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.

Structure of the L1 protuberance in the ribosome

Abstract

The L1 protuberance of the 50S ribosomal subunit is implicated in the release/disposal of deacylated tRNA from the E site. The apparent mobility of this ribosomal region has thus far prevented an accurate determination of its three-dimensional structure within either the 50S subunit or the 70S ribosome. Here we report the crystal structure at 2.65 Å resolution of ribosomal protein L1 from Sulfolobus acidocaldarius in complex with a specific 55-nucleotide fragment of 23S rRNA from Thermus thermophilus. This structure fills a major gap in current models of the 50S ribosomal subunit. The conformations of L1 and of the rRNA fragment differ dramatically from those within the crystallographic model of the T. thermophilus 70S ribosome. Incorporation of the L1–rRNA complex into the structural models of the T. thermophilus 70S ribosome and the Deinococcus radiodurans 50S subunit gives a reliable representation of most of the L1 protuberance within the ribosome.

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

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Components of the L1–rRNA complex.
Figure 2: Structure of the RNA fragment and its interactions with the protein.
Figure 3: Representation of the L1 protuberance within the ribosome.

Accession codes

Accessions

Protein Data Bank

References

  1. Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905–920 (2000).

    Article  CAS  Google Scholar 

  2. Harms, J. et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107, 679–688 (2001).

    Article  CAS  Google Scholar 

  3. Yusupov, M.M. et al. Crystal structure of the ribosome at 5.5 Å resolution. Science 292, 883–896 (2001).

    Article  CAS  Google Scholar 

  4. Zimmermann, R.A. Interactions among protein and RNA components of the ribosome. in Ribosomes. Structure, Function and Genetics (eds. Chambliss, G. et al.) 135–169 (University Park Press, Baltimore; 1980).

    Google Scholar 

  5. Malhotra, A. et al. Escherichia coli 70 S ribosome at 15 Å resolution by cryo-electron microscopy: localization of fMet-tRNAfMet and fitting of L1 protein. J. Mol. Biol. 280, 103–116 (1998).

    Article  CAS  Google Scholar 

  6. Agrawal, R.K. et al. Visualization of tRNA movements on the E. coli 70S ribosome during the elongation cycle. J. Cell Biol. 150, 447–460 (2000).

    Article  CAS  Google Scholar 

  7. Moazed, D. & Noller, H.F. Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell 57, 585–597 (1989).

    Article  CAS  Google Scholar 

  8. Wower, J. et al. Transit of tRNA through the Escherichia coli ribosome. Cross-linking of the 3′ end of tRNA to specific nucleotides of the 23 S ribosomal RNA at the A, P, and E sites. J. Biol. Chem. 275, 37887–37894 (2000).

    Article  CAS  Google Scholar 

  9. Kirillov, S.V., Wower, J., Hixson, S.H. & Zimmermann, R.A. Transit of tRNA through the Escherichia coli ribosome: cross-linking of the 3′ end of tRNA to ribosomal proteins at the P and E sites. FEBS Lett. 514, 60–66 (2002).

    Article  CAS  Google Scholar 

  10. Gabashvili, I.S. et al. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100, 537–549 (2000).

    Article  CAS  Google Scholar 

  11. Gomez-Lorenzo, M.G. et al. Tree-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 Å resolution. EMBO J. 19, 2710–2718 (2000).

    Article  CAS  Google Scholar 

  12. Baier, G. et al. Structural and functional equivalence between ribosomal proteins of Escherichia coli L1 and Methanococcus vannielii L6. Syst. Appl. Microbiol. 12, 119–126 (1989).

    Article  CAS  Google Scholar 

  13. Hanner, M. et al. Autogenous translational regulation of the ribosomal MvaL1 operon in the archaebacterium Methanococcus vannielii. J. Bacteriol. 176, 409–418 (1994).

    Article  CAS  Google Scholar 

  14. Nevskaya, N. et al. Archaeal ribosomal protein L1: the structure provides new insights into RNA binding of the L1 protein family. Structure 8, 363–371 (2000).

    Article  CAS  Google Scholar 

  15. Nevskaya, N. et al. Structure of ribosomal protein L1 from Methanococcus thermolithotrophicus. Functionally important structural invariants on the L1 surface. Acta Crystallogr. D 58, 1023–1029 (2002).

