E protein, Virology 182:655.CrossRefGoogle Scholar
  13. Den Boon, J. A., Snijder, E. J., Chirnside, E. D., De Vries, A. A. F., Horzinek, M. C., and Spaan, W. J. M., 1991b, Equine arteritis virus is not a togavirus but belongs to the coronavirus-like super-family, J. Virol. 65:2910.Google Scholar
  14. Den Boon, J. A., Faaberg, K. S., Meulenberg, J. J. M., Wassenaar, A. L. M., Plagemann, P. G. W., Gorbalenya, A. E., and Snijder, E. J., 1995a, Processing and evolution of the N-terminal region of the arterivirus ORFIa protein: Identification of two papainlike cysteine proteases, J. Virol, in press.Google Scholar
  15. Den Boon, J. A., Spaan, W. J. M., and Snijder, E. J., 1995b, manuscript in preparation.Google Scholar
  16. Den Boon, J. A. Kleijnen, M. F., Spaan, W. J. M., and Snijder, E. J., 1995c, manuscript in preparation.Google Scholar
  17. 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. 65:3067.Google Scholar
  18. Denison, M. R., Zoltick, P. W., Hughes, A., Giangreco, B., Olsen, A. L., Perlman, S., Leibowitz, J. L., and Weiss, S. R., 1992, Intracellular processing of the N-terminal ORFla proteins of the Coronavirus MHV-A59 requires multiple proteolytic events, Virology 189:274.PubMedCrossRefGoogle Scholar
  19. de Vries, A. A. F., Chirnside, E. D., Bredenbeek, P. J., Gravenstein, L. A., Horzinek, M. C., and Spaan, W. J. M., 1990, All subgenomic mRNAs of equine arteritis virus contain a common leader sequence, Nucleic Acids Res. 18:3241.PubMedCrossRefGoogle Scholar
  20. de Vries, A. A. F., Chirnside, E. D., Horzinek, M. C., and Rottier, P. J. M., 1992, Structural proteins of equine arteritis virus, J. Virol. 66:6294.PubMedGoogle Scholar
  21. Dolja, V. V., Karasev, A. V., and Koonin, E. V., 1994, Molecular biology and evolution of closteroviruses: Sophisticated build-up of large RNA genomes, Annu. Rev. Phytopathol. (in press).Google Scholar
  22. Doll, E. R., Bryans, J. T., McCollum, W. H. M., and Wallace, M. E., 1957, Isolation of a filterable agent causing arteritis of horses and abortion by mares. Its differentiation from the equine abortion (influenza) virus, Cornell Vet. 47:3.PubMedGoogle Scholar
  23. Dougherty, W. G., and Semler, B. L., 1993, Expression of virus-encoded proteinases: Functional and structural similarities with cellular enzymes, Microbiol. Rev. 57:781.PubMedGoogle Scholar
  24. Dubois-Dalcq, M. E., Doller, E. W., Haspel, M. V., and Holmes, K. V., 1982, Cell tropism and expression of mouse hepatitis virus (MHV) in mouse spinal chord cultures, Virology 119:317.PubMedCrossRefGoogle Scholar
  25. Godeny, E. K., Chen, L., Kumar, S. N., Methven, S. L., Koonin, E. V., and Brinton, M. A., 1993a. Complete genomic sequence and phylogenetic analysis of the lactate dehydrogenase-elevating virus, Virology 194:585.PubMedCrossRefGoogle Scholar
  26. Godeny, E. K., Zeng, L., Smith, S. L., and Brinton, M. A., 1993b, Simian haemorrhagic fever virus: Another member of the coronavirus-like superfamily, in: Abstracts of the IXth International Congress of Virology, p. 22, Glasgow, Scotland.Google Scholar
  27. Goldbach, R., and Wellink, J., 1988, Evolution of plus-strand RNA viruses, Intervirology 29:260.PubMedGoogle Scholar
  28. Gorbalenya, A. E., and Koonin, E. V., 1993, Helicases: Amino acid sequence comparisons and structure-function relationships, Curr. Opin. Struct. Biol. 3:419.CrossRefGoogle Scholar
  29. Gorbalenya, A. E., Koonin, E. V., Donchenko, A. P., and Blinov, V. M., 1989a, Coronavirus genome: Prediction of putative functional domains in the non-structural polyprotein by comparativeamino acid sequence analysis, Nucleic Acids Res. 17:4847.PubMedCrossRefGoogle Scholar
  30. Gorbalenya, A. E., Donchenko, A. P., Blinov, V. M., and Koonin, E. V., 1989b, Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: A distinct protein super-family with a common structural fold, FEBS Lett. 243:103.PubMedCrossRefGoogle Scholar
