Home LiteratureArticle Details
PMID: 7536729 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The methylthio group (ms2) of N6-(4-hydroxyisopentenyl)-2-methylthioadenosine (ms2io6A) present next to the anticodon contributes to the decoding efficiency of the tRNA.

Journal of bacteriology ·Vol. 177 ·No. 8 ·1995-04-00 ·Pages 1967-75

Esberg B, Björk GR

Abstract

A Salmonella typhimurium LT2 mutant which harbors a mutation (miaB2508::Tn10dCm) that results in a reduction in the activities of the amber suppressors supF30 (tRNA(CUATyr)), supD10 (tRNA(CUASer)), and supJ60 (tRNA(CUALeu)) was isolated. The mutant was deficient in the methylthio group (ms2) of N6-(4-hydroxyisopentenyl)-2-methylthioadenosine (ms2io6A), a modified nucleoside that is normally present next to the anticodon (position 37) in tRNAs that read codons that start with uridine. Consequently, the mutant had i6A37 instead of ms2io6A37 in its tRNA. Only small amounts of io6A37 was found. We suggest that the synthesis of ms2io6A occurs in the following order: A-37-->i6A37-->ms2i6A37-->ms2io6A37. The mutation miaB2508::Tn10dCm was 60% linked to the nag gene (min 15) and 40% linked to the fur gene and is located counterclockwise from both of these genes. The growth rates of the mutant in four growth media did not significantly deviate from those of a wild-type strain. The polypeptide chain elongation rate was also unaffected in the mutant. However, the miaB2508::Tn10dCm mutation rendered the cell more resistant or sensitive, compared with a wild-type cell, to several amino acid analogs, suggesting that this mutation influences the regulation of several amino acid biosynthetic operons. The efficiencies of the aforementioned amber suppressors were decreased to as low as 16%, depending on the suppressor and the codon context monitored, demonstrating that the ms2 group of ms2io6A contributes to the decoding efficiency of tRNA. However, the major impact of the ms2io6 modification in the decoding process comes from the io6 group alone or from the combination of the ms2 and io6 groups, not from the ms2 group alone.

