How Translational Accuracy Influences Reading Frame Maintenance

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1999 Mar 17

PMID 10075915

Citations 64

Authors

P J Farabaugh

G R Bjork

Affiliations

Soon will be listed here.

Abstract

Most missense errors have little effect on protein function, since they only exchange one amino acid for another. However, processivity errors, frameshifting or premature termination result in a synthesis of an incomplete peptide. There may be a connection between missense and processivity errors, since processivity errors now appear to result from a second error occurring after recruitment of an errant aminoacyl-tRNA, either spontaneous dissociation causing premature termination or translational frameshifting. This is clearest in programmed translational frameshifting where the mRNA programs errant reading by a near-cognate tRNA; this error promotes a second frameshifting error (a dual-error model of frameshifting). The same mechanism can explain frameshifting by suppressor tRNAs, even those with expanded anticodon loops. The previous model that suppressor tRNAs induce quadruplet translocation now appears incorrect for most, and perhaps for all of them. We suggest that the 'spontaneous' tRNA-induced frameshifting and 'programmed' mRNA-induced frameshifting use the same mechanism, although the frequency of frameshifting is very different. This new model of frameshifting suggests that the tRNA is not acting as the yardstick to measure out the length of the translocation step. Rather, the translocation of 3 nucleotides may be an inherent feature of the ribosome.

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References

Huttenhofer A, Weiss-Brummer B, DIRHEIMER G, Martin R . A novel type of + 1 frameshift suppressor: a base substitution in the anticodon stem of a yeast mitochondrial serine-tRNA causes frameshift suppression. EMBO J. 1990; 9(2):551-8. PMC: 551700. DOI: 10.1002/j.1460-2075.1990.tb08142.x. View

Crick F, Barnett L, Brenner S, WATTS-TOBIN R . General nature of the genetic code for proteins. Nature. 1961; 192:1227-32. DOI: 10.1038/1921227a0. View

Blinkowa A, Walker J . Programmed ribosomal frameshifting generates the Escherichia coli DNA polymerase III gamma subunit from within the tau subunit reading frame. Nucleic Acids Res. 1990; 18(7):1725-9. PMC: 330589. DOI: 10.1093/nar/18.7.1725. View

Flower A, McHenry C . The gamma subunit of DNA polymerase III holoenzyme of Escherichia coli is produced by ribosomal frameshifting. Proc Natl Acad Sci U S A. 1990; 87(10):3713-7. PMC: 53973. DOI: 10.1073/pnas.87.10.3713. View

Belcourt M, Farabaugh P . Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990; 62(2):339-52. PMC: 7133245. DOI: 10.1016/0092-8674(90)90371-k. View

Nierhaus K . The allosteric three-site model for the ribosomal elongation cycle: features and future. Biochemistry. 1990; 29(21):4997-5008. DOI: 10.1021/bi00473a001. View

Donly B, Edgar C, Adamski F, Tate W . Frameshift autoregulation in the gene for Escherichia coli release factor 2: partly functional mutants result in frameshift enhancement. Nucleic Acids Res. 1990; 18(22):6517-22. PMC: 332604. DOI: 10.1093/nar/18.22.6517. View

Tsuchihashi Z, Brown P . Sequence requirements for efficient translational frameshifting in the Escherichia coli dnaX gene and the role of an unstable interaction between tRNA(Lys) and an AAG lysine codon. Genes Dev. 1992; 6(3):511-9. DOI: 10.1101/gad.6.3.511. View

Atkins J, Weiss R, Thompson S, GESTELAND R . Towards a genetic dissection of the basis of triplet decoding, and its natural subversion: programmed reading frame shifts and hops. Annu Rev Genet. 1991; 25:201-28. DOI: 10.1146/annurev.ge.25.120191.001221. View

10.

Sroga G, Nemoto F, Kuchino Y, Bjork G . Insertion (sufB) in the anticodon loop or base substitution (sufC) in the anticodon stem of tRNA(Pro)2 from Salmonella typhimurium induces suppression of frameshift mutations. Nucleic Acids Res. 1992; 20(13):3463-9. PMC: 312503. DOI: 10.1093/nar/20.13.3463. View

11.

Peter K, Lindsley D, Peng L, Gallant J . Context rules of rightward overlapping reading. New Biol. 1992; 4(5):520-6. View

12.

Jakubowski H, Goldman E . Editing of errors in selection of amino acids for protein synthesis. Microbiol Rev. 1992; 56(3):412-29. PMC: 372878. DOI: 10.1128/mr.56.3.412-429.1992. View

13.

HOLLEY R . Structure of an alanine transfer ribonucleic acid. JAMA. 1965; 194(8):868-71. View

14.

Newmark R, Cantor C . Nuclear magnetic resonance study of the interactions of guanosine and cytidine in dimethyl sulfoxide. J Am Chem Soc. 1968; 90(18):5010-7. DOI: 10.1021/ja01020a041. View

15.

Riddle D, Carbon J . Frameshift suppression: a nucleotide addition in the anticodon of a glycine transfer RNA. Nat New Biol. 1973; 242(121):230-4. DOI: 10.1038/newbio242230a0. View

16.

Menninger J . Ribosome editing and the error catastrophe hypothesis of cellular aging. Mech Ageing Dev. 1977; 6(2):131-142. DOI: 10.1016/0047-6374(77)90014-8. View

17.

Weissenbach J, DIRHEIMER G, Falcoff R, Sanceau J, FALCOFF E . Yeast tRNALeu (anticodon U--A--G) translates all six leucine codons in extracts from interferon treated cells. FEBS Lett. 1977; 82(1):71-6. DOI: 10.1016/0014-5793(77)80888-0. View

18.

RANDERATH E, Gupta R, Chia L, Chang S, Randerath K . Yeast tRNA Leu UAG. Purification, properties and determination of the nucleotide sequence by radioactive derivative methods. Eur J Biochem. 1979; 93(1):79-94. DOI: 10.1111/j.1432-1033.1979.tb12797.x. View

19.

Caplan A, Menninger J . Tests of the ribosomal editing hypothesis: amino acid starvation differentially enhances the dissociation of peptidyl-tRNA from the ribosome. J Mol Biol. 1979; 134(3):621-37. DOI: 10.1016/0022-2836(79)90370-x. View

20.

Matzke A, Barta A, Kuechler E . Mechanism of translocation: relative arrangement of tRNA and mRNA on the ribosome. Proc Natl Acad Sci U S A. 1980; 77(9):5110-4. PMC: 350006. DOI: 10.1073/pnas.77.9.5110. View