1887

Abstract

Tamana bat virus (TABV, isolated from the bat ) is currently classified as a tentative species in the genus . We report here the determination and analysis of its complete coding sequence. Low but significant similarity scores between TABV and member-viruses of the genus were identified in the amino acid sequences of the structural, NS3 and NS5 genes. A series of cysteines located in the envelope protein and the most important enzymatic domains of the virus helicase/NTPase, methyltransferase and RNA-dependent RNA polymerase were found to be highly conserved. In the serine-protease domain, the catalytic sites were conserved, but variations in sequence were found in the putative substrate-binding sites, implying possible differences in the protease specificity. In accordance with this finding, the putative cleavage sites of the TABV polyprotein by the virus protease are substantially different from those of flaviviruses. The phylogenetic position of TABV could not be determined precisely, probably due to the extremely significant genetic divergence from other member-viruses of the family . However, analysis based on both genetic distances and maximum-likelihood confirmed that TABV is more closely related to the flaviviruses than to the other genera. These findings have implications for the evolutionary history and taxonomic classification of the family as a whole: (i) the possibility that flaviviruses were derived from viruses infecting mammals rather than from mosquito viruses cannot be excluded; (ii) using the current criteria for the definition of genera in the family , TABV should be assigned to a new genus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-10-2443
2002-10-01
2024-11-13
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/10/0832443a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-10-2443&mimeType=html&fmt=ahah

References

  1. Arias C. F., Preugschat F., Strauss J. H. 1993; Dengue 2 virus NS2B and NS3 form a stable complex that can cleave NS3 within the helicase domain. Virology 193:888–899
    [Google Scholar]
  2. Bazan J. F., Fletterick R. J. 1989; Detection of a trypsin-like serine protease domain in flaviviruses and pestiviruses. Virology 171:637–639
    [Google Scholar]
  3. Bellgard M. I., Gojobori T. 1999; Significant differences between the G+C content of synonymous codons in orthologous genes and the genomic G+C content. Gene 238:33–37
    [Google Scholar]
  4. Billoir F., de Chesse R., Tolou H., de Micco P., Gould E. A., de Lamballerie X. 2000; Phylogeny of the genus Flavivirus using complete coding sequences of arthropod-borne viruses and viruses with no known vector. Journal of General Virology 81:781–790
    [Google Scholar]
  5. Bousalem M., Douzery E. J. P., Fargette D. 2000; High genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of Yam mosaic virus : a contribution to understanding potyvirus evolution. Journal of General Virology 81:243–255
    [Google Scholar]
  6. Cammisa-Parks H., Cisar L. A., Kane A., Stollar V. 1992; The complete nucleotide sequence of cell fusing agent (CFA): homology between the nonstructural proteins encoded by CFA and the nonstructural proteins encoded by arthropod-borne flaviviruses. Virology 189:511–524
    [Google Scholar]
  7. Chambers T. J., Weir R. C., Grakoui A., McCourt D. W., Bazan J. F., Fletterick R. J., Rice C. M. 1990; Evidence that the N-terminal domain of nonstructural protein NS3 from yellow fever virus is a serine protease responsible for site-specific cleavages in the viral polyprotein. Proceedings of the National Academy of Sciences, USA 87:8898–8902
    [Google Scholar]
  8. Falgout B., Pethel M., Zhang Y. M., Lai C. J. 1991; Both nonstructural proteins NS2B and NS3 are required for the proteolytic processing of dengue virus nonstructural proteins. Journal of Virology 65:2467–2475
    [Google Scholar]
  9. Forwood J. K., Brooks A., Briggs L. J., Xiao C. Y., Jans D. A., Vasudevan S. G. 1999; The 37-amino-acid interdomain of dengue virus NS5 protein contains a functional NLS and inhibitory CK2 site. Biochemical and Biophysical Research Communications 257:731–737
    [Google Scholar]
  10. Frolova T. V., Pogodina V. V., Frolova M. P., Karmysheva V. I. 1982; Characteristics of long-term persisting strains of tick-borne encephalitis virus in different forms of the chronic process in animals. Voprosy Virusologii 27:473–479 (in Russian
    [Google Scholar]
