Programmed −1 Frameshifting in Eukaryotes

  • Philip J. Farabaugh


By far the most numerous and the most ubiquitous of frameshift sites are a class of −1 frameshift sites first described in metazoan retroviruses. These sites have been found in retroviruses,27,36,40, 41, 42, 43,56,59,63,64 coronaviruses, 5,17,18,25,35 arteriviruses,31,61 astroviruses,44,57,99 giardiaviruses,96 toroviruses,80 several plant viruses,4,47,62,73,103 Drosophila retrotransposons, 16,58,72,76 a virus-like element in yeast,20,37,92 a bacterial gene,3,30,89 bacteriophage genes13,14,24,54 and bacterial insertion sequences.26,50,71,75,77,82,94,95 Sequence comparison and molecular genetic analysis of many of these sites has identified a canonical structure for these frameshift sites. Their prevalence across such an evolutionarily diverse distribution argues that such sites have evolved several times, each time converging on a single simple solution.


Feline Immunodeficiency Virus Infectious Bronchitis Virus Mouse Mammary Tumor Virus Rous Sarcoma Virus Ribosomal Frameshifting 
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  1. 1.
    Barrell BG, Air GM, Hutchison CA, III. Overlapping genes in bacteriophage OX174. Nature 1976; 264:34–41.PubMedCrossRefGoogle Scholar
  2. 2.
    Barrell BG, Shaw DC, Walker JE et al. Overlapping genes in bacteriophages phiX174 and G4. Biochem Soc Trans 1978; 6:63–67.PubMedGoogle Scholar
  3. 3.
    Blinkowa AL, Walker JR. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III γ subunit from within the τ subunit reading frame. Nucleic Acids Res 1990; 18: 1725–1729.PubMedCrossRefGoogle Scholar
  4. 4.
    Brault V, Miller WA. Translational frameshifting mediated by a viral sequence in plant cells. Proc Natl Acad Sci USA 1992; 89:2262–2266.PubMedCrossRefGoogle Scholar
  5. 5.
    Brierley I, Broursnell M, Birns M et al. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J 1987; 6: 3779–3785.PubMedGoogle Scholar
  6. 6.
    Brierley I, Digard P, Inglis SC. Characterization of an efficient coronavirus ribosomal frameshifting signal: Requirement for an RNA pseudoknot. Cell 1989; 57:537–547.PubMedCrossRefGoogle Scholar
  7. 7.
    Brierley I, Jenner AJ, Inglis SC. Mutational analysis of the “slippery-sequence” component of a coronavirus ribosomal frameshifting signal. J Mol Biol 1992; 227:463–479.PubMedCrossRefGoogle Scholar
  8. 8.
    Brierley I, Rolley NJ, Jenner AJ et al. Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal. J Mol Biol 1991; 220:889–902.PubMedCrossRefGoogle Scholar
  9. 9.
    Chamorro M, Parkin N, Varmus HE. An RNA pseudoknot and an optimal heptameric shift site are required for highly efficient ribosomal frameshifting on a retroviral messenger RNA. Proc Natl Acad Sci USA 1992; 89:713–717.PubMedCrossRefGoogle Scholar
  10. 10.
    Chen X, Chamorro M, Lee SI et al. Structural and functional studies of retroviral RNA pseudoknots involved in ribosomal frameshifting: Nucleotides at the junction of the two stems are important for efficient ribosomal frameshifting. EMBO J 1995; 14:842–852.PubMedGoogle Scholar
  11. 11.
    Coffin J. Structure of the retroviral genome. In: Weiss R, Teich N, Varmus H et al, eds. RNA Tumor Viruses: Molecular Biology of Tumor Viruses. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory, 1984:306.Google Scholar
  12. 12.
    Coffin J. Structure of the retroviral genome. In: Weiss R, Teich N, Varmus H et al, eds. RNA Tumor Viruses: Molecular Biology of Tumor Viruses. Supplements and Appendixes. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1985:23.Google Scholar
  13. 13.
    Condron BG, Atkins JF, Gesteland RF. Frameshifting in gene 10 of bacteriophage T7. J Bacteriol 1991; 173:6998–7003.PubMedGoogle Scholar
  14. 14.
