Features of the mammalian orthoreovirus 3 Dearing l1 single-stranded RNA that direct packaging and serotype restriction Free

Abstract

A series of recombinant mammalian orthoreoviruses (mammalian orthoreovirus 3 Dearing, MRV-3De) were generated that express an MRV-3De 3–CAT fusion protein. Individual viruses contain L1CAT double-stranded (ds) RNAs that range in length from a minimum of 1020 bp to 4616 bp. The engineered dsRNAs were generated from -transcribed single-stranded (ss) RNAs and incorporated into infectious virus particles by using reverse genetics. In addition to defining the sequences required for these ssRNAs to be ‘identified’ as l1 ssRNAs, the individual nucleotides in these regions that ‘mark’ each ssRNA as originating from mammalian orthoreovirus 1 Lang (MRV-1La), mammalian orthoreovirus 2 D5/Jones (MRV-2Jo) or MRV-3De have been identified. A C at position 81 in the MRV-1La 5′ 129 nt sequence was able to be replaced with a U, as normally present in MRV-3De; this toggled the activity of the MRV-1La ssRNA to that of an MRV-3De 5′ l1. RNA secondary-structure predictions for the 5′ 129 nt of both the biologically active MRV-3De l1 ssRNA and the U81-MRV-3De-restored MRV-1La 5′ ssRNA predicted a common structure.

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2007-12-01
2024-03-19
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References

  1. Barro M., Mandiola P., Chen D., Patton J. T., Spencer E. 2001; Identification of sequences in rotavirus mRNAs important for minus strand synthesis using antisense oligonucleotides. Virology 288:71–80 [CrossRef]
    [Google Scholar]
  2. Boyce M., Roy P. 2007; Recovery of infectious bluetongue virus from RNA. J Virol 81:2179–2186 [CrossRef]
    [Google Scholar]
  3. Chandran K., Parker J. S., Ehrlich M., Kirchhausen T., Nibert M. L. 2003; The delta region of outer-capsid protein micro 1 undergoes conformational change and release from reovirus particles during cell entry. J Virol 77:13361–13375 [CrossRef]
    [Google Scholar]
  4. Chen D., Luongo C. L., Nibert M. L., Patton J. T. 1999; Rotavirus open cores catalyze 5′-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 265:120–130 [CrossRef]
    [Google Scholar]
  5. Chen D., Barros M., Spencer E., Patton J. T. 2001; Features of the 3′-consensus sequence of rotavirus mRNAs critical to minus strand synthesis. Virology 282:221–229 [CrossRef]
    [Google Scholar]
  6. Coombs K. M. 2006; Reovirus structure and morphogenesis. Curr Top Microbiol Immunol 309:117–167
    [Google Scholar]
  7. Damodaran K. V., Reddy V. S., Johnson J. E., Brooks C. L. III 2002; A general method to quantify quasi-equivalence in icosahedral viruses. J Mol Biol 324:723–737 [CrossRef]
    [Google Scholar]
  8. Dennehy J. J., Turner P. E. 2004; Reduced fecundity is the cost of cheating in RNA virus φ 6. Proc Biol Sci 271:2275–2282 [CrossRef]
    [Google Scholar]
  9. Grimes J. M., Burroughs J. N., Gouet P., Diprose J. M., Malby R., Zientara S., Mertens P. P., Stuart D. I. 1998; The atomic structure of the bluetongue virus core. Nature 395:470–478 [CrossRef]
    [Google Scholar]
  10. Gunning P., Leavitt J., Muscat G., Ng S. Y., Kedes L. 1987; A human β -actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci U S A 84:4831–4835 [CrossRef]
    [Google Scholar]
  11. Ikegami N., Gomatos P. J. 1972; Inhibition of host and viral protein syntheses during infection at the nonpermissive temperature with ts mutants of reovirus 3. Virology 47:306–319 [CrossRef]
    [Google Scholar]
  12. Jiang J., Coombs K. M. 2005; Infectious entry of reovirus cores into mammalian cells enhanced by transfection. J Virol Methods 128:88–92 [CrossRef]
    [Google Scholar]
  13. Kobayashi T., Antar A. A. R., Boehme K. W., Danthi P., Eby E. A., Guglielmi K. M., Holm G. H., Johnson E. M., Maginnis M. S. other authors 2007; A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147–157 [CrossRef]
    [Google Scholar]
  14. Komoto S., Sasaki J., Taniguchi K. 2006; Reverse genetics system for introduction of site-specific mutations into the double-stranded RNA genome of infectious rotavirus. Proc Natl Acad Sci U S A 103:4646–4651 [CrossRef]
    [Google Scholar]
  15. Mansell E. A., Ramig R. F., Patton J. T. 1994; Temperature-sensitive lesions in the capsid proteins of the rotavirus mutants tsF and tsG that affect virion assembly. Virology 204:69–81 [CrossRef]
    [Google Scholar]
  16. Markotter W., Theron J., Nel L. H. 2004; Segment specific inverted repeat sequences in bluetongue virus mRNA are required for interaction with the virus non structural protein NS2. Virus Res 105:1–9 [CrossRef]
    [Google Scholar]
  17. Mathews D. H., Disney M. D., Childs J. L., Schroeder S. J., Zuker M., Turner D. H. 2004; Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A 101:7287–7292 [CrossRef]
    [Google Scholar]
  18. Monnier N., Higo-Moriguchi K., Sun Z. Y., Prasad B. V., Taniguchi K., Dormitzer P. R. 2006; High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J Virol 80:1513–1523 [CrossRef]
    [Google Scholar]
  19. Moody M. D., Joklik W. K. 1989; The function of reovirus proteins during the reovirus multiplication cycle: analysis using monoreassortants. Virology 173:437–446 [CrossRef]
    [Google Scholar]
  20. Patton J. T. 2001; Rotavirus RNA replication and gene expression. Novartis Found Symp 238:64–77
    [Google Scholar]
  21. Patton J. T., Spencer E. 2000; Genome replication and packaging of segmented double-stranded RNA viruses. Virology 277:217–225 [CrossRef]
    [Google Scholar]
  22. Patton J. T., Wentz M., Xiaobo J., Ramig R. F. 1996; cis -Acting signals that promote genome replication in rotavirus mRNA. J Virol 70:3961–3971
    [Google Scholar]
  23. Poranen M. M., Tuma R. 2004; Self-assembly of double-stranded RNA bacteriophages. Virus Res 101:93–100 [CrossRef]
    [Google Scholar]
  24. Ramig R. F., Ward R. L. 1991; Genomic segment reassortment in rotaviruses and other reoviridae. Adv Virus Res 39:163–207
    [Google Scholar]
  25. Ramig R. F., Cross R. K., Fields B. N. 1977; Genome RNAs and polypeptides of reovirus serotypes 1, 2, and 3. J Virol 22:726–733
    [Google Scholar]
  26. Roner M. R., Joklik W. K. 2001; Reovirus reverse genetics: incorporation of the CAT gene into the reovirus genome. Proc Natl Acad Sci U S A 98:8036–8041 [CrossRef]
    [Google Scholar]
  27. Roner M. R., Roehr J. 2006; The 3′ sequences required for incorporation of an engineered ssRNA into the reovirus genome. Virol J 3:1 [CrossRef]
    [Google Scholar]
  28. Roner M. R., Steele B. G. 2007; Localizing the reovirus packaging signals using an engineered m1 and s2 ssRNA. Virology 358:89–97 [CrossRef]
    [Google Scholar]
  29. Roner M. R., Sutphin L. A., Joklik W. K. 1990; Reovirus RNA is infectious. Virology 179:845–852 [CrossRef]
    [Google Scholar]
  30. Roner M. R., Lin P. N., Nepluev I., Kong L. J., Joklik W. K. 1995; Identification of signals required for the insertion of heterologous genome segments into the reovirus genome. Proc Natl Acad Sci U S A 92:12362–12366 [CrossRef]
    [Google Scholar]
  31. Roner M. R., Nepliouev I., Sherry B., Joklik W. K. 1997; Construction and characterization of a reovirus double temperature-sensitive mutant. Proc Natl Acad Sci U S A 94:6826–6830 [CrossRef]
    [Google Scholar]
  32. Roner M. R., Bassett K., Roehr J. 2004; Identification of the 5′ sequences required for incorporation of an engineered ssRNA into the reovirus genome. Virology 329:348–360 [CrossRef]
    [Google Scholar]
  33. Skehel J. J., Joklik W. K. 1969; Studies on the in vitro transcription of reovirus RNA catalyzed by reovirus cores. Virology 39:822–831 [CrossRef]
    [Google Scholar]
  34. Spence R. P., Moore N. F., Nuttall P. A. 1984; The biochemistry of orbiviruses. Brief review. Arch Virol 82:1–18 [CrossRef]
    [Google Scholar]
  35. Stuart D. I., Gouet P., Grimes J., Malby R., Diprose J., Zientara S., Burroughs J. N., Mertens P. P. 1998; Structural studies of orbivirus particles. Arch Virol Suppl 14:235–250
    [Google Scholar]
  36. Tanaka S., Roy P. 1994; Identification of domains in bluetongue virus VP3 molecules essential for the assembly of virus cores. J Virol 68:2795–2802
    [Google Scholar]
  37. Tortorici M. A., Shapiro B. A., Patton J. T. 2006; A base-specific recognition signal in the 5′ consensus sequence of rotavirus plus-strand RNAs promotes replication of the double-stranded RNA genome segments. RNA 12:133–146 [CrossRef]
    [Google Scholar]
  38. Tosteson M. T., Nibert M. L., Fields B. N. 1993; Ion channels induced in lipid bilayers by subvirion particles of the nonenveloped mammalian reoviruses. Proc Natl Acad Sci U S A 90:10549–10552 [CrossRef]
    [Google Scholar]
  39. Urbano P., Urbano F. G. 1994; The Reoviridae family. Comp Immunol Microbiol Infect Dis 17:151–161 [CrossRef]
    [Google Scholar]
  40. Wentz M. J., Patton J. T., Ramig R. F. 1996; The 3′-terminal consensus sequence of rotavirus mRNA is the minimal promoter of negative-strand RNA synthesis. J Virol 70:7833–7841
    [Google Scholar]
  41. Wiener J. R., Joklik W. K. 1989; The sequences of the reovirus serotype 1, 2, and 3 L1 genome segments and analysis of the mode of divergence of the reovirus serotypes. Virology 169:194–203 [CrossRef]
    [Google Scholar]
  42. Wiener J. R., McLaughlin T., Joklik W. K. 1989; The sequences of the S2 genome segments of reovirus serotype 3 and of the dsRNA-negative mutant ts447. Virology 170:340–341 [CrossRef]
    [Google Scholar]
  43. Xu W., Patrick M. K., Hazelton P. R., Coombs K. M. 2004; Avian reovirus temperature-sensitive mutant tsA12 has a lesion in major core protein sigmaA and is defective in assembly. J Virol 78:11142–11151 [CrossRef]
    [Google Scholar]
  44. Zhang C., Lee C. S., Guo P. 1994; The proximate 5′ and 3′ ends of the 120-base viral RNA (pRNA) are crucial for the packaging of bacteriophage Φ29 DNA. Virology 201:77–85 [CrossRef]
    [Google Scholar]
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