Abstract
New examples of high-level ribosomal frameshift and readthrough events have been described over the past year and a half. These include −1 frameshifiting at tandem codons and + 1 frameshifiting at neighboring slow codons. Several bizarre examples of ribosome jumping and multiple stop-codon readthrough continue to perplex investigators in this field.
Abbreviations: carA-carbamoylphosphate synthetase, IS-insertion sequence, ORF-open reading frame, RF-release factor, TMV-tobacco mosaic virus, UTR-untranslated region
References
- 1.Flower A.M., McHenry C.S. Vol. 87. 1990. The Gamma Subunit of DNA Polymerase III Holoenzyme of E. coli is Produced by Ribosomal Frameshifting; pp. 3713–3717. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Blinkowa A.L., Walker J.R. Programmed Ribosomal Frameshifting Generates the E coli DNA Polymerase III Gamma Subunit from Within the Tau Subunit Reading Frame. Nucleic Acids Res. 1990;18:1725–1729. doi: 10.1093/nar/18.7.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Tsuchihashi Z., Kornberg A. Vol. 87. 1990. Translational Frameshifting Generates the Gamma Subunit of DNA Polymerise III Holoenzyme; pp. 2516–2520. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Weiss R.B., Dunn D.M., Shuh M., Atkins J.F., Gesteland R.F. E. coli Ribosomes Re-phase on Retroviral Frameshift Signals at Rates Ranging from 2 to 50 Percent. New Biol. 1989;1:159–169. [PubMed] [Google Scholar]
- 5.Jacks T., Madhani H.D., Masiarz F.R., Varmus H. Signals for Ribosomal Frameshifting in the Rous Sarcoma Virus Gag-Pol Region. Cell. 1988;55:447–458. doi: 10.1016/0092-8674(88)90031-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Tsuchihashi Z. Translational Frameshifting in the E. coli dnaX Gene In Vitro. Nucleic Acids Res. 1991;19:2457–2462. doi: 10.1093/nar/19.9.2457. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Galas D., Chandler M. Bacterial Insertion Sequences. In: Berg D.E., Howe M., editors. Mobile DNA 1989. American Society for Microbiology; Washington DC: 1989. pp. 109–162. [Google Scholar]
- 8.Sekine Y., Ohtsudo E. Vol. 86. 1989. Frameshifting is Required for Production of the Transposase Encoded by Insertion Sequence 1; pp. 4609–4613. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Esciioriias I.M., Prere M.F., Fayet O., Salnignol I., Galas D., Zerbib D., Chandler M. Translational Control of Transposition Activity of the Bacterial Insertion Sequence ISI. EMBO J. 1991;10(3):705–712. doi: 10.1002/j.1460-2075.1991.tb08000.x. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Thorough physical and genetic evaluation of the expression and control of ISI Iransposase activity. In vivo alteration of the level of ORFA-B versus ORFA activity demonstrates it is the ratio of these two products, and not their absolute levels, that detennine the transposition frequency of ISI.
- 10.Luthi K., Moser M., Ryser J., Weber H. Evidence for a Role of Translational Frameshifting in the Expression of Transposition Activity of the Bacterial Insertion Element ISI. Genre. 1990;88:15–20. doi: 10.1016/0378-1119(90)90054-u. [DOI] [PubMed] [Google Scholar]
- 11.Polard P., Prere M.F., Chandler M., Fayet O. Programmed Translational Frameshifting and Initiation at an AUU Codon in Gene Expression of Bacterial Insertion Sequence IS911. J Mol Biol. 1991 doi: 10.1016/0022-2836(91)90490-w. of outstanding interest. in press. [DOI] [PubMed] [Google Scholar]; A more complex and high-level - I frameshift window- from IS911 is partially dissected. Both 5′ and 3′ flanking elements appear to be involved in stimulating an Ai,G motif. Interesting amino acid sequence homology between ORES and retroviral integrase is discussed.
- 12.Weiss R.B., Dunn D.M., Atkins J.F., Gesitiand R.F. Ribosomal Frameshifting from −2 to + 50 Nucleotides. Prog Nucleic Acids Res Mol Biol. 1990;39:159–183. doi: 10.1016/s0079-6603(08)60626-1. [DOI] [PubMed] [Google Scholar]
- 13.Sipley J., Stassi D., Dunn J., Goldatan E. Analysis of Bacteriophage 17 Gene 10A and Frameshifted 108 Proteins. Gene Fxpression. 1991;1(2):127–136. [PMC free article] [PubMed] [Google Scholar]
- 14.Condron B.G., Gesteland R.F., Atkins J.F. Studies of Frameshifting in Gene 10 of Bacteriophage T7. J Bacleriol. 1991;173(21):6998–7003. doi: 10.1128/jb.173.21.6998-7003.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Dinman J.D., Icho T., Wickner R.B. Vol. 88. 1991. A - 1 Ribosomal Frameshift in a Double-Stranded RNA Virus of Yeast Forms a Gag-Pot Fusion Protein; pp. 174–178. (Proc Nalt Acad Sci USA). of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Compensating mutations suggest that h type pseudoknot formation spaced four nucleotides 3′ of a G-GGU-L3LIA motif stimulates −1 frameshifting at a 2% level in S. cerevisiae. Other heptamer motifs in this context can yield up to 12% frameshifting.
