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. 1992 Apr 11;20(7):1523–1530. doi: 10.1093/nar/20.7.1523

Aminoacyl-tRNA synthetase-induced cleavage of tRNA.

S Beresten 1, M Jahn 1, D Söll 1
PMCID: PMC312233  PMID: 1579445

Abstract

Aminoacyl-tRNA synthetases interact with their cognate tRNAs in a highly specific fashion. We have examined the phenomenon that upon complex formation E. coli glutaminyl-tRNA synthetase destabilizes tRNA(Gln) causing chain scissions in the presence of Mg2+ ions. The phosphodiester bond cleavage produces 3'-phosphate and 5'-hydroxyl ends. This kind of experiment is useful for detecting conformational changes in tRNA. Our results show that the cleavage is synthetase-specific, that mutant and wild-type tRNA(Gln) species can assume a different conformation, and that modified nucleosides in tRNA enhance the structural stability of the molecule.

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Selected References

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

  1. Beresten S. F., Zargarova T. A., Favorova O. O., Rubikaite B. I., Ryazanov A. G., Kisselev L. L. Molecular and cellular studies of tryptophanyl-tRNA synthetase using monoclonal antibodies. Evaluation of a common antigenic determinant in eukaryotic, prokaryotic and archaebacterial enzymes which maps outside the catalytic domain. Eur J Biochem. 1989 Oct 1;184(3):575–581. doi: 10.1111/j.1432-1033.1989.tb15052.x. [DOI] [PubMed] [Google Scholar]
  2. Björk G. R., Ericson J. U., Gustafsson C. E., Hagervall T. G., Jönsson Y. H., Wikström P. M. Transfer RNA modification. Annu Rev Biochem. 1987;56:263–287. doi: 10.1146/annurev.bi.56.070187.001403. [DOI] [PubMed] [Google Scholar]
  3. Brown R. S., Hingerty B. E., Dewan J. C., Klug A. Pb(II)-catalysed cleavage of the sugar-phosphate backbone of yeast tRNAPhe--implications for lead toxicity and self-splicing RNA. Nature. 1983 Jun 9;303(5917):543–546. doi: 10.1038/303543a0. [DOI] [PubMed] [Google Scholar]
  4. Celis J. E., Coulondre C., Miller J. H. Suppressor su+7 inserts tryptophan in addition to glutamine. J Mol Biol. 1976 Jul 5;104(3):729–734. doi: 10.1016/0022-2836(76)90132-7. [DOI] [PubMed] [Google Scholar]
  5. Dietrich A., Romby P., Maréchal-Drouard L., Guillemaut P., Giegé R. Solution conformation of several free tRNALeu species from bean, yeast and Escherichia coli and interaction of these tRNAs with bean cytoplasmic Leucyl-tRNA synthetase. A phosphate alkylation study with ethylnitrosourea. Nucleic Acids Res. 1990 May 11;18(9):2589–2597. doi: 10.1093/nar/18.9.2589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dock-Bregeon A. C., Garcia A., Giegé R., Moras D. The contacts of yeast tRNA(Ser) with seryl-tRNA synthetase studied by footprinting experiments. Eur J Biochem. 1990 Mar 10;188(2):283–290. doi: 10.1111/j.1432-1033.1990.tb15401.x. [DOI] [PubMed] [Google Scholar]
  7. Dock-Bregeon A. C., Moras D. Conformational changes and dynamics of tRNAs: evidence from hydrolysis patterns. Cold Spring Harb Symp Quant Biol. 1987;52:113–121. doi: 10.1101/sqb.1987.052.01.016. [DOI] [PubMed] [Google Scholar]
  8. Garret M., Labouesse B., Litvak S., Romby P., Ebel J. P., Giegé R. Tertiary structure of animal tRNATrp in solution and interaction of tRNATrp with tryptophanyl-tRNA synthetase. Eur J Biochem. 1984 Jan 2;138(1):67–75. doi: 10.1111/j.1432-1033.1984.tb07882.x. [DOI] [PubMed] [Google Scholar]
  9. Hoben P., Söll D. Glutaminyl-tRNA synthetase of Escherichia coli. Methods Enzymol. 1985;113:55–59. doi: 10.1016/s0076-6879(85)13011-9. [DOI] [PubMed] [Google Scholar]
  10. Jahn M., Rogers M. J., Söll D. Anticodon and acceptor stem nucleotides in tRNA(Gln) are major recognition elements for E. coli glutaminyl-tRNA synthetase. Nature. 1991 Jul 18;352(6332):258–260. doi: 10.1038/352258a0. [DOI] [PubMed] [Google Scholar]
  11. Kazakov S., Altman S. Site-specific cleavage by metal ion cofactors and inhibitors of M1 RNA, the catalytic subunit of RNase P from Escherichia coli. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9193–9197. doi: 10.1073/pnas.88.20.9193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Muramatsu T., Nishikawa K., Nemoto F., Kuchino Y., Nishimura S., Miyazawa T., Yokoyama S. Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature. 1988 Nov 10;336(6195):179–181. doi: 10.1038/336179a0. [DOI] [PubMed] [Google Scholar]
  13. Pan T., Gutell R. R., Uhlenbeck O. C. Folding of circularly permuted transfer RNAs. Science. 1991 Nov 29;254(5036):1361–1364. doi: 10.1126/science.1720569. [DOI] [PubMed] [Google Scholar]
  14. Perona J. J., Swanson R. N., Rould M. A., Steitz T. A., Söll D. Structural basis for misaminoacylation by mutant E. coli glutaminyl-tRNA synthetase enzymes. Science. 1989 Dec 1;246(4934):1152–1154. doi: 10.1126/science.2686030. [DOI] [PubMed] [Google Scholar]
  15. Perret V., Garcia A., Grosjean H., Ebel J. P., Florentz C., Giegé R. Relaxation of a transfer RNA specificity by removal of modified nucleotides. Nature. 1990 Apr 19;344(6268):787–789. doi: 10.1038/344787a0. [DOI] [PubMed] [Google Scholar]
  16. Quigley G. J., Teeter M. M., Rich A. Structural analysis of spermine and magnesium ion binding to yeast phenylalanine transfer RNA. Proc Natl Acad Sci U S A. 1978 Jan;75(1):64–68. doi: 10.1073/pnas.75.1.64. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Riehl N., Giegé R., Ebel J. P., Ehresmann B. Effect of elongation factor Tu on the conformation of phenylalanyl-tRNAPhe. FEBS Lett. 1983 Apr 5;154(1):42–46. doi: 10.1016/0014-5793(83)80871-0. [DOI] [PubMed] [Google Scholar]
  18. Romby P., Moras D., Bergdoll M., Dumas P., Vlassov V. V., Westhof E., Ebel J. P., Giegé R. Yeast tRNAAsp tertiary structure in solution and areas of interaction of the tRNA with aspartyl-tRNA synthetase. A comparative study of the yeast phenylalanine system by phosphate alkylation experiments with ethylnitrosourea. J Mol Biol. 1985 Aug 5;184(3):455–471. doi: 10.1016/0022-2836(85)90294-3. [DOI] [PubMed] [Google Scholar]
  19. Romby P., Moras D., Dumas P., Ebel J. P., Giegé R. Comparison of the tertiary structure of yeast tRNA(Asp) and tRNA(Phe) in solution. Chemical modification study of the bases. J Mol Biol. 1987 May 5;195(1):193–204. doi: 10.1016/0022-2836(87)90336-6. [DOI] [PubMed] [Google Scholar]
  20. Rould M. A., Perona J. J., Steitz T. A. Structural basis of anticodon loop recognition by glutaminyl-tRNA synthetase. Nature. 1991 Jul 18;352(6332):213–218. doi: 10.1038/352213a0. [DOI] [PubMed] [Google Scholar]
  21. Rould M. A., Perona J. J., Söll D., Steitz T. A. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 A resolution. Science. 1989 Dec 1;246(4934):1135–1142. doi: 10.1126/science.2479982. [DOI] [PubMed] [Google Scholar]
  22. Rubelj I., Weygand-Durasević I., Kućan Z. Evidence for two types of complexes formed by yeast tyrosyl-tRNA synthetase with cognate and non-cognate tRNA. Effect of ribonucleoside triphosphates. Eur J Biochem. 1990 Nov 13;193(3):783–788. doi: 10.1111/j.1432-1033.1990.tb19400.x. [DOI] [PubMed] [Google Scholar]
  23. Ruff M., Krishnaswamy S., Boeglin M., Poterszman A., Mitschler A., Podjarny A., Rees B., Thierry J. C., Moras D. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp). Science. 1991 Jun 21;252(5013):1682–1689. doi: 10.1126/science.2047877. [DOI] [PubMed] [Google Scholar]
  24. Sampson J. R., Uhlenbeck O. C. Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1033–1037. doi: 10.1073/pnas.85.4.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schulman L. H., Pelka H. An anticodon change switches the identity of E. coli tRNA(mMet) from methionine to threonine. Nucleic Acids Res. 1990 Jan 25;18(2):285–289. doi: 10.1093/nar/18.2.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Silberklang M., Gillum A. M., RajBhandary U. L. Use of in vitro 32P labeling in the sequence analysis of nonradioactive tRNAs. Methods Enzymol. 1979;59:58–109. doi: 10.1016/0076-6879(79)59072-7. [DOI] [PubMed] [Google Scholar]
  27. Söll D. The accuracy of aminoacylation--ensuring the fidelity of the genetic code. Experientia. 1990 Dec 1;46(11-12):1089–1096. doi: 10.1007/BF01936918. [DOI] [PubMed] [Google Scholar]
  28. Vlassov V. V., Kern D., Romby P., Giegé R., Ebel J. P. Interaction of tRNAPhe and tRNAVal with aminoacyl-tRNA synthetases. A chemical modification study. Eur J Biochem. 1983 May 16;132(3):537–544. doi: 10.1111/j.1432-1033.1983.tb07395.x. [DOI] [PubMed] [Google Scholar]
  29. Weber F., Dietrich A., Weil J. H., Maréchal-Drouard L. A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucleic Acids Res. 1990 Sep 11;18(17):5027–5030. doi: 10.1093/nar/18.17.5027. [DOI] [PMC free article] [PubMed] [Google Scholar]

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