Home LiteratureArticle Details
PMID: 3186700 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Translation of the sequence AGG-AGG yields 50% ribosomal frameshift.

Spanjaard RA, van Duin J

Abstract

We have inserted the sequence 5'-AAG-GAGGU-3', which is complementary to the 3' terminus of Escherichia coli 16S rRNA, in a reading frame and analyzed its effect on the accuracy and overall rate of translation in vivo. Translation over the sequence yields a 50% ribosomal frameshift if the reading phase is A-AGG-AGG-U. The other two possible frames do not give shifts. The introduction of a UAA stop codon before (UAA-AGG-AGG-U) but not after (A-AGG-AGG-UAA) the AGG codons abolishes the frameshift. The change in the reading phase occurs exclusively to the +1 direction. Efficient frameshifting is also induced by the sequence A-AGA-AGA-U. The arginine codons AGG and AGA are read by minor tRNA. Suppression of frameshifting takes place when a gene for minor tRNA(Arg) is introduced on a multicopy plasmid. We suggest that frameshifting during translation of the A-AGG-AGG-U sequence is due to the erroneous decoding of the tandem AGG codons and arises by depletion of tRNA(Arg). The complementarity of tandem AGG codons to the 3' terminus of 16S rRNA is a coincidence and apparently not related to the shift. Replacing the AGG-AGG sequence by the optimal arginine codons CGU-CGU does not increase the overall rate of translation.

MeSH Terms
Base Sequence Codon Molecular Sequence Data Protein Biosynthesis RNA, Ribosomal/metabolism RNA, Ribosomal, 16S/metabolism RNA, Transfer, Arg/metabolism Ribosomes/metabolism T-Phages/genetics
Chemicals
Codon RNA, Ribosomal RNA, Ribosomal, 16S RNA, Transfer, Arg
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Spanjaard R A
Department of Biochemistry, Leiden University, The Netherlands.
van Duin J
References (34)
34 references, click to expand
  1. A ribosome binding site sequence is necessary for efficient expression of the distal gene of a translationally-coupled gene pair.
    Nucleic Acids Res. 1984 Jun 11;12(11):4757-68 PMID: 6377236
  2. 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
  3. Effect of distribution of unfavourable codons on the maximum rate of gene expression by an heterologous organism.
    J Theor Biol. 1986 May 7;120(1):99-110 PMID: 3528671
  4. Codon usage in regulatory genes in Escherichia coli does not reflect selection for 'rare' codons.
    Nucleic Acids Res. 1986 Oct 10;14(19):7737-49 PMID: 3534792
  5. Codon usage can affect efficiency of translation of genes in Escherichia coli.
    Nucleic Acids Res. 1984 Sep 11;12(17):6663-71 PMID: 6091031
  6. Intermediates in the synthesis of TolC protein include an incomplete peptide stalled at a rare Arg codon.
    Eur J Biochem. 1985 Oct 1;152(1):151-5 PMID: 3899641
  7. Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting.
    Science. 1985 Dec 13;230(4731):1237-42 PMID: 2416054
  8. Codon usage and gene expression.
    Nucleic Acids Res. 1986 Apr 11;14(7):3075-87 PMID: 2938078
  9. Elongation factor Tu.guanosine 3'-diphosphate 5'-diphosphate complex increases the fidelity of proofreading in protein biosynthesis: mechanism for reducing translational errors introduced by amino acid starvation.
    Proc Natl Acad Sci U S A. 1986 Apr;83(7):2027-31 PMID: 3515344
  10. Expression of peptide chain release factor 2 requires high-efficiency frameshift.
    Nature. 1986 Jul 17-23;322(6076):273-5 PMID: 3736654
  11. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  12. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity.
    Proc Natl Acad Sci U S A. 1974 Oct;71(10):4135-9 PMID: 4530290
  13. Kinetic amplification of enzyme discrimination.
    Biochimie. 1975;57(5):587-95 PMID: 1182215
  14. Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene.
    Nature. 1976 Apr 8;260(5551):500-7 PMID: 1264203
  15. Proofreading of the codon-anticodon interaction on ribosomes.
    Proc Natl Acad Sci U S A. 1977 Jan;74(1):198-202 PMID: 319457
  16. Mistranslation in E. coli.
    Cell. 1977 Jan;10(1):131-7 PMID: 138485
  17. Nucleotide sequence of an arginine transfer ribonucleic acid from bacteriophage T4.
    J Biol Chem. 1977 Nov 25;252(22):8245-53 PMID: 410812
  18. On the physical basis for ambiguity in genetic coding interactions.
    Proc Natl Acad Sci U S A. 1978 Feb;75(2):610-4 PMID: 273223
  19. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  20. Normal tRNAs promote ribosomal frameshifting.
    Cell. 1979 Dec;18(4):1119-31 PMID: 391405
  21. Translational accuracy enhanced in vitro by (p)ppGpp.
    Mol Gen Genet. 1980;180(1):139-45 PMID: 6934363
  22. DNA sequence of the transfer RNA region of bacteriophage T4: implications for transfer RNA synthesis.
    Proc Natl Acad Sci U S A. 1981 Feb;78(2):889-92 PMID: 6262781
  23. Feedback regulation of ribosomal protein synthesis in E. coli: localization of the mRNA target sites for repressor action of ribosomal protein L1.
    Cell. 1981 Apr;24(1):243-9 PMID: 7016337
  24. 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
  25. Plasmid vectors for high-efficiency expression controlled by the PL promoter of coliphage lambda.
    Gene. 1981 Oct;15(1):81-93 PMID: 6271633
  26. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments.
    Gene. 1982 Oct;19(3):269-76 PMID: 6295880
  27. Mechanism of ribosome frameshifting during translation of the genetic code.
    Nature. 1983 Mar 31-Apr 6;302(5907):389-93 PMID: 6339944
  28. Tests of the ribosome editor hypothesis. II. Relaxed (relA) and stringent (relA+) E. coli differ in rates of dissociation of peptidyl-tRNA from ribosomes.
    Mol Gen Genet. 1983;190(2):215-21 PMID: 6348473
  29. Is there proofreading during polypeptide synthesis?
    EMBO J. 1982;1(6):741-5 PMID: 6765234
  30. 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):4298-302 PMID: 3035577
  31. Translational frameshifting: where will it stop?
    Cell. 1987 Jul 3;50(1):1-2 PMID: 3297347
  32. Lysis gene of bacteriophage MS2 is activated by translation termination at the overlapping coat gene.
    J Mol Biol. 1987 Jun 5;195(3):517-24 PMID: 3656424
  33. 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
  34. Role of mRNA translational efficiency in bovine growth hormone expression in Escherichia coli.
    Proc Natl Acad Sci U S A. 1984 Sep;81(17):5403-7 PMID: 6089201
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1988-11-00
Pages
7967-71
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC282334
Subset
IM
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: product@genelibs.com