    Condron BG, Gesteland RF, Atkins JF. An analysis of sequences stimulating frameshifting in the decoding of gene 10 of bacteriophage T7. Nucleic Acids Res 1991; 19:5607–5612.PubMedCrossRefGoogle Scholar
  15. 15.
    Cui Y, Hagan KW, Zhang S et al. Identification and characterization of genes that are required for the accelerated degradation of mRNAs containing a premature translational termination codon. Genes Dev 1995; 9:423–436.PubMedCrossRefGoogle Scholar
  16. 16.
    Danilevskaya O, Slot F, Pavlova M et al. Structure of the Drosophila HeT-A transposon: a retrotransposon-like element forming telomeres. Chromosoma 1994; 103:215–224.PubMedCrossRefGoogle Scholar
  17. 17.
    den Boon JA, Snijder EJ, Chirnside ED et al. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 1991; 65:2910–2920.Google Scholar
  18. 18.
    Denison MR, Zoltick PW, Leibowitz JL et al. Identification of polypeptides encoded in open reading frame 1b of the putative polymerase gene of the murine coronavirus mouse hepatitis virus A59-J Virol 1991; 65:3076–3082.Google Scholar
  19. 19.
    Dickson C, Eisenman R, Fan H et al. Protein biosynthesis and assembly. In: Weiss R, Teich N, Varmus H et al, eds. RNA Tumor Viruses. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1984: 513–648.Google Scholar
  20. 20.
    Dinman JD, Icho T, Wickner RB. A −1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc Natl Acad Sci USA 1991; 88:174–178.PubMedCrossRefGoogle Scholar
  21. 21.
    Dinman JD, Wickner RB. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J Virol 1992; 66:3669–3676.PubMedGoogle Scholar
  22. 22.
    Dinman JD, Wickner RB. Translational maintenance of frame: Mutants of Saccharomyces cerevisiae with altered −1 ribosomal frameshifting efficiencies. Genetics 1994; 136:75–86.PubMedGoogle Scholar
  23. 23.
    Dinman JD, Wickner RB. 5S rRNA is involved in fidelity of translational reading frame. Genetics 1995; in press.Google Scholar
  24. 24.
    Dunn JJ, Studier FW. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol 1983; 166:477–535.PubMedCrossRefGoogle Scholar
  25. 25.
    Eleouet JF, Rasschaert D, Lambert P et al. Complete sequence (20 kilobases) of the polyprotein-encoding gene 1 of transmissible gastroenteritis virus. Virology 1995; 206:817–822.PubMedCrossRefGoogle Scholar
  26. 26.
    Escoubas J, Prere M, Fayet O et al. Translational control of transposition activity of the bacterial insertion sequence IS1. EMBO J 1991; 10:705–712.PubMedGoogle Scholar
  27. 27.
    Falk H, Mador N, Udi R et al. Two cisacting signals control ribosomal frameshift between human T-cell leukemia virus type II gag and pro genes. J Virol 1993; 67:6273–6277.PubMedGoogle Scholar
  28. 28.
    Farabaugh P. Post-transcriptional regulation of transposition by Ty retrotransposons of Saccharomyces cerevisiae. J Biol Chem 1995; 270:10361–10364.PubMedGoogle Scholar
  29. 29.
    Felsenstein K, Goff S. Expression of the gag-pol fusion protein of Moloney murine leukemia virus without gag protein does not induce virion formation or proteolytic processing. J Virol 1988; 62:2179–2182.PubMedGoogle Scholar
  30. 30.
    Flower AM, McHenry CS. The γ subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci USA 1990; 87:3713–3717.PubMedCrossRefGoogle Scholar
  31. 31.
    Godeny EK, Chen L, Kumar SN et al. Complete genomic sequence and phylogenetic analysis of the lactate dehydrogenaseelevating virus (LDV). Virology 1993; 194:585–596.PubMedCrossRefGoogle Scholar
  32. 32.
    Harrell CM, McKenzie AR, Patino MM et al. Ferritin mRNA: Interactions of iron regulatory element with translational regulator protein P-90 and the effect on basepaired flanking regions. Proc Natl Acad Sci USA 1991; 88:4166–4170.PubMedCrossRefGoogle Scholar
  33. 33.
