Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Nov;175(22):7209–7215. doi: 10.1128/jb.175.22.7209-7215.1993

tRNA modification activity is necessary for Tet(M)-mediated tetracycline resistance.

V Burdett 1
PMCID: PMC206862  PMID: 8226667

Abstract

Tet(M) protein interacts with the protein biosynthetic machinery to render this process resistant to the tetracycline in vivo and in vitro (V. Burdett, J. Biol. Chem. 266:2872-2877, 1991). To understand this process more completely, a mutant of Escherichia coli which is altered in the ability of Tet(M) to confer resistance has been identified. This mutation maps to miaA and displays phenotypes characteristic of previously isolated miaA mutations. The miaA gene product modifies A37 adjacent to the anticodon of several tRNA species. Both the mutant isolated in this work and previously isolated miaA mutants confer tetracycline sensitivity in the presence of functional Tet(M), both share a slow growth phenotype, and in neither case is a wild-type phenotype restored in trans by F'112 carrying the 89- to 98-min region of the chromosome. These similar phenotypes further substantiate the assignment of the mutation described here to the miaA locus.

Full text

PDF
7209

Selected References

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

  1. Banuett F., Herskowitz I. Identification of polypeptides encoded by an Escherichia coli locus (hflA) that governs the lysis-lysogeny decision of bacteriophage lambda. J Bacteriol. 1987 Sep;169(9):4076–4085. doi: 10.1128/jb.169.9.4076-4085.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bouadloun F., Srichaiyo T., Isaksson L. A., Björk G. R. Influence of modification next to the anticodon in tRNA on codon context sensitivity of translational suppression and accuracy. J Bacteriol. 1986 Jun;166(3):1022–1027. doi: 10.1128/jb.166.3.1022-1027.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buck M., Griffiths E. Iron mediated methylthiolation of tRNA as a regulator of operon expression in Escherichia coli. Nucleic Acids Res. 1982 Apr 24;10(8):2609–2624. doi: 10.1093/nar/10.8.2609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burdett V., Inamine J., Rajagopalan S. Heterogeneity of tetracycline resistance determinants in Streptococcus. J Bacteriol. 1982 Mar;149(3):995–1004. doi: 10.1128/jb.149.3.995-1004.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Burdett V. Nucleotide sequence of the tet(M) gene of Tn916. Nucleic Acids Res. 1990 Oct 25;18(20):6137–6137. doi: 10.1093/nar/18.20.6137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burdett V. Purification and characterization of Tet(M), a protein that renders ribosomes resistant to tetracycline. J Biol Chem. 1991 Feb 15;266(5):2872–2877. [PubMed] [Google Scholar]
  8. Burdett V. Streptococcal tetracycline resistance mediated at the level of protein synthesis. J Bacteriol. 1986 Feb;165(2):564–569. doi: 10.1128/jb.165.2.564-569.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Connolly D. M., Winkler M. E. 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):3233–3246. doi: 10.1128/jb.171.6.3233-3246.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Connolly D. M., Winkler M. E. Structure of Escherichia coli K-12 miaA and characterization of the mutator phenotype caused by miaA insertion mutations. J Bacteriol. 1991 Mar;173(5):1711–1721. doi: 10.1128/jb.173.5.1711-1721.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dower W. J., Miller J. F., Ragsdale C. W. High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988 Jul 11;16(13):6127–6145. doi: 10.1093/nar/16.13.6127. [DOI] [PMC free article] [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. Epe B., Woolley P., Hornig H. Competition between tetracycline and tRNA at both P and A sites of the ribosome of Escherichia coli. FEBS Lett. 1987 Mar 23;213(2):443–447. doi: 10.1016/0014-5793(87)81539-9. [DOI] [PubMed] [Google Scholar]
  15. Geigenmüller U., Nierhaus K. H. Tetracycline can inhibit tRNA binding to the ribosomal P site as well as to the A site. Eur J Biochem. 1986 Dec 15;161(3):723–726. doi: 10.1111/j.1432-1033.1986.tb10499.x. [DOI] [PubMed] [Google Scholar]
  16. Goldman R. A., Cooperman B. S., Strycharz W. A., Williams B. A., Tritton T. R. Photoincorporation of tetracycline into Escherichia coli ribosomes. FEBS Lett. 1980 Aug 25;118(1):113–118. doi: 10.1016/0014-5793(80)81230-0. [DOI] [PubMed] [Google Scholar]
