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Nucleic Acids Res. Apr 25, 1993; 21(8): 1837–1843.
PMCID: PMC309422

Analysis of effects of tRNA:message stability on frameshift frequency at the Escherichia coli RF2 programmed frameshift site.


The codon that is in-frame prior to +1 frameshifting at the E.coli prfB (RF2 gene) frameshift site is randomized to create thirty-two variants. These alleles vary 1000-fold in frameshift-dependent expression in fusions to lacZ. Frameshifting is more frequent at sites where the in-frame codon ends in uridine, as if third position wobble pairs to message uridine facilitate slippage into the +1 frame. Consistent with other studies of programmed frameshift sites, efficient frameshifting depends on stable message:tRNA base pairs after rephasing. For complexes with mispairs, frameshift frequency depends on the nature, number, and position of mispairs. Central purine:purine mispairs are especially inhibitory. Relative stabilities of +1 rephased complexes are estimated from published data on the stabilities of tRNA:tRNA complexes. Stability correlates with frameshifting over its entire range, which suggests that stability is an important determinant of the probability of translation of the rephased complex.

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  • Atkins JF, Weiss RB, Gesteland RF. Ribosome gymnastics--degree of difficulty 9.5, style 10.0. Cell. 1990 Aug 10;62(3):413–423. [PubMed]
  • Hatfield D, Oroszlan S. The where, what and how of ribosomal frameshifting in retroviral protein synthesis. Trends Biochem Sci. 1990 May;15(5):186–190. [PubMed]
  • Craigen WJ, Cook RG, Tate WP, Caskey CT. Bacterial peptide chain release factors: conserved primary structure and possible frameshift regulation of release factor 2. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3616–3620. [PMC free article] [PubMed]
  • Mellor J, Fulton SM, Dobson MJ, Wilson W, Kingsman SM, Kingsman AJ. A retrovirus-like strategy for expression of a fusion protein encoded by yeast transposon Ty1. Nature. 1985 Jan 17;313(5999):243–246. [PubMed]
  • Clare J, Farabaugh P. Nucleotide sequence of a yeast Ty element: evidence for an unusual mechanism of gene expression. Proc Natl Acad Sci U S A. 1985 May;82(9):2829–2833. [PMC free article] [PubMed]
  • Jacks T, Madhani HD, Masiarz FR, Varmus HE. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988 Nov 4;55(3):447–458. [PubMed]
  • 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 U S A. 1991 Jan 1;88(1):174–178. [PMC free article] [PubMed]
  • den Boon JA, Snijder EJ, Chirnside ED, de Vries AA, Horzinek MC, Spaan WJ. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol. 1991 Jun;65(6):2910–2920. [PMC free article] [PubMed]
  • Blinkowa AL, Walker JR. Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res. 1990 Apr 11;18(7):1725–1729. [PMC free article] [PubMed]
  • Flower AM, McHenry CS. The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci U S A. 1990 May;87(10):3713–3717. [PMC free article] [PubMed]
  • Tsuchihashi Z, Kornberg A. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2516–2520. [PMC free article] [PubMed]
  • Condron BG, Atkins JF, Gesteland RF. Frameshifting in gene 10 of bacteriophage T7. J Bacteriol. 1991 Nov;173(21):6998–7003. [PMC free article] [PubMed]
  • Sipley J, Stassi D, Dunn J, Goldman E. Analysis of bacteriophage T7 gene 10A and frameshifted 10B proteins. Gene Expr. 1991 May;1(2):127–136. [PubMed]
  • Vögele K, Schwartz E, Welz C, Schiltz E, Rak B. High-level ribosomal frameshifting directs the synthesis of IS150 gene products. Nucleic Acids Res. 1991 Aug 25;19(16):4377–4385. [PMC free article] [PubMed]
  • ten Dam EB, Pleij CW, Bosch L. RNA pseudoknots: translational frameshifting and readthrough on viral RNAs. Virus Genes. 1990 Jul;4(2):121–136. [PubMed]
  • Brierley I, Rolley NJ, Jenner AJ, Inglis SC. Mutational analysis of the RNA pseudoknot component of a coronavirus ribosomal frameshifting signal. J Mol Biol. 1991 Aug 20;220(4):889–902. [PubMed]
  • Tsuchihashi Z. Translational frameshifting in the Escherichia coli dnaX gene in vitro. Nucleic Acids Res. 1991 May 11;19(9):2457–2462. [PMC free article] [PubMed]