    Hatfield DL, Levin JG, Rein A et al. Translational suppression in retroviral gene expression. Adv Virus Res 1992; 41:193–239.PubMedCrossRefGoogle Scholar
  34. 34.
    He F, Jacobson A. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev 1995; 9:437–454.PubMedCrossRefGoogle Scholar
  35. 35.
    Herold J, Siddell SG. An ‘elaborated’ pseudoknot is required for high frequency frameshifting during translation of HCV 229E polymerase mRNA. Nucleic Acids Res 1993; 21:5838–5842.PubMedCrossRefGoogle Scholar
  36. 36.
    Hyun NS, Copeland TD, Hatanaka M et al. Characterization of ribosomal frameshifting for expression of pol gene products of human T-cell leukemia virus type I. J Virol 1993; 67:196–203.Google Scholar
  37. 37.
    Icho T, Wickner RB. 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 1989; 264:6716–6723.PubMedGoogle Scholar
  38. 38.
    Inglis S, Rolley N, Brierley I. The ribosomal frame-shift signal of infectious bronchitis virus. In: McCarthy J, Tuite M, eds. Post-Transcriptional Control of Gene Expression. Berlin: Springer-Verlag, 1990: 603–610.CrossRefGoogle Scholar
  39. 39.
    Jacks T. Translational suppression in gene expression in retroviruses and retrotransposons. Curr Top Microbiol Immunol 1990; 157:93–124.PubMedCrossRefGoogle Scholar
  40. 40.
    Jacks T, Madhani HD, Masiarz FR et al. Signals for ribosomal frameshifting in the Rous Sarcoma virus gag-pol region. Cell 1988; 55:447–458.PubMedCrossRefGoogle Scholar
  41. 41.
    Jacks T, Power MD, Masiarz FR et al. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 1988; 331:280–283.PubMedCrossRefGoogle Scholar
  42. 42.
    Jacks T, Townsley K, Varmus HE et al. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci USA 1987; 84:4298–4302.PubMedCrossRefGoogle Scholar
  43. 43.
    Jacks T, Varmus HE. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science 1985; 230:1237–1242.PubMedCrossRefGoogle Scholar
  44. 44.
    Jiang B, Monroe SS, Koonin EV et al. RNA sequence of astrovirus: distinctive genomic organization and a putative retrovirus-like ribosomal frameshifting signal that directs the viral replicase synthesis. Proc Natl Acad Sci USA 1993; 90:10539–10543.PubMedCrossRefGoogle Scholar
  45. 45.
    Kang HS, Hines JV, Tinoco I, Jr. Conformation of a nonframeshifting RNA pseudoknot from mouse mammary tumor virus. J Mol Biol 1996; 259:135–147.PubMedCrossRefGoogle Scholar
  46. 46.
    Kawakami K, Pande S, Faiola B et al. A rare tRNA-Arg(CCU) that regulates Tyl element ribosomal frameshifting is essential for Tyl retrotransposition in Saccharomyces cerevisiae. Genetics 1993; 135:309–320.PubMedGoogle Scholar
  47. 47.
    Kim KH, Lommel SA. Identification and analysis of the site of −1 ribosomal frameshifting in red clover necrotic mosaic virus. Virology 1994; 200:574–582.PubMedCrossRefGoogle Scholar
  48. 48.
    Kirchner J, Sandmeyer S, Forrest D. Transposition of a Ty3 GAG3-POL3. fusion mutant is limited by availability of capsid protein. J Virol 1992; 66:6081–6092.Google Scholar
  49. 49.
    Kollmus H, Hentze M, Hauser H. Regulated ribosomal frameshifting by an RNA-protein interaction. RNA 1996; 2:316–323.PubMedGoogle Scholar
  50. 50.
    Kropinski AM, Farinha MA, Jansons I. Nucleotide sequence of the Pseudomonas aeruginosa insertion sequence IS222: another member of the IS3 family. Plasmid 1994; 31:222–228.PubMedCrossRefGoogle Scholar
  51. 51.
    Kuhn TS. The Structure of Scientific Revolutions. Chicago: University of Chicago Press, 1970.Google Scholar
  52. 52.
    Le SY, Chen JH, Maizel JV. Thermodynamic stability and statistical significance of potential stem-loop structures situated at the frameshift sites of retroviruses. Nucleic Acids Res 1989; 17:6143–52.PubMedCrossRefGoogle Scholar
  53. 53.