  31. Gorbalenya, A. E., Koonin, E. V., and Lai, M. M. C., 1991, Putative papain-related thiol proteases of positive-stranded RNA viruses, FEBS Lett. 288:201.PubMedCrossRefGoogle Scholar
  32. 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
  33. Holmes, K. V., Doller, E. W., and Sturman, L. S., 1981, Tunicamycin resistant glycosylation of a Coronavirus glycoprotein: Demonstration of a novel type of viral glycoprotein, Virology 115:334.PubMedCrossRefGoogle Scholar
  34. Horzinek, M. C., Maess J., and Laufs, R., 1971, Studies on the structure of togaviruses. II. Analysis of equine arteritis, rubella, bovine viral diarrhoea, and hog cholera viruses, Arch. Gesamte Virusforsch. 33:306.PubMedCrossRefGoogle Scholar
  35. Hyllseth, B., Structural proteins of equine arteritis virus, 1973, Arch. Gesamte Virusforsch. 40:177.PubMedCrossRefGoogle Scholar
  36. Jacks, T., Madhani, H. D., Masiarz, F. R., and Varmus, H. E., 1988, Signals for ribosomal frameshifting in the Rouse sarcoma virus gag-pol region, Cell 55:447.PubMedCrossRefGoogle Scholar
  37. Jacobs, L., Spaan, W. J. M., Horzinek, M. C., and van der Zeijst, B. A. M., 1981, Synthesis of subgenomic mRNAs of mouse hepatitis virus is initiated independently: evidence from UV transcription mapping, J. Virol. 39:401.PubMedGoogle Scholar
  38. Jore, J, de Geus, B., Jackson, R. J., Pouwels, P. H., and Enger-Valk, B. E., 1988, Poliovirus 3CD is the active protease for processing of the precursor protein PI in vitro, f. Gen. Virol. 69:1627.CrossRefGoogle Scholar
  39. Koonin, E. V., and Dolja, V. V., 1993, Evolution and taxonomy of positive-strand RNA viruses: Implications of comparative analysis of amino acid sequences, Crit. Rev. Biochem. Mol. Biol. 28:375.PubMedCrossRefGoogle Scholar
  40. Kuo, L. L., Harty, J. T., Erickson, L., Palmer, G. A., and Plagemann, P. G. W., 1991, A nested set of eight RNAs is formed in macrophages infected with lactate dehydrogenase-elevating virus, J. Virol 65:5118.PubMedGoogle Scholar
  41. Lai, M. M. C., 1990, Coronavirus—organization, replication and expression of genome, Arma. Rev. Microbiol. 44:303.CrossRefGoogle Scholar
  42. Lai, M. M. C., 1992, RNA recombination in animal and plant viruses, Microbiol. Rev. 56:61.PubMedGoogle Scholar
  43. Lai, M. M. C., Patton, C. D., Baric, R. S., and Stohlman, S. A., 1983, Presence of leader sequences in the mRNA of mouse hepatitis virus, J. Virol. 46:1027.PubMedGoogle Scholar
  44. Lee, H. J., Shieh, C. K., Gorbalenya, A. E., Koonin, E. V., Lamonica, N., Tuler, J., Bagdzhadzhuyan, 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
  45. Meulenberg, J. J. M., Hulst, M. M., De Meijer, E. J., Moonen, P. L. J. M., Den Besten, A., De Kluyver, E. P., Wensvoort, G., and Moormann, R. J. M., 1993a, Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV, Virology 192:62.PubMedCrossRefGoogle Scholar
  46. Meulenberg, J. J. M., De Meijer, E., and Moormann, R. J. M., 1993b, Subgenomic RNAs of Lelystad virus contain a conserved leader-body junction sequence, J. Gen. Virol. 74:1697.PubMedCrossRefGoogle Scholar
  47. Plagemann, P. G., and Moennig, V., 1992, Lactate dehydrogenase-elevating virus, equine arteritis virus and simian haemorrhagic fever virus, a new group of positive strand RNA viruses. Adv. Virus Res. 41:99.PubMedCrossRefGoogle Scholar
  48. Poch, O., Sauvaget, I., Delarue, M., and Tordo, N., 1989, Identification of four conserved motifs among the RNA dependent polymerase encoding elements, EMBO f. 8:3867.Google Scholar
  49. Rottier, P. J. M., Horzinek, M. C., and van der Zeijst, B. A. M., 1981, Viral protein synthesis in mouse hepatitis virus strain A59-infected cells: effect of tunicamycin, J. Virol. 40:350.PubMedGoogle Scholar
  50. Sawicki, S. G., and Sawicki, D. L., 1990, Subgenomic mouse hepatitis virus replicative intermediates function in RNA synthesis, J. Virol. 64:1050.PubMedGoogle Scholar
  51. Schaad, M. C., Stohlman, S. A., Egbert, J., Lum, K., Fu, K., Wei, T., and Baric, R. S., 1990, Genetics of mouse hepatitis virus transcription: Identification of cistrons which may function in positive and negative strand RNA synthesis, Virology 177:634.PubMedCrossRefGoogle Scholar