- 16.Lee F.I.J., Shish C.K., Gorbalenya A.E., Koonin E.V., Iamonica N., Tuler J., Bagdzhazyzhyan K., Lai M.M.C. The Complete Sequence (22 Kilobases) of Murine Coronavirus Gene 1 En coding the Putative Proteases and RNA Polymerase. Virology. 1991;180:567–582. doi: 10.1016/0042-6822(91)90071-I. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Den Boon J.A., Snijder E.J., Chrinsidf E.D., De Vries A.A.F., Horzinek M.C., Spaan W.L.M. Equine Arteritis Virus is not a Togavirus but Belongs to the Coronavirus-Like Superfamily. J Virology. 1991;65:2910–2920. doi: 10.1128/jvi.65.6.2910-2920.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Brierly I.P., Rouey N.J., Jenner A.J., Inghs S.C. Mutational Analysis of the RNA Pseudoknot Component of a Coronavirus Ribosomal Frameshifting Signal. J Mol Biol. 1991;220(4):889–902. doi: 10.1016/0022-2836(91)90361-9. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Extensive mutational analysis of the 3′ pseudoknot requirement for -frameshifting in the infectious bronchitis virus ORFI-2 overlap using in vitro translation in rabbit reticulocyte lysates. Minimum and maximum loop sizes are determined and stem base pairs are probed.
- 19.Themorro M., Parkin N., Varmus F.I.E. 1991. An RNA Pseudoknot and an Optimal Heptameric Shift Site are Required for Highly Efficient Ribosomal Frameshifting on a Retroviral mRNA. (Proc Nalt Acad Sci USA). of interest. in press. [DOI] [PMC free article] [PubMed] [Google Scholar]; The 3′ stimulator in the mouse mammary tumor virus gag-pro overlap is shown, by compensating mutations, to he a pseudoknot. The malleability of the heptamer motif is also examined.
- 20.Belcotirt M.F., Farabagh P.J. Ribosomal Frameshifting in the Yeast Retrotransposon Ty: Transfer RNAs Induce Slippage on a Z-Nucleotide Minimal Site. Cell. 1990;62(2):339–352. doi: 10.1016/0092-8674(90)90371-K. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; The + I frameshift in Tyl is narrowed down to just seven nucleotides. Additionally, the detailed mechanism is examined in terms of both the ability of yeast tRNALeu(AUG) to form base pairs with both CLIP and UIJA leucine cottons, and the speed of decoding by a rare tRNAArg.
- 21.Xu H., Boeke J.D. Host Genes that Influence Transposition in Yeast: the Abundance of a Rare tRNA Regulates TyI Transposition Frequency. Proc Natl Acad Sci USA. 1990;87:8360–11364. doi: 10.1073/pnas.87.21.8360. of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Elegant genetic selection demonstrating that Tyl transposition frequency can be altered by changing the rate of frameshifting.
- 22.Curran J.F., Yarus M. Use of tRNA Suppressors to Probe Regulation of E. coli Release Factor 2. J Mol Biol. 1988;203:75–83. doi: 10.1016/0022-2836(88)90092-7. [DOI] [PubMed] [Google Scholar]
- 23.Donly C., Williams J., Richardson C., Tate W. Frameshifting at the Internal Stop Codon Within the mRNA for Bacterial Release Factor 2 on Eukaryotic Ribosomes. Biochem Biophys Acta. 1990;1050(1–3):283–287. doi: 10.1016/0167-4781(90)90182-2. [DOI] [PubMed] [Google Scholar]
- 24.Kawakami K., Nakamura Y. Vol. 87. 1990. Autogenous Suppression of an Opal Mutation in the Gene Encoding Peptide Chain Release Factor 2; pp. 8432–8436. (Proc Natl Acad Sci USA). of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; A TGA mutation within the protein that recognizes TGA; the Klein bottle equivalent amongst intrtgenic suppressors.
- 25.Weiss R.B., Huang W.M., Dunn D.M. A Nascent Peptide Chain is Required for Ribosomal Bypass of the Coding Gap in Bacteriophage T4 Gene 60. Cell. 1990;62:117–126. doi: 10.1016/0092-8674(90)90245-A. of outstanding interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Novel effect of a nascent peptide sequence stimulating the 50-nucleotide jump across the gene 60 coding gap within a lord. fusion. Other major sequence elements within the coding gap are defined in terms of a tRNA hopping mechanism, whose beginning and end points are somehow defined by a stop colon, short stem and optimal gap size.