    Lee S, Urnen J, Varmus H. A genetic screen identifies cellular factors involved in retroviral −1 frameshifting. Proc Natl Acad Sci USA 1995; 92:6587–6591.PubMedCrossRefGoogle Scholar
  54. 54.
    Levin ME, Hendrix RW, Casjens SR. A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. J Mol Biol 1993; 234:124–139.PubMedCrossRefGoogle Scholar
  55. 55.
    Madhani HD, Jacks T, Varmus HE. Signals for the expression of the HIV pol gene by ribosomal frameshifting. In: Franza BR, Cullen BR, Wong-Staal F, eds. The Control of Human Retrovirus Gene Expression. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1988:119–125.Google Scholar
  56. 56.
    Makinen K, Næss V, Tamm T et al. The putative replicase of the cocksfoot mottle sobemovirus is translated as a part of the polyprotein by −1 ribosomal frameshift. Virology 1995; 207:566–571.PubMedCrossRefGoogle Scholar
  57. 57.
    Marczinke B, Bloys AJ, Brown TD et al. The human astrovirus RNA-dependent RNA polymerase coding region is expressed by ribosomal frameshifting. J Virol 1994; 68:5588–5595.PubMedGoogle Scholar
  58. 58.
    Marlor RL, Parkhurst SM, Corces VG. The Drosophila melanogaster gypsy transposable element encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 1986; 6:1129–1134.PubMedGoogle Scholar
  59. 59.
    Maurer B, Bannert H, Darai G et al. Analysis of the primary structure of the long terminal repeat and the gag and pol genes of the human spumaretrovirus. J Virol 1988; 62:1590–1597.PubMedGoogle Scholar
  60. 60.
    Menninger J. Ribosome editing and the error catastrophe hypothesis of cellular aging. Mech Ageing Dev 1977; 6:131–142.PubMedCrossRefGoogle Scholar
  61. 61.
    Meulenberg JJ, Hulst MM, de Meijer EJ et al. Lelystad virus, the causative agent of porcine epidemic abortion and respiratory syndrome (PEARS), is related to LDV and EAV. Virology 1993; 192:62–72.PubMedCrossRefGoogle Scholar
  62. 62.
    Miller WA, Waterhouse PM, Gerlach WL. Sequence and organization of barley yellow dwarf virus genomic RNA. Nucleic Acids Res 1988; 16:6097–6111.PubMedCrossRefGoogle Scholar
  63. 63.
    Morikawa S, Bishop DHL. Identification and analysis of the gag-pol ribosomal frameshift site of feline immunodeficiency virus. Virology 1992; 186:389–397.PubMedCrossRefGoogle Scholar
  64. 64.
    Nam S, Copeland T, Hatanaka M et al. Characterization of ribosomal frameshifting for expression of pol gene products of human T-cell leukemia virus type I. J Virol 1993; 67:196–203.PubMedGoogle Scholar
  65. 65.
    Palmer E, Wilhelm JM, Sherman F. Phenotypic suppression of nonsense mutants in yeast by aminoglycoside antibiotics. Nature 1979; 277:148–150.PubMedCrossRefGoogle Scholar
  66. 66.
    Panet A, Baltimore D, Hanafusa T. Quantitation of avian RNA tumor virus reverse transcriptase by radioimmunoassay. J Virol 1975; 16:146–152.PubMedGoogle Scholar
  67. 67.
    Park J, Morrow CD. Overexpression of the gag-pol precursor from human immunodeficiency virus type 1 proviral genomes results in efficient poteolytic processing in the absence of virion production. J Virol 1992; 65:5111–5117.Google Scholar
  68. 68.
    Parkin N, Chamorro M, Varmus H. Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on a downstream mRNA secondary structure: demonstration by expression in vivo. J Virol 1992; 66:5147–5151.PubMedGoogle Scholar
  69. 69.
    Pinto I, Na JG, Sherman F et al. cis-and trans-acting suppressors of a translation initiation defect at the cycl locus of Saccharomyces cerevisiae. Genetics 1992; 132:97–112.PubMedGoogle Scholar
  70. 70.
