Home LiteratureArticle Details
PMID: 12110594 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Class I tyrosyl-tRNA synthetase has a class II mode of cognate tRNA recognition.

The EMBO journal ·Vol. 21 ·No. 14 ·2002-07-15 ·Pages 3829-40

Yaremchuk A, Kriklivyi I, Tukalo M, Cusack S

Abstract

Bacterial tyrosyl-tRNA synthetases (TyrRS) possess a flexibly linked C-terminal domain of approximately 80 residues, which has hitherto been disordered in crystal structures of the enzyme. We have determined the structure of Thermus thermophilus TyrRS at 2.0 A resolution in a crystal form in which the C-terminal domain is ordered, and confirm that the fold is similar to part of the C-terminal domain of ribosomal protein S4. We have also determined the structure at 2.9 A resolution of the complex of T.thermophilus TyrRS with cognate tRNA(tyr)(G Psi A). In this structure, the C-terminal domain binds between the characteristic long variable arm of the tRNA and the anti-codon stem, thus recognizing the unique shape of the tRNA. The anticodon bases have a novel conformation with A-36 stacked on G-34, and both G-34 and Psi-35 are base-specifically recognized. The tRNA binds across the two subunits of the dimeric enzyme and, remarkably, the mode of recognition of the class I TyrRS for its cognate tRNA resembles that of a class II synthetase in being from the major groove side of the acceptor stem.

MeSH Terms
Amino Acid Sequence Base Sequence Crystallography Models, Molecular Molecular Sequence Data Nucleic Acid Conformation Protein Conformation RNA, Transfer/chemistry,metabolism Sequence Homology, Amino Acid Substrate Specificity Thermus thermophilus/enzymology Tyrosine-tRNA Ligase/chemistry,metabolism
Chemicals
RNA, Transfer Tyrosine-tRNA Ligase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yaremchuk Anna
European Molecular Biology Laboratory, Grenoble Outstation, c/o ILL, 156X, F-38042 Grenoble cedex 9, France.
Kriklivyi Ivan
Tukalo Michael
Cusack Stephen
References (55)
55 references, click to expand
  1. Structural and kinetic bases for the recognition of tRNATyr by tyrosyl-tRNA synthetase.
    J Mol Biol. 1989 Feb 20;205(4):729-35 PMID: 2467006
  2. Structure and dynamics of the anticodon arm binding domain of Bacillus stearothermophilus Tyrosyl-tRNA synthetase.
    Structure. 2002 Mar;10(3):311-7 PMID: 12005430
  3. Crystal structure of a deletion mutant of a tyrosyl-tRNA synthetase complexed with tyrosine.
    J Mol Biol. 1987 Mar 20;194(2):287-97 PMID: 3612807
  4. Dissection of the structure and activity of the tyrosyl-tRNA synthetase by site-directed mutagenesis.
    Biochemistry. 1987 Dec 15;26(25):8031-7 PMID: 3442641
  5. Evolution of aminoacyl-tRNA synthetases--analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events.
    Genome Res. 1999 Aug;9(8):689-710 PMID: 10447505
  6. tRNA-like recognition of group I introns by a tyrosyl-tRNA synthetase.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):2630-5 PMID: 11854463
  7. Asymmetry of tyrosyl-tRNA synthetase in solution.
    Biochemistry. 1988 Feb 9;27(3):1041-9 PMID: 3365365
  8. Eleven down and nine to go.
    Nat Struct Biol. 1995 Oct;2(10):824-31 PMID: 7552701
  9. Synthetase competition and tRNA context determine the in vivo identify of tRNA discriminator mutants.
    J Mol Biol. 1992 Dec 20;228(4):1055-62 PMID: 1474577
  10. Alternative designs for construction of the class II transfer RNA tertiary core.
    RNA. 2000 Nov;6(11):1585-96 PMID: 11105758
  11. Crystal structure of Staphylococcus aureus tyrosyl-tRNA synthetase in complex with a class of potent and specific inhibitors.
    Protein Sci. 2001 Oct;10(10):2008-16 PMID: 11567092
  12. Species-specific microhelix aminoacylation by a eukaryotic pathogen tRNA synthetase dependent on a single base pair.
    Biochemistry. 1995 Oct 3;34(39):12489-95 PMID: 7547995
  13. Aminoacyl-tRNA synthetases from baker's yeast: reacting site of enzymatic aminoacylation is not uniform for all tRNAs.
    FEBS Lett. 1975 Aug 15;56(2):212-4 PMID: 1098930
  14. Structure of tyrosyl-tRNA synthetase refined at 2.3 A resolution. Interaction of the enzyme with the tyrosyl adenylate intermediate.
    J Mol Biol. 1989 Jul 5;208(1):83-98 PMID: 2504923
  15. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features.
    Biopolymers. 1983 Dec;22(12):2577-637 PMID: 6667333
  16. An engineered class I transfer RNA with a class II tertiary fold.
    RNA. 1999 Mar;5(3):434-45 PMID: 10094311
  17. Macromolecular recognition through electrostatic repulsion.
    EMBO J. 1995 Jun 15;14(12):2945-50 PMID: 7796819
  18. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  19. Integration of macromolecular diffraction data.
    Acta Crystallogr D Biol Crystallogr. 1999 Oct;55(Pt 10):1696-702 PMID: 10531519
  20. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 A resolution.
    Science. 1989 Dec 1;246(4934):1135-42 PMID: 2479982
  21. Two classes of tRNA synthetases suggested by sterically compatible dockings on tRNA acceptor stem.
    Cell. 2001 Jan 26;104(2):191-3 PMID: 11269237
  22. Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase.
    Structure. 1995 Jan 15;3(1):17-31 PMID: 7743129
  23. Recognition of tRNA(Tyr) by tyrosyl-tRNA synthetase.
    Biochimie. 1990 Aug;72(8):589-98 PMID: 2126463
  24. Automated protein model building combined with iterative structure refinement.
    Nat Struct Biol. 1999 May;6(5):458-63 PMID: 10331874
  25. Ligand binding stoichiometries, subunit structure, and slow transitions in aminoacyl-tRNA synthetases.
    Biochemistry. 1977 Sep 6;16(18):4005-13 PMID: 199234
  26. Structure of Hsp15 reveals a novel RNA-binding motif.
    EMBO J. 2000 Feb 15;19(4):749-57 PMID: 10675344
  27. Tyrosyl-tRNA synthetase acts as an asymmetric dimer in charging tRNA. A rationale for half-of-the-sites activity.
    Biochemistry. 1988 Jul 26;27(15):5525-30 PMID: 3179266
  28. The crystal structure of ribosomal protein S4 reveals a two-domain molecule with an extensive RNA-binding surface: one domain shows structural homology to the ETS DNA-binding motif.