  11. Frolova T. V., Frolova M. P., Pogodona V. V., Sobolev S. G., Karmysheva V. I. 1987; Pathogenesis of persistent and chronic forms of tick-borne encephalitis (experimental study). Zhurnal Nevrologii i Psikhiatrii Imeni S. S. Korsakova 87:170–178 (in Russian
    [Google Scholar]
  12. Gaunt M. W., Sall A. A., de Lamballerie X., Falconar A. K. I., Dzhivanian T. I., Gould E. A. 2001; Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. Journal of General Virology 82:1867–1876
    [Google Scholar]
  13. Goldbach R. 1992; The recombinative nature of potyviruses: implications for setting up true phylogenetic taxonomy. Archives of Virology Supplementum 5:299–304
    [Google Scholar]
  14. Gorbalenya A. E., Donchenko A. P., Koonin E. V., Blinov V. M. 1989a; N-terminal domains of putative helicases of flavi- and pestiviruses may be serine proteases. Nucleic Acids Research 17:3889–3897
    [Google Scholar]
  15. Gorbalenya A. E., Koonin E. V., Donchenko A. P., Blinov V. M. 1989b; Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Research 17:4713–4730
    [Google Scholar]
  16. Gubler D. J. 1999; Dengue viruses ( Flaviviridae ). In Encyclopedia of Virology pp 375–384 Edited by Granoff A., Webster R. G. New York: Academic Press;
    [Google Scholar]
  17. Heinz F. X., Collett M. S., Purcell R. H., Gould E. A., Howard C. R., Houghton M., Moormann R. J. M., Rice C. M., Thiel H.-J. 2000; Flaviviridae. In Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses pp 859–878 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. San Diego: Academic Press;
    [Google Scholar]
  18. Jenkins G. M., Pagel M., Gould E. A., Zanotto P. M. de A., Holmes E. C. 2001; Evolution of base composition and codon usage bias in the genus Flavivirus. Journal of Molecular Evolution 52:383–390
    [Google Scholar]
  19. Koonin E. V. 1993; Computer-assisted identification of a putative methyltransferase domain in NS5 protein of flaviviruses and λ2 protein of reovirus. Journal of General Virology 74:733–740
    [Google Scholar]
  20. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245
    [Google Scholar]
  21. Kuno G., Chang G.-J. J., Tsuchiya K. R., Karabatsos N., Cropp C. B. 1998; Phylogeny of the genus Flavivirus. Journal of Virology 72:73–83
    [Google Scholar]
  22. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157:105–132
    [Google Scholar]
  23. Lain S., Riechmann J. L., Martin M. T., Garcia J. A. 1989; Homologous potyvirus and flavivirus proteins belonging to a superfamily of helicase-like proteins. Gene 82:357–362
    [Google Scholar]
  24. Lobigs M. 1992; Proteolytic processing of a Murray Valley encephalitis virus non-structural polyprotein segment containing the viral proteinase: accumulation of a NS3–4A precursor which requires mature NS3 for efficient processing. Journal of General Virology 73:2305–2312
    [Google Scholar]
  25. Mandl C. W., Guirakhoo F., Holzmann H., Heinz F. X., Kunz C. 1989; Antigenic structure of the flavivirus envelope protein E at the molecular level, using tick-borne encephalitis virus as a model. Journal of Virology 63:564–571
    [Google Scholar]
  26. Meyers G., Thiel H.-J. 1996; Molecular characterization of pestiviruses. Advances in Virus Research 47:53–118
    [Google Scholar]
  27. Nishizawa M., Nishizawa K. 1998; Biased usages of arginines and lysines in proteins are correlated with local-scale fluctuations of the G+C content of DNA sequences. Journal of Molecular Evolution 47:385–393
    [Google Scholar]
  28. Page R. D. M. 1996; TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12:357–358
    [Google Scholar]
  29. Platt K. B., Mangiafico J. A., Rocha O. J., Zaldivar M. E., Mora J., Trueba G., Rowley W. A. 2000; Detection of dengue virus neutralizing antibodies in bats from Costa Rica and Ecuador. Journal of Medical Entomology 37:965–967
    [Google Scholar]
  30. Poch O., Sauvaget I., Delarue M., Tordo N. 1989; Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO Journal 8:3867–3874
    [Google Scholar]
  31. Porterfield J. S. 1999; Encephalitis viruses ( Flaviviridae ): encephalitis viruses and related viruses causing hemorrhagic disease. In Encyclopedia of Virology pp 424–430 Edited by Granoff A., Webster R. G. New York: Academic Press;
    [Google Scholar]
  32. Price J. L. 1978; Isolation of Rio Bravo and a hitherto undescribed agent, Tamana bat virus, from insectivorous bats in Trinidad, with serological evidence of infection in bats and man. American Journal of Tropical Medicine and Hygiene 27:153–161
    [Google Scholar]