Related Genes
MeSH Terms
Anticodon/chemistry,genetics Base Sequence Codon/genetics Genes, Bacterial Isopentenyladenosine/analogs & derivatives,chemistry Molecular Sequence Data Molecular Structure Mutation RNA, Bacterial/chemistry,genetics RNA, Transfer, Amino Acid-Specific/chemistry,genetics Salmonella typhimurium/genetics,growth & development,metabolism Suppression, Genetic
Chemicals
Anticodon Codon RNA, Bacterial RNA, Transfer, Amino Acid-Specific N(6)-(4-hydroxyisopentenyl)-2-methylthioadenosine Isopentenyladenosine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Esberg B
Department of Microbiology, Umeå University, Sweden.
Björk G R
References (57)
57 references, click to expand
  1. Characterization of Tn10d-Cam: a transposition-defective Tn10 specifying chloramphenicol resistance.
    Mol Gen Genet. 1988 Aug;213(2-3):332-8 PMID: 2847006
  2. Phage P22-mutants with increased or decreased transduction abilities.
    Mol Gen Genet. 1972;119(1):75-88 PMID: 4564719
  3. Transfer RNA structure and coding specificity. I. Evidence that a D-arm mutation reduces tRNA dissociation from the ribosome.
    J Mol Biol. 1989 Apr 5;206(3):489-501 PMID: 2469803
  4. Genetic and physiological relationships among the miaA gene, 2-methylthio-N6-(delta 2-isopentenyl)-adenosine tRNA modification, and spontaneous mutagenesis in Escherichia coli K-12.
    J Bacteriol. 1989 Jun;171(6):3233-46 PMID: 2656644
  5. Temperature jump relaxation studies on the interactions between transfer RNAs with complementary anticodons. The effect of modified bases adjacent to the anticodon triplet.
    J Biomol Struct Dyn. 1985 Oct;3(2):387-408 PMID: 3917029
  6. tRNA(Trp) translation of leader peptide codon 12 and other factors that regulate expression of the tryptophanase operon.
    J Bacteriol. 1990 Jun;172(6):3100-7 PMID: 2345136
  7. Fluorescence characterization of the interaction of various transfer RNA species with elongation factor Tu.GTP: evidence for a new functional role for elongation factor Tu in protein biosynthesis.
    Biochemistry. 1990 May 8;29(18):4268-77 PMID: 2190631
  8. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576-9 PMID: 2112744
  9. tRNA anticodons with the modified nucleoside 2-methylthio-N6-(4-hydroxyisopentenyl)adenosine distinguish between bases 3' of the codon.
    J Mol Biol. 1991 Apr 5;218(3):509-16 PMID: 2016742
  10. ms2i6A deficiency enhances proofreading in translation.
    J Mol Biol. 1991 Dec 20;222(4):1161-71 PMID: 1762149
  11. Rapid mapping in Salmonella typhimurium with Mud-P22 prophages.
    J Bacteriol. 1992 Mar;174(5):1673-81 PMID: 1311301
  12. Induction kinetics of the L-arabinose operon of Escherichia coli.
    J Bacteriol. 1973 Jul;115(1):9-14 PMID: 4577756
  13. Lac repressor can be fused to beta-galactosidase.
    Nature. 1974 Jun 7;249(457):561-3 PMID: 4599764
  14. Pleiotropy of hisT mutants blocked in pseudouridine synthesis in tRNA: leucine and isoleucine-valine operons.
    Proc Natl Acad Sci U S A. 1974 May;71(5):1857-61 PMID: 4151955
  15. Culture medium for enterobacteria.
    J Bacteriol. 1974 Sep;119(3):736-47 PMID: 4604283
  16. Complications in the simplest cellular enzyme assay: lysis of Escherichia coli for the assay of beta-galactosidase.
    Anal Biochem. 1975 Feb;63(2):350-60 PMID: 1092200
  17. Maturation of a hypermodified nucleoside in transfer RNA.
    Nucleic Acids Res. 1975 May;2(5):691-8 PMID: 49880
  18. Physiological and biochemical studies on the function of 5-methyluridine in the transfer ribonucleic acid of Escherichia coli.
    J Bacteriol. 1975 Oct;124(1):99-111 PMID: 1100618
  19. Chemical measurement of steady-state levels of ten aminoacyl-transfer ribonucleic acid synthetases in Escherichia coli.
    J Bacteriol. 1977 Jan;129(1):378-87 PMID: 318645
  20. Generalized indicator plate for genetic, metabolic, and taxonomic studies with microorganisms.
    Appl Environ Microbiol. 1977 Feb;33(2):434-44 PMID: 322611
  21. 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):663-77 PMID: 330867
  22. Alterations in tRNAs containing 2-methylthio-N6-(delta2-isopentenyl)-adenosine during growth of enteropathogenic Escherichia coli in the presence of iron-binding proteins.
    Eur J Biochem. 1978 Jan 16;82(2):503-13 PMID: 342239
  23. Alterations in the tRNA's of Escherichia coli recovered from lethally infected animals.
    Infect Immun. 1978 Nov;22(2):312-7 PMID: 365754
  24. beta-Galactosidase chimeras: primary structure of a lac repressor-beta-galactosidase protein.
    Proc Natl Acad Sci U S A. 1978 Oct;75(10):4824-7 PMID: 105358
  25. 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):7362-7 PMID: 379002
  26. The effect of an Escherichia coli regulatory mutation on transfer RNA structure.
    J Mol Biol. 1979 Nov 25;135(1):111-26 PMID: 93644