    Pleij CW, Rietveld K, Bosch L. A new principle of RNA folding based on pseudoknotting. Nucleic Acids Res 1985; 13:1717–1731.PubMedCrossRefGoogle Scholar
  71. 71.
    Polard P, Prère MF, Chandler M et al. Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J Mol Biol 1991; 222:465–477.PubMedCrossRefGoogle Scholar
  72. 72.
    Priimagi AF, Mizrokhi LJ, Ilyin YV. The Drosophila mobile element jockey belongs to LINEs and contains coding sequences homologous to some retroviral proteins. Gene 1988; 70:253–262.PubMedCrossRefGoogle Scholar
  73. 73.
    Prüfer D, Tacke E, Schmitz J et al. Ribosomal frameshifting in plants: A novel signal directs the −1 frameshift in the synthesis of the putative viral replicase of potato leafroll luteovirus. EMBO J 1992; 11:1111–1117.PubMedGoogle Scholar
  74. 74.
    Reil H, Kollmus H, Weidle UH et al. A heptanucleotide sequence mediates ribosomal frameshifting in mammalian cells. J Virol 1993; 67:5579–5584.PubMedGoogle Scholar
  75. 75.
    Rezsohazy R, Hallet B, Mahillon J et al. IS231V and W from Bacillus thuringiensis subsp. israelensis, two distant members of the IS231 family of insertion sequences. Plasmid 1993; 30:141–149.PubMedCrossRefGoogle Scholar
  76. 76.
    Saigo K, Kugimiya W, Matsuo Y et al. Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature 1984; 312:659–661.PubMedCrossRefGoogle Scholar
  77. 77.
    Sekine U, Ohtsubo E. Frameshifting is required for production of the transposase encoded by insertion sequence 1. Proc Natl Acad Sci USA 1989; 86:4609–4613.PubMedCrossRefGoogle Scholar
  78. 78.
    Shen LX, Tinoco I, Jr. The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumor virus. J Mol Biol 1995; 247:963–978.PubMedCrossRefGoogle Scholar
  79. 79.
    Singh A, Ursic D, Davies J. Phenotypic suppression and misreading in Saccharomyces cerevisiae. Nature 1979; 277:146–148.PubMedCrossRefGoogle Scholar
  80. 80.
    Snijder EJ, den Boon JA, Bredenbeek PJ et al. The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro-and coronaviruses are evolutionarily related. Nucleic Acids Res 1990; 18:4535–4542.PubMedCrossRefGoogle Scholar
  81. 81.
    Somogyi P, Jenner AJ, Brierley I et al. Ribosomal pausing during translation of an RNA pseudoknot. Mol Cell Biol 1993; 13:6931–6940.PubMedGoogle Scholar
  82. 82.
    Steibl HD, Lewecke FM. IS1222: analysis and distribution of a new insertion sequence in Enterobacter agglomerans 339. Gene 1995; 156:37–42.PubMedCrossRefGoogle Scholar
  83. 83.
    Stromberg K, Hurley NE, Davis NL et al. Structural studies of avian myeloblastosis virus: comparison of polypeptides in virion and core component by dodecyl sulfate-polyacrylamide gel electrophoresis. J Virol 1974; 13:513–528.PubMedGoogle Scholar
  84. 84.
    ten Dam E, Brierley I, Inglis S, Pleij C. Identification and analysis of the pseudo-knot-containing gag-pro ribosomal frameshift signal of simian retrovirus-1. Nucleic Acids Res 1994; 22:2304–2310.PubMedCrossRefGoogle Scholar
  85. 85.
    ten Dam E, Pleij C, Bosch L. RNA pseudoknots: translational frameshifting and readthrough of viral RNAs. Virus Genes 1990; 4:121–136.PubMedCrossRefGoogle Scholar
  86. 86.
    ten Dam E, Verlaan P, Pleij C. Analysis of the role of the pseudoknot component in the SRV-1 gag-pro ribosomal frameshift signal: loop lengths and stability of the stem regions. RNA 1995; 1:146–154.PubMedGoogle Scholar
  87. 87.
    Thompson RC, Dix DB, Eccleston JF. Single turnover kinetic studies of guanosine triphosphate hydrolysis and peptide formation in the elongation factor Tu-dependent binding of aminoacyl-tRNA to Escherichia coli ribosomes. J Biol Chem 1980; 255:11088–11090.PubMedGoogle Scholar
  88. 88.