    Article  Google Scholar 

  16. Egebjerg, J., Christiansen, J. & Garret, R.A. Attachment sites of primary binding proteins L1, L2 and L23 on 23S ribosomal RNA of Escherichia coli. J. Mol. Biol. 222, 251–264 (1991).

    Article  CAS  Google Scholar 

  17. Doring, T., Greuer, B. & Brimacombe, R. The three-dimensional folding of ribosomal RNA; localization of a series of intra-RNA cross-links in 23S RNA induced by treatment of Escherichia coli 50S ribosomal subunits with bis-(2-chloroethyl)-methylamine. Nucleic Acids Res. 19, 3517–3524 (1991).

    Article  CAS  Google Scholar 

  18. Nikonov, S. et al. Crystal structure of the RNA binding ribosomal protein L1 from Thermus thermophilus. EMBO J. 15, 1350–1359 (1996).

    Article  CAS  Google Scholar 

  19. Stanley, J., Sloof, P. & Ebel, J.-P. The binding site of ribosomal protein L1 from Escherichia coli on the 23S ribosomal RNA from Bacillus stearothermophilus. A possible base-pairing scheme differing from that proposed for Escherichia coli. Eur. J. Biochem. 85, 309–316 (1978).

    Article  CAS  Google Scholar 

  20. Zimmermann, R.A., Thurlow, D.L., Finn, R.S., Marsh, T.L. & Ferrett, L.K. Conservation of specific protein-RNA interactions in ribosome evolution. in Genetics and Evolution of RNA Polymerase, tRNA and Ribosomes (eds. Osava, S., Ozeki, H., Uchida, H. & Yura, T.) 569–584 (University of Tokyo Press, Tokyo; 1980)

    Google Scholar 

  21. Gourse, R.L., Thurlow, D.L., Gerbi, S.A. & Zimmermann, R.A. Specific binding of a prokaryotic ribosomal protein to a eukaryotic ribosomal RNA: implications for evolution and autoregulation. Proc. Natl. Acad. Sci. USA 78, 2722–2726 (1981).

    Article  CAS  Google Scholar 

  22. Baier, G., Piendl, W., Redl, B. & Stoffler, G. Structure, organization and evolution of the L1 equivalent ribosomal protein gene of the archaebacterium Methanococcus vannielii. Nucleic Acids Res. 18, 719–724 (1990).

    Article  CAS  Google Scholar 

  23. Yusupov, M.M. & Spirin, A.S. Are there proteins between the ribosomal subunits? Hot tritium bombardment experiments. FEBS Lett. 197, 229–233 (1986).

    Article  CAS  Google Scholar 

  24. Drygin, D. & Zimmermann, R.A. Magnesium ions mediate contacts between phosphoryl oxygens at positions 2122 and 2176 of the 23S rRNA and ribosomal protein L1. RNA 6, 1714–1726 (2000).

    Article  CAS  Google Scholar 

  25. Kraft, A., Lutz, C., Lingenhel, A., Gröbner, P. & Piendl, W. Control of ribosomal protein L1 synthesis in mesophilic and thermophilic archaea. Genetics 152, 1363–1372 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Brinkmann, U., Mattes, R.E. & Buckel, P. High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene 85, 109–114 (1989).

    Article  CAS  Google Scholar 

  27. Tishchenko, S. et al. Crystals of ribosomal protein L1 from a hyperthermophilic archaeon Methanococcus jannaschii. Biochem. Mol. Biol. Int. 45, 349–354 (1998).

    CAS  PubMed  Google Scholar 

  28. Kabsch, W. Integration, scaling, space-group assignment and post refinement. XDS. in International Tables for Crystallography (eds. Rossmann, M.G. & Arnold, E.) F (Kluwer Academic Publishers, Dordrecht; 2001).

    Google Scholar 

  29. Brunger, A.T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905–921 (1998).

    Article  CAS  Google Scholar 

  30. Jones, T.A., Zhou, J.Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Russian Academy of Sciences and the Russian Foundation for Basic Research. The research of M.G. was supported in part by the International Research Scholar's award from the Howard Hughes Medical Institute. The research of W.P. was supported by the Austrian Science Fund and the Austrian-Russian Collaboration Program. The research of R.A.Z. was supported by a grant from the U.S. National Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stanislav Nikonov.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nikulin, A., Eliseikina, I., Tishchenko, S. et al. Structure of the L1 protuberance in the ribosome. Nat Struct Mol Biol 10, 104–108 (2003). https://doi.org/10.1038/nsb886

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb886

This article is cited by

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