Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1992 Aug 11;20(15):3911–3917. doi: 10.1093/nar/20.15.3911

The effects of a unique D-loop structure of a minor tRNA(UUALeu) from Streptomyces on its structural stability and amino acid accepting activity.

Y Ueda 1, I Kumagai 1, K Miura 1
PMCID: PMC334066  PMID: 1380690

Abstract

Streptomyces bldA gene, which encodes a tRNA corresponding to a very minor leucine codon, UUA, regulates pleiotropic gene expression which is involved in sporulation and secondary metabolism. The unique structural feature of this tRNA is the lack of GG sequence in dihydrouridine loop (D-loop) that generally is conserved in tRNAs involved in cytoplasmic protein biosynthesis. In order to investigate the relationship between the D-loop structure and the stability and leucine accepting activity of this tRNA, the wild and D-loop mutant tRNA transcripts were constructed with T7 RNA polymerase in vitro. The wild type tRNA(UUALeu) showed the structural stability and leucine accepting activity at physiological temperature for Streptomyces. The E.coli type D-loop mutant, which has a larger loop size and contains a GG doublet, exhibited increased thermostability. The kinetical analyses of the aminoacylation reaction of tRNA(UUALeu) with S.lividans and E.coli leucyl-tRNA synthetase (LeuRS) suggest there is a unique recognition mechanism of Streptomyces LeuRS toward tRNA(UUALeu).

Full text

PDF
3911

Images in this article

Selected References

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

  1. Babcock M. J., Kendrick K. E. Transcriptional and translational features of a sporulation gene of Streptomyces griseus. Gene. 1990 Oct 30;95(1):57–63. doi: 10.1016/0378-1119(90)90413-l. [DOI] [PubMed] [Google Scholar]
  2. Blank H. U., Söll D. The nucleotide sequence of two leucine tRNA species from Escherichia coli K12. Biochem Biophys Res Commun. 1971 Jun 4;43(5):1192–1197. doi: 10.1016/0006-291x(71)90589-4. [DOI] [PubMed] [Google Scholar]
  3. Chen K. S., Peters T. C., Walker J. R. A minor arginine tRNA mutant limits translation preferentially of a protein dependent on the cognate codon. J Bacteriol. 1990 May;172(5):2504–2510. doi: 10.1128/jb.172.5.2504-2510.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen M. X., Bouquin N., Norris V., Casarégola S., Séror S. J., Holland I. B. A single base change in the acceptor stem of tRNA(3Leu) confers resistance upon Escherichia coli to the calmodulin inhibitor, 48/80. EMBO J. 1991 Oct;10(10):3113–3122. doi: 10.1002/j.1460-2075.1991.tb07865.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Donis-Keller H. Phy M: an RNase activity specific for U and A residues useful in RNA sequence analysis. Nucleic Acids Res. 1980 Jul 25;8(14):3133–3142. doi: 10.1093/nar/8.14.3133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Epp J. K., Burgett S. G., Schoner B. E. Cloning and nucleotide sequence of a carbomycin-resistance gene from Streptomyces thermotolerans. Gene. 1987;53(1):73–83. doi: 10.1016/0378-1119(87)90094-1. [DOI] [PubMed] [Google Scholar]
  7. Fernández-Moreno M. A., Caballero J. L., Hopwood D. A., Malpartida F. The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces. Cell. 1991 Aug 23;66(4):769–780. doi: 10.1016/0092-8674(91)90120-n. [DOI] [PubMed] [Google Scholar]
  8. Garcia G. M., Mar P. K., Mullin D. A., Walker J. R., Prather N. E. The E. coli dnaY gene encodes an arginine transfer RNA. Cell. 1986 May 9;45(3):453–459. doi: 10.1016/0092-8674(86)90331-4. [DOI] [PubMed] [Google Scholar]
  9. Hara O., Hutchinson C. R. Cloning of midecamycin(MLS)-resistance genes from Streptomyces mycarofaciens, Streptomyces lividans and Streptomyces coelicolor A3(2). J Antibiot (Tokyo) 1990 Aug;43(8):977–991. doi: 10.7164/antibiotics.43.977. [DOI] [PubMed] [Google Scholar]
  10. Heinzel P., Werbitzky O., Distler J., Piepersberg W. A second streptomycin resistance gene from Streptomyces griseus codes for streptomycin-3"-phosphotransferase. Relationships between antibiotic and protein kinases. Arch Microbiol. 1988;150(2):184–192. doi: 10.1007/BF00425160. [DOI] [PubMed] [Google Scholar]
  11. Hopwood D. A., Bibb M. J., Chater K. F., Kieser T. Plasmid and phage vectors for gene cloning and analysis in Streptomyces. Methods Enzymol. 1987;153:116–166. doi: 10.1016/0076-6879(87)53052-x. [DOI] [PubMed] [Google Scholar]
  12. Horii M., Ishizaki T., Paik S. Y., Manome T., Murooka Y. An operon containing the genes for cholesterol oxidase and a cytochrome P-450-like protein from a Streptomyces sp. J Bacteriol. 1990 Jul;172(7):3644–3653. doi: 10.1128/jb.172.7.3644-3653.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kumagai I., Pieler T., Subramanian A. R., Erdmann V. A. Nucleotide sequence and secondary structure analysis of spinach chloroplast 4.5 S RNA. J Biol Chem. 1982 Nov 10;257(21):12924–12928. [PubMed] [Google Scholar]
  14. Lawlor E. J., Baylis H. A., Chater K. F. Pleiotropic morphological and antibiotic deficiencies result from mutations in a gene encoding a tRNA-like product in Streptomyces coelicolor A3(2). Genes Dev. 1987 Dec;1(10):1305–1310. doi: 10.1101/gad.1.10.1305. [DOI] [PubMed] [Google Scholar]
  15. Leskiw B. K., Lawlor E. J., Fernandez-Abalos J. M., Chater K. F. TTA codons in some genes prevent their expression in a class of developmental, antibiotic-negative, Streptomyces mutants. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2461–2465. doi: 10.1073/pnas.88.6.2461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. McCue L. A., Kwak J., Babcock M. J., Kendrick K. E. Molecular analysis of sporulation in Streptomyces griseus. Gene. 1992 Jun 15;115(1-2):173–179. doi: 10.1016/0378-1119(92)90556-5. [DOI] [PubMed] [Google Scholar]
  17. Omer C. A., Lenstra R., Litle P. J., Dean C., Tepperman J. M., Leto K. J., Romesser J. A., O'Keefe D. P. Genes for two herbicide-inducible cytochromes P-450 from Streptomyces griseolus. J Bacteriol. 1990 Jun;172(6):3335–3345. doi: 10.1128/jb.172.6.3335-3345.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pissowotzki K., Mansouri K., Piepersberg W. Genetics of streptomycin production in Streptomyces griseus: molecular structure and putative function of genes strELMB2N. Mol Gen Genet. 1991 Dec;231(1):113–123. doi: 10.1007/BF00293829. [DOI] [PubMed] [Google Scholar]
  19. Raibaud A., Zalacain M., Holt T. G., Tizard R., Thompson C. J. Nucleotide sequence analysis reveals linked N-acetyl hydrolase, thioesterase, transport, and regulatory genes encoded by the bialaphos biosynthetic gene cluster of Streptomyces hygroscopicus. J Bacteriol. 1991 Jul;173(14):4454–4463. doi: 10.1128/jb.173.14.4454-4463.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Robbins P. W., Overbye K., Albright C., Benfield B., Pero J. Cloning and high-level expression of chitinase-encoding gene of Streptomyces plicatus. Gene. 1992 Feb 1;111(1):69–76. doi: 10.1016/0378-1119(92)90604-n. [DOI] [PubMed] [Google Scholar]
  21. Roberts R. J. Staphylococcal transfer ribonucleic acids. II. Sequence analysis of isoaccepting glycine transfer ribonucleic acids IA and IB from Staphylococcus epidermidis Texas 26. J Biol Chem. 1974 Aug 10;249(15):4787–4796. [PubMed] [Google Scholar]
  22. Schauer A., Ranes M., Santamaria R., Guijarro J., Lawlor E., Mendez C., Chater K., Losick R. Visualizing gene expression in time and space in the filamentous bacterium Streptomyces coelicolor. Science. 1988 May 6;240(4853):768–772. doi: 10.1126/science.3363358. [DOI] [PubMed] [Google Scholar]
  23. Tamura F., Nishimura S., Ohki M. The E. coli divE mutation, which differentially inhibits synthesis of certain proteins, is in tRNASer1. EMBO J. 1984 May;3(5):1103–1107. doi: 10.1002/j.1460-2075.1984.tb01936.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Vögtli M., Hütter R. Characterisation of the hydroxystreptomycin phosphotransferase gene (sph) of Streptomyces glaucescens: nucleotide sequence and promoter analysis. Mol Gen Genet. 1987 Jun;208(1-2):195–203. doi: 10.1007/BF00330442. [DOI] [PubMed] [Google Scholar]
  25. Yamaizumi Z., Kuchino Y., Harada F., Nishimura S., McCloskey J. A. Primary structure of Escherichia coli tRNA UUR Leu. Presence of an unknown adenosine derivative in the first position of the anticodon which recognizes the UU codon series. J Biol Chem. 1980 Mar 10;255(5):2220–2225. [PubMed] [Google Scholar]
  26. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  27. Zalacain M., González A., Guerrero M. C., Mattaliano R. J., Malpartida F., Jiménez A. Nucleotide sequence of the hygromycin B phosphotransferase gene from Streptomyces hygroscopicus. Nucleic Acids Res. 1986 Feb 25;14(4):1565–1581. doi: 10.1093/nar/14.4.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES