Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1990 Sep 11;18(17):5031–5036. doi: 10.1093/nar/18.17.5031

Frameshift suppression at tandem AGA and AGG codons by cloned tRNA genes: assigning a codon to argU tRNA and T4 tRNA(Arg).

R A Spanjaard 1, K Chen 1, J R Walker 1, J van Duin 1
PMCID: PMC332114  PMID: 2205835

Abstract

Arginine is coded for by CGN (N = G, A, U, C), AGA and AGG. In Escherichia coli there is little tRNA for AGA and AGG and the use of these codons is strongly avoided in virtually all genes. Recently, we demonstrated that the presence of tandem AGA or AGG codons in mRNA causes frameshifts with high frequency. Here, we show that phaseshifts can be suppressed when cells are transformed with the gene for tRNA(T4Arg) or E. coli tRNA(argU,Arg) demonstrating that such errors are the result of tRNA depletion. Bacteriophage T4 encoded tRNA(Arg) (anticodon UCU) corrects shifts at AGA-AGA but not at AGG-AGG, suggesting that this tRNA can only read AGA. Similarly, comparison of the translational efficiencies in an argU (Ts) mutant and in its isogenic wild type parent indicates that argU tRNA (anticodon UCU) reads AGA but not AGG. An argU (Ts) mutant barely reads through AGA-AGA at 42 degrees C but translation of AGG-AGG is hardly, if at all, affected. Overexpression of argU+ relaxes the codon specificity. The thermosensitive mutant in argU, previously called dnaY because it is defective in DNA replication, can be complemented for growth by the gene for tRNA(T4Arg). This implies that the sole function of the argU gene product is to sustain protein synthesis and that its role in replication is probably indirect.