- 26.Atkins J.A., Weiss R.B., Gesteland R.E. Ribosome Gymnastics Degree of Difficulty 9.5, Style 10.0. Cell. 1990;62(2):413–423. doi: 10.1016/0092-8674(90)90007-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Huang W.M., Ao S., Casjens S., Orlandi R., Zeikus R., Weiss R., Wince D., Fang M. A Persistent Untranslated Sequence Within Bacteriophage T4 DNA Topoisomerase Gene 60. Science. 1988;239:1005–1012. doi: 10.1126/science.2830666. [DOI] [PubMed] [Google Scholar]
- 28.Burke-Aguero DH, Hearst JE.: An RNA HoUiday Junction? Structural and Dynamic Considerations of the Bacteriophage T4 Gene 60 Interruption. J Mol Biol 213:199–201. [DOI] [PubMed]
- 29.Wong S.C., Abdeial A.T. Unorthodox Expression of an Enzymc: Evidence for an Untranslated Region Within carA of Pseudomonas aeruginosa. J Bacleriol. 1990;172:630–642. doi: 10.1128/jb.172.2.630-642.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Kane P.M., Yamashiro C.T., Wolxczyk D.F., Neff N., Goebl M., Stevens T.H. Protein Splicing Converts the Yeast TFP1 Gene Product to the 60-kD Subunit of the Vacuolar H+-Adenosine Triphosphatase. Science. 1990;250:651–657. doi: 10.1126/science.2146742. [DOI] [PubMed] [Google Scholar]
- 31.Skuizeski J.M., Nichois L.M., Gesteiand R.E., Atkins J.F. The Signal for a Leaky UAG Stop Codon in Several Plant Viruses Includes the Two Downstream Codons. J Mol Biol. 1991;218(2):365–373. doi: 10.1016/0022-2836(91)90718-l. [DOI] [PubMed] [Google Scholar]
- 32.Feng Y.-X., Copeland T.D., Oroszian S., Rein A., Levin J.G. Vol. 87. 1990. pp. 8860–8863. (Proc Natl Acad Sci USA). [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Willis N.M., Gesteland R.F., Atkins J.F. Vol. 88. 1991. Evidence that a Down stream Pseudoknot is Required for Translational Readthrough of the Moloney Murine Leukemia Virus gag Stop Codon; pp. 6991–6995. (Proc Natl Acad Sci USA). of interest. [DOI] [PMC free article] [PubMed] [Google Scholar]; Readthrough of the UAG stop from Moloney murine leukemia virus gag-pol is shown to require the formation of 3′ pseudoknots, which are analogous to structures that stimulate −1 frameshifting.
- 34.Honign1an A., Wolf D., Yaish S., Falk H., Panet A. Cis Acting RNA Sequences Control the gag-pot Translation Readthrough in Murine Leukemia Virus. Virology. 1991;183:313–319. doi: 10.1016/0042-6822(91)90144-Z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Ten Dani E.B., Pleij C.W.A., Bosch L. RNA Pseudoknots: Translational Frameshifting and Readthrough on Viral RNAs. Virus Genes. 1990;4(2):121–136. doi: 10.1007/BF00678404. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Hilj K.E., Lloyd R.S., Yang J.-G., Read R., Burk R.F. The cDNA for Rat Selenoprotein P Contains 10 TGA Colons in the Open Reading Frame. J Biol Chem. 1991;266(16):10050–10053. of outstanding interest. [PubMed] [Google Scholar]; Cloning and sequencing reveals 10 TGA colons that apparently encode selenocysteine. Protein sequencing of several peptide fragments of selenoprotein P confirm the content of a large portion of the postulated ORF. The mechanism and efficiency of decoding this ORF are unknown.
- 37.Zinoni F., Heider J., Bock A. Vol. 87. 1990. Features of the Formate Dehydrogenase mRNA Necessary for Decoding of the UGA Codon as Selenocysteine; pp. 4660–4664. (Proc Natl Acad Sci USA). of interst. [DOI] [PMC free article] [PubMed] [Google Scholar]; Selenocysteine insertion is shown to be dependent on local mRNA sequence. As many as 40 nucleotides 3′ are required and eight nucleotides 5′ enhance seleno cysteine incorporation. Additionally, this LIGA cotton is shown to he non-leaky and not easily suppressed by conventional UGAGA Suppressor tRNAS.
- 38.Berry M.J., Banu L., Chen Y., Mandel S.J., Kieffer J.D., Harney J.W., Larsen P.R. Recognition of UGA as a Selenocysteine Codon in Type I Deiodinase Requires Sequences in the 3′ Untranslated Region. Nature. 1991;353:273–276. doi: 10.1038/353273a0. of outstanding interest. [DOI] [PubMed] [Google Scholar]; Transient in vivo assays in COS cells and Xenopusocchtes demonstrate that a 3′ LJTR is required for expression of rat and human deiodinase activity. The loss of activity caused by deletion of the 3'-UTR can be restored by inserting a 3′ UTR from the rat glutathione peroxidase gene.