  52. Sethna, P. B., Hung, S. L., and Brian, D. A., 1989, Coronavirus subgenomic minus-strand RNAs and the potential for mRNA replicons Proc. Natl. Acad. Sci. USA 86:5626.PubMedCrossRefGoogle Scholar
  53. Shirako, Y., and Strauss, J. H., 1994, Regulation of Sindbis virus RNA replication: Uncleaved P123 and nsP4 function in minus-strand RNA synthesis, whereas cleaved products from P123 are required for efficient plus-strand synthesis, J. Virol. 68:1874.PubMedGoogle Scholar
  54. Snijder, E. J., and Horzinek, M. C., 1993, Toroviruses: Replication, evolution and comparison with other members of the coronavirus-like superfamily, J. Gen. Virol. 74:2305.PubMedCrossRefGoogle Scholar
  55. Snijder, E. J., den Boon, J. A., Bredenbeek, P. J., Horzinek, M. C., Rijnbrand, R., and Spaan, W. J. M., 1990a, The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and corona-viruses are evolutionarily related, Nucleic Acids Res. 18:4535.PubMedCrossRefGoogle Scholar
  56. Snijder, E. J., Horzinek, M. C., and Spaan, W. J. M., 1990b, A 3′-coterminal nested set of independently transcribed messenger RNAs is generated during Berne virus replication, J. Virol. 64:331.PubMedGoogle Scholar
  57. Snijder, E. J., den Boon, J. A., Horzinek, M. C., and Spaan, W. J. M., 1991, Comparison of the genome organization of toro- and coronaviruses: Both divergence from a common ancestor and RNA recombination have played a role in Berne virus evolution, Virology 180:448.PubMedCrossRefGoogle Scholar
  58. Snijder, E. J., Wassenaar, A. L. M., and Spaan, W. J. M., 1992, The 5′ end of the equine arteritis virus genome encodes a papainlike cysteine protease, J. Virol. 66:7040.PubMedGoogle Scholar
  59. Snijder, E. J., Wassenaar, A. L. M., and Spaan, W. J. M., 1994a, Proteolytic processing of the equine arteritis virus replicase ORFla protein, J. Virol. 68:5755.PubMedGoogle Scholar
  60. Snijder, E. J., Wassenaar, A. L. M., Spaan, W. J. M., and Gorbalenya, A. E., 1995, The arterivirus nsp2 protease: an unusual cysteine protease with similarities to both papainlike and chymotryp-sinlike proteases, J. Biol. Chem, in press.Google Scholar
  61. Spaan, W. J. M., Delius, H., Skinner, M., Armstrong, J., Rottier, P. J. M., Smeekens, S., van der Zeijst, B. A. M., and Siddell, S. G., 1983, Coronavirus mRNA synthesis involves fusion of noncontiguous sequences, EMBO J. 2:1839.PubMedGoogle Scholar
  62. Spaan, W. J. M., Cavanagh, D., and Horzinek, M. C., 1988, Coronaviruses: Structure and genome expression, J. Gen. Virol. 69:2939.PubMedCrossRefGoogle Scholar
  63. Strauss, J. H., and Strauss, E. G., 1988, Evolution of RNA viruses, Annu. Rev. Microbiol 42:657.PubMedCrossRefGoogle Scholar
  64. Strauss, J. H., and Strauss, E. G., 1990, Alphavirus proteinases, Semin. Virol 1:347.Google Scholar
  65. Ten Dam, E. B., Pleij, C. W. A., and Bosch, L., 1990, RNA pseudoknots; translational frameshifting and read-through on viral RNAs, Virus Genes 4:121.PubMedCrossRefGoogle Scholar
  66. Van Berlo, M. F., Horzinek, M. C., and van der Zeijst, B. A. M., 1982, Equine arteritis virus-infected cells contain six polyadenylated virus-specific RNAs, Virology 118:345.PubMedCrossRefGoogle Scholar
  67. Ypma-Wong, M. F., Dewalt, P. G., Johnson, V. H., Lamb, J. G., and Semler, B. L., 1988, Protein 3CD is the major poliovirus proteinase responsible for cleavage of the PI capsid precursor, Virology 166:165.CrossRefGoogle Scholar
  68. Zimmern, D., 1987, Evolution of RNA viruses, in RNA Genetics, vol. 2 (J. J. Holland, E. Domingo, and P. Ahlquist, eds.), pp. 211–240. Boca Raton, FL, CRC Press.Google Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Eric J. Snijder
    • 1
  • Willy J. M. Spaan
    • 1
  1. 1.Department of Virology, Institute of Medical MicrobiologyLeiden UniversityLeidenThe Netherlands

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