Full text

PDF
5031

Images in this article

5033Image
on p.5033
5033Image
on p.5033
5034Image
on p.5034

Selected References

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

  1. Atkins J. F., Gesteland R. F., Reid B. R., Anderson C. W. Normal tRNAs promote ribosomal frameshifting. Cell. 1979 Dec;18(4):1119–1131. doi: 10.1016/0092-8674(79)90225-3. [DOI] [PubMed] [Google Scholar]
  2. Beier H., Barciszewska M., Sickinger H. D. The molecular basis for the differential translation of TMV RNA in tobacco protoplasts and wheat germ extracts. EMBO J. 1984 May;3(5):1091–1096. doi: 10.1002/j.1460-2075.1984.tb01934.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Björk G. R., Ericson J. U., Gustafsson C. E., Hagervall T. G., Jönsson Y. H., Wikström P. M. Transfer RNA modification. Annu Rev Biochem. 1987;56:263–287. doi: 10.1146/annurev.bi.56.070187.001403. [DOI] [PubMed] [Google Scholar]
  4. Blanar M. A., Sandler S. J., Armengod M. E., Ream L. W., Clark A. J. Molecular analysis of the recF gene of Escherichia coli. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4622–4626. doi: 10.1073/pnas.81.15.4622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Byström A. S., Hjalmarsson K. J., Wikström P. M., Björk G. R. The nucleotide sequence of an Escherichia coli operon containing genes for the tRNA(m1G)methyltransferase, the ribosomal proteins S16 and L19 and a 21-K polypeptide. EMBO J. 1983;2(6):899–905. doi: 10.1002/j.1460-2075.1983.tb01519.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen K. S., Peters T. C., Walker J. R. A minor arginine tRNA mutant limits translation preferentially of a protein dependent on the cognate codon. J Bacteriol. 1990 May;172(5):2504–2510. doi: 10.1128/jb.172.5.2504-2510.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Clare J. J., Belcourt M., Farabaugh P. J. Efficient translational frameshifting occurs within a conserved sequence of the overlap between the two genes of a yeast Ty1 transposon. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6816–6820. doi: 10.1073/pnas.85.18.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Felmlee T., Pellett S., Welch R. A. Nucleotide sequence of an Escherichia coli chromosomal hemolysin. J Bacteriol. 1985 Jul;163(1):94–105. doi: 10.1128/jb.163.1.94-105.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garcia G. M., Mar P. K., Mullin D. A., Walker J. R., Prather N. E. The E. coli dnaY gene encodes an arginine transfer RNA. Cell. 1986 May 9;45(3):453–459. doi: 10.1016/0092-8674(86)90331-4. [DOI] [PubMed] [Google Scholar]
  11. Henson J. M., Chu H., Irwin C. A., Walker J. R. Isolation and characterization of dnaX and dnaY temperature-sensitive mutants of Escherichia coli. Genetics. 1979 Aug;92(4):1041–1059. doi: 10.1093/genetics/92.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kao S. H., McClain W. H. U-G-A suppressor of bacteriophage T4 associated with arginine transfer RNA. J Biol Chem. 1977 Nov 25;252(22):8254–8257. [PubMed] [Google Scholar]
  13. Kiesewetter S., Fischer W., Sprinzl M. Sequences of three minor tRNAsArg from E. coli. Nucleic Acids Res. 1987 Apr 10;15(7):3184–3184. doi: 10.1093/nar/15.7.3184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lindsey D. F., Mullin D. A., Walker J. R. Characterization of the cryptic lambdoid prophage DLP12 of Escherichia coli and overlap of the DLP12 integrase gene with the tRNA gene argU. J Bacteriol. 1989 Nov;171(11):6197–6205. doi: 10.1128/jb.171.11.6197-6205.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mazzara G. P., Plunkett G., 3rd, McClain W. H. 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):889–892. doi: 10.1073/pnas.78.2.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mazzara G. P., Seidman J. G., McClain W. H., Yesian H., Abelson J., Guthrie C. Nucleotide sequence of an arginine transfer ribonucleic acid from bacteriophage T4. J Biol Chem. 1977 Nov 25;252(22):8245–8253. [PubMed] [Google Scholar]
  17. Muramatsu T., Nishikawa K., Nemoto F., Kuchino Y., Nishimura S., Miyazawa T., Yokoyama S. Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature. 1988 Nov 10;336(6195):179–181. doi: 10.1038/336179a0. [DOI] [PubMed] [Google Scholar]
  18. Remaut E., Stanssens P., Fiers W. Plasmid vectors for high-efficiency expression controlled by the PL promoter of coliphage lambda. Gene. 1981 Oct;15(1):81–93. doi: 10.1016/0378-1119(81)90106-2. [DOI] [PubMed] [Google Scholar]
  19. Remaut E., Tsao H., Fiers W. Improved plasmid vectors with a thermoinducible expression and temperature-regulated runaway replication. Gene. 1983 Apr;22(1):103–113. doi: 10.1016/0378-1119(83)90069-0. [DOI] [PubMed] [Google Scholar]
  20. Sekiya T., Takeishi K., Ukita T. Specificity of yeast glutamic acid transfer RNA for codon recognition. Biochim Biophys Acta. 1969 Jun 17;182(2):411–426. doi: 10.1016/0005-2787(69)90192-0. [DOI] [PubMed] [Google Scholar]
  21. Spanjaard R. A., van Duin J. Translation of the sequence AGG-AGG yields 50% ribosomal frameshift. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7967–7971. doi: 10.1073/pnas.85.21.7967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Varenne S., Lazdunski C. 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. doi: 10.1016/s0022-5193(86)80020-0. [DOI] [PubMed] [Google Scholar]
  23. Wilson R. K., Roe B. A. Presence of the hypermodified nucleotide N6-(delta 2-isopentenyl)-2-methylthioadenosine prevents codon misreading by Escherichia coli phenylalanyl-transfer RNA. Proc Natl Acad Sci U S A. 1989 Jan;86(2):409–413. doi: 10.1073/pnas.86.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yanofsky C. Mutations affecting tRNATrp and its charging and their effect on regulation of transcription termination at the attenuator of the tryptophan operon. J Mol Biol. 1977 Jul 15;113(4):663–677. doi: 10.1016/0022-2836(77)90229-7. [DOI] [PubMed] [Google Scholar]
  25. Zurawski G., Elseviers D., Stauffer G. V., Yanofsky C. Translational control of transcription termination at the attenuator of the Escherichia coli tryptophan operon. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5988–5992. doi: 10.1073/pnas.75.12.5988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES