1887

Abstract

Influenza A and B viruses share common sequences and potentially similar panhandle structures in the terminal noncoding regions of virion RNA (vRNA). Interesting differences exist, however, in the number of conserved nucleotides at the 5′ and 3′ ends of the vRNAs, in base pairs constituting the panhandle duplex, and the length of uridine stretch (U stretch) juxtaposed to the RNA duplex. To analyse the contribution of these signals to the specificity between the two viruses, a transient ribonucleo-protein transfection method was used for the expression of the chloramphenicol acetyltransferase (CAT) reporter gene flanked by the noncoding nucleotides derived from influenza B vRNA. While the base pairing in the RNA duplex was primarily important for template activity, mismatch mutations G11 × G12′ and C12 × A13′ in the terminal RNA duplex region were utilized by influenza B virus, whereas these mutations were detrimental for influenza A virus. Different activity profiles were observed in the length preference of the RNA duplexes: maximum template activity was observed with 11 base pairs for influenza B virus, and 8 base pairs for influenza A virus. When the mutants with various lengths of U stretch were tested, highest CAT activities were observed with 5 to 7 uridine residues in influenza A virus, whereas in influenza B virus the activity was drastically decreased with 7 uridine residues. We suggest that the specific interaction of influenza virus RNA polymerase with these noncoding -acting signals in transcription of the RNA genome, along with unique coding strategies adopted by influenza B virus, has contributed to the divergence of these two closely related viruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-79-4-673
1998-04-01
2022-05-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/79/4/9568960.html?itemId=/content/journal/jgv/10.1099/0022-1317-79-4-673&mimeType=html&fmt=ahah

References

  1. Akoto E. A., Siasubramanian N., Nayak D. P. 1987; Primary structure of the polymerase acidic (PA) gene of an influenza B virus (B/SING/222/79). Virology 159:147–153
    [Google Scholar]
  2. Almond J. W., Haymerle H. A., Felsenreich V. D., Reeve P. 1979; The structural and infected cell polypeptides of influenza B virus. Journal of General Virology 45:611–621
    [Google Scholar]
  3. Barclay W. S., Palese P. 1995; Influenza B viruses with site-specific mutations introduced into the HA gene. Journal of Virology 69:1275–1279
    [Google Scholar]
  4. Bergman M., Muster T. 1996; Mutations in the noncoding sequences of the influenza A virus segments affect viral vRNA formation. Virus Research 44:23–31
    [Google Scholar]
  5. DeBorde D. C., Donabedian A. M., Herlocher M. L., Naeve C. W., Maassab H. F. 1988; Sequence comparison of wild-type and cold-adapted B/Ann Arbor/1/66 influenza virus genes. Virology 163:429–443
    [Google Scholar]
  6. Desselberger U., Racaniello V. R., Zazra J. J., Palese P. 1980; The 3′ and 5′ terminal sequences of influenza virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8:315–328
    [Google Scholar]
  7. Enami M., Palese P. 1991; High-efficiency formation of influenza virus transfectants. Journal of Virology 65:2711–2713
    [Google Scholar]
  8. Flick R., Neumann G., Hoffmann E., Neumeier E., Hobom G. 1996; Promoter elements in the influenza vRNA terminal structure. RNA 2:1046–1057
    [Google Scholar]
  9. Fodor E., Pritlove D. C., Brownlee G. G. 1995; Characterization of the RNA-fork model of virion RNA in the initiation of transcription in influenza A virus. Journal of Virology 69:4012–4019
    [Google Scholar]
  10. Fodor E., Pritlove D. C., Gould K. G., Brownlee G. G. 1996; The ‘RNA-fork’ model for the initiation of influenza transcription. In Options for the Control of Influenza III pp. 381–388 Brown L. E., Hampson A. W., Webster R. G. Edited by Amsterdam: Elsevier;
    [Google Scholar]
  11. Gorman M., Moffat L. F., Howard B. H. 1982; Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Molecular and Cellular Biology 2:1044–1051
    [Google Scholar]
  12. Hagen M., Chung T. D. Y., Butcher J. A., Krystal M. 1994; Recombinant influenza virus polymerase: requirement of both 5′ and 3′ viral ends for endonuclease activity. Journal of Virology 68:1509–1515
    [Google Scholar]
  13. Hall C. B., Douglas R. G., Geiman J. M. Jr Meagher M. P. 1979; Viral shedding patterns of children with influenza B infection. Journal of Infectious Diseases 140:610–613
    [Google Scholar]
  14. Horvath C. M., Williams M. A., Lamb R. A. 1990; Eukaryotic coupled translation of tandem cistron: identification of the influenza B virus BM2 polypeptide. EMBO Journal 9:2639–2647
    [Google Scholar]
  15. Kemdirim S., Palefsky J., Briedis D. J. 1986; Influenza B virus PB1 protein: nucleotide sequence of the genome RNA segment predicts a high degree of structural homology with the corresponding influenza A virus polymerase protein. Virology 152:126–135
    [Google Scholar]
  16. Kim H. W., Brandt C. D., Arrobio J. O., Murphy B., Chanock R. M., Parrot R. H. 1979; Influenza A and B virus infection in infants and young children during the years 1957-1976. American Journal of Epidemiology 109:464–476
    [Google Scholar]
  17. Kim H.-J., Fodor E., Brownlee G. G., Seong B. L. 1997; Mutational analysis of the RNA-fork model of the influenza A virus vRNA promoter in vivo . Journal of General Virology 78:353–357
    [Google Scholar]
  18. Kingsbury D. W. 1990; Orthomyxoviridae and their replication. In Fields Virology, 2nd edn. pp. 1075–1091 Fields B. W., Knipe D. M. Edited by New York: Raven Press;
    [Google Scholar]
  19. Lamb R. A., Choppin P. W. 1983; The gene structure and replication of influenza virus. Annual Review of Biochemistry 52:467–506
    [Google Scholar]
  20. Lamb R. A., Horvath C. M. 1991; Diversity of coding strategies in influenza viruses. Trends in Genetics 7:261–266
    [Google Scholar]
  21. 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]
  22. Li X., Palese P. 1994; Characterization of the polyadenylation signal of influenza virus RNA. Journal of Virology 68:1245–1249
    [Google Scholar]
  23. Luo G., Luytjes W., Enami M., Palese P. 1991; The poly-adenylation signal of influenza virus RNA involves a stretch of uridine followed by the RNA duplex of the panhandle structure. Journal of Virology 65:2861–2867
    [Google Scholar]
  24. Luytjes W., Krystal M., Enami M., Parvin J. D., Palese P. 1989; Amplification, expression, and packaging of a foreign gene by influenza virus. Cell 59:1107–1113
    [Google Scholar]
  25. Martín J., Albo C., Ortín J., Melero J. A., Portela A. 1992; In vitro reconstitution of active influenza virus ribonucleoprotein complexes using viral proteins purified from infected cells. Journal of General Virology 73:1855–1859
    [Google Scholar]
  26. Mena I., de la Luna S., Albo C., Martín J., Nieto A., Ortín J., Portela A. 1994; Synthesis of biologically active influenza virus core proteins using a vaccinia virus-T7 RNA polymerase expression system. Journal of General Virology 75:2109–2114
    [Google Scholar]
  27. Murphy B. R., Webster R. G. 1990; Orthomyxoviruses. In Fields Virology, 2nd edn. pp. 1091–1152 Fields B. N., Knipe D. M. Edited by New York: Raven Press;
    [Google Scholar]
  28. Muster T., Subbarao E. K., Enami M., Murphy B. P., Palese P. 1991; An influenza A virus containing influenza B virus 5′ and 3′ noncoding regions of the neuraminidase gene is attenuated in mice. Proceedings of the National Academy of Sciences, USA 88:5177–5181
    [Google Scholar]
  29. Neumann G., Hobom G. 1995; Mutational analysis of influenza virus promoter elements in vivo . Journal of General Virology 76:1709–1717
    [Google Scholar]
  30. Neumann G., Zobel A., Hobom G. 1994; RNA polymerase I-mediated expression of influenza viral RNA molecules. Virology 202:477–479
    [Google Scholar]
  31. Nolan T. F., Goodman R. A., Hinman A. R., Noble G. R., Kendal A. P., Thacker S. B. 1980; Morbidity and mortality associated with influenza B in the United States, 1979-1980. A report from the Centers for Disease Control. Journal of Infectious Diseases 142:360
    [Google Scholar]
  32. Piccone M. E., Fernandez-Sesma A., Palese P. 1993; Mutational analysis of the influenza virus vRNA promoter. Virus Research 28:99–112
    [Google Scholar]
  33. Robertson J. S. 1979; 5′ and 3′ terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Research 6:3745–3757
    [Google Scholar]
  34. Saks M. E., Sampson J. R., Abelson J. N. 1994; The transfer RNA identify problem: a search for rules. Science 263:191–197
    [Google Scholar]
  35. Seong B. L., Brownlee G. G. 1992a; A new method for reconstituting influenza polymerase and RNA in vitro : a study of the promoter elements for cRNA and vRNA synthesis in vitro and viral rescue in vivo. Virology 186:247–260
    [Google Scholar]
  36. Seong B. L., Brownlee G. G. 1992b; Nucleotides 9 to 11 of the influenza A virion RNA promoter are crucial for activity in vitro . Journal of General Virology 73:3115–3124
    [Google Scholar]
  37. Shaw M. W., Choppin P. W., Lamb R. A. 1983; A previously unrecognized influenza B virus glycoprotein from a bicistronic mRNA that also encodes the viral neuraminidase. Proceedings of the National Academy of Sciences, USA 80:4879–4883
    [Google Scholar]
  38. Shaw M. W., Arden N. H., Maassab H. 1992; New aspects of influenza viruses. Clinical Microbiology Reviews 5:74–92
    [Google Scholar]
  39. Smith F. I., Palese P. 1989; Variation in influenza virus genes: epidemiological, pathogenic, and evolutionary consequences. In The Influenza Viruses pp. 319–359 Krug R. M. Edited by New York: Plenum Press;
    [Google Scholar]
  40. Stoeckle M. Y., Shaw M. W., Choppin P. W. 1987; Segment-specific and common nucleotide sequences in the noncoding regions of influenza B virus genome RNAs. Proceedings of the National Academy of Sciences, USA 84:2703–2707
    [Google Scholar]
  41. Tiley L. S., Hagen M., Matthews J. T., Krystal M. 1994; Sequence-specific binding of the influenza virus RNA polymerase to sequences located at the 5′ ends of the viral RNAs. Journal of Virology 68:5108–5116
    [Google Scholar]
  42. Yamanaka K., Ogasawara N., Yoshikawa H., Ishihama A., Nagata K. 1991; In vivo analysis of the promoter structure of the influenza virus RNA genome using a transfection system with an engineered RNA. Proceedings of the National Academy of Sciences, USA 88:5369–5373
    [Google Scholar]
  43. Yamashita M., Krystal M., Fitch W. M., Palese P. 1988; Influenza B virus evolution: co-circulating lineages and comparison of evolutionary patterns with those of influenza A and C viruses. Virology 163:112–123
    [Google Scholar]
  44. Zhang H., Air G. M. 1994; Expression of functional influenza A polymerase proteins and template from cloned cDNAs in recombinant vaccinia virus infected cells. Biochemical and Biophysical Research Communications 200:95–101
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-79-4-673
Loading
/content/journal/jgv/10.1099/0022-1317-79-4-673
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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