Skip to main content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Proc Natl Acad Sci U S A. 1988 Jun; 85(12): 4242–4246.
PMCID: PMC280403
PMID: 3288988

Codon choice and gene expression: synonymous codons differ in their ability to direct aminoacylated-transfer RNA binding to ribosomes in vitro.

Abstract

Phe-tRNA (anticodon GAA)--polypeptide-chain elongation factor Tu-GTP ternary complexes react faster with ribosomes programmed with UUC codons than with ribosomes programmed with UUU codons. A similar preference is shown by Leu-tRNA2 (anticodon GAG) complexes, which react faster with ribosomes programmed with CUC than with those programmed with CUU. The difference is seen in the rate of ternary-complex binding to the ribosome; no differences are seen in peptide-bond formation. Highly expressed mRNAs in Escherichia coli favor codons terminating in cytosine rather than uracil when both codons are read by a single tRNA with an anticodon beginning with guanine. The results suggest that intrinsic differences between the efficiencies of synonymous codons play an important role in modulating gene expression in E. coli.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (1.1M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  • Post LE, Strycharz GD, Nomura M, Lewis H, Dennis PP. Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1697–1701. [PMC free article] [PubMed] [Google Scholar]
  • Bennetzen JL, Hall BD. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
  • Carter PW, Bartkus JM, Calvo JM. Transcription attenuation in Salmonella typhimurium: the significance of rare leucine codons in the leu leader. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8127–8131. [PMC free article] [PubMed] [Google Scholar]
  • Robinson M, Lilley R, Little S, Emtage JS, Yarranton G, Stephens P, Millican A, Eaton M, Humphreys G. Codon usage can affect efficiency of translation of genes in Escherichia coli. Nucleic Acids Res. 1984 Sep 11;12(17):6663–6671. [PMC free article] [PubMed] [Google Scholar]
  • Pedersen S. Escherichia coli ribosomes translate in vivo with variable rate. EMBO J. 1984 Dec 1;3(12):2895–2898. [PMC free article] [PubMed] [Google Scholar]
  • Varenne S, Knibiehler M, Cavard D, Morlon J, Lazdunski C. Variable rate of polypeptide chain elongation for colicins A, E2 and E3. J Mol Biol. 1982 Jul 25;159(1):57–70. [PubMed] [Google Scholar]
  • Thompson RC, Dix DB, Eccleston JF. Single turnover kinetic studies of guanosine triphosphate hydrolysis and peptide formation in the elongation factor Tu-dependent binding of aminoacyl-tRNA to Escherichia coli ribosomes. J Biol Chem. 1980 Dec 10;255(23):11088–11090. [PubMed] [Google Scholar]
  • Ikemura T. 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. [PubMed] [Google Scholar]
  • Parker J, Johnston TC, Borgia PT, Holtz G, Remaut E, Fiers W. Codon usage and mistranslation. In vivo basal level misreading of the MS2 coat protein message. J Biol Chem. 1983 Aug 25;258(16):10007–10012. [PubMed] [Google Scholar]
  • Thomposon RC, Dix DB. Accuracy of protein biosynthesis. A kinetic study of the reaction of poly(U)-programmed ribosomes with a leucyl-tRNA2-elongation factor Tu-GTP complex. J Biol Chem. 1982 Jun 25;257(12):6677–6682. [PubMed] [Google Scholar]
  • Hershey JW, Yanov J, Johnston K, Fakunding JL. Purification and characterization of protein synthesis initiation factors IF1, IF2, and IF3 from Escherichia coli. Arch Biochem Biophys. 1977 Aug;182(2):626–638. [PubMed] [Google Scholar]
  • Thompson RC, Dix DB, Gerson RB, Karim AM. A GTPase reaction accompanying the rejection of Leu-tRNA2 by UUU-programmed ribosomes. Proofreading of the codon-anticodon interaction by ribosomes. J Biol Chem. 1981 Jan 10;256(1):81–86. [PubMed] [Google Scholar]
  • Woo SL. A sensitive and rapid method for recombinant phage screening. Methods Enzymol. 1979;68:389–395. [PubMed] [Google Scholar]
  • Wood WI, Gitschier J, Lasky LA, Lawn RM. Base composition-independent hybridization in tetramethylammonium chloride: a method for oligonucleotide screening of highly complex gene libraries. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1585–1588. [PMC free article] [PubMed] [Google Scholar]
  • Eccleston JF, Messerschmidt RG, Yates DW. A simple rapid mixing device. Anal Biochem. 1980 Jul 15;106(1):73–77. [PubMed] [Google Scholar]
  • Varenne S, Buc J, Lloubes R, Lazdunski C. Translation is a non-uniform process. Effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J Mol Biol. 1984 Dec 15;180(3):549–576. [PubMed] [Google Scholar]
  • Dennis PP, Bremer H. Macromolecular composition during steady-state growth of Escherichia coli B-r. J Bacteriol. 1974 Jul;119(1):270–281. [PMC free article] [PubMed] [Google Scholar]
  • Pierucci O. Dimensions of Escherichia coli at various growth rates: model for envelope growth. J Bacteriol. 1978 Aug;135(2):559–574. [PMC free article] [PubMed] [Google Scholar]
  • Karim AM, Thompson RC. Guanosine 5'-O-(3-thiotriphosphate) as an analog of GTP in protein biosynthesis. The effects of temperature and polycations on the accuracy of initial recognition of aminoacyl-tRNA ternary complexes by ribosomes. J Biol Chem. 1986 Mar 5;261(7):3238–3243. [PubMed] [Google Scholar]
  • Dix DB, Wittenberg WL, Uhlenbeck OC, Thompson RC. Effect of replacing uridine 33 in yeast tRNAPhe on the reaction with ribosomes. J Biol Chem. 1986 Aug 5;261(22):10112–10118. [PubMed] [Google Scholar]
  • Eccleston JF, Dix DB, Thompson RC. The rate of cleavage of GTP on the binding of Phe-tRNA.elongation factor Tu.GTP to poly(U)-programmed ribosomes of Escherichia coli. J Biol Chem. 1985 Dec 25;260(30):16237–16241. [PubMed] [Google Scholar]
  • Labuda D, Pörschke D. Codon-induced transfer RNA association. A property of transfer RNA involved in its adaptor function? J Mol Biol. 1983 Jun 15;167(1):205–209. [PubMed] [Google Scholar]
  • Labuda D, Striker G, Porschke D. Mechanism of codon recognition by transfer RNA and codon-induced tRNA association. J Mol Biol. 1984 Apr 25;174(4):587–604. [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

-