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:

Ordered duplex RNA controls capsid architecture in an icosahedral animal virus

Nature volume 361, pages 176–179 (1993)Cite this article

Abstract

SMALL spherical viruses are among the simplest replicating systems in biology, yet the factors affecting their assembly, stability and disassembly are still poorly understood. A molecular switch is required for the assembly of icosahedral virus particles containing more than 60 identical subunits because strict symmetry cannot be maintained in subunit packing1. All previously reported viruses with this type of structure use a portion of the capsid protein to regulate interactions between chemically equivalent but structurally distinct interfaces2–4. We have investigated the T = 3 quasiequivalent5 nodaviruses, which are small non-enveloped viruses with a single-stranded RNA genome that infect insects6, mice7 and fish8. They undergo a well-characterized series of steps in assembly and maturation9,10, which in some respects are similar to the picornaviruses11, despite their different capsid architecture. Here we report the X-ray structure of Flock House virus at 3.0 Å resolution, which reveals an ordered RNA duplex of 20 nucleotides and a protein segment that control the subunit interactions in this animal virus. The RNA interacts with a helical protein domain of the subunit that lies inside the capsid shell. One of the helices that binds the RNA is part of a 44-amino-acid polypeptide which is autocatalytically cleaved from the initial subunit translation product after virion assembly. The structure indicates that RNA associated with the cleaved polypeptide may be important in the infection process.

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. Caspar, D. L. D. Biophys. J. 32, 103–138 (1980).

    Article  ADS  CAS  Google Scholar 

  2. Harrison, S. C., Olson, A. J., Schutt, C. E. Winkler, F. K. & Bricogne, G. Nature 276, 368–373 (1978).

    Article  ADS  CAS  Google Scholar 

  3. Abad-Zapatero, C. et al. Nature 286, 33–39 (1980).

    Article  ADS  CAS  Google Scholar 

  4. Hogle, J. M., Maeda, A. & Harrison, S. C. J. molec. Biol. 191, 625–638 (1986).

    Article  CAS  Google Scholar 

  5. Caspar, D. L. D. & Klug, A. Cold Spring Harbor Symp. quant Biol. 27, 1–24 (1962).

    Article  CAS  Google Scholar 

  6. Hendry, D. A. in Viruses of Invertebrates (ed. Kurstak, E.) 227–276 (Dekker, New York, 1991).

    Google Scholar 

  7. Newman, J. F. E. & Brown, F. J. gen. Virol. 21, 371–384 (1973).

    Article  CAS  Google Scholar 

  8. Mori, K.-I. et al. Virology 187, 368–371 (1992).

    Article  CAS  Google Scholar 

  9. Gallagher, T. M. & Rueckert, R. R. J. Virol. 62, 3399–3406 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Kaesberg, P. et al. J. molec. Biol. 214, 423–435 (1990).

    Article  CAS  Google Scholar 

  11. Fernandez-Tomas, C. B. & Baltimore, D. J. Virol. 12, 1122–1130 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Rossmann, M. G. & Johnson, J. E. A. Rev. Biochem. 58, 533–573 (1989).

    Article  CAS  Google Scholar 

  13. Li, T., Chen, Z., Johnson, J. E. & Thomas, G. J. Biochemistry 29, 5018–5026 (1990).

    Article  CAS  Google Scholar 

  14. Chen, Z. et al. Science 245, 154–159 (1989).

    Article  ADS  CAS  Google Scholar 

  15. Tsao, J. et al. Science 251, 1456–1464 (1991).

    Article  ADS  CAS  Google Scholar 

  16. McKenna, R. et al. Nature 355, 137–143 (1992).

    Article  ADS  CAS  Google Scholar 

  17. Kraulis, P. J. J. appl. Crystallogr. 24, 946–950 (1991).

    Article  Google Scholar 

  18. Smith, T. J. J. appl. Crystallogr. 23, 141–142 (1990).

    Article  Google Scholar 

  19. Fisher, A. J., McKinney, B. R., Wery, J.-P. & Johnson, J. E. Acta. crystallogr. B48, 515–520 (1992).

    Article  Google Scholar 

  20. Hosur, M. V. et al. Proteins: Struct. Funct. Genet. 2, 167–176 (1987).

    Article  CAS  Google Scholar 

  21. Arnold, E. et al. Acta crystallogr. A43, 346–361 (1987).

    Article  Google Scholar 

  22. Jones, T. A. J. appl. Crystallogr. 11, 268–272 (1978).

    Article  CAS  Google Scholar 

  23. Hogle, J., Kirchhausen, T. & Harrison, S. C. J. molec. Biol. 171, 95–100 (1983).

    Article  CAS  Google Scholar 

  24. Silva, A. M. & Rossmann, M. G. J. molec. Biol. 197, 69–87 (1987).

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Andrew J. Fisher

    Present address: Institute for Enzyme Research, University of Wisconsin, Madison, Wisconsin, 53705, USA

  2. John E. Johnson: To whom correspondence should be addressed

Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, Indiana, 47907-1392, USA

    Andrew J. Fisher & John E. Johnson

Authors
  1. Andrew J. Fisher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John E. Johnson
    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

Fisher, A., Johnson, J. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361, 176–179 (1993). https://doi.org/10.1038/361176a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/361176a0

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