  • Tu C, Tzeng TH, Bruenn JA. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8636–8640. [PMC free article] [PubMed]
  • Craigen WJ, Caskey CT. Expression of peptide chain release factor 2 requires high-efficiency frameshift. Nature. 1986 Jul 17;322(6076):273–275. [PubMed]
  • Curran JF, Yarus M. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol. 1989 Sep 5;209(1):65–77. [PubMed]
  • Belcourt MF, Farabaugh PJ. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990 Jul 27;62(2):339–352. [PubMed]
  • Pedersen WT, Curran JF. Effects of the nucleotide 3' to an amber codon on ribosomal selection rates of suppressor tRNA and release factor-1. J Mol Biol. 1991 May 20;219(2):231–241. [PubMed]
  • Weiss RB, Dunn DM, Dahlberg AE, Atkins JF, Gesteland RF. Reading frame switch caused by base-pair formation between the 3' end of 16S rRNA and the mRNA during elongation of protein synthesis in Escherichia coli. EMBO J. 1988 May;7(5):1503–1507. [PMC free article] [PubMed]
  • Weiss RB, Dunn DM, Atkins JF, Gesteland RF. Slippery runs, shifty stops, backward steps, and forward hops: -2, -1, +1, +2, +5, and +6 ribosomal frameshifting. Cold Spring Harb Symp Quant Biol. 1987;52:687–693. [PubMed]
  • Jacks T, Townsley K, Varmus HE, Majors J. Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4298–4302. [PMC free article] [PubMed]
  • Moore R, Dixon M, Smith R, Peters G, Dickson C. Complete nucleotide sequence of a milk-transmitted mouse mammary tumor virus: two frameshift suppression events are required for translation of gag and pol. J Virol. 1987 Feb;61(2):480–490. [PMC free article] [PubMed]
  • 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 Oct 25;19(20):5607–5612. [PMC free article] [PubMed]
  • Brierley I, Jenner AJ, Inglis SC. Mutational analysis of the "slippery-sequence" component of a coronavirus ribosomal frameshifting signal. J Mol Biol. 1992 Sep 20;227(2):463–479. [PubMed]
  • Freier SM, Kierzek R, Jaeger JA, Sugimoto N, Caruthers MH, Neilson T, Turner DH. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9373–9377. [PMC free article] [PubMed]
  • Grosjean HJ, de Henau S, Crothers DM. On the physical basis for ambiguity in genetic coding interactions. Proc Natl Acad Sci U S A. 1978 Feb;75(2):610–614. [PMC free article] [PubMed]
  • 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 U S A. 1992 Jan 15;89(2):713–717. [PMC free article] [PubMed]
  • Weiss RB, Dunn DM, Shuh M, Atkins JF, Gesteland RF. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol. 1989 Nov;1(2):159–169. [PubMed]
  • Hatfield D, Feng YX, Lee BJ, Rein A, Levin JG, Oroszlan S. Chromatographic analysis of the aminoacyl-tRNAs which are required for translation of codons at and around the ribosomal frameshift sites of HIV, HTLV-1, and BLV. Virology. 1989 Dec;173(2):736–742. [PubMed]
  • Curran JF, Yarus M. Base substitutions in the tRNA anticodon arm do not degrade the accuracy of reading frame maintenance. Proc Natl Acad Sci U S A. 1986 Sep;83(17):6538–6542. [PMC free article] [PubMed]
  • Curran JF, Yarus M. Reading frame selection and transfer RNA anticodon loop stacking. Science. 1987 Dec 11;238(4833):1545–1550. [PubMed]
  • Grosjean H, Söll DG, Crothers DM. Studies of the complex between transfer RNAs with complementary anticodons. I. Origins of enhanced affinity between complementary triplets. J Mol Biol. 1976 May 25;103(3):499–519. [PubMed]
  • Yarus M, Cline SW, Wier P, Breeden L, Thompson RC. Actions of the anticodon arm in translation on the phenotypes of RNA mutants. J Mol Biol. 1986 Nov 20;192(2):235–255. [PubMed]
  • Weiss RB, Dunn DM, Atkins JF, Gesteland RF. Ribosomal frameshifting from -2 to +50 nucleotides. Prog Nucleic Acid Res Mol Biol. 1990;39:159–183. [PubMed]
  • Jukes TH. Possibilities for the evolution of the genetic code from a preceding form. Nature. 1973 Nov 2;246(5427):22–26. [PubMed]
  • Wilson RK, Roe BA. Presence of the hypermodified nucleotide N6-(delta 2-isopentenyl)-2-methylthioadenosine prevents codon misreading by Escherichia coli phenylalanyl-transfer RNA. Proc Natl Acad Sci U S A. 1989 Jan;86(2):409–413. [PMC free article] [PubMed]

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