Home LiteratureArticle Details
PMID: 11544186 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Translational misreading: a tRNA modification counteracts a +2 ribosomal frameshift.

Genes & development ·Vol. 15 ·No. 17 ·2001-09-01 ·Pages 2295-306

Brégeon D, Colot V, Radman M, Taddei F

Abstract

Errors during gene expression from DNA to proteins via transcription and translation may be deleterious for the functional maintenance of cells. In this paper, extensive genetic studies of the misreading of a GA repeat introduced into the lacZ gene of Escherichia coli indicate that in this bacteria, errors occur predominantly by a +2 translational frameshift, which is controlled by a tRNA modification involving the MnmE and GidA proteins. This ribosomal frameshift results from the coincidence of three events: (1) decreased codon-anticodon affinity at the P-site, which is caused by tRNA hypomodification in mnmE(-) and gidA(-) strains; (2) a repetitive mRNA sequence predisposing to slippage; and (3) increased translational pausing attributable to the presence of a rare codon at the A-site. Based on genetic analysis, we propose that GidA and MnmE act in the same pathway of tRNA modification, the absence of which is responsible for the +2 translational frameshift. The difference in the impact of the mutant gene on cell growth, however, indicates that GidA has at least one other function.

MeSH Terms
Algal Proteins/metabolism Arabinose/pharmacology Base Sequence Cell Division Codon DNA Transposable Elements/genetics Escherichia coli/genetics,metabolism Evolution, Molecular Frameshift Mutation Genes, Reporter Genotype Lac Operon Models, Chemical Molecular Sequence Data Mutagenesis Mutation Phenotype Plant Proteins Plasmids/metabolism Protein Biosynthesis RNA, Transfer/metabolism Ribosomes/metabolism Thiouridine/analogs & derivatives,pharmacology Transcription, Genetic beta-Galactosidase/metabolism
Chemicals
Algal Proteins Codon DNA Transposable Elements Plant Proteins Thiouridine 5-methylaminomethyl-2-thiouridine RNA, Transfer Arabinose beta-Galactosidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Brégeon D
INSERM EPI9916, Faculté de Médecine Necker-Enfants Malades, 75730 Paris Cedex 15, France. [email protected]
Colot V
Radman M
Taddei F
References (57)
57 references, click to expand
  1. The allosteric three-site model for the ribosomal elongation cycle: features and future.
    Biochemistry. 1990 May 29;29(21):4997-5008 PMID: 2198935
  2. MTO1 codes for a mitochondrial protein required for respiration in paromomycin-resistant mutants of Saccharomyces cerevisiae.
    J Biol Chem. 1998 Oct 23;273(43):27945-52 PMID: 9774408
  3. Effects of mutagenesis of a conserved base-paired site near the decoding region of Escherichia coli 16 S ribosomal RNA.
    J Mol Biol. 1990 Mar 5;212(1):127-33 PMID: 1690811
  4. A procedure for in vitro amplification of DNA segments that lie outside the boundaries of known sequences.
    Nucleic Acids Res. 1988 Aug 25;16(16):8186 PMID: 3047679
  5. Codon usage tabulated from international DNA sequence databases: status for the year 2000.
    Nucleic Acids Res. 2000 Jan 1;28(1):292 PMID: 10592250
  6. Increased ribosomal accuracy increases a programmed translational frameshift in Escherichia coli.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2315-9 PMID: 8460140
  7. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates.
    J Mol Biol. 1996 Aug 2;260(5):649-63 PMID: 8709146
  8. Mistranslation in E. coli.
    Cell. 1977 Jan;10(1):131-7 PMID: 138485
  9. Errors and alternatives in reading the universal genetic code.
    Microbiol Rev. 1989 Sep;53(3):273-98 PMID: 2677635
  10. Protein oxidation in response to increased transcriptional or translational errors.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5746-9 PMID: 10811907
  11. Effects of amino acid substitutions at the active site in Escherichia coli beta-galactosidase.
    Genetics. 1988 Nov;120(3):637-44 PMID: 2906303
  12. Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors.
    Proc Natl Acad Sci U S A. 1987 Sep;84(17):6220-4 PMID: 3306672
  13. Novel E. coli mutants deficient in biosynthesis of 5-methylaminomethyl-2-thiouridine.
    Nucleic Acids Res. 1984 Apr 25;12(8):3521-34 PMID: 6427754
  14. Ribosome editing and the error catastrophe hypothesis of cellular aging.
    Mech Ageing Dev. 1977 Mar-Apr;6(2):131-142 PMID: 321889
  15. The elongation phase of protein synthesis.
    Prog Nucleic Acid Res Mol Biol. 1996;54:293-332 PMID: 8768078
  16. Evolution of a second gene for beta-galactosidase in Escherichia coli.
    Proc Natl Acad Sci U S A. 1973 Jun;70(6):1841-5 PMID: 4124306
  17. Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine.
    J Bacteriol. 1985 Jan;161(1):368-76 PMID: 3881393
  18. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients.
    Science. 1998 Jan 9;279(5348):242-7 PMID: 9422699
  19. How translational accuracy influences reading frame maintenance.
    EMBO J. 1999 Mar 15;18(6):1427-34 PMID: 10075915
  20. Mutation, recombination, and incipient speciation of bacteria in the laboratory.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7348-51 PMID: 10377417
  21. 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;52:687-93 PMID: 3135981
  22. Translational accuracy and the fitness of bacteria.
    Annu Rev Genet. 1992;26:29-50 PMID: 1482115
  23. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes.
    J Mol Biol. 1981 Feb 15;146(1):1-21 PMID: 6167728
  24. Transcriptional fidelity and proofreading by RNA polymerase II.
    Cell. 1998 May 15;93(4):627-37 PMID: 9604937
  25. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo.
    J Mol Biol. 1989 Sep 5;209(1):65-77 PMID: 2478714
  26. The paromomycin resistance mutation (parr-454) in the 15 S rRNA gene of the yeast Saccharomyces cerevisiae is involved in ribosomal frameshifting.
    Mol Gen Genet. 1989 Jun;217(2-3):362-9 PMID: 2671660
  27. A new model for phenotypic suppression of frameshift mutations by mutant tRNAs.
    Mol Cell. 1998 Mar;1(4):471-82 PMID: 9660932
  28. Dinucleotide deletions in neuronal transcripts: a novel type of mutation in non-familial Alzheimer's disease and Down syndrome patients.
    Prog Brain Res. 1998;117:379-95 PMID: 9932421
  29. MSS1, a nuclear-encoded mitochondrial GTPase involved in the expression of COX1 subunit of cytochrome c oxidase.
    J Mol Biol. 1993 Jul 5;232(1):79-88 PMID: 8392589
  30. Transfer RNA(5-methylaminomethyl-2-thiouridine)-methyltransferase from Escherichia coli K-12 has two enzymatic activities.
    J Biol Chem. 1987 Jun 25;262(18):8488-95 PMID: 3298234
  31. RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease.
    J Neurosci. 1999 Mar 15;19(6):1959-64 PMID: 10066249
  32. Uses of transposons with emphasis on Tn10.
    Methods Enzymol. 1991;204:139-80 PMID: 1658561
  33. Mode of action of chloramphenicol.
    Nature. 1952 Nov 29;170(4335):931-2 PMID: 13013268
  34. The Escherichia coli trmE (mnmE) gene, involved in tRNA modification, codes for an evolutionarily conserved GTPase with unusual biochemical properties.
    EMBO J. 1999 Dec 15;18(24):7063-76 PMID: 10601028
  35. The modification of the wobble base of tRNAGlu modulates the translation rate of glutamic acid codons in vivo.
    J Mol Biol. 1998 Dec 4;284(3):621-31 PMID: 9826503
  36. External suppression of a frameshift mutant in salmonella.
    J Mol Biol. 1968 Jun 28;34(3):541-57 PMID: 4938557
  37. The role of RNA polymerase in transcriptional fidelity.
    Mol Microbiol. 1991 May;5(5):999-1004 PMID: 1659650
  38. Cell cycle-dependent transcription from the gid and mioC promoters of Escherichia coli.
    J Bacteriol. 1994 Mar;176(6):1609-15 PMID: 8132454
  39. Novel temperature-sensitive mutants of Escherichia coli that are unable to grow in the absence of wild-type tRNA6Leu.
    J Bacteriol. 1998 Jun;180(11):2931-5 PMID: 9603884
  40. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
    J Bacteriol. 1995 Jul;177(14):4121-30 PMID: 7608087
  41. Enhanced ribosome frameshifting in stationary phase cells.
    J Mol Biol. 1996 Oct 25;263(2):140-8 PMID: 8913297
  42. Two mutations giving low-level streptomycin resistance in Escherichia coli K 12.
    Genet Res. 1970 Dec;16(3):359-65 PMID: 4997534
  43. The frequency of errors in protein biosynthesis.
    Biochem J. 1972 Aug;128(5):1353-6 PMID: 4643706
  44. Isolation and characterization of the newly evolved ebg beta-galactosidase of Escherichia coli K-12.
    J Bacteriol. 1975 Nov;124(2):849-56 PMID: 241745
  45. Protein oxidation and aging.
    Science. 1992 Aug 28;257(5074):1220-4 PMID: 1355616
  46. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  47. Mutations in RNA: a first example of molecular misreading in Alzheimer's disease.
    Trends Neurosci. 1998 Aug;21(8):331-5 PMID: 9720597
  48. Identification of the paromomycin-resistance mutation in the 15 S rRNA gene of yeast mitochondria.
    J Biol Chem. 1982 May 25;257(10):5921-8 PMID: 6279619
  49. Transfer RNA modification: influence on translational frameshifting and metabolism.
    FEBS Lett. 1999 Jun 4;452(1-2):47-51 PMID: 10376676
  50. Programmed translational frameshifting.
    Microbiol Rev. 1996 Mar;60(1):103-34 PMID: 8852897
  51. Modified nucleosides in the first positions of the anticodons of tRNA(Leu)4 and tRNA(Leu)5 from Escherichia coli.
    Biochemistry. 1999 Jan 5;38(1):207-17 PMID: 9890900
  52. An estimate of the global error frequency in translation.
    Mol Gen Genet. 1982;188(2):169-72 PMID: 6759868
  53. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons.
    Am J Pathol. 1999 May;154(5):1423-9 PMID: 10329595
  54. Counteraction by MutT protein of transcriptional errors caused by oxidative damage.
    Science. 1997 Oct 3;278(5335):128-30 PMID: 9311918
  55. Isolation and partial characterization of three Escherichia coli mutants with altered transfer ribonucleic acid methylases.
    J Bacteriol. 1975 Apr;122(1):257-65 PMID: 1091626
  56. EFTu provides an internal kinetic standard for translational accuracy.
    Trends Biochem Sci. 1988 Mar;13(3):91-3 PMID: 3072707
  57. Genomic organization and physical mapping of the transfer RNA genes in Escherichia coli K12.
    J Mol Biol. 1990 Apr 20;212(4):579-98 PMID: 2184240
Article Info
Journal
Genes & development
Abbr.
Genes Dev
ISSN
0890-9369
DOI
10.1101/gad.207701
Email
[email protected]
Published
2001-09-01
Pages
2295-306
Language
English
Region
United States
NLM ID
8711660
PMCID
PMC312767
Subset
IM
External Links
PubMed source DOI: 10.1101/gad.207701 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2