  33. Pugachev K. V., Nomokonova N. Y., Dobrikova E. Y., Wolf Y. I. 1993; Site-directed mutagenesis of the tick-borne encephalitis virus NS3 gene reveals the putative serine protease domain of the NS3 protein. FEBS Letters 9:115–118
    [Google Scholar]
  34. Rice C. M. 1996; Flaviviridae : the viruses and their replication. In Fields Virology pp 931–959 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  35. Rice C. M., Strauss J. H. 1990; Production of flavivirus polypeptides by proteolytic processing. Seminars in Virology 1:357–367
    [Google Scholar]
  36. Roehrig J. T., Hunt A. R., Johnson A. J., Hawkes R. A. 1989; Synthetic peptides derived from the deduced amino acid sequence of the E-glycoprotein of Murray Valley encephalitis virus elicit antiviral antibody. Virology 171:49–60
    [Google Scholar]
  37. Stadler K., Allison S. L., Schalich J., Heinz F. X. 1997; Proteolytic activation of tick-borne encephalitis virus by furin. Journal of Virology 71:8475–8481
    [Google Scholar]
  38. Steffens S., Thiel H.-J., Behrens S.-E. 1999; The RNA-dependent RNA polymerases of different members of the family Flaviviridae exhibit similar properties in vitro. Journal of General Virology 80:2583–2590
    [Google Scholar]
  39. Steiner D. F., Smeekens S. P., Ohagi S., Chan S. J. 1992; The new enzymology of precursor processing endoproteases. Journal of Biological Chemistry 267:23435–23438
    [Google Scholar]
  40. Sulkin S. E., Sims R. A., Allen R. 1966; Isolation of St Louis encephalitis from bats ( Tadarida mexicana ) in Texas. Science 152:223–225
    [Google Scholar]
  41. Sulkin S. E., Allen R., Miura T., Toyokawa K. 1970; Studies of arthropod-borne virus infections in Chiroptera. VI. Isolation of Japanese B encephalitis virus from naturally infected bats. American Journal of Tropical Medicine and Hygiene 19:77–87
    [Google Scholar]
  42. Swofford D. L. 2000 PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods), version 4 Sunderland, MA: Sinauer;
    [Google Scholar]
  43. Tan B. H., Fu J., Sugrue R. J., Yap E. H., Chan Y. C., Tan Y. H. 1996; Recombinant dengue type 1 virus NS5 protein expressed in Escherichia coli exhibits RNA-dependent RNA polymerase activity. Virology 216:317–325
    [Google Scholar]
  44. Theiler M., Downs W. G. 1973 The Arthropod-borne Viruses of Vertebrates: an Account of the Rockefeller Foundation Virus Program (1951–1970 London: Yale University Press;
    [Google Scholar]
  45. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673–4680
    [Google Scholar]
  46. Tolou H. J. G., Couissinier-Paris P., Durand J.-P., Mercier V., de Pina J.-J., de Micco P., Billoir F., Charrel R. N., de Lamballerie X. 2001; Evidence for recombination in natural populations of dengue virus type 1 based on the analysis of complete genome sequences. Journal of General Virology 82:1283–1290
    [Google Scholar]
  47. Valle R. P., Falgout B. 1998; Mutagenesis of the NS3 protease of dengue virus type 2. Journal of Virology 72:624–632
    [Google Scholar]
  48. von Heijne G. 1984; How signal sequences maintain cleavage specificity. Journal of Molecular Biology 173:243–251
    [Google Scholar]
  49. Warrener P., Tamura J. K., Collett M. S. 1993; RNA-stimulated NTPase activity associated with yellow fever virus NS3 protein expressed in bacteria. Journal of Virology 67:989–996
    [Google Scholar]
  50. Wengler G., Wengler G. 1993; The NS3 nonstructural protein of flaviviruses contains an RNA triphosphatase activity. Virology 197:265–273
    [Google Scholar]
  51. Wengler G., Czaya G., Farber P. M., Hegemann J. H. 1991; In vitro synthesis of West Nile virus proteins indicates that the amino-terminal segment of the NS3 protein contains the active centre of the protease which cleaves the viral polyprotein after multiple basic amino acids. Journal of General Virology 72:851–858
    [Google Scholar]
  52. Worobey M., Holmes E. C. 2001; Homologous recombination in GB virus C/hepatitis G virus. Molecular Biology and Evolution 18:254–261
    [Google Scholar]
  53. Yang Z. 1997; paml: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in the Biosciences 13:555–556
    [Google Scholar]
  54. Zhang L., Mohan P. M., Padmanabhan R. 1992; Processing and localization of Dengue virus type 2 polyprotein precursor NS3-NS4A-NS4B-NS5. Journal of Virology 66:7549–7554
    [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-83-10-2443
Loading
/content/journal/jgv/10.1099/0022-1317-83-10-2443
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error