    Tsuchihashi Z. Translational frameshifting in the Escherichia coli dnaX gene in vitro. Nucleic Acids Res 1991; 19:2457–2462.PubMedCrossRefGoogle Scholar
  89. 89.
    Tsuchihashi Z, Kornberg A. Translational frameshifting generates the γ subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci USA 1990; 87:2516–2520.PubMedCrossRefGoogle Scholar
  90. 90.
    Tu C, Tzeng TH, Bruenn JA. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc Natl Acad Sci USA 1992; 89:8636–8640.PubMedCrossRefGoogle Scholar
  91. 91.
    Turner DH, Sugimoto N. RNA structure prediction. Annu Rev Biophys Biophys Chem 1988; 17:167–92.PubMedCrossRefGoogle Scholar
  92. 92.
    Tzeng T-H, Tu C-L, Bruenn JA. Ribosomal frameshifting requires a pseudoknot in the Saccharomyces cerevisiae double-stranded RNA virus. J Virology 1992; 66:999–1006.PubMedGoogle Scholar
  93. 93.
    Van Ryk D, Lee Y, Nazar R. Efficient expression and utilization of a mutant 5S rRNA in Saccharomyces cerevisiae. J Biol Chem 1990; 265:8377–8381.PubMedGoogle Scholar
  94. 94.
    Vögele K, Schwartz E, Welz C et al. Highlevel ribosomal frameshifting directs the synthesis of IS150 gene products. Nucleic Acids Res 1991; 19:4377–4385.PubMedCrossRefGoogle Scholar
  95. 95.
    Walker DC, Klaenhammer TR. Isolation of a novel IS3 group insertion element and construction of an integration vector for Lactobacillus spp. J Bacteriol 1994; 176:5330–5340.PubMedGoogle Scholar
  96. 96.
    Wang AL, Yang HM, Shen KA et al. Giardiavirus double-stranded RNA genome encodes a capsid polypeptide and a gag-pollike fusion protein by a translation frameshift. Proc Natl Acad Sci USA 1993; 90:8595–8599.PubMedCrossRefGoogle Scholar
  97. 97.
    Weiss RB, Dunn DM, Shuh M et al. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol 1989; 1:159–169.PubMedGoogle Scholar
  98. 98.
    Wickner R. Yeast virology. FASEB J 1989; 3:2257–2265.PubMedGoogle Scholar
  99. 99.
    Willcocks MM, Brown TD, Madeley CR et al. The complete sequence of a human astrovirus. J Gen Virol 1994; 75:1785–1788.PubMedCrossRefGoogle Scholar
  100. 100.
    Wilson W, Braddock M, Adams SE et al. HIV expression strategies: ribomal frameshifting is directed by a short sequence in both mammalian and yeast systems. Cell 1988; 55:1159–1169.PubMedCrossRefGoogle Scholar
  101. 101.
    Wolin SL, Walter P. Ribosome pausing and stacking during translation of a eukaryotic mRNA. EMBO J 1988; 7:3559–3569.PubMedGoogle Scholar
  102. 102.
    Wyatt JR, Puglisi JD, Tinoco I, Jr. RNA pseudoknots. Stability and loop size requirements. J Mol Biol 1990; 214:455–470.PubMedCrossRefGoogle Scholar
  103. 103.
    Xiong Z, Lommel SA. The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1. Virology 1989; 171:543–554.PubMedCrossRefGoogle Scholar
  104. 104.
    Xu H, Boeke JD. Host genes that influence transposition in yeast: the abundance of a rare tRNA regulates Tyl transposition frequency. Proc Natl Acad Sci USA 1990; 87:8360–8364.PubMedCrossRefGoogle Scholar
  105. 105.
    Yelverton E, Lindsley D, Yamauchi P et al. The function of a ribosomal frameshifting signal from human immunodeficiency virus-1 in Escherichia coli. Mol Microbiol 1994; 11:303–313.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1997

Authors and Affiliations

  • Philip J. Farabaugh
    • 1
  1. 1.Department of Biological SciencesUniversity of Maryland Baltimore CountyBaltimoreUSA

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