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PMID: 7828587 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

The identity of the base following the stop codon determines the efficiency of in vivo translational termination in Escherichia coli.

The EMBO journal ·Vol. 14 ·No. 1 ·1995-01-03 ·Pages 151-8

Poole ES, Brown CM, Tate WP

Abstract

A statistical analysis of > 2000 Escherichia coli genes suggested that the base following the translational stop codon might be an important feature of the signal for termination. The strengths of each of 12 possible 'four base stop signals' (UAAN, UGAN and UAGN) were tested in an in vivo termination assay that measured termination efficiency by its direct competition with frameshifting. Termination efficiencies varied significantly depending on both the stop codon and the fourth base, ranging from 80 (UAAU) to 7% (UGAC). For both the UAAN and UGAN series, the fourth base hierarchy was U > G > A approximately C. UAG stop codons, which are used rarely in E. coli, showed efficiencies comparable with UAAN and UGAN, but differed in that the hierarchy of the fourth base was G > U approximately A > C. The rate of release factor selection varied 30-fold at UGAN stop signals, and 10-fold for both the UAAN and UAGN series; it correlated well with the frequency with which the different UAAN and UGAN signals are found at natural termination sites. The results suggest that the identity of the base following the stop codon determines the efficiency of translational termination in E. coli. They also provide a rationale for the use of the strong UAAU signal in highly expressed genes and for the occurrence of the weaker UGAC signal at several recording sites.

MeSH Terms
Base Composition Base Sequence Codon, Terminator/genetics Escherichia coli/genetics Genes, Bacterial Molecular Sequence Data Peptide Chain Termination, Translational/genetics Reading Frames/genetics Structure-Activity Relationship
Chemicals
Codon, Terminator
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Poole E S
Department of Biochemistry, University of Otago, Dunedin, New Zealand.
Brown C M
Tate W P
References (50)
50 references, click to expand
  1. Mitochondrial phosphate transport. Large scale isolation and characterization of the phosphate transport protein from beef heart mitochondria.
    J Biol Chem. 1984 Jul 25;259(14):9115-20 PMID: 6746642
  2. Selenocysteine: the 21st amino acid.
    Mol Microbiol. 1991 Mar;5(3):515-20 PMID: 1828528
  3. Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli.
    Proc Natl Acad Sci U S A. 1986 Jul;83(13):4650-4 PMID: 2941757
  4. Expression of peptide chain release factor 2 requires high-efficiency frameshift.
    Nature. 1986 Jul 17-23;322(6076):273-5 PMID: 3736654
  5. Quantitative analysis of the relationship between nucleotide sequence and functional activity.
    Nucleic Acids Res. 1986 Aug 26;14(16):6661-79 PMID: 3092188
  6. The effect of codon usage on the oligonucleotide composition of the E. coli genome and identification of over- and underrepresented sequences by Markov chain analysis.
    Nucleic Acids Res. 1987 Mar 25;15(6):2627-38 PMID: 3550700
  7. 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
  8. 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):1503-7 PMID: 2457498
  9. Effects of release factor context at UAA codons in Escherichia coli.
    J Bacteriol. 1988 Oct;170(10):4714-7 PMID: 3049546
  10. Conditionally lethal and recessive UGA-suppressor mutations in the prfB gene encoding peptide chain release factor 2 of Escherichia coli.
    J Bacteriol. 1988 Nov;170(11):5378-81 PMID: 3053663
  11. Use of tRNA suppressors to probe regulation of Escherichia coli release factor 2.
    J Mol Biol. 1988 Sep 5;203(1):75-83 PMID: 3054124
  12. Transfer ribonucleic acid-mediated suppression of termination codons in Escherichia coli.
    Microbiol Rev. 1988 Sep;52(3):354-74 PMID: 3054467
  13. Errors and alternatives in reading the universal genetic code.
    Microbiol Rev. 1989 Sep;53(3):273-98 PMID: 2677635
  14. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo.
    J Mol Biol. 1989 Sep 5;209(1):65-77 PMID: 2478714
  15. Structure and function of suppressor tRNAs in higher eukaryotes.
    Crit Rev Biochem Mol Biol. 1990;25(2):71-96 PMID: 2183969
  16. The signal for the termination of protein synthesis in procaryotes.
    Nucleic Acids Res. 1990 Apr 25;18(8):2079-86 PMID: 2186375
  17. The where, what and how of ribosomal frameshifting in retroviral protein synthesis.
    Trends Biochem Sci. 1990 May;15(5):186-90 PMID: 2193436
  18. Ribosome gymnastics--degree of difficulty 9.5, style 10.0.
    Cell. 1990 Aug 10;62(3):413-23 PMID: 2199062
  19. Third position base changes in codons 5' and 3' adjacent UGA codons affect UGA suppression in vivo.
    Biochim Biophys Acta. 1990 Aug 27;1050(1-3):259-62 PMID: 2207152
  20. Recent advances in peptide chain termination.
    Mol Microbiol. 1990 Jun;4(6):861-5 PMID: 2215213
  21. Processivity errors of gene expression in Escherichia coli.
    J Mol Biol. 1990 Oct 20;215(4):511-21 PMID: 2121997
  22. Ribosomal frameshifting from -2 to +50 nucleotides.
    Prog Nucleic Acid Res Mol Biol. 1990;39:159-83 PMID: 2247607
  23. A rRNA-mRNA base pairing model for UGA-dependent termination.
    Biochimie. 1991 Jul-Aug;73(7-8):1121-9 PMID: 1742356
  24. Biased DNA repair.
    Nature. 1992 Feb 13;355(6361):595-6 PMID: 1538746
  25. Translational termination: "stop" for protein synthesis or "pause" for regulation of gene expression.
    Biochemistry. 1992 Mar 10;31(9):2443-50 PMID: 1547227
  26. Influence of codon context on UGA suppression and readthrough.
    J Mol Biol. 1992 May 20;225(2):261-9 PMID: 1375653
  27. Recoding: reprogrammed genetic decoding.
    Science. 1992 Sep 18;257(5077):1640-1 PMID: 1529352
  28. Analysis of effects of tRNA:message stability on frameshift frequency at the Escherichia coli RF2 programmed frameshift site.
    Nucleic Acids Res. 1993 Apr 25;21(8):1837-43 PMID: 8493101
  29. Two regions of the Escherichia coli 16S ribosomal RNA are important for decoding stop signals in polypeptide chain termination.
    Nucleic Acids Res. 1993 May 11;21(9):2109-15 PMID: 8502551
  30. Termination of translation in bacteria may be modulated via specific interaction between peptide chain release factor 2 and the last peptidyl-tRNA(Ser/Phe).
    Nucleic Acids Res. 1993 Jun 25;21(12):2891-7 PMID: 8332498
  31. The EMBL data library.
    Nucleic Acids Res. 1993 Jul 1;21(13):2967-71 PMID: 8332519
  32. The translational termination signal database.
    Nucleic Acids Res. 1993 Jul 1;21(13):3119-23 PMID: 8332534
  33. Competition between frameshifting, termination and suppression at the frameshift site in the Escherichia coli release factor-2 mRNA.
    Nucleic Acids Res. 1993 Nov 11;21(22):5074-8 PMID: 7504811
  34. The concentration of polypeptide chain release factors 1 and 2 at different growth rates of Escherichia coli.
    J Mol Biol. 1994 May 6;238(3):302-8 PMID: 8176726
  35. Interactions of a small RNA with antibiotic and RNA ligands of the 30S subunit.
    Nature. 1994 Aug 25;370(6491):659-62 PMID: 8065453
  36. Release factors differing in specificity for terminator codons.
    Proc Natl Acad Sci U S A. 1968 Oct;61(2):768-74 PMID: 4879404
  37. The genetic code--yesterday, today, and tomorrow.
    Cold Spring Harb Symp Quant Biol. 1966;31:1-9 PMID: 5237190
  38. The translational termination signal database (TransTerm) now also includes initiation contexts.
    Nucleic Acids Res. 1994 Sep;22(17):3620-4 PMID: 7937070
  39. The influence of the reading context upon the suppression of nonsense codons.
    Mol Gen Genet. 1969 Oct 13;105(2):125-30 PMID: 5367414
  40. The influence of the reading context upon the suppression of nonsense codons. 3.
    Cold Spring Harb Symp Quant Biol. 1969;34:513-20 PMID: 5266175
  41. Tryptophan transfer RNA as the UGA suppressor.
    J Mol Biol. 1971 Jun 14;58(2):439-58 PMID: 4933412
  42. The influence of the reading context upon the suppression of nonsense codons.
    Mol Gen Genet. 1977 Mar 7;151(2):137-49 PMID: 327262
  43. The influence of codon context on genetic code translation.
    Nature. 1980 Jul 10;286(5769):123-7 PMID: 7402305
  44. Prevalence of amber suppressor-containing coliforms in the natural environment.
    Nature. 1980 Jul 31;286(5772):524-5 PMID: 6995858
  45. Context effects: translation of UAG codon by suppressor tRNA is affected by the sequence following UAG in the message.
    J Mol Biol. 1983 Feb 15;164(1):73-87 PMID: 6188841
  46. A temperature-sensitive mutant of Escherichia coli that shows enhanced misreading of UAG/A and increased efficiency for some tRNA nonsense suppressors.
    Mol Gen Genet. 1984;193(1):38-45 PMID: 6419024
  47. Frameshift autoregulation in the gene for Escherichia coli release factor 2: partly functional mutants result in frameshift enhancement.
    Nucleic Acids Res. 1990 Nov 25;18(22):6517-22 PMID: 2251114
  48. Codon recognition in polypeptide chain termination: site directed crosslinking of termination codon to Escherichia coli release factor 2.
    Nucleic Acids Res. 1990 Nov 25;18(22):6537-44 PMID: 2251116
  49. 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):231-41 PMID: 2038055
  50. 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):3616-20 PMID: 3889910
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1995-01-03
Pages
151-8
Language
English
Region
England
NLM ID
8208664
PMCID
PMC398062
Subset
IM
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