  17. Goldman R. A., Hasan T., Hall C. C., Strycharz W. A., Cooperman B. S. Photoincorporation of tetracycline into Escherichia coli ribosomes. Identification of the major proteins photolabeled by native tetracycline and tetracycline photoproducts and implications for the inhibitory action of tetracycline on protein synthesis. Biochemistry. 1983 Jan 18;22(2):359–368. doi: 10.1021/bi00271a020. [DOI] [PubMed] [Google Scholar]
  18. Halegoua S., Hirashima A., Inouye M. Puromycin-resistant biosynthesis of a specific outer-membrane lipoprotein of Escherichia coli. J Bacteriol. 1976 Apr;126(1):183–191. doi: 10.1128/jb.126.1.183-191.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hamel E., Koka M., Nakamoto T. Requirement of an Escherichia coli 50 S ribosomal protein component for effective interaction of the ribosome with T and G factors and with guanosine triphosphate. J Biol Chem. 1972 Feb 10;247(3):805–814. [PubMed] [Google Scholar]
  20. Kajitani M., Ishihama A. Identification and sequence determination of the host factor gene for bacteriophage Q beta. Nucleic Acids Res. 1991 Mar 11;19(5):1063–1066. doi: 10.1093/nar/19.5.1063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kleckner N., Chan R. K., Tye B. K., Botstein D. Mutagenesis by insertion of a drug-resistance element carrying an inverted repetition. J Mol Biol. 1975 Oct 5;97(4):561–575. doi: 10.1016/s0022-2836(75)80059-3. [DOI] [PubMed] [Google Scholar]
  22. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  23. Levy S. B., McMurry L. M., Burdett V., Courvalin P., Hillen W., Roberts M. C., Taylor D. E. Nomenclature for tetracycline resistance determinants. Antimicrob Agents Chemother. 1989 Aug;33(8):1373–1374. doi: 10.1128/aac.33.8.1373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Michel-Briand Y., Uccelli V., Laporte J. M., Plesiat P. Elimination of plasmids from Enterobacteriaceae by 4-quinolone derivatives. J Antimicrob Chemother. 1986 Dec;18(6):667–674. doi: 10.1093/jac/18.6.667. [DOI] [PubMed] [Google Scholar]
  25. Noda A., Courtright J. B., Denor P. F., Webb G., Kohara Y., Ishihama A. Rapid identification of specific genes in E. coli by hybridization to membranes containing the ordered set of phage clones. Biotechniques. 1991 Apr;10(4):474, 476-7. [PubMed] [Google Scholar]
  26. Oliva B., Chopra I. Tet determinants provide poor protection against some tetracyclines: further evidence for division of tetracyclines into two classes. Antimicrob Agents Chemother. 1992 Apr;36(4):876–878. doi: 10.1128/aac.36.4.876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Rasmussen B., Noller H. F., Daubresse G., Oliva B., Misulovin Z., Rothstein D. M., Ellestad G. A., Gluzman Y., Tally F. P., Chopra I. Molecular basis of tetracycline action: identification of analogs whose primary target is not the bacterial ribosome. Antimicrob Agents Chemother. 1991 Nov;35(11):2306–2311. doi: 10.1128/aac.35.11.2306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Salyers A. A., Speer B. S., Shoemaker N. B. New perspectives in tetracycline resistance. Mol Microbiol. 1990 Jan;4(1):151–156. doi: 10.1111/j.1365-2958.1990.tb02025.x. [DOI] [PubMed] [Google Scholar]
  30. Sancar A., Hack A. M., Rupp W. D. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. doi: 10.1128/jb.137.1.692-693.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sprinzl M., Hartmann T., Meissner F., Moll J., Vorderwülbecke T. Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Res. 1987;15 (Suppl):r53–188. doi: 10.1093/nar/15.suppl.r53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sternberg N. L., Maurer R. Bacteriophage-mediated generalized transduction in Escherichia coli and Salmonella typhimurium. Methods Enzymol. 1991;204:18–43. doi: 10.1016/0076-6879(91)04004-8. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Wolfe S. A., Smith J. M. Nucleotide sequence and analysis of the purA gene encoding adenylosuccinate synthetase of Escherichia coli K12. J Biol Chem. 1988 Dec 15;263(35):19147–19153. [PubMed] [Google Scholar]
  35. 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]
  36. Zurawski G., Brown K., Killingly D., Yanofsky C. Nucleotide sequence of the leader region of the phenylalanine operon of Escherichia coli. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4271–4275. doi: 10.1073/pnas.75.9.4271. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES