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. 1982 Apr 24;10(8):2609–2624. doi: 10.1093/nar/10.8.2609

Iron mediated methylthiolation of tRNA as a regulator of operon expression in Escherichia coli.

M Buck, E Griffiths
PMCID: PMC320637  PMID: 7043398

Abstract

E. coli growing in the presence of iron-binding proteins produced tRNAtrp and tRNAphe molecules containing i6A instead of ms2i6A adjacent to the anticodon. These undermodified tRNAs functioned less efficiently than the fully modified molecules when translating synthetic polynucleotides containing contiguous codons in an in vitro system, but did not limit the translation of MS2 RNA. We examined the possibility that the altered tRNAs with lowered translational efficiencies could relieve transcription termination at the trp and phe attenuators and lead to increased operon expression under iron restricted conditions. Using trpR mutants we found that there was indeed greater expression of the trp operon during iron restricted growth. This increase was attributable solely to the tRNA alteration induced by iron restriction.

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Selected References

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

  1. Agris P. F., Koh H., Söll D. The effect of growth temperatures on the in vivo ribose methylation of Bacillus stearothermophilus transfer RNA. Arch Biochem Biophys. 1973 Jan;154(1):277–282. doi: 10.1016/0003-9861(73)90058-1. [DOI] [PubMed] [Google Scholar]
  2. Camakaris H., Camakaris J., Pittard J. Regulation of aromatic amino acid biosynthesis in Escherichia coli K-12: control of the aroF-tyrA operon in the absence of repression control. J Bacteriol. 1980 Aug;143(2):613–620. doi: 10.1128/jb.143.2.613-620.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Griffiths E., Humphreys J. 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):503–513. doi: 10.1111/j.1432-1033.1978.tb12044.x. [DOI] [PubMed] [Google Scholar]
  6. Griffiths E., Rogers H. J., Bullen J. J. Iron, plasmids and infection. Nature. 1980 Apr 10;284(5756):508–509. doi: 10.1038/284508a0. [DOI] [PubMed] [Google Scholar]
  7. Hecht S. M., Kirkegaard L. H., Bock R. M. Chemical modifications of transfer RNA species. Desulfurization with Raney nickel. Proc Natl Acad Sci U S A. 1971 Jan;68(1):48–51. doi: 10.1073/pnas.68.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hoburg A., Aschhoff H. J., Kersten H., Manderschied U., Gassen H. G. Function of modified nucleosides 7-methylguanosine, ribothymidine, and 2-thiomethyl-N6-(isopentenyl)adenosine in procaryotic transfer ribonucleic acid. J Bacteriol. 1979 Nov;140(2):408–414. doi: 10.1128/jb.140.2.408-414.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Huang P. C., Mann M. B. Comparative fingerprint and composition analysis of the three forms of 32P-labeled phenylalanine tRNA from chloramphenicol-treated Escherichia coli. Biochemistry. 1974 Nov 5;13(23):4704–4710. doi: 10.1021/bi00720a004. [DOI] [PubMed] [Google Scholar]
  10. Ishida T., Sueoka N. Effect of ambient conditions on conformations of tryptophan transfer ribonucleic acid of Escherichia coli. J Biol Chem. 1968 Oct 25;243(20):5329–5336. [PubMed] [Google Scholar]
  11. Jones C. R., Kearns D. R. Nuclear magnetic resonance of the base-pairing structure of the native and denatured conformers of Escherichia coli transfer RNATrp. J Mol Biol. 1976 Jun 5;103(4):747–764. doi: 10.1016/0022-2836(76)90207-2. [DOI] [PubMed] [Google Scholar]
  12. Joseph D. R., Muench K. H. Tryptophanyl transfer ribonucleic acid synthetase of Escherichia coli. I. Purification of the enzyme and of tryptrophan transfer ribonucleic acid. J Biol Chem. 1971 Dec 25;246(24):7602–7609. [PubMed] [Google Scholar]
