Abstract
sufS was found to suppress the only known suppressible-1 frameshift mutation, trpE91, at a site identified as GGA and mapped within the single gene of the only tRNA that can decode GGA in Escherichia coli. It mapped to the same gene in Salmonella typhimurium. sufS alleles were recessive, and dominant alleles could not be isolated. This is in contrast to all other tRNA structural gene mutations identified thus far that cause frameshift suppression. The recessiveness implies that all sufS alleles are poor competitors against their wild-type tRNA(Gly2) counterparts. The base G immediately 5' of the GGA suppression site influenced the level but was not critical for suppression by sufS601. From this result, it is inferred that sufS601 causes frameshifting by doublet decoding.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- An G., Friesen J. D. The nucleotide sequence of tufB and four nearby tRNA structural genes of Escherichia coli. Gene. 1980 Dec;12(1-2):33–39. doi: 10.1016/0378-1119(80)90013-x. [DOI] [PubMed] [Google Scholar]
- Atkins J. F., Elseviers D., Gorini L. Low activity of -galactosidase in frameshift mutants of Escherichia coli. Proc Natl Acad Sci U S A. 1972 May;69(5):1192–1195. doi: 10.1073/pnas.69.5.1192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Atkins J. F., Nichols B. P., Thompson S. The nucleotide sequence of the first externally suppressible--1 frameshift mutant, and of some nearby leaky frameshift mutants. EMBO J. 1983;2(8):1345–1350. doi: 10.1002/j.1460-2075.1983.tb01590.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Atkins J. F., Ryce S. UGA and non-triplet suppressor reading of the genetic code. Nature. 1974 Jun 7;249(457):527–530. doi: 10.1038/249527a0. [DOI] [PubMed] [Google Scholar]
- Bonekamp F., Jensen K. F. The AGG codon is translated slowly in E. coli even at very low expression levels. Nucleic Acids Res. 1988 Apr 11;16(7):3013–3024. doi: 10.1093/nar/16.7.3013. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bossi L., Smith D. M. Suppressor sufJ: a novel type of tRNA mutant that induces translational frameshifting. Proc Natl Acad Sci U S A. 1984 Oct;81(19):6105–6109. doi: 10.1073/pnas.81.19.6105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brierley I., Boursnell M. E., Binns M. M., Bilimoria B., Blok V. C., Brown T. D., Inglis S. C. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J. 1987 Dec 1;6(12):3779–3785. doi: 10.1002/j.1460-2075.1987.tb02713.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bruce A. G., Atkins J. F., Gesteland R. F. tRNA anticodon replacement experiments show that ribosomal frameshifting can be caused by doublet decoding. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5062–5066. doi: 10.1073/pnas.83.14.5062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buckley K. J., Hayashi M. Role of premature translational termination in the regulation of expression of the phi X174 lysis gene. J Mol Biol. 1987 Dec 20;198(4):599–607. doi: 10.1016/0022-2836(87)90203-8. [DOI] [PubMed] [Google Scholar]
- Chang S., Carbon J. The nucleotide sequence of a precursor to the glycine- and threonine-specific transfer ribonucleic acids of Escherichia coli. J Biol Chem. 1975 Jul 25;250(14):5542–5555. [PubMed] [Google Scholar]
- Chen E. Y., Seeburg P. H. Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA. 1985 Apr;4(2):165–170. doi: 10.1089/dna.1985.4.165. [DOI] [PubMed] [Google Scholar]
- Colson C., Van Pel A. DNA restriction and modification systems in Salmonella. I. SA and SB, two Salmonella typhimurium systems determined by genes with a chromosomal location comparable to that of the Escherichia coli hsd genes. Mol Gen Genet. 1974 Apr 3;129(4):325–337. doi: 10.1007/BF00265696. [DOI] [PubMed] [Google Scholar]
- Dayhuff T. J., Atkins J. F., Gesteland R. F. Characterization of ribosomal frameshift events by protein sequence analysis. J Biol Chem. 1986 Jun 5;261(16):7491–7500. [PubMed] [Google Scholar]
- Dunn J. J., Studier F. W. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol. 1983 Jun 5;166(4):477–535. doi: 10.1016/s0022-2836(83)80282-4. [DOI] [PubMed] [Google Scholar]
- Falahee M. B., Weiss R. B., O'Connor M., Doonan S., Gesteland R. F., Atkins J. F. Mutants of translational components that alter reading frame by two steps forward or one step back. J Biol Chem. 1988 Dec 5;263(34):18099–18103. [PubMed] [Google Scholar]
- Greeb J., Atkins J. F., Loper J. C. Histidinol dehydrogenase (his D) mutants of Salmonella typhimurium. J Bacteriol. 1971 May;106(2):421–431. doi: 10.1128/jb.106.2.421-431.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartman P. E., Hartman Z., Stahl R. C. Classification and mapping of spontaneous and induced mutations in the histidine operon of Salmonella. Adv Genet. 1971;16:1–34. doi: 10.1016/s0065-2660(08)60352-1. [DOI] [PubMed] [Google Scholar]
- Heller K., Mann B. J., Kadner R. J. Cloning and expression of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J Bacteriol. 1985 Mar;161(3):896–903. doi: 10.1128/jb.161.3.896-903.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoppe I., Johnston H. M., Biek D., Roth J. R. A refined map of the hisG gene of Salmonella typhimurium. Genetics. 1979 May;92(1):17–26. doi: 10.1093/genetics/92.1.17. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudson L., Rossi J., Landy A. Dual function transcripts specifying tRNA and mRNA. Nature. 1981 Dec 3;294(5840):422–427. doi: 10.1038/294422a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes D., Atkins J. F., Thompson S. Mutants of elongation factor Tu promote ribosomal frameshifting and nonsense readthrough. EMBO J. 1987 Dec 20;6(13):4235–4239. doi: 10.1002/j.1460-2075.1987.tb02772.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes D. The isolation and mapping of EF-Tu mutations in Salmonella typhimurium. Mol Gen Genet. 1986 Jan;202(1):108–111. doi: 10.1007/BF00330525. [DOI] [PubMed] [Google Scholar]
- Hughes D., Thompson S., O'Connor M., Tuohy T., Nichols B. P., Atkins J. F. Genetic characterization of frameshift suppressors with new decoding properties. J Bacteriol. 1989 Feb;171(2):1028–1034. doi: 10.1128/jb.171.2.1028-1034.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jacks T., Madhani H. D., Masiarz F. R., Varmus H. E. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell. 1988 Nov 4;55(3):447–458. doi: 10.1016/0092-8674(88)90031-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jin D. J., Gross C. A. Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J Mol Biol. 1988 Jul 5;202(1):45–58. doi: 10.1016/0022-2836(88)90517-7. [DOI] [PubMed] [Google Scholar]
- Kawakami K., Inada T., Nakamura Y. 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):5378–5381. doi: 10.1128/jb.170.11.5378-5381.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawakami K., Jönsson Y. H., Björk G. R., Ikeda H., Nakamura Y. Chromosomal location and structure of the operon encoding peptide-chain-release factor 2 of Escherichia coli. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5620–5624. doi: 10.1073/pnas.85.15.5620. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kohno T., Roth J. R. Proflavin mutagenesis of bacteria. J Mol Biol. 1974 Oct 15;89(1):17–32. doi: 10.1016/0022-2836(74)90160-0. [DOI] [PubMed] [Google Scholar]
- Murgola E. J., Pagel F. T. Codon recognition by glycine transfer RNAs of Escherichia coli in vivo. J Mol Biol. 1980 Apr 25;138(4):833–844. doi: 10.1016/0022-2836(80)90067-4. [DOI] [PubMed] [Google Scholar]
- Murgola E. J. tRNA, suppression, and the code. Annu Rev Genet. 1985;19:57–80. doi: 10.1146/annurev.ge.19.120185.000421. [DOI] [PubMed] [Google Scholar]
- Ovchinnikov Y. A., Monastyrskaya G. S., Guriev S. O., Kalinina N. F., Sverdlov E. D., Gragerov A. I., Bass I. A., Kiver I. F., Moiseyeva E. P., Igumnov V. N. RNA polymerase rifampicin resistance mutations in Escherichia coli: sequence changes and dominance. Mol Gen Genet. 1983;190(2):344–348. doi: 10.1007/BF00330662. [DOI] [PubMed] [Google Scholar]
- Pope W. T., Reeves R. H. Purification and characterization of a tRNA methylase from Salmonella typhimurium. J Bacteriol. 1978 Oct;136(1):191–200. doi: 10.1128/jb.136.1.191-200.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reeves R. H., Roth J. R. Transfer ribonucleic acid methylase deficiency found in UGA supressor strains. J Bacteriol. 1975 Oct;124(1):332–340. doi: 10.1128/jb.124.1.332-340.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Riddle D. L., Roth J. R. Frameshift suppressors. II. Genetic mapping and dominance studies. J Mol Biol. 1972 May 28;66(3):483–493. doi: 10.1016/0022-2836(72)90428-7. [DOI] [PubMed] [Google Scholar]
- Riyasaty S., Atkins J. F. External suppression of a frameshift mutant in salmonella. J Mol Biol. 1968 Jun 28;34(3):541–557. doi: 10.1016/0022-2836(68)90179-4. [DOI] [PubMed] [Google Scholar]
- Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, edition VII. Microbiol Rev. 1988 Dec;52(4):485–532. doi: 10.1128/mr.52.4.485-532.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Squires C., Carbon J., Hill C. W. Glycine transfer RNA of Escherichia coli. I. Structural genes for two glycine tRNA species. J Mol Biol. 1970 Sep 28;52(3):557–569. doi: 10.1016/0022-2836(70)90419-5. [DOI] [PubMed] [Google Scholar]
- Van Delft J. H., Bosch L. Control of the tRNA-tufB operon in Escherichia coli. 3. Feedback inhibition of tufB expression by an EF-Tu with a deletion in the guanine-nucleotide-binding domain. Eur J Biochem. 1988 Aug 1;175(2):375–378. doi: 10.1111/j.1432-1033.1988.tb14206.x. [DOI] [PubMed] [Google Scholar]
- Van Delft J. H., Schmidt D. S., Bosch L. The tRNA-tufB operon transcription termination and processing upstream from tufB. J Mol Biol. 1987 Oct 20;197(4):647–657. doi: 10.1016/0022-2836(87)90471-2. [DOI] [PubMed] [Google Scholar]
- Way J. C., Davis M. A., Morisato D., Roberts D. E., Kleckner N. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene. 1984 Dec;32(3):369–379. doi: 10.1016/0378-1119(84)90012-x. [DOI] [PubMed] [Google Scholar]
- Weiss R. B., Dunn D. M., Atkins J. F., Gesteland R. F. 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;52:687–693. doi: 10.1101/sqb.1987.052.01.078. [DOI] [PubMed] [Google Scholar]
- Whitfield H. J., Jr, Martin R. G., Ames B. N. Classification of aminotransferase (C gene) mutants in the histidine operon. J Mol Biol. 1966 Nov 14;21(2):335–355. doi: 10.1016/0022-2836(66)90103-3. [DOI] [PubMed] [Google Scholar]
- Wilson W., Braddock M., Adams S. E., Rathjen P. D., Kingsman S. M., Kingsman A. J. HIV expression strategies: ribosomal frameshifting is directed by a short sequence in both mammalian and yeast systems. Cell. 1988 Dec 23;55(6):1159–1169. doi: 10.1016/0092-8674(88)90260-7. [DOI] [PubMed] [Google Scholar]