Completion of the Tula hantavirus genome sequence: properties of the L segment and heterogeneity found in the 3' termini of S and L genome RNAs Free

Abstract

In this study the L segment and the 5′ and termini of the S, M and L segments of the prototype Tula hantavirus (TUL) were sequenced, thus completing the first determination of the genome sequence of a hantavirus that has not been linked to any human disease. The TUL L segment comprises 6541 nt with one ORF of 6459 nt in the antigenome sense. This ORF potentially encodes a 2153 aa protein with a predicted molecular mass of 247 kDa. The amino acid sequence includes all the motifs conserved in RNA-dependent RNA polymerases. The 5′ termini of all three genome RNAs (vRNAs) had the expected sequences conserved in hantaviruses. The 3′ termini of M vRNAs were also conserved. However, the 3′ termini of S and L vRNAs were heterogeneous as most of the sequenced 3′ termini had either deletions of 1 to 22 nt or an extra 1 to 3 nt. No increase in the level of heterogeneity was seen in vRNAs of virions collected 3, 6, 9 and 12 days postinfection, suggesting that the heterogeneity already exists at the early stages of infection. The S and L vRNAs from infected cells had more truncated 3′ termini than vRNAs from pelleted virus. Heterogeneity of the 3′ termini of genome RNAs could decrease the efficiency of antigenome and mRNA syntheses and contribute to the slow growth observed for TUL and other hantaviruses in cell culture.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-79-11-2615
1998-11-01
2024-03-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/79/11/9820136.html?itemId=/content/journal/jgv/10.1099/0022-1317-79-11-2615&mimeType=html&fmt=ahah

References

  1. Antic D., Lim B. U., Kang C. Y. 1991; Nucleotide sequence and coding capacity of the large (L) genomic RNA segment of Seoul 80-39 virus, a member of the hantavirus genus. Virus Research 19:59–66
    [Google Scholar]
  2. Arikawa J., Lapenotiere H. F., lacono-Connors L., Wang M. G., Schmaljohn C. S. 1990; Coding properties of the S and the M genome segments of Sapporo rat virus: comparison to other causative agents of hemorrhagic fever with renal syndrome. Virology 176:114–125
    [Google Scholar]
  3. Bowen M. D., Kariwa H., Rollin P. E., Peters C. J., Nichol S. T. 1995; Genetic characterization of a human isolate of Puumala hantavirus from France. Virus Research 38:279–289
    [Google Scholar]
  4. Bridgen A., Elliott R. M. 1996; Rescue of a segmented negativestrand RNA virus entirely from cloned complementary DNAs. Proceedings of the National Academy of Sciences, USA 93:15400–15404
    [Google Scholar]
  5. Chizhikov V. E., Spiropoulou C. F., Morzunov S. P., Monroe M. C., Peters C. J., Nichol S. T. 1995; Complete genetic characterization and analysis of isolation of Sin Nombre virus. Journal of Virology 69:8132–8136
    [Google Scholar]
  6. Chomczynski P., Sacchi N. 1987; Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Annals of Biochemistry 162:156–159
    [Google Scholar]
  7. Dunn E. F., Jin H., Elliott R. M. 1995; Transcription of a recombinant bunyavirus RNA template by transiently expressed bunyavirus proteins. Virology 211:133–143
    [Google Scholar]
  8. Felsenstein J. 1993; PHYLIP (Phylogeny Inference Package).
    [Google Scholar]
  9. Fodor E., Pritlove D. C., Brownlee G. G. 1994; The influenza virus panhandle is involved in the initiation of transcription. Journal of Virology 68:4092–4096
    [Google Scholar]
  10. Fodor E., Pritlove D. C., Brownlee G. G. 1995; Characterization of the RNA-fork model of the virion RNA in the initiation of transcription in influenza A virus. Journal of Virology 69:4012–4019
    [Google Scholar]
  11. Garcin D., Lezzi M., Dobbs M., Elliott R. M., Schmaljohn C., Kang C. Y., Kolakofsky D. 1995; The 5ʹ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. Journal of Virology 69:5754–5762
    [Google Scholar]
  12. Giebel L. B., Stohwasser R., Zoeller L., Bautz E. K., Darai G. 1989; Determination of the coding capacity of the M genome segment of nephropathia epidemica virus strain Haellnaes B1 by molecular cloning and nucleotide sequence analysis. Virology 172:498–505
    [Google Scholar]
  13. Hutchinson K. L., Peters C. J., Nichol S. T. 1996; Sin Nombre virus mRNA synthesis. Virology 224:139–149
    [Google Scholar]
  14. Leahy M. B., Dessens J. T., Nuttall P. A. 1997; Striking conformational similarities between the transcription promoters of Thogoto and influenza A viruses: evidence for intrastrand base pairing in the 5ʹ promoter arm. Journal of Virology 71:8352–8356
    [Google Scholar]
  15. Lee Y. S., Seong B. L. 1996; Mutational analysis of influenza B virus RNA transcription in vitro. Journal of Virology 70:1232–1236
    [Google Scholar]
  16. Meyer B. J., Schmaljohn C. 1997; Molecular analysis of hantavirus persistent infections suggests that terminally deleted L RNAs have a causal role in persistence. >Abstracts of the 10th International Conference on Negative Strand Viruses Dublin, Ireland: p 166
    [Google Scholar]
  17. Morzunov S. P., Rowe J. E., Ksiazek T. G., Peters C. J., St Jeor S. C., Nichol S. T. 1998; Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. Journal of Virology 72:57–64
    [Google Scholar]
  18. Müller R., Poch O., Delarue M., Bishop D. H. L., Bouloy M. 1994; Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. Journal of General Virology 75:1345–1352
    [Google Scholar]
  19. Parrington M. A., Kang C. Y. 1990; Nucleotide sequence analysis of the S genomic segment of Prospect Hill virus : comparison with the prototype hantavirus. Virology 175:167–175
    [Google Scholar]
  20. Piiparinen H., Vapalahti O., Plyusnin A., Vaheri A., Lankinen H. 1997; Sequence analysis of the Puumala hantavirus Sotkamo strain L segment. Virus Research 51:1–7
    [Google Scholar]
  21. Plyusnin A., Vapalahti O., Lankinen H., Lehväslaiho H., Apekina N., Myasnikov Y., Kallio-Kokko H., Henttonen H., Lundkvist Å., Brummer-Korvenkontio M., Gavrilovskaya I., Vaheri A. 1994; Tula virus: a newly detected hantavirus carried by European common voles. Journal of Virology 68:7833–7839
    [Google Scholar]
  22. Plyusnin A., Cheng Y., Vapalahti O., Pejcoch M., Unar J., Jelinkova Z., Lehväslaiho H., Lundkvist A., Vaheri A. 1995; Genetic variation in Tula hantaviruses: sequence analysis of the S and M segments of strains from central Europe. Virus Research 39:237–250
    [Google Scholar]
  23. Plyusnin A., Cheng Y., Lehväslaiho H., Vaheri A. 1996a; Unique and conserved features of Tula hantavirus M gene encoding envelope glycoproteins Gl and G2. Virus Genes 12:257–263
    [Google Scholar]
  24. Plyusnin A., Vapalahti O., Vaheri A. 1996b; Hantaviruses: genome structure, expression and evolution. Journal of General Virology 77:2677–2687
    [Google Scholar]
  25. 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]
  26. Prehaud C., Lopez N., Blok M. J., Obry V., Bouloy M. 1997; Analysis of the 3ʹ terminal sequence recognized by the Rift Valley fever virus transcription complex in its ambisense S segment. Virology 227:189–197
    [Google Scholar]
  27. Ravkov E. V., Rollin P. E., Ksiazek T. G., Peters C. J., Nichol S. T. 1995; Genetic and serologic analysis of the Black Creek Canal virus and its association with human disease and Sigmodon hispidus infection. Virology 210:482–489
    [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74:5463–5467
    [Google Scholar]
  29. Schmaljohn C. S. 1990; Nucleotide sequence of the L genome segment of Hantaan virus. Nucleic Acids Research 18:6728
    [Google Scholar]
  30. Schmaljohn C. S. 1996; Molecular biology of hantaviruses. In The Bunyaviridae pp 63–90 Elliott R. M. Edited by New York & London: Plenum Press;
    [Google Scholar]
  31. Schmaljohn C. S., Hjelle B. 1997; Hantaviruses : a global disease problem. Emerging Infectious Diseases 3:95–104
    [Google Scholar]
  32. Schmaljohn C. S., Jennings G. B., Hay J., Dalrymple J. M. 1986; Coding strategy of the S genome segment of Hantaan virus. Virology 155:633–643
    [Google Scholar]
  33. Schmaljohn C. S., Schmaljohn A. L., Dalrymple J. M. 1987; Hantaan virus M RNA: coding strategy, nucleotide sequence, and gene order. Virology 157:31–39
    [Google Scholar]
  34. Spiropoulou C. F., Morzunov S., Feldmann H., Sanchez A., Peters C. J., Nichol S. T. 1994; Genome structure and variability of a virus causing hantavirus pulmonary syndrome. Virology 200:715–723
    [Google Scholar]
  35. Stohwasser R., Giebel L. B., Zoeller L., Bautz E. K., Darai G. 1990; Molecular characterization of the RNA S segment of nephro- pathia epidemica virus strain Haellnaes Bl. Virology 174:79–86
    [Google Scholar]
  36. Stohwasser R., Raab K., Darai G., Bautz E. K. F. 1991; Primary structure of the large (L) RNA segment of nephropathia epidemica virus strain Hallnas Bl coding for the viral RNA polymerase. Virology 183:386–391
    [Google Scholar]
  37. Vapalahti O. P., Kallio-Kokko H., Salonen E.-M., Brummer-Korvenkontio M., Vaheri A. 1992; Cloning and sequencing of Puumala virus Sotkamo strain S and M RNA segments : evidence for strain variation in hantaviruses and expression of the nucleocapsid protein. Journal of General Virology 73:829–838
    [Google Scholar]
  38. Vapalahti O., Lundkvist Å., Kukkonen S. K. J., Cheng Y., Gilljam M., Kanerva M., Manni T., Pejcoch M., Niemimaa J., Kaikusalo A., Henttonen H., Vaheri A., Plyusnin A. 1996; Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae . Journal of General Virology 77:3063–3067
    [Google Scholar]
  39. Yoo D. W., Kang C. Y. 1987; Nucleotide sequence of the M segment of the genomic RNA of Hantaan virus 76-118. Nucleic Acids Research 15:6299–6300
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-79-11-2615
Loading
/content/journal/jgv/10.1099/0022-1317-79-11-2615
Loading

Data & Media loading...

Most cited Most Cited RSS feed