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. 1986 Jun;166(3):1022–1027. doi: 10.1128/jb.166.3.1022-1027.1986

Influence of modification next to the anticodon in tRNA on codon context sensitivity of translational suppression and accuracy.

F Bouadloun, T Srichaiyo, L A Isaksson, G R Björk
PMCID: PMC215227  PMID: 3086285

Abstract

Effects on translation in vivo by modification deficiencies for 2-methylthio-N6-isopentenyladenosine (ms2i6A) (Escherichia coli) or 2-methylthio-N6-(4-hydroxyisopentenyl)adenosine (ms2io6A) (Salmonella typhimurium) in tRNA were studied in mutant strains. These hypermodified nucleosides are present on the 3' side of the anticodon (position 37) in tRNA reading codons starting with uridine. In E. coli, translational error caused by tRNA was strongly reduced in the case of third-position misreading of a tryptophan codon (UGG) in a particular codon context but was not affected in the case of first-position misreading of an arginine codon (CGU) in another codon context. Misreading of UGA nonsense codons at two different positions was codon context dependent. The efficiencies of some tRNA nonsense suppressors were decreased in a tRNA-dependent manner. Suppressor tRNA which lacks ms2i6A-ms2io6A becomes more sensitive to codon context. Our results therefore indicate that, besides improving translational efficiency, ms2i6A37 and ms2io6A37 modifications in tRNA are also involved in decreasing the intrinsic codon reading context sensitivity of tRNA. Possible consequences for regulation of gene expression are discussed.

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Selected References

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

  1. Akaboshi E., Inouye M., Tsugita A. Effect of neighboring nucleotide sequences on suppression efficiency in amber mutants of T4 phage lysozyme. Mol Gen Genet. 1976 Nov 24;149(1):1–4. doi: 10.1007/BF00275955. [DOI] [PubMed] [Google Scholar]
  2. Andersson D. I., Bohman K., Isaksson L. A., Kurland C. G. Translation rates and misreading characteristics of rpsD mutants in Escherichia coli. Mol Gen Genet. 1982;187(3):467–472. doi: 10.1007/BF00332630. [DOI] [PubMed] [Google Scholar]
  3. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bartz J. K., Kline L. K., Söll D. N6-(Delta 2-isopentenyl)adenosine: biosynthesis in vitro in transfer RNA by an enzyme purified from Escherichia coli. Biochem Biophys Res Commun. 1970 Sep 30;40(6):1481–1487. doi: 10.1016/0006-291x(70)90035-5. [DOI] [PubMed] [Google Scholar]
  5. Bossi L. 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. doi: 10.1016/0022-2836(83)90088-8. [DOI] [PubMed] [Google Scholar]
  6. Bossi L., Ruth J. R. The influence of codon context on genetic code translation. Nature. 1980 Jul 10;286(5769):123–127. doi: 10.1038/286123a0. [DOI] [PubMed] [Google Scholar]
  7. Bouadloun F., Donner D., Kurland C. G. Codon-specific missense errors in vivo. EMBO J. 1983;2(8):1351–1356. doi: 10.1002/j.1460-2075.1983.tb01591.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Buck M., Ames B. N. A modified nucleotide in tRNA as a possible regulator of aerobiosis: synthesis of cis-2-methyl-thioribosylzeatin in the tRNA of Salmonella. Cell. 1984 Feb;36(2):523–531. doi: 10.1016/0092-8674(84)90245-9. [DOI] [PubMed] [Google Scholar]
  9. Buck M., Griffiths E. Regulation of aromatic amino acid transport by tRNA: role of 2-methylthio-N6-(delta2-isopentenyl)-adenosine. Nucleic Acids Res. 1981 Jan 24;9(2):401–414. doi: 10.1093/nar/9.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Buck M., McCloskey J. A., Basile B., Ames B. N. cis 2-Methylthio-ribosylzeatin (ms2io6A) is present in the transfer RNA of Salmonella typhimurium, but not Escherichia coli. Nucleic Acids Res. 1982 Sep 25;10(18):5649–5662. doi: 10.1093/nar/10.18.5649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Colby D. S., Schedl P., Guthrie C. A functional requirement for modification of the wobble nucleotide in tha anticodon of a T4 suppressor tRNA. Cell. 1976 Nov;9(3):449–463. doi: 10.1016/0092-8674(76)90090-8. [DOI] [PubMed] [Google Scholar]
  12. Edelmann P., Gallant J. Mistranslation in E. coli. Cell. 1977 Jan;10(1):131–137. doi: 10.1016/0092-8674(77)90147-7. [DOI] [PubMed] [Google Scholar]
  13. Eisenberg S. P., Yarus M., Soll L. The effect of an Escherichia coli regulatory mutation on transfer RNA structure. J Mol Biol. 1979 Nov 25;135(1):111–126. doi: 10.1016/0022-2836(79)90343-7. [DOI] [PubMed] [Google Scholar]
  14. Ericson J. U., Björk G. R. Pleiotropic effects induced by modification deficiency next to the anticodon of tRNA from Salmonella typhimurium LT2. J Bacteriol. 1986 Jun;166(3):1013–1021. doi: 10.1128/jb.166.3.1013-1021.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Feinstein S. I., Altman S. Coding properties of an ochre-suppressing derivative of Escherichia coli tRNAITyr. J Mol Biol. 1977 May 25;112(3):453–470. doi: 10.1016/s0022-2836(77)80192-7. [DOI] [PubMed] [Google Scholar]
  16. Feinstein S. I., Altman S. Context effects on nonsense codon suppression in Escherichia coli. Genetics. 1978 Feb;88(2):201–219. doi: 10.1093/genetics/88.2.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fluck M. M., Epstein R. H. Isolation and characterization of context mutations affecting the suppressibility of nonsense mutations. Mol Gen Genet. 1980;177(4):615–627. doi: 10.1007/BF00272672. [DOI] [PubMed] [Google Scholar]
  18. Fluck M. M., Salser W., Epstein R. H. The influence of the reading context upon the suppression of nonsense codons. Mol Gen Genet. 1977 Mar 7;151(2):137–149. doi: 10.1007/BF00338688. [DOI] [PubMed] [Google Scholar]
  19. Gefter M. L., Russell R. L. Role modifications in tyrosine transfer RNA: a modified base affecting ribosome binding. J Mol Biol. 1969 Jan 14;39(1):145–157. doi: 10.1016/0022-2836(69)90339-8. [DOI] [PubMed] [Google Scholar]
  20. Grosjean H., Nicoghosian K., Haumont E., Söll D., Cedergren R. Nucleotide sequences of two serine tRNAs with a GGA anticodon: the structure-function relationships in the serine family of E. coli tRNAs. Nucleic Acids Res. 1985 Aug 12;13(15):5697–5706. doi: 10.1093/nar/13.15.5697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hagervall T. G., Björk G. R. Undermodification in the first position of the anticodon of supG-tRNA reduces translational efficiency. Mol Gen Genet. 1984;196(2):194–200. doi: 10.1007/BF00328050. [DOI] [PubMed] [Google Scholar]
  22. Hall B., Gallant J. Defective translation in RC - cells. Nat New Biol. 1972 May 31;237(74):131–135. doi: 10.1038/newbio237131a0. [DOI] [PubMed] [Google Scholar]
  23. Kersten H. On the biological significance of modified nucleosides in tRNA. Prog Nucleic Acid Res Mol Biol. 1984;31:59–114. doi: 10.1016/s0079-6603(08)60375-x. [DOI] [PubMed] [Google Scholar]
  24. Loftfield R. B., Vanderjagt D. The frequency of errors in protein biosynthesis. Biochem J. 1972 Aug;128(5):1353–1356. doi: 10.1042/bj1281353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miller J. H., Albertini A. M. Effects of surrounding sequence on the suppression of nonsense codons. J Mol Biol. 1983 Feb 15;164(1):59–71. doi: 10.1016/0022-2836(83)90087-6. [DOI] [PubMed] [Google Scholar]
  26. Murgola E. J., Pagel F. T., Hijazi K. A. Codon context effects in missense suppression. J Mol Biol. 1984 May 5;175(1):19–27. doi: 10.1016/0022-2836(84)90442-x. [DOI] [PubMed] [Google Scholar]
  27. Murgola E. J., Prather N. E., Pagel F. T., Mims B. H., Hijazi K. A. Missense and nonsense suppressors derived from a glycine tRNA by nucleotide insertion and deletion in vivo. Mol Gen Genet. 1984;193(1):76–81. doi: 10.1007/BF00327417. [DOI] [PubMed] [Google Scholar]
  28. O'Farrell P. H. The suppression of defective translation by ppGpp and its role in the stringent response. Cell. 1978 Jul;14(3):545–557. doi: 10.1016/0092-8674(78)90241-6. [DOI] [PubMed] [Google Scholar]
  29. Parker J. Specific mistranslation in hisT mutants of Escherichia coli. Mol Gen Genet. 1982;187(3):405–409. doi: 10.1007/BF00332619. [DOI] [PubMed] [Google Scholar]
  30. Petrullo L. A., Gallagher P. J., Elseviers D. The role of 2-methylthio-N6-isopentenyladenosine in readthrough and suppression of nonsense codons in Escherichia coli. Mol Gen Genet. 1983;190(2):289–294. doi: 10.1007/BF00330653. [DOI] [PubMed] [Google Scholar]
  31. Pieczenik G. Predicting coding function from nucleotide sequence or survival of "fitness" of tRNA. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3539–3543. doi: 10.1073/pnas.77.6.3539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Putnam S. L., Koch A. L. Complications in the simplest cellular enzyme assay: lysis of Escherichia coli for the assay of beta-galactosidase. Anal Biochem. 1975 Feb;63(2):350–360. doi: 10.1016/0003-2697(75)90357-7. [DOI] [PubMed] [Google Scholar]
  33. Salser W., Fluck M., Epstein R. The influence of the reading context upon the suppression of nonsense codons. 3. Cold Spring Harb Symp Quant Biol. 1969;34:513–520. doi: 10.1101/sqb.1969.034.01.058. [DOI] [PubMed] [Google Scholar]
  34. Salser W. The influence of the reading context upon the suppression of nonsense codons. Mol Gen Genet. 1969 Oct 13;105(2):125–130. doi: 10.1007/BF00445682. [DOI] [PubMed] [Google Scholar]
  35. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983 Sep;47(3):410–453. doi: 10.1128/mr.47.3.410-453.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sprinzl M., Moll J., Meissner F., Hartmann T. Compilation of tRNA sequences. Nucleic Acids Res. 1985;13 (Suppl):r1–49. doi: 10.1093/nar/13.suppl.r1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  38. Vacher J., Grosjean H., Houssier C., Buckingham R. H. The effect of point mutations affecting Escherichia coli tryptophan tRNA on anticodon-anticodon interactions and on UGA suppression. J Mol Biol. 1984 Aug 5;177(2):329–342. doi: 10.1016/0022-2836(84)90460-1. [DOI] [PubMed] [Google Scholar]
  39. Vold B. S., Lazar J. M., Gray A. M. Characterization of a deficiency of N6-(delta 2-isopentenyl)-2-methylthioadenosine in the Escherichia coli mutant trpX by use of antibodies to N6-(delta 2-isopentenyl)adenosine. J Biol Chem. 1979 Aug 10;254(15):7362–7367. [PubMed] [Google Scholar]
  40. Wagner E. G., Kurland C. G. Translational accuracy enhanced in vitro by (p)ppGpp. Mol Gen Genet. 1980;180(1):139–145. doi: 10.1007/BF00267363. [DOI] [PubMed] [Google Scholar]
  41. Winston F., Botstein D., Miller J. H. Characterization of amber and ochre suppressors in Salmonella typhimurium. J Bacteriol. 1979 Jan;137(1):433–439. doi: 10.1128/jb.137.1.433-439.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yahata H., Ocada Y., Tsugita A. Adjacent effect on suppression efficiency. II. Study on ochre and amber mutants of T4 phage lysozyme. Mol Gen Genet. 1970;106(3):208–212. doi: 10.1007/BF00340380. [DOI] [PubMed] [Google Scholar]
  43. 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]
  44. Yarus M. Translational efficiency of transfer RNA's: uses of an extended anticodon. Science. 1982 Nov 12;218(4573):646–652. doi: 10.1126/science.6753149. [DOI] [PubMed] [Google Scholar]

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