Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Functional convergence of two lysyl-tRNA synthetases with unrelated topologies

Nature Structural Biology volume 9, pages 257–262 (2002)Cite this article

Abstract

Lysyl-tRNA can be synthesized by both a class I (LysRS-I) and a class II (LysRS-II) lysyl-tRNA synthetase. The crystal structure of LysRS-I from Pyrococcus horikoshii at 2.6 Å resolution reveals extensive similarity with glutamyl-tRNA synthetase (GluRS). A comparison of the structures of LysRS-I and LysRS-II in complex with lysine shows that both enzymes use similar strategies for substrate recognition within unrelated active site topologies. A docking model based upon the GluRS–tRNA complex suggests how LysRS-I and LysRS-II can recognize the same molecular determinants in tRNALys, as shown by biochemical results, while approaching the acceptor helix of the tRNA from opposite sides.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The structure of P. horikoshii LysRS-I.
Figure 2: The l-lysine recognition.
Figure 3: The tRNA recognition.
Figure 4: Functional convergence of unrelated structural modules.

Similar content being viewed by others

Accession codes

Accessions

Protein Data Bank

References

  1. Ibba, M. & Söll, D. Annu. Rev. Biochem. 69, 617–650 (2000).

    Article  CAS  Google Scholar 

  2. Eriani, G., Delarue, M., Poch, O., Gangloff, J. & Moras, D. Nature 347, 203–206 (1990).

    Article  CAS  Google Scholar 

  3. Cusack, S. Nature Struct. Biol. 2, 824–831 (1995).

    Article  CAS  Google Scholar 

  4. Woese, C.R., Olsen, G. J., Ibba, M. & Söll, D. Microbiol. Mol. Biol. Rev. 64, 202–236 (2000).

    Article  CAS  Google Scholar 

  5. Chihade, J.W., Brown, J.R., Schimmel, P.R. & Ribas de Pouplana, L. Proc. Natl. Acad. Sci. USA 97, 12153–12157 (2000).

    Article  CAS  Google Scholar 

  6. Ibba, M., Becker, H.D., Stathopoulos, C., Tumbula, D.L. & Söll, D. Trends Biochem. Sci. 25, 311–316 (2000).

    Article  CAS  Google Scholar 

  7. Bult, C.J. et al. Science 273, 1058–1073 (1996).

    Article  CAS  Google Scholar 

  8. Smith, D.R.. et al. J. Bacteriol. 179, 7135–7155 (1997).

    Article  CAS  Google Scholar 

  9. Ibba, M. et al. Science 278, 1119–1122 (1997).

    Article  CAS  Google Scholar 

  10. Ibba, M., Bono, J.L., Rosa, P.A. & Söll, D. Proc. Natl. Acad. Sci. USA 94, 14383–14388 (1997).

    Article  CAS  Google Scholar 

  11. Prodom release 2001.1 (http://protein.toulouse.inra.fr/prodom/doc/prodom.html).

  12. Ibba, M. et al. Proc. Natl. Acad. Sci. USA 96, 418–423 (1999).

    Article  CAS  Google Scholar 

  13. Onesti, S. et al. Biochemistry 39, 12853–12861 (2000).

    Article  CAS  Google Scholar 

  14. Cusack, S., Yaremchuk, A. & Tukalo, M. EMBO J. 15, 6321–6334 (1996).

    Article  CAS  Google Scholar 

  15. Sugiura, I. et al. Structure 8, 197–208 (2000).

    Article  CAS  Google Scholar 

  16. Nureki, O. et al. Science 24, 578–582 (1998).

    Article  Google Scholar 

  17. Fukai, S. et al. Cell 103, 793–803 (2000).

    Article  CAS  Google Scholar 

  18. Cusack, S., Yaremchuk, A. & Tukalo, M. EMBO J. 19, 2351–2361 (2000).

    Article  CAS  Google Scholar 

  19. Liu, J. et al. J. Biol. Chem. 270, 15162–15169 (1995).

    Article  CAS  Google Scholar 

  20. Nureki, O. et al. Science 267, 1958–1965 (1995).

    Article  CAS  Google Scholar 

  21. Sekine, S., Nureki, O., Shimada, A., Vassylyev, D.G. & Yokoyama, S. Nature Struct. Biol. 8, 203–206 (2001).

    Article  CAS  Google Scholar 

  22. Ribas de Pouplana, L. & Schimmel, P. Cell 104, 191–193 (2001).

    Article  CAS  Google Scholar 

  23. Delagoutte, B., Moras, D. & Cavarelli, J. EMBO J. 19, 5599–5610 (2000).

    Article  CAS  Google Scholar 

  24. Sekine, S. et al. J. Mol. Biol. 256, 685–700 (1996).

    Article  CAS  Google Scholar 

  25. Commans, S., Lazard, M., Delort, F., Blanquet, S. & Plateau, P. J. Mol. Biol. 278, 801–813 (1998).

    Article  CAS  Google Scholar 

  26. McClain, W.H., Foss, K., Jenkins, R.A. & Schneider, J. Proc. Natl. Acad. Sci. USA 87, 9260–9264 (1990).

    Article  CAS  Google Scholar 

  27. Tamura, K., Himeno, H., Asahara, H., Hasegawa, T. & Shimizu, M. Nucleic Acids Res. 20, 2335–2339 (1992).

    Article  CAS  Google Scholar 

  28. Ribas de Pouplana, L. & Schimmel, P. Trends Biochem. Sci. 26, 591–596 (2001).

    Article  CAS  Google Scholar 

  29. Otwinowski, Z. & Minor, W. Methods Enzymol. 276, 307–326 (1997).

    Article  CAS  Google Scholar 

  30. Weeks, C.M. & Miller, R. J. Appl. Crystallogr. 32, 120–124 (1999).

    Article  CAS  Google Scholar 

  31. de La Fortelle, E. & Bricogne, G. Methods Enzymol. 276, 472–494 (1997).

    Article  CAS  Google Scholar 

  32. Abrahams, J.P. & Leslie, A.G.W. Acta Crystallogr. D 52, 30–42 (1996).

    Article  CAS  Google Scholar 

  33. Collaborative Computational Project, Number 4. Acta Crystallogr. D 50, 760–763 (1994).

  34. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. Acta Crystallogr. A 47, 110–119 (1991).

    Article  Google Scholar 

  35. Adams, P.D., Pannu, N.S., Read, R.J. & Brünger, A.T. Proc. Natl. Acad. Sci. USA 94, 5018–5023 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Supported in part by Grants-in-Aid for Science Research on Priority Areas to S.Y. and O.N. from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and to D.S. from the National Institute of General Medical Sciences. We are greatly indebted to M. Kawamoto (JASRI) for his help in data collection at Spring-8. We also thank L. Ribas de Pouplana for his helpful discussion on the sterically compatible docking of two LysRS families on tRNALys.

Author information

Author notes

  1. Takaho Terada, Osamu Nureki and Dieter Söll: These authors contributed equally to this work.

Authors and Affiliations

  1. RIKEN Genomic Sciences Center, 1-7-22 Suehiro-cho, Tsurumi, 230-0045, Yokohama, Japan

    Takaho Terada, Osamu Nureki & Shigeyuki Yokoyama

  2. RIKEN Harima Institute at Spring-8, 1-1-1 Kohto, Mikazuki-cho, Sayo, 679-5148, Hyogo, Japan

    Takaho Terada, Osamu Nureki & Shigeyuki Yokoyama

  3. Department of Biophysics Biochemistry, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, 113, Tokyo, Japan

    Osamu Nureki, Ryuichiro Ishitani & Shigeyuki Yokoyama

  4. Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, 06520-8114, Connecticut, USA

    Alexandre Ambrogelly & Dieter Söll

  5. Department of Microbiology, The Ohio State University, Columbus, 43210-1292, Ohio, USA

    Michael Ibba

  6. Department of Chemistry, Yale University, New Haven, 06520-8114, Connecticut, USA

    Dieter Söll

Authors
  1. Takaho Terada
    View author publications

    Search author on:PubMed Google Scholar

  2. Osamu Nureki
    View author publications

    Search author on:PubMed Google Scholar

  3. Ryuichiro Ishitani
    View author publications

    Search author on:PubMed Google Scholar

  4. Alexandre Ambrogelly
    View author publications

    Search author on:PubMed Google Scholar

  5. Michael Ibba
    View author publications

    Search author on:PubMed Google Scholar

  6. Dieter Söll
    View author publications

    Search author on:PubMed Google Scholar

  7. Shigeyuki Yokoyama
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Shigeyuki Yokoyama.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Terada, T., Nureki, O., Ishitani, R. et al. Functional convergence of two lysyl-tRNA synthetases with unrelated topologies. Nat Struct Mol Biol 9, 257–262 (2002). https://doi.org/10.1038/nsb777

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nsb777

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing