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Journal of Molecular Evolution

, Volume 40, Issue 5, pp 499–508 | Cite as

The class II aminoacyl-tRNA synthetases and their active site: Evolutionary conservation of an ATP binding site

  • Gilbert Eriani
  • Jean Cavarelli
  • Franck Martin
  • Laurent Ador
  • Bernard Rees
  • Jean -Claude Thierry
  • Jean Gangloff
  • Dino Moras
Articles

Abstract

Previous sequence analyses have suggested the existence of two distinct classes of aminoacyl-tRNA synthetase. The partition was established on the basis of exclusive sets of sequence motifs (Eriani et al. [1990] Nature 347:203–306). X-ray studies have now well defined the structural basis of the two classes: the class I enzymes share with dehydrogenases and kinases the classic nucleotide binding fold called the Rossmann fold, whereas the class II enzymes possess a different fold, not found elsewhere, built around a six-stranded antiparallel β-sheet. The two classes of synthetases catalyze the same global reaction that is the attachment of an amino acid to the tRNA, but differ as to where on the terminal adenosine of the tRNA the amino acid is placed: class I enzymes act on the 2′ hydroxyl whereas the class II enzymes prefer the 3′ hydroxyl group. The three-dimensional structure of aspartyl-tRNA synthetase from yeast, a typical class II enzyme, is described here, in relation to its function. The crucial role of the sequence motifs in substrate binding and enzyme structure is high-lighted. Overall these results underline the existence of an intimate evolutionary link between the aminoacyl-tRNA synthetases, despite their actual structural diversity.

Key words

Two classes of aminoacyl-tRNA synthetases Sequence comparisons Homology X-ray structure Structure-function relationships Origin of aminoacyl-tRNA synthetases Two ancestral molecules Genetic code 

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References

  1. Anselme J, Härtlein M (1989) Asparaginyl-tRNA synthetase from Escherichia coli has significant sequence homologies with yeast aspartyl-tRNA synthetase. Gene 84:481–485Google Scholar
  2. Akins RA, Lambowitz AM (1987) A protein required for splicing group I introns in Neurospora crassa mitochondria is mitochondrial tyrosyl-tRNA synthetase or a derivative thereof. Cell 50:331–345Google Scholar
  3. Artymiuk PJ, Rice DW, Poirrette AR, Willet P (1994) A tale of two synthetases. Nature Structural Biology 1:758–760Google Scholar
  4. Biou V, Yaremchuk A, Tukalo M, Cusack S (1994) The 2.9 Å crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNASer. Science 263:1404–1410Google Scholar
  5. Cassio D, Waller JP (1971) Modification of methionyl-tRNA synthetase by proteolytic cleavage and properties of the trypsin-modified enzyme. Eur J Biochem 20:283–300Google Scholar
  6. Cavarelli J, Eriani G, Rees B, Ruff M, Boeglin M, Mitschler A, Martin F, Gangloff J, Thierry JC, Moras D (1994) The active site of yeast aspartyl-tRNA synthetase: structural and functional aspects of the aminoacylation reaction. EMBO J 13:327–337Google Scholar
  7. Cavarelli J, Rees B, Ruff M, Thierry JC, Moras D (1993) Yeast tRNAAsp recognition by its cognate class II aminoacyl-tRNA synthetase. Nature 362:181–184Google Scholar
  8. Carter G (1993) Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu Rev Biochem 62:715–748Google Scholar
  9. Cerini C, Kerjan P, Astier M, Gratecos D, Mirande M, Semeria MA (1991) Component of the multisynthetase complex is a multifunctional aminoacyl-tRNA synthetase. EMBO J 10:4267–4277Google Scholar
  10. Cusack S, Berthet-Colominas C, Härtlein M, Nassar N, Leberman R (1990) A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 Å. Nature 347:249–255Google Scholar
  11. Cusack S, Härtlein M, Leberman R (1991) Sequence, structural and evolutionary relationships between class 2 aminoacyl-tRNA synthetases. Nucleic Acids Res 19:3489–3498Google Scholar
  12. Eriani G, Delarue M, Poch O, Gangloff J, Moras D (1990) Partition of synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347:203–206Google Scholar
  13. Eriani G, Dirheimer G, Gangloff J (1991) Cysteinyl-tRNA synthetase: determination of the last E. coli aminoacyl-tRNA synthetase primary structure. Nucleic Acids Res 19:265–269Google Scholar
  14. Eriani G, Cavarelli J, Martin F, Dirheimer G, Moras D, Gangloff J (1993) Role of dimerization in yeast aspartyl-tRNA synthetase and importance of the class II invariant proline. Proc Natl Acad Sci USA 90:10816–10820Google Scholar
  15. Fraser FT, Rich A (1975) Amino acids are not all initially attached to the same position on transfer RNA molecules. Proc Natl Acad Sci USA 72:3044–3048Google Scholar
  16. Freist W, Sternbach H, Cramer F (1987) Isoleucyl-tRNA synthetase from baker's yeast and from Escherichia coli MRE600. Eur J Biochem 169:33–39Google Scholar
  17. Freist W, Sternbach H (1988) Tyrosyl-tRNA synthetase from baker's yeast. Order of substrate addition, discrimination of 20 amino acids in aminoacylation of tRNA TyrCCA and tRNA TyrCCA(3′NH2). Eur J Biochem 177:425–433Google Scholar
  18. Freist W, Sternbach H, Cramer F (1989) Arginyl-tRNA synthetase from yeast. Discrimination between 20 amino acids in aminoacylation of tRNA ArgCCA and tRNA ArgCCA(3′NH2). Eur J Biochem 186:535–541Google Scholar
  19. Gatti PL, Tzagoloff A (1991) Structure and evolution of a group of related aminoacyl-tRNA synthetases. J Mol Biol 218:557–568Google Scholar
  20. Griffin BE, Jarmen M, Reese CB, Sulston JE, Trentham DR (1966) Some observations relating to acyl mobility in aminoacyl soluble ribonucleic acids. Biochemistry 5:3638–3649Google Scholar
  21. Guildo MD (1993) Origin glutaminyl-tRNA synthetase: an example of palimpset? J Mol Evol 37:5–10Google Scholar
  22. Hountondji C, Dessen P, Blanquet S (1986) Sequence similarities among the family of aminoacyl-tRNA synthetases. Biochimie 68: 1071–1078Google Scholar
  23. Igloi GL, von der Haar F, Cramer F (1978) Aminoacyl-tRNA synthetases from yeast: generality of chemical proofreading in the prevention of misaminoacylation of tRNA. Biochemistry 17:3459–3467Google Scholar
  24. Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946–950CrossRefGoogle Scholar
  25. Lévêque F, Plateau P, Dessen P, Blanquet S (1990) Homology of lysS and lysU, the two Escherichia coli genes encoding distinct lysyl-tRNA synthetase species. Nucleic Acids Res 18:305–312Google Scholar
  26. Lu Y, Hill KAW (1994) The invariant arginine of motif 2 of Escherichia coli alanyl-tRNA synthetase is important for catalysis but not for substrate binding. J Biol Chem 269:12137–12141Google Scholar
  27. Mosyak L, Saffro M (1993) Phenylalanyl-tRNA synthetase from Thermus thermophilus has four antiparallel folds of which only two are catalytically functional. Biochimie 75:1091–1098Google Scholar
  28. Ribas de Pouplana L, Buechter DD, Davis MW, Schimmel P (1993) Idiographic representation of conserved domain of a class II tRNA synthetase of unknown structure. Protein Sci 2:2259–2262Google Scholar
  29. Risler JL, Zelver C, Brunie S (1981) Methionyl-tRNA synthetase shows the nucleotide binding fold observed in dehydrogenases. Nature 292:385–386Google Scholar
  30. Rossmann MG, Moras D, Osen KW (1974) Chemical and biological evolution of a nucleotide binding domain. Nature 250:194–199Google Scholar
  31. Rould MA, Perona JJ, Söll D, Steitz TA (1989) Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNAGln and ATP at 2,8 Å resolution. Science 246:1135–1142Google Scholar
  32. Rubin J, Blow D (1981) Amino acid activation in crystalline tyrosyl-tRNA synthetase from Bacillus stearothermophilus. J Mol Biol 145:489–500Google Scholar
  33. Ruff M, Krishnaswamy S, Boeglin M, Poterszman A, Mitschler A, Rees B, Thierry JC, Moras D (1991) Class II aminoacyl-transfer RNA synthetase: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNAAsp. Science 252:1682–1689Google Scholar
  34. Schimmel P, Söll D (1979) Aminoacyl-tRNA synthetases: general features and recognition of transfer RNAs. Ann Rev. Biochem 48: 601–648Google Scholar
  35. Sellami M, Chatton B, Fasiolo F, Dirheimer G, Ebel JP, Gangloff J (1986) Nucleotide sequence of the gene coding for yeast cytoplasmic aspartyl-tRNA synthetase (APS); mapping of the 5′ and 3′ termini of AspRS mRNA. Nucleic Acids Res 14:1657–1666Google Scholar
  36. Sonnebom TM (1965) In: Bryson V, Vogel HJ (eds) Evolving genes and proteins. Academic Press, New York, pp 337–397Google Scholar
  37. Sprinzl M, Cramer F (1975) Site of aminoacylation of tRNAs from Escherichia coli with respect to the 2′- or 3′-hydroxyl group of the terminal adenosine. Proc Natl Acad Sci USA 72:3049–3053Google Scholar
  38. von der Haar F, Cramer F (1976) Hydrolytic action of aminoacyl-tRNA synthetases from baker's yeast: “chemical proofreading” preventing acylation of tRNAIle with misactivated valine. Biochemistry 15:4131–4138Google Scholar
  39. Webster TA, Tsai H, Kula M, Mackie GA, Schimmel P (1984) Specific sequence homology and three-dimensional structure of an aminoacyl transfer RNA synthetase. Science 226:1315–1317Google Scholar
  40. Woese C (1965) The genetic code. Harper and Row, New York, pp 156–160Google Scholar
  41. Wong JTF (1975) A co-evolution theory of the genetic code. Proc Natl Acad Sci USA 72:1909–1912Google Scholar

Copyright information

© Springer-Verlag New York Inc 1995

Authors and Affiliations

  • Gilbert Eriani
    • 1
  • Jean Cavarelli
    • 2
  • Franck Martin
    • 1
  • Laurent Ador
    • 1
  • Bernard Rees
    • 2
  • Jean -Claude Thierry
    • 2
  • Jean Gangloff
    • 1
  • Dino Moras
    • 2
  1. 1.UPR 9002, Structure des Macromolécules Biologiques et Mécanismes de ReconnaissanceLaboratoire de Biologie Structurale, Institut de Biologie Moléculaire et Cellulaire du CNRSStrasbourgFrance
  2. 2.UPR 9004, Laboratoire de Biologic StructuraleInstitut de Biologie Moléculaire et Cellulaire du CNRSStrasbourgFrance

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