    EMBO J. 1998 Aug 17;17(16):4545-58 PMID: 9707415
  29. Protein structure comparison by alignment of distance matrices.
    J Mol Biol. 1993 Sep 5;233(1):123-38 PMID: 8377180
  30. Species-specific tRNA recognition in relation to tRNA synthetase contact residues.
    J Mol Biol. 1997 May 30;269(1):1-9 PMID: 9192996
  31. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp).
    Science. 1991 Jun 21;252(5013):1682-9 PMID: 2047877
  32. Recognition nucleotides of Escherichia coli tRNA(Leu) and its elements facilitating discrimination from tRNASer and tRNA(Tyr).
    J Mol Biol. 1993 May 20;231(2):219-29 PMID: 8510145
  33. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps.
    Acta Crystallogr D Biol Crystallogr. 1999 Apr;55(Pt 4):938-40 PMID: 10089341
  34. The 2.9 A crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNA(Ser).
    Science. 1994 Mar 11;263(5152):1404-10 PMID: 8128220
  35. Conversion of aminoacylation specificity from tRNA(Tyr) to tRNA(Ser) in vitro.
    Nucleic Acids Res. 1990 Dec 11;18(23):6815-9 PMID: 2263446
  36. Modeling with in vitro kinetic parameters for the elaboration of transfer RNA identity in vivo.
    Biochemistry. 1989 Jun 13;28(12):4942-7 PMID: 2548595
  37. The anticodon-binding domain of tyrosyl-tRNA synthetase: state of folding and origin of the crystallographic disorder.
    Biochemistry. 2000 Feb 22;39(7):1739-47 PMID: 10677223
  38. Raster3D: photorealistic molecular graphics.
    Methods Enzymol. 1997;277:505-24 PMID: 18488322
  39. The solution structure of ribosomal protein S4 delta41 reveals two subdomains and a positively charged surface that may interact with RNA.
    EMBO J. 1998 Aug 17;17(16):4559-71 PMID: 9707416
  40. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  41. [Comparative analysis of interaction sites of Thermus thermophilus and Escherichia coli tRNA(Tyr) with homologous aminoacyl-tRNA synthetases by means of chemical modification and nuclease hydrolysis].
    Bioorg Khim. 1998 Aug;24(8):593-600 PMID: 9784879
  42. Discrimination between transfer-RNAs by tyrosyl-tRNA synthetase.
    Biochimie. 1993;75(12):1099-108 PMID: 8199245
  43. How glutaminyl-tRNA synthetase selects glutamine.
    Structure. 1998 Apr 15;6(4):439-49 PMID: 9562563
  44. Neutron scattering studies of escherichia coli tyrosyl-trna synthetase and of its interaction with trna tyr.
    J Mol Biol. 1982 Aug 25;159(4):651-64 PMID: 6754952
  45. An essential residue in the flexible peptide linking the two idiosynchratic domains of bacterial tyrosyl-tRNA synthetases.
    Biochemistry. 2001 Jun 19;40(24):7192-9 PMID: 11401566
  46. The 2 A crystal structure of leucyl-tRNA synthetase and its complex with a leucyl-adenylate analogue.
    EMBO J. 2000 May 15;19(10):2351-61 PMID: 10811626
  47. Major tyrosine identity determinants in Methanococcus jannaschii and Saccharomyces cerevisiae tRNA(Tyr) are conserved but expressed differently.
    Eur J Biochem. 2001 Feb;268(3):761-7 PMID: 11168416
  48. Novel predicted RNA-binding domains associated with the translation machinery.
    J Mol Evol. 1999 Mar;48(3):291-302 PMID: 10093218
  49. Major anticodon-binding region missing from an archaebacterial tRNA synthetase.
    J Biol Chem. 1999 Dec 10;274(50):35601-6 PMID: 10585437
  50. Tyrosyl-tRNA synthetase forms a mononucleotide-binding fold.
    J Mol Biol. 1982 Jul 15;158(4):699-709 PMID: 7120416
  51. Structural basis for transfer RNA aminoacylation by Escherichia coli glutaminyl-tRNA synthetase.
    Biochemistry. 1993 Aug 31;32(34):8758-71 PMID: 8364025
  52. tRNA aminoacylation by arginyl-tRNA synthetase: induced conformations during substrates binding.
    EMBO J. 2000 Nov 1;19(21):5599-610 PMID: 11060012
  53. Crystallization and preliminary crystallographic analysis of Thermus thermophilus leucyl-tRNA synthetase and its complexes with leucine and a non-hydrolysable leucyl-adenylate analogue.
    Acta Crystallogr D Biol Crystallogr. 2000 May;56(Pt 5):667-9 PMID: 10771445
  54. ESPript: analysis of multiple sequence alignments in PostScript.
    Bioinformatics. 1999 Apr;15(4):305-8 PMID: 10320398
  55. The crystal structure of the ternary complex of T.thermophilus seryl-tRNA synthetase with tRNA(Ser) and a seryl-adenylate analogue reveals a conformational switch in the active site.
    EMBO J. 1996 Jun 3;15(11):2834-42 PMID: 8654381
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
DOI
10.1093/emboj/cdf373
Published
2002-07-15
Pages
3829-40
Language
English
Region
England
NLM ID
8208664
PMCID
PMC126118
Subset
IM
External Links
PubMed source DOI: 10.1093/emboj/cdf373 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2