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.

  • Article
  • Published:

The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis

Nature volume 338, pages 394–401 (1989)Cite this article

Abstract

Three of the four yeast ubiquitin genes encode hybrid proteins which are cleaved to yield ubiquitin and previously unidentified ribosomal proteins. The transient association between ubiquitin and these proteins promotes their incorporation into nascent ribosomes and is required for efficient ribosome biogenesis. These results suggest a novel 'chaperone' function for ubiquitin, in which its covalent association with other proteins promotes the formation of specific cellular structures.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Similar content being viewed by others

References

  1. Hershko, A., Ciechanover, A., Heller, H., Haas, A. L. & Rose, I. A. Proc. natn. Acad. Sci. U.S.A. 77, 1783–1786 (1980).

    Article  ADS  CAS  Google Scholar 

  2. Finley, D., Ciechanover, A. & Varshavsky, A. Cell 37, 43–55 (1984).

    Article  CAS  Google Scholar 

  3. Ciechanover, A., Finley, D. & Varshavsky, A. Cell 37, 57–66 (1984).

    Article  CAS  Google Scholar 

  4. Jentsch, S., McGrath, J. P. & Varshavsky, A. Nature 329, 131–134 (1987).

    Article  ADS  CAS  Google Scholar 

  5. Goebl, M. G. et al. Science 241, 1331–1335 (1988).

    Article  ADS  CAS  Google Scholar 

  6. Kulka, R. G. et al. J. biol. Chem. 263, 15726–15731 (1988).

    CAS  PubMed  Google Scholar 

  7. Schlesinger, M. J. & Bond, U. Oxford Surveys on Eukaryotic genes 4, 77–91 (1987).

    CAS  PubMed  Google Scholar 

  8. Finley, D., Özkaynak, E. & Varshavsky, A. Cell 48, 1035–1046 (1987).

    Article  CAS  Google Scholar 

  9. Tanaka, K., Matsumoto, K. & Toh-e, A. EMBO J. 7, 495–502 (1988).

    Article  CAS  Google Scholar 

  10. Treger, J. M., Heichman, K. A. & McEntee, K. Molec. cell. Biol. 8, 1132–1136 (1988).

    Article  CAS  Google Scholar 

  11. Goff, S. A., Voeilmy, R. & Goldberg, A. in Ubiquitin (ed. Rechsteiner, M.) 207–238 (Plenum, New York, 1988).

    Book  Google Scholar 

  12. Hershko, A. J. biol. Chem. 263, 15237–15240 (1988).

    CAS  PubMed  Google Scholar 

  13. Varshavsky, A., Bachmair, A., Finley, D., Gonda, D. & Wünning, I. in Ubiquitin (ed. Rechsteiner, M.) 287–324 (Plenum, New York, 1988).

    Book  Google Scholar 

  14. Finley, D. & Varshavsky, A. Trends Biochem. Sci. 10, 343–346 (1985).

    Article  CAS  Google Scholar 

  15. Pickart, C. M. in Ubiquitin (ed. Rechsteiner, M.) 77–100 (Plenum, New York, 1988).

    Book  Google Scholar 

  16. Bonner, W. M., Hatch, C. L. & Wu, R. S. in Ubiquitin (ed. Rechsteiner, M.) 157–172 (Plenum, New York, 1988).

    Book  Google Scholar 

  17. Ball, E. et al. Cell 51, 221–228 (1987).

    Article  CAS  Google Scholar 

  18. Siegelman, M. et al. Science 231, 823–829 (1986).

    Article  ADS  CAS  Google Scholar 

  19. Yarden, T. et al. Nature 323, 226–232 (1986).

    Article  ADS  CAS  Google Scholar 

  20. Leung, D. W. et al. Nature 330, 537–543 (1987).

    Article  ADS  CAS  Google Scholar 

  21. Perry, G., Friedman, R., Shaw, G. & Chau, V. Proc. natn. Acad. Sci. U.S.A. 84, 3033–3036 (1987).

    Article  ADS  CAS  Google Scholar 

  22. Manetto, V. et al. Proc. natn. Acad. Sci. U.S.A. 85, 4501–4505 (1988).

    Article  ADS  CAS  Google Scholar 

  23. Chau, V. et al. Science (in the press).

  24. Özkaynak, E., Finley, D., Solomon, M. J. & Varshavsky, A. EMBO J. 6, 1429–1439 (1987).

    Article  Google Scholar 

  25. Finley, D. et al. in Ubiquitin (ed. Rechsteiner, M.) 39–75 (Plenum, New York, 1988).

  26. Ecker, D. J., Khan, M. I., Marsh, J., Butt, T. R. & Crooke, S. T. J. biol. Chem. 262, 3524–3527 (1987).

    CAS  PubMed  Google Scholar 

  27. Bitter, G. A. & Egan, K. M. Gene 69, 193–207 (1988).

    Article  CAS  Google Scholar 

  28. Lund, P. K. et al. J. biol. Chem. 260, 7609–7613 (1985).

    CAS  PubMed  Google Scholar 

  29. Warner, J. R. in The Molecular Biology of the Yeast. Saccharomyces cerevisiae: Metabolism and gene Expression (eds Strathern, J., Jones, E. & Broach, J.) 529–560 (Cold Spring Harbor Laboratory, New York, 1981).

    Google Scholar 

  30. Planta, R. J. & Raué, H. A. Trends Genet. 4, 64–68 (1988).

    Article  CAS  Google Scholar 

  31. Carter, C. J., Cannon, M. & Jiménez, A. Eur. J. Biochem. 107, 173–183 (1980).

    Article  CAS  Google Scholar 

  32. van Holde, K. E. & Hill, W. E. in Ribosomes (eds Nomura, M., Tissieres, A. & Lengyel, P.) 53–91 (Cold Spring Harbor Laboratory, New York, 1974).

    Google Scholar 

  33. Gill, G. & Ptashne, M. Nature 334, 721–724 (1988).

    Article  ADS  CAS  Google Scholar 

  34. Tollervey, D. EMBO J. 6, 4169–4175 (1987).

    Article  CAS  Google Scholar 

  35. Munro, S. & Pelham, H. R. B. Cell 46, 291–300 (1986).

    Article  CAS  Google Scholar 

  36. Bachmair, A., Finley, D. & Varshavsky, A. Science 234, 179–186 (1986).

    Article  ADS  CAS  Google Scholar 

  37. Redman, K. & Rechsteiner, M. Nature (in the press).

  38. Blomstrom, D. C., Fahey, D., Kutney, R., Korant, B. D. & Knight, E. Jr J. Biol. Chem. 261, 8811–8816 (1986).

    CAS  PubMed  Google Scholar 

  39. Haas, A. L., Ahrens, P., Bright, P. M. & Ankel, H. J. biol. Chem. 262, 11315–11323 (1987).

    CAS  PubMed  Google Scholar 

  40. Toniolo, D., Persico, M. & Alcalay, M. Proc. natn. Acad. Sci. U.S.A. 85, 851–855 (1988).

    Article  ADS  CAS  Google Scholar 

  41. Clarke, L. E. et al. Nature 337, 709–716 (1989).

    Article  Google Scholar 

  42. Butt, T. R., Khan, M. I., Marsh, J., Ecker, D. J. & Crooke, S. T. J. biol. Chem. 263, 16364–16371 (1988).

    CAS  PubMed  Google Scholar 

  43. Ellis, J. Nature 328, 378–379 (1987).

    Article  ADS  CAS  Google Scholar 

  44. Hemmingsen, S. M. et al. Nature 333, 330–334 (1988).

    Article  ADS  CAS  Google Scholar 

  45. Laemmli, U. K. & Favre, M. J. molec. Biol. 80, 575–599 (1973).

    Article  CAS  Google Scholar 

  46. Sherman, F., Fink, G. R. & Hicks, J. B. Methods in Yeast Genetics (Cold Spring Harbor Laboratory, New York, 1986).

    Google Scholar 

  47. Maniatis, T., Fritsch, E. F., & Sambrook, J. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory, New York, 1982).

    Google Scholar 

  48. Vieira, J. & Messing, J. Gene 19, 259–268 (1982).

    Article  CAS  Google Scholar 

  49. Hill, J. E., Myers, A. M., Koerner, T. J. & Tzagoloff, A. Yeast 2, 163–167 (1986).

    Article  CAS  Google Scholar 

  50. Parent, S. A., Fenimore, C. M. & Bostian, K. A. yeast 1, 83–138 (1985).

    Article  CAS  Google Scholar 

  51. Guarente, L., Yocum, R. R. & Gifford, P. Proc. natn. Acad. Sci. U.S.A. 79, 7410–7414 (1982).

    Article  ADS  CAS  Google Scholar 

  52. Sprague, G. F. Jr, Jensen, R. & Hershkowitz, I. Cell 32, 409–415 (1983).

    Article  CAS  Google Scholar 

  53. Warner, J. R., Mitra, G., Schwindinger, W. F., Studeny, M. & Fried, H. M. Molec. cell. Biol. 5, 1512–1521 (1985).

    Article  CAS  Google Scholar 

  54. Rotenberg, M. O., Moritz, M. & Woolford, J. L. Jr Genes Dev. 2, 160–172 (1988).

    Article  CAS  Google Scholar 

  55. Munro, S. thesis, Univ. Cambridge (1987).

Download references

Author information

Author notes

  1. Daniel Finley

    Present address: Department of Cellular and Molecular Physiology, Harvard Medical School, Boston, Massachusetts, 02115, USA

Authors and Affiliations

  1. Department of Biology, Massachusetts Institute of Technology, Cambridge, Massachusetts, 02139, USA

    Daniel Finley, Bonnie Bartel & Alexander Varshavsky

Authors
  1. Daniel Finley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bonnie Bartel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander Varshavsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Finley, D., Bartel, B. & Varshavsky, A. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338, 394–401 (1989). https://doi.org/10.1038/338394a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/338394a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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