  13. Juarez H., Skjold A. C., Hedgcoth C. Precursor relationship of phenylalanine transfer ribonucleic acid from Escherichia coli treated with chloramphenicol or starved for iron, methionine, or cysteine. J Bacteriol. 1975 Jan;121(1):44–54. doi: 10.1128/jb.121.1.44-54.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kitchingman G. R., Fournier M. J. Modification-deficient transfer ribonucleic acids from relaxed control Escherichia coli: structures of the major undermodified phenylalanine and leucine transfer RNAs produced during leucine starvation. Biochemistry. 1977 May 17;16(10):2213–2220. doi: 10.1021/bi00629a027. [DOI] [PubMed] [Google Scholar]
  15. Kitchingman G. R., Webb E., Fournier M. J. Unique phenylalanine transfer ribonucleic acids in relaxed control Escherichia coli: genetic origin and some functional properties. Biochemistry. 1976 May 4;15(9):1848–1857. doi: 10.1021/bi00654a010. [DOI] [PubMed] [Google Scholar]
  16. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  17. Laten H., Gorman J., Bock R. M. Isopentenyladenosine deficient tRNA from an antisuppressor mutant of Saccharomyces cerevisiae. Nucleic Acids Res. 1978 Nov;5(11):4329–4342. doi: 10.1093/nar/5.11.4329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lee F., Bertrand K., Bennett G., Yanofsky C. Comparison of the nucleotide sequences of the initial transcribed regions of the tryptophan operons of Escherichia coli and Salmonella typhimurium. J Mol Biol. 1978 May 15;121(2):193–217. doi: 10.1016/s0022-2836(78)80005-9. [DOI] [PubMed] [Google Scholar]
  19. MONOD J., COHEN-BAZIRE G., COHN M. Sur la biosynthèse de la beta-galactosidase (lactase) chez Escherichia coli; la spécificité de l'induction. Biochim Biophys Acta. 1951 Nov;7(4):585–599. doi: 10.1016/0006-3002(51)90072-8. [DOI] [PubMed] [Google Scholar]
  20. Mann M. B., Huang P. C. Behavior of chloramphenicol-induced phenylalanine transfer ribonucleic acid during recovery from chloramphenicol treatment in Escherichia coli. Biochemistry. 1973 Dec 18;12(26):5289–5294. doi: 10.1021/bi00750a011. [DOI] [PubMed] [Google Scholar]
  21. McCandliss R. J., Herrmann K. M. Iron, an essential element for biosynthesis of aromatic compounds. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4810–4813. doi: 10.1073/pnas.75.10.4810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McCray J. W., Jr, Herrmann K. M. Derepression of certain aromatic amino acid biosynthetic enzymes of Escherichia coli K-12 by growth in Fe3+-deficient medium. J Bacteriol. 1976 Feb;125(2):608–615. doi: 10.1128/jb.125.2.608-615.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rogers H. J., Synge C., Kimber B., Bayley P. M. Production of enterochelin by Escherichia coli 0111. Biochim Biophys Acta. 1977 Apr 27;497(2):548–557. doi: 10.1016/0304-4165(77)90211-2. [DOI] [PubMed] [Google Scholar]
  24. Rose J. K., Mosteller R. D., Yanofsky C. Tryptophan messenger ribonucleic acid elongation rates and steady-state levels of tryptophan operon enzymes under various growth conditions. J Mol Biol. 1970 Aug;51(3):541–550. doi: 10.1016/0022-2836(70)90007-0. [DOI] [PubMed] [Google Scholar]
  25. Rose J. K., Yanofsky C. Metabolic regulation of the tryptophan operon of Escherichia coli: repressor-independent regulation of transcription initiation frequency. J Mol Biol. 1972 Aug 14;69(1):103–118. doi: 10.1016/0022-2836(72)90026-5. [DOI] [PubMed] [Google Scholar]
  26. Rosenberg A. H., Gefter M. L. An iron-dependent modification of several transfer RNA species in Escherichia coli. J Mol Biol. 1969 Dec 28;46(3):581–584. doi: 10.1016/0022-2836(69)90197-1. [DOI] [PubMed] [Google Scholar]
  27. Stulberg M. P., Sutton M., Isham K. R. Undermethylated transfer RNA does not support phage RNA-directed in vitro protein synthesis. Biochim Biophys Acta. 1976 Jul 2;435(3):251–257. doi: 10.1016/0005-2787(76)90106-4. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Wettstein F. O., Stent G. S. Physiologically induced changes in the property of phenylalanine tRNA in Escherichia coli. J Mol Biol. 1968 Nov 28;38(1):25–40. doi: 10.1016/0022-2836(68)90126-5. [DOI] [PubMed] [Google Scholar]
  30. Yanofsky C. Attenuation in the control of expression of bacterial operons. Nature. 1981 Feb 26;289(5800):751–758. doi: 10.1038/289751a0. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]

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