Skip to main content
NCBI home page
Wiley - PMC COVID-19 Collection logoLink to Wiley - PMC COVID-19 Collection
. 2004 Jan 29;11(12):1115–1127. doi: 10.1002/yea.320111202

Ribosomal frameshifting in yeast viruses

Jonathan D Dinman 1,2
PMCID: PMC7169727  PMID: 8619310

Abstract

Proper maintenance of translational reading frame by ribosomes is essential for cell growth and viability. In the last 10 years it has been shown that a number of viruses induce ribosomes to shift reading frame in order to regulate the expression of gene products having enzymatic functions. Studies on ribosomal frameshifting in viruses of yeast have been particularly enlightening. The roles of viral mRNA sequences and secondary structures have been elucidated and a picture of how these interact with host chromosomal gene products is beginning to emerge. The efficiency of ribosomal frameshifting is important for viral particle assembly, and has identified ribosomal frameshifting as a potential target for antiviral agents. The availability of mutants of host chromosomal gene products involved in maintaining the efficiency of ribosomal frameshifting bodes well for the use of yeast in future studies of ribosomal frameshifting.

Keywords: Saccharomyces cerevisiae, ribosomes, ribosomal frameshifting, L‐A dsRNA virus, Ty, retrotransposon, retrovirus, hungry codons, polyamines

References

  • 1. Atkins, J. F. , Weills, R. B. , Thompson, S. and Gesteland, R. F. E. (1991). Toward a genetic dissection of the basis of triplet decoding, and its natural subversion: programmed reading frame shifts and hops. Annu. Rev. Genet. 25, 201–228. [DOI] [PubMed] [Google Scholar]
  • 2. Balasundaram, D. , Dinman, J. D. , Wickner, R. B. , Tabor, C. W. and Tabor, H. (1994). Spermidine deficiency increases +1 ribosomal frameshifting efficiency and inhibits Ty1 retrotransposition in Saccharomyces cerevisiae . Proc. Natl. Acad. Sci. USA 91, 172–176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3. Balasundaram, D. , Dinman, J. D. , Tabor, C. W. and Tabor, H. (1994). SPE1 and SPE2: Two essential genes in the biosynthesis of polyamines that modulate +1 ribosomal frameshifting in Saccharomyces cerevisiae . J. Bacteriol. 176, 7126–7128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4. Belcourt, M. F. and Farabaugh, P. J. (1990). Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 62, 339–352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5. Blanc, A. , Goyer, C. and Sonenberg, N. (1992). The coat protein of the yeast double‐stranded RNA virus L‐A attaches covalently to the cap structure of eukaryotic mRNA. Mol. Cell. Biol. 12, 3390–3398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6. Boeke, J. D. , Garfinkel, D. J. , Styles, C. A. and Fink, G. R. (1985). Ty elements transpose through an RNA intermediate. Cell 40, 491–500. [DOI] [PubMed] [Google Scholar]
  • 7. Boeke, J. D. and Sandmeyer, S. B. (1991). Yeast transposable elements In Jones E. W., Pringle J. R. and Broach J. R. (Eds), The Molecular Biology of the Yeast Saccharomyces, vol. 1 Cold Spring Harbor Press, Plainview, NY, pp. 193–261. [Google Scholar]
  • 8. Brierley, I. A. , Dingard, P. and Inglis, S. C. (1989). Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57, 537–547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9. Brierley, I. A. , Rolley, N. J. , Jenner, A. J. and Inglis, S. C. (1991). Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal. J. Mol. Biol. 220, 889–902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10. Brierley, I. A. , Jenner, A. J. and Inglis, S. C. (1992). Mutational analysis of the ‘slippery‐sequence’ component of a coronavirus ribosomal frameshifting signal. J. Mol. Biol. 227, 463–479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11. Bruenn, J. A. (1980). Virus‐like particle of yeast. Ann. Rev. Microbiol. 34, 49–68. [DOI] [PubMed] [Google Scholar]
  • 12. Bussey, H. (1991). K1 killer toxin, a poreforming protein from yeast. Mol. Microbiol. 5, 2339–2343. [DOI] [PubMed] [Google Scholar]
  • 13. Chandler, M. and Fayet, O. (1993). Translational frameshifting in the control of transposition in bacteria. Mol. Microbiol. 7, 497–503. [DOI] [PubMed] [Google Scholar]
  • 14. Cheng, R. H. , Caston, J. R. , Wang, G. , et al. (1994). Fungal virus capsids, cytoplasmic compartments for the replication of double‐stranded RNA, formed as icosahedral shells of asymmetric gag dimers. J. Mol. Biol. 224, 255–258. [DOI] [PubMed] [Google Scholar]
  • 15. Clare, J. J. and Farabaugh, P. J. (1985). Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc. Natl. Acad. Sci. USA 82, 2829–2833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16. Cui, Y. , Hagan, K. W. , Zhang, S. and Peltz, S. W. (1995). Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes & Dev. 9, 423–436. [DOI] [PubMed] [Google Scholar]
  • 17. Cui, Y. , Dinman, J. D. , Weng, Y. , and Peltz, S. W. (1995). mof4–1 is a unique allele of UPF1 involved in maintenance of translational reading frame. Proc. Natl. Acad. Sci. USA., submitted.
  • 18. Dinman, J. D. , Icho, T. and Wickner, R. B. (1991). A – 1 ribosomal frameshift in a double‐stranded RNA virus forms a gag‐pol fusion protein. Proc. Natl. Acad. Sci. USA 88, 174–178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19. Dinman, J. D. and Wickner, R. B. (1992). Ribosomal frameshifting efficiency and gag/gag‐pol ratio are critical for yeast M1 double‐stranded RNA virus propagation. J. Virol. 66, 3669–3676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20. Dinman, J. D. and Wickner, R. B. (1994). Translational maintenance of frame: mutants of Saccharomyces cerevisiae with altered – 1 ribosomal frameshifting efficiencies. Genetics 136, 75–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21. Dinman, J. D. and Wickner, R. B. (1995). 5S rRNA is involved in fidelity of translational reading frame. Genetics, in press. [DOI] [PMC free article] [PubMed]
  • 22. Esteban, R. and Wickner, R. B. (1986). Three different M1 RNA‐containing viruslike particle types in Saccharomyces cerevisiae: in vitro M1 double‐stranded RNA synthesis. Mol. Cell. Biol. 6, 1552–1561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23. Farabaugh, P. J. , Zhao, H. and Vimaladithan. (1993). A novel programmed frameshift expresses the POL3 gene of retrotransposon Ty3 of yeast: frameshifting without tRNA slippage. Cell 74, 93–103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24. Farabaugh, P. J. (1993). Alternative readings of the genetic code. Cell 74, 591–596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. Farabaugh, P. J. (1995). Post‐transcriptional regulation of transposition by Ty retrotransposons of Saccharomyces cerevisiae . J. Biol. Chem. 270, 10361–10364. [DOI] [PubMed] [Google Scholar]
  • 26. Fujimura, T. and Wickner, R. B. (1988). Gene overlap results in a viral protein having an RNA binding domain and a major coat protein domain. Cell 55, 663–671. [DOI] [PubMed] [Google Scholar]
  • 27. Fujimura, T. and Wickner, R. B. (1992). Interaction of two cis sites with the RNA replicase of the yeast L‐A virus. J. Biol. Chem. 267, 2708–2713. [PubMed] [Google Scholar]
  • 28. Garfinkel, D. J. , Boeke, J. D. and Fink, G. R. (1985). Ty element transposition: reverse transcriptase and virus‐like particles. Cell 42, 507–517. [DOI] [PubMed] [Google Scholar]
  • 29. Hatfield, D. , Levin, J. G. , Rein, A. and Oroszlan, S. (1992). Translational suppression in retroviral gene expression. Adv. Virus Res. 41, 193–239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30. Hayashi, S.‐I. and Murakami, Y. (1995). Rapid and regulated degradation of ornithine decarboxylase. Biochem. J. 306, 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31. He, F. and Jacobson, A. (1995). Identification of a novel component of the nonsense‐mediated mRNA decay pathway by use of an interacting protein screen. Genes & Dev. 9, 437–454. [DOI] [PubMed] [Google Scholar]
  • 32. Hopper, J. E. , Bostian, K. A. , Rowe, L. B. and Tipper, D. J. (1977). Translation of the L‐species dsRNA genome of the killer‐associated virus‐like particles of Saccharomyces cerevisiae . J. Biol. Chem. 252, 9010–9017. [PubMed] [Google Scholar]
  • 33. Icho, T. and Wickner, R. B. (1989). The double‐stranded RNA genome of yeast virus L‐A encodes its own putative RNA polymerase by fusing two open reading frames. J. Biol. Chem. 264, 6716–6723. [PubMed] [Google Scholar]
  • 34. Jacks, T. , Madhani, H. D. , Masiraz, F. R. and Varmus, H. E. (1988). Signals for ribosomal frameshifting in the Rous sarcoma virus gag‐pol region. Cell 55, 447–458. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35. Jacks, T. (1990). Translational suppression in gene expression in retroviruses and retrotransposons. Curr. Top. Microbiol. Immunol. 157, 93–124. [DOI] [PubMed] [Google Scholar]
  • 36. Kawakami, K. , Shafer, B. K. , Garfinkel, D. J. , Strathern, J. N. and Nakamura, Y. (1992). Ty element‐induced temperature‐sensitive mutations of Saccharomyces cerevisiae . Genetics 131, 821–832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37. Kawakami, K. , Pande, S. , Faiola, B. , et al. (1993). A rare tRNA‐Arg(CUU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae . Genetics 135, 309–320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. Kirchner, J. , Sandmeyer, S. and Forrest, D. (1992). Transposition of a Ty3 GAG3‐POL3 fusion mutant is limited by availability of capsid protein. J. Virol. 66, 6081–6092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39. Lee, S. I. , Umen, J. G. , Guthrie, C. and Varmus, H. E. (1995). A genetic screen identifies cellular factors involved in retroviral – 1 ribosomal frameshifting. Proc. Natl. Acad. Sci. USA, in press. [DOI] [PMC free article] [PubMed]
  • 40. Leeds, P. , Wood, J. M. , Lee, B.‐S. and Culbertson, M. R. (1992). Gene products that promote mRNA turnover in Saccharomyces cerevisiae . Mol. Cell. Biol. 12, 2165–2177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41. Levin, H. L. , Weaver, D. C. and Boeke, J. D. (1993). Novel gene expression mechanism in a fission yeast retroelement: Tf1 proteins are derived from a single primary translation product. EMBO J. 12, 4885–4895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42. Mann, R. , Mulligan, R. C. and Baltimore, D. (1983). Construction of a retrovirus packaging mutant and its use to produce helper‐free defective retrovirus. Cell 33, 153–159. [DOI] [PubMed] [Google Scholar]
  • 43. Matsufuji, S. , Matsufuji, T. , Miyazaki, Y. , et al. (1995). Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 80, 51–60. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44. Mellor, J. , Malim, M. H. , Gull, K. , et al. (1985). Reverse transcriptase activity and Ty RNA are associated with virus‐like particles in yeast. Nature 318, 583–586. [DOI] [PubMed] [Google Scholar]
  • 45. Morikawa, S. and Bishop, D. H. L. (1992). Identification and analysis of the gag‐pol ribosomal frameshift site of feline immunodeficiency virus. Virology 186, 389–397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46. Pande, S. , Vimaladithan, V. , Zhao, H. and Farabaugh, P. J. (1995). Pulling the ribosome out of frame by +1 at a programmed frameshift site by cognate binding of aminoacyl‐tRNA. Mol. Cell. Biol. 15, 298–304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47. Peltz, S. W. , He, F. , Welch, E. and Jacobson, A. J. (1994). Nonsense‐mediated mRNA decay in yeast. Prog. Nucl. Acid Res. 47, 271–298. [DOI] [PubMed] [Google Scholar]
  • 48. Ribas, J. C. and Wickner, R. B. (1992). RNA‐dependent RNA polymerase consensus sequence of the L‐A double‐stranded RNA virus: definition of essential domains. Proc. Natl. Acad. Sci. USA 89, 2185–2189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49. Rom, E. and Kahana, C. (1994). Polyamines regulate the expression of ornithine decarboxylase antizyme in vitro by inducing ribosomal frameshifting. Proc. Natl. Acad. Sci. USA 91, 3959–3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50. Sandmeyer, S. B. (1992). Yeast retrotransposons. Curr. Opin. Genet. Dev. 2, 705–711. [DOI] [PubMed] [Google Scholar]
  • 51. Somogyi, P. , Jenner, A. J. , Brierley, I. A. and Inglis, S. C. (1993). Ribosomal pausing during translation of an RNA pseudoknot. Mol. Cell. Biol. 13, 6931–6940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52. ten Dam, E. B. , Pleij, C. W. A. and Bosch, L. (1990). RNA pseudoknots: Translational frameshifting and readthrough on viral RNAs. Virus Genes 4, 121–136. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53. ten Dam, E. , Pleij, K. and Draper, D. (1992). Structural and functional aspects of RNA pseudo‐knots. Biochemistry 31, 11665–11676. [DOI] [PubMed] [Google Scholar]
  • 54. Tu, C. , Tzeng, T.‐H. and Bruenn, J. A. (1992). Ribosomal movement impeded at a pseudoknot required for ribosomal frameshifting. Proc. Natl. Acad. Sci. USA 89, 8636–8640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55. Vimaladithan, A. and Farabaugh, P. J. (1994). Special peptidyl‐tRNA molecules can promote translational frameshifting without slippage. Mol. Cell. Biol. 14, 8107–8116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56. Watanabe, S. and Temin, H. (1982). Encapsidation sequences for spleen necrosis virus, an avian retrovirus, are between the 5′ long terminal repeat and the start of the gag gene. Proc. Natl. Acad. Sci. USA 79, 5986–5990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57. Weng, Y. , Czaplinski, K. and Peltz, S. (1995). Linking mRNA turnover and translational termination by the Upf1 protein. Genes & Dev., submitted.
  • 58. Wickner, R. B. (1992). Double‐stranded and single‐stranded RNA viruses of Saccharomyces cerevisiae . Annu. Rev. Microbiol. 46, 347–375. [DOI] [PubMed] [Google Scholar]
  • 59. Woolford, J. L. and Warner, J. R. (1991). The ribosome and its synthesis In Broach J. R., Pringle J. R. and Jones E. W. (Eds), The Molecular and Cellular Biology of the Yeast Saccharomyces, vol. 1 Cold Spring Harbor Press, NY, pp. 587–626. [Google Scholar]
  • 60. Xu, H. and Boeke, J. D. (1990). Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Ty1 transposition frequency. Proc. Natl. Acad. Sci. USA 87, 8360–8364. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Yeast (Chichester, England) are provided here courtesy of Wiley

RESOURCES