Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs

Abstract

THE aminoacyl-transfer RNA synthetases (aaRS) catalyse the attachment of an amino acid to its cognate transfer RNA molecule in a highly specific two-step reaction. These proteins differ widely in size and oligomeric state, and have limited sequence homology. Out of the 18 known aaRS, only 9 (ref. 1), referred to as class I synthetases (GlnRS, TyrRS, MetRS, GluRS, ArgRS, ValRS, IleRS, LeuRS, TrpRS), display two short common consensus sequences ('HIGH' and 'KMSKS') which indicate, as observed in three crystal structures2–4, the presence of a structural domain (the Rossman fold) that binds ATP. We report here the sequence of Escherichia coll ProRS, a dimer of relative molecular mass 127,402, which is homologous to both ThrRS and SerRS. These three latter aaRS share three new sequence motifs with AspRS, AsnRS, LysRS, HisRS and the β subunit of PheRS. These three motifs (motifs 1, 2 and 3), in a search through the entire data bank, proved to be specific for this set of aaRS (referred to as class II). Class II may also contain AlaRS and GlyRS, because these sequences have a typical motif 3. Surprisingly, this partition of aaRS in two classes is found to be strongly correlated on the functional level with the acylation occurring either on the 2′ OH (class I) or 3′ OH (class II) of the ribose of the last nucleotide of tRNA.

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References

  1. 1

    Burbaum, J., Starzyk, R. M. & Schimmel, P. Proteins 7, 99–111 (1990).

    CAS  Article  Google Scholar 

  2. 2

    Brick, P., Bhat, T. N. & Blow, D. M. J. molec. Biol. 208, 83–98 (1988).

    Article  Google Scholar 

  3. 3

    Zelwer, C., Risler, J.-L. & Brunie, S. J. molec. Biol. 155, 63–81 (1982).

    CAS  Article  Google Scholar 

  4. 4

    Rould, M. A., Perona, J. J., Söll, D. & Steitz, T. A. Science 246, 1135–1142 (1989).

    ADS  CAS  Article  Google Scholar 

  5. 5

    Bohman, K. & Isaksson, L. A. Molec. gen. Genet. 177, 603–605 (1980).

    CAS  Article  Google Scholar 

  6. 6

    Dale, R. M. K., McClure, B. A. & Houchins, J. P. Plasmid 13, 31–40 (1985).

    CAS  Article  Google Scholar 

  7. 7

    Tabor, S. & Richardson, C. C. Proc. natn. Acad. Sci. U.S.A. 84, 4767–4771 (1987).

    ADS  CAS  Article  Google Scholar 

  8. 8

    Brendel, V. & Trifonov, E. V. Nucleic Acids Res. 10, 4411–4427 (1984).

    Article  Google Scholar 

  9. 9

    Springer, M., Graffe, M., Dondon, J. & Grunberg-Manago, M. EMBO J. 8, 2417–2427 (1989).

    CAS  Article  Google Scholar 

  10. 10

    Moine, H. thesis., Univ. Louis Pasteur, Strasbourg (1990).

  11. 11

    Molina, A. J., Peterson, R. & Yang, D.C.H. J. biol. Chem. 264, 16608–16612 (1989).

    Google Scholar 

  12. 12

    Gampel, A. & Tzagoloff, A. Proc. natn. Acad Sci. U.S.A. 86, 6023–6027 (1989).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Anselme, J. & Härtlein, M. Gene 84, 481–485 (1989).

    CAS  Article  Google Scholar 

  14. 14

    Leveque, F., Plateau, P., Dessen, P. & Blanquet, S. Nucleic. Acids Res. 18, 305–312 (1990).

    CAS  Article  Google Scholar 

  15. 15

    Wek, R. C., Jackson, B. M. & Hinnenbusch, A. G. Proc. natn. Acad. Sci. U.S.A. 86, 4579–4583 (1989).

    ADS  CAS  Article  Google Scholar 

  16. 16

    Gribskov, M., MacLachlan, A. D. & Eisenberg, D. Proc. natn. Acad. Sci. U.S.A. 84, 4355–4358 (1987).

    ADS  CAS  Article  Google Scholar 

  17. 17

    Jasin, M., Regan, L. & Schimmel, P. R. Nature 306, 441–447 (1983).

    ADS  CAS  Article  Google Scholar 

  18. 18

    Prevost, G., Eriani, G., Kern, D., Dirheimer, G. & Gangloff, J. Eur. J. Biochem. 180, 351–358 (1989).

    CAS  Article  Google Scholar 

  19. 19

    Eriani, G. thesis., Univ. Louis Pasteur, Strasbourg (1990).

  20. 20

    Hecht, S. M. in Transfer-RNA Structure, Properties and Recognition (eds Schimmel, P. R., Söll, D. & Abelson, J. N.) 345–360 (Cold Spring Harbor Laboratory, New York, 1979).

    Google Scholar 

  21. 21

    Weiner, A. M. & Maizels, N. Proc. natn. Acad. Sci. U.S.A. 84, 7383–7387 (1987).

    ADS  CAS  Article  Google Scholar 

  22. 22

    Fraser, T. H. & Rich, A. Proc. natn. Acad. Sci. U.S.A. 72, 3044–3048 (1975).

    ADS  CAS  Article  Google Scholar 

  23. 22b

    von der Haar, F. & Cramer, F. Biochemistry 15, 4131–4136 (1976).

    CAS  Article  Google Scholar 

  24. 23

    Fersht, A. R. & Kaethner, M. M. Biochemistry 15, 3342–3346 (1976).

    CAS  Article  Google Scholar 

  25. 24

    Brune, M., Schumann, R. & Wittinghofer, F. Nucleic Acids Res. 13, 7139–7147 (1985).

    CAS  Article  Google Scholar 

  26. 25

    Devereux, J., Haeberli, P. & Smithies, O. Nucleic Acids Res. 12, 387–395 (1984).

    CAS  Article  Google Scholar 

  27. 26

    Eriani, G., Dirheimer, G. & Gangloff, J. Nucleic Acids Res. 17, 5725–5736 (1989).

    CAS  Article  Google Scholar 

  28. 27

    Berger, S. L., Wallace, D. M., Puskas, R. S. & Eschenfeldt, W. H. Biochemistry 22, 2365–2373 (1983).

    CAS  Article  Google Scholar 

  29. 28

    Argos, P. J. molec. Biol. 193, 385–396 (1987).

    CAS  Article  Google Scholar 

  30. 29

    Mirande, M. & Waller, J. P. J. biol. Chem. 263, 18443–18451 (1988).

    CAS  PubMed  Google Scholar 

  31. 30

    Nilssen, T. W. et al. Proc. natn. Acad. Sci. U.S.A. 85, 3604–3607 (1988).

    ADS  Article  Google Scholar 

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Eriani, G., Delarue, M., Poch, O. et al. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature 347, 203–206 (1990). https://doi.org/10.1038/347203a0

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