  27. The influence of codon context on genetic code translation.
    Nature. 1980 Jul 10;286(5769):123-7 PMID: 7402305
  28. Selection for loss of tetracycline resistance by Escherichia coli.
    J Bacteriol. 1981 Feb;145(2):1110-1 PMID: 7007341
  29. Positive selection for loss of tetracycline resistance.
    J Bacteriol. 1980 Aug;143(2):926-33 PMID: 6259126
  30. Regulation of aromatic amino acid transport by tRNA: role of 2-methylthio-N6-(delta2-isopentenyl)-adenosine.
    Nucleic Acids Res. 1981 Jan 24;9(2):401-14 PMID: 7010315
  31. Iron mediated methylthiolation of tRNA as a regulator of operon expression in Escherichia coli.
    Nucleic Acids Res. 1982 Apr 24;10(8):2609-24 PMID: 7043398
  32. Quantitative enzymatic hydrolysis of tRNAs: reversed-phase high-performance liquid chromatography of tRNA nucleosides.
    J Chromatogr. 1982 Jul 9;230(2):297-308 PMID: 7050138
  33. Effects of surrounding sequence on the suppression of nonsense codons.
    J Mol Biol. 1983 Feb 15;164(1):59-71 PMID: 6188840
  34. Complete analysis of tRNA-modified nucleosides by high-performance liquid chromatography: the 29 modified nucleosides of Salmonella typhimurium and Escherichia coli tRNA.
    Anal Biochem. 1983 Feb 15;129(1):1-13 PMID: 6190418
  35. 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):523-31 PMID: 6362893
  36. 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):329-42 PMID: 6379198
  37. 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):5697-706 PMID: 3898020
  38. Pleiotropic effects induced by modification deficiency next to the anticodon of tRNA from Salmonella typhimurium LT2.
    J Bacteriol. 1986 Jun;166(3):1013-21 PMID: 2423501
  39. Influence of modification next to the anticodon in tRNA on codon context sensitivity of translational suppression and accuracy.
    J Bacteriol. 1986 Jun;166(3):1022-7 PMID: 3086285
  40. Genetic analysis in Salmonella typhimurium with a small collection of randomly spaced insertions of transposon Tn10 delta 16 delta 17.
    J Bacteriol. 1987 May;169(5):1787-93 PMID: 3032894
  41. Transfer RNA modification.
    Annu Rev Biochem. 1987;56:263-87 PMID: 3304135
  42. Effects of miaA on translation and growth rates.
    Mol Gen Genet. 1987 Jul;208(3):373-6 PMID: 3312947
  43. Molecular cloning of the Escherichia coli miaA gene involved in the formation of delta 2-isopentenyl adenosine in tRNA.
    J Bacteriol. 1988 Sep;170(9):4147-52 PMID: 3045085
  44. The gene for a tRNA modifying enzyme, m5U54-methyltransferase, is essential for viability in Escherichia coli.
    Proc Natl Acad Sci U S A. 1992 May 1;89(9):3995-8 PMID: 1373891
  45. Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron- and pH-regulated protein synthesis.
    J Bacteriol. 1992 Jul;174(13):4317-23 PMID: 1624426
  46. Isolation of the gene (miaE) encoding the hydroxylase involved in the synthesis of 2-methylthio-cis-ribozeatin in tRNA of Salmonella typhimurium and characterization of mutants.
    J Bacteriol. 1993 Dec;175(24):7776-85 PMID: 8253666
  47. Regulatory circuits involved with pH-regulated gene expression in Salmonella typhimurium.
    Microbiology. 1994 Feb;140 ( Pt 2):341-52 PMID: 8180699
  48. Summary: the modified nucleosides of RNA.
    Nucleic Acids Res. 1994 Jun 25;22(12):2183-96 PMID: 7518580
  49. vacC, a virulence-associated chromosomal locus of Shigella flexneri, is homologous to tgt, a gene encoding tRNA-guanine transglycosylase (Tgt) of Escherichia coli K-12.
    J Bacteriol. 1994 Aug;176(15):4627-34 PMID: 8045893
  50. Synthesis and function of isopentenyl adenosine derivatives in tRNA.
    Biochimie. 1994;76(12):1152-60 PMID: 7748950
  51. Acetylornithinase of Escherichia coli: partial purification and some properties.
    J Biol Chem. 1956 Jan;218(1):97-106 PMID: 13278318
  52. The in vitro synthesis of 2'-omethylguanosine and 2-methylthio 6N (gamma,gamma, dimethylallyl) adenosine in transfer RNA of Escherichia coli.
    Biochem Biophys Res Commun. 1969 Aug 7;36(3):435-41 PMID: 4898378
  53. An iron-dependent modification of several transfer RNA species in Escherichia coli.
    J Mol Biol. 1969 Dec 28;46(3):581-4 PMID: 4904109
  54. 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):1481-7 PMID: 4326583
  55. Role modifications in tyrosine transfer RNA: a modified base affecting ribosome binding.
    J Mol Biol. 1969 Jan 14;39(1):145-57 PMID: 4938812
  56. Physiologically induced changes in the property of phenylalanine tRNA in Escherichia coli.
    J Mol Biol. 1968 Nov 28;38(1):25-40 PMID: 4941472
  57. 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):409-13 PMID: 2643111
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1995-04-00
Pages
1967-75
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC176837
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