‘Primer alignment-and-extension’: a novel mechanism of viral RNA recombination responsible for the rescue of inactivated poliovirus cDNA clones Free

Abstract

In the course of experiments designed to assess the potential role of alternative open reading frames (ORF) present in the 5′-terminal untranslated region (5′-UTR) of poliovirus type 1 (Mahoney strain) genomic RNA, we came across a double mutation that completely abrogated the infectivity of full-length cDNA clones. The infectivity was rescued in by cotransfecting COS-1 cells with short RNA transcripts of the wild-type 5′-UTR of poliovirus type 2 Lansing, provided a free 3′-OH was available. Direct sequencing of the viral RNA revealed that the infectious viruses recovered were recombinants Lansing/Mahoney, with variable points of ‘crossing-over’. A novel mechanism of RNA–RNA recombination, which we propose to call ‘primer alignment-and-extension’, is described that would explain the high rate of recombination of RNA viruses observed in natural conditions.

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1999-08-01
2024-03-28
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References

  1. Agol V. I., Grachev V. P., Drozdov S. G., Kolesnikova M. S., Koslov V. G., Ralf N. M., Romanova L. I., Tolskaya E. A., Tyufanov A. V., Viktorova E. G. 1984; Construction and properties of intertypic poliovirus recombinants: first approximation mapping of the major determinants of neurovirulence. Virology 136:41–55
    [Google Scholar]
  2. Bujarski J. 1996; Experimental systems of genetic recombination and defective RNA formation in RNA viruses. Seminars in Virology 7:361–362
    [Google Scholar]
  3. Bujarski J., Nagy P. D. 1996; Different mechanisms of homologous and non-homologous recombination in brome mosaic virus: role of RNA sequences and replicase proteins. Seminars in Virology 7:363–372
    [Google Scholar]
  4. Chetverin A. B., Chetverina H. V., Demidenko A. A., Ugarov V. I. 1997; Non homologous RNA recombination in a cell-free system: evidence for a transesterification mechanism guided by secondary structure. Cell 88:503–513
    [Google Scholar]
  5. Degener A. M., Pagnotti P., Facchini J., Perez Bercoff R. 1983; Genomic RNA of mengovirus. VI. Translation of its two cistrons in lysates of interferon-treated cells. Journal of Virology 45:889–894
    [Google Scholar]
  6. Degener A. M., Silveira Carneiro J., Cassetti C., Pierangeli A., Pagnotti P., Bucci M., Perez Bercoff R. 1995; Role of the pyrimidine-rich tract on the translation of chimeric polio–hepatitis A mRNAs with engineered 5′-terminal untranslated region. Virus Research 37:291–303
    [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. 1985; A comprehensive set of sequence analysis of programs for the VAX. Nucleic Acids Research 12:387–395
    [Google Scholar]
  8. Hirst G. K. 1962; Genetic recombination with Newcastle disease virus, poliovirus, and influenza. Cold Spring Harbor Symposia on Quantitative Biology 27:303–308
    [Google Scholar]
  9. Jang S. K., Wimmer E. 1990; Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57 KDa RNA-binding protein. Genes & Development 4:1560–1572
    [Google Scholar]
  10. Kirkegaard K., Baltimore D. 1986; The mechanism of RNA recombination in poliovirus. Cell 47:433–443
    [Google Scholar]
  11. Lai M. M. C. 1992; RNA recombination in animal and plant viruses. Microbiological Reviews 56:61–79
    [Google Scholar]
  12. Lai M. M. C. 1996; Recombination in large RNA viruses: coronaviruses. Seminars in Virology 7:381–388
    [Google Scholar]
  13. Lipskaya G. Y., Muzychenko A. R., Kutikova O. K., Maslova S. V., Equestre M., Drozdov S. G., Perez Bercoff R., Agol V. 1991; Frequent isolation of intertypic poliovirus recombinants with serotype 2 specificity from vaccine-associated polio cases. Journal of Medical Virology 35:290–296
    [Google Scholar]
  14. Meerovitch K., Pelletier J., Sonenberg N. 1989; A cellular protein that binds to the 5′-non coding region of poliovirus RNA: implication for internal translation initiation. Genes & Development 3:1026–1034
    [Google Scholar]
  15. Nicholson R., Pelletier J., Sonenberg N. 1991; Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vitro translation studies. Journal of Virology 65:6886–6894
    [Google Scholar]
  16. Pelletier J., Sonenberg N. 1988; Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:426–429
    [Google Scholar]
  17. Pelletier J., Flynn M. E., Kaplan G., Racaniello V., Sonenberg N. 1988; Mutational analysis of upstream AUG codons of poliovirus RNA. Journal of Virology 62:4486–4492
    [Google Scholar]
  18. Perez Bercoff R. 1982; But is the 5′-end of messenger RNA always involved in initiation?. In Protein Biosynthesis in Eukaryotes pp 245–252 Edited by Bercoff R. Perez. New York: Plenum;
    [Google Scholar]
  19. Perez Bercoff R. 1987; Picornaviruses at the molecular level. In The Molecular Basis of Viral Replication pp 197–215 Edited by Bercoff R. Perez. New York: Plenum;
    [Google Scholar]
  20. Perez Bercoff R., Kaempfer R. 1982; Genomic RNA of mengovirus. V. Recognition of common features by ribosomes and eukaryotic initiation factor eIF-2. Journal of Virology 41:30–41
    [Google Scholar]
  21. Pierangeli A., Bucci M., Pagnotti P., Degener A., Perez Bercoff R. 1995; Mutational analysis of the 3′-terminal extra-cistronic region of poliovirus RNA: secondary structure is not the only requirement for minus strand RNA replication. FEBS Letters 374:327–332
    [Google Scholar]
  22. Pierangeli A., Bucci M., Forzan M., Pagnotti P., Equestre M., Perez Bercoff R. 1998; Identification of an alternative open reading frame (‘‘hidden gene’’?) stringently required for the infectivity of poliovirus cDNA clones. Microbiologica 21:309–320
    [Google Scholar]
  23. Rueckert R. R. 1990; Picornaviridae : the viruses and their replication. In Virology pp 705–738 Edited by Fields B. N., Knipe D. M., Chanock R. M., Melnick J. L., Roizman B., Shope R. E. New York: Raven Press;
    [Google Scholar]
  24. Sambrook J., Fritsch F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  25. Silveira Carneiro J., Equestre M., Pagnotti P., Gradi A., Sonenberg N., Perez Bercoff R. 1995; 5′-UTR of hepatitis A virus RNA: mutations in the 5′-most pyrimidine-rich tract reduce its ability to direct internal initiation of translation. Journal of General Virology 76:1189–1196
    [Google Scholar]
  26. Tolskaya E. A., Romanova L. I., Kolesnikova M. S., Agol V. I. 1983; Intertypic recombination in poliovirus: genetic and biochemical studies. Virology 124:121–132
    [Google Scholar]
  27. van Marle G., Luytjes W., Snijder E. J., Spaan W. J. M. 1998 Nidovirus discontinuous mRNA transcription involves base-pairing between the leader and promoter sequences. Abstracts of the Fifth International Symposium on Positive Strand RNA Viruses St Petersburg, FL, USA: May 23–28
    [Google Scholar]
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