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Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids

Nature Structural Biology volume 2, pages 1026–1030 (1995)Cite this article

Abstract

The 1250 Å diameter herpes simplex virus-1 (HSV-1) capsid shell consists of four major structural proteins, of which VP26 (∼12,000 Mr) is the smallest. Using 400 kV electron cryomicroscopy and computer reconstruction, we have determined the three-dimensional structures of the wild-type capsid and a recombinant baculovirus-generated HSV-1 capsid which lacks VP26. Their difference map demonstrates the presence of VP26 hexamers attached to all the hexons in the wild-type capsid, and reveals that the VP26 molecule consists of a large and a small domain. Although both hexons and pentons are predominantly composed of VP5, VP26 is not present on the penton. Based on the interactions involving VP26 and the hexon subunits, we propose a mechanism for VP26 assembly which would account for its distribution. Possible roles of VP26 in capsid stability and DNA packaging are discussed.

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References

  1. Whitley, R.J. & Gnann, Jr., J.W.G. in The Human Herpesviruses (eds Roizman, B., Whitley, R.J. & Lopez, C.) 69–105 (Raven, N. Y., 1993).

    Google Scholar 

  2. Rixon, F.J. Structure and assembly of herpesviruses. Sem. Virol. 4, 135–144 (1993).

    Article  CAS  Google Scholar 

  3. Roizman, B. & Sears, A.E. in The Human Herpesviruses (eds Roizman, B., Whitley, R.J. & Lopez, C.) 11–68 (Raven Press, N Y, 1993).

    Google Scholar 

  4. Batterson, W., Furlong, D. & Roizman, B. Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol. 45, 397–407 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Davison, M.D., Rixon, F.J. & Davison, A.J. Identification of genes encoding two capsid proteins (VP24 and VP26) of herpes simplex virus type 1. J. gen. Virol. 73, 2709–2713 (1992).

    Article  CAS  PubMed  Google Scholar 

  6. Rixon, F.J., Cross, A.M., Addison, C. & Preston, V.G. The products of herpes simplex virus gene UL26 which are involved in DNA packaging are strongly associated with empty but not with full capsids. J. gen. Virol. 69, 2879–2891 (1988).

    Article  CAS  PubMed  Google Scholar 

  7. Schrag, J.D., Prasad, B.V.V., Rixon, F.J. & Chiu, W. Three-dimensional structure of the HSV1 nucleocapsid. Cell 56, 651–660 (1989).

    Article  CAS  PubMed  Google Scholar 

  8. Booy, F.P., et al. Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 64, 1007–1015 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhou, Z.H., Prasad, B.V.V., Jakana, J., Rixon, F. & Chiu, W. Protein subunit structures in the herpes simplex virus A-capsid determined from 400 kV spot-scan electron cryomicroscopy. J. molec. Biol. 242, 458–469 (1994).

    Article  Google Scholar 

  10. Newcomb, W.W., et al. Structure of the herpes simplex virus capsid: molecular composition of the pentons and the triplexes. J. molec. Biol. 232, 499–511 (1993).

    Article  CAS  PubMed  Google Scholar 

  11. Trus, B.L., Newcomb, W.W., Booy, F.P., Brown, J.C. & Steven, A.C. Distinct monoclonal antibodies separately label the hexons or the pentons of herpes simples virus capsid. Proc. natn. Acad. Sci. U.S.A. 89, 11508–11512 (1992).

    Article  CAS  Google Scholar 

  12. Booy, F.P., et al. Finding a needle in a haystack: detection of a small protein (the 12-kDa VP26) in a large complex (the 200-MDa capsid of herpes simplex virus). Proc. natn. Acad. Sci. U.S.A. 91, 5652–5656 (1994).

    Article  CAS  Google Scholar 

  13. Tatman, J.D., Preston, V.G., Nicholson, P., Elliott, R.M. & Rixon, F.J. Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses. J. gen. Virol. 75, 1101–1113 (1994).

    Article  CAS  PubMed  Google Scholar 

  14. Thomsen, D.R., Roof, L.L. & Homa, F.L. Assembly of herpes simplex virus (HSV) intermediate capsids in insect cells infected with recombinant Baculoviruses expressing HSV capsid proteins. J. Virol. 68, 2442–2457 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Steven, A.C. et al. Hexavalent capsomers of herpes simplex virus type II: Symmetry, shape, dimensions, and oligomericstatus. J. Virol. 57, 578–584 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Liddington, R.C. et al. Structure of simian virus 40 at 3.8 Å resolution. Nature 354, 278–284 (1991).

    Article  CAS  PubMed  Google Scholar 

  17. Cheng, R.H. et al. Functional implications of quasi-equivalence in a T=3 icosahedral animal virus established by cryo-electron microscopy and X-ray crystallography. Structure 2, 271–282 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. McNabb, D.S. & Courtney, R.J. Identification and characterization of the herpes simplex virus type 1 virion protein encoded by the UL35 open reading frame. J. Virol. 66, 2653–2663 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. McNabb, D.S. & Courtney, R.J. Posttranslational modification and subcellular localization of the p12 capsid protein of herpes simplex virus type 1. J. Virol. 66, 4839–4847 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Newcomb, W.W. & Brown, J.C. Induced extrusion of DNA from the capsid of herpes simplex virus type-1. J. Virol. 68, 433–440 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Brink, J., Chiu, W. & Dougherty, M. Computer-controlled spot-scan imaging of crotoxin complex crystals with 400 keV electrons at near atomic resolution. Ultramicroscopy 68, 229–240 (1992).

    Article  Google Scholar 

  22. Zhou, Z.H. et al. CTF determination of images of ice-embedded single particles using a graphics interface. J. struct. Biol. in the press.

  23. Erickson, H.P. & Klug, A. The Fourier transform of an electron micrograph: effects of defocusing and aberrations, and implications for the use of underfocus contrast enhancement. Phil. Trans. R. Soc.B 261, 105–118 (1970).

    Article  Google Scholar 

  24. Schmid, M.F., Jakana, J., Matsudaira, P. & Chiu, W. Effects of radiation damage with 400kV electrons on frozen, hydrated actin bundles. J. struct. Biol. 108, 62–68 (1992).

    Article  CAS  PubMed  Google Scholar 

  25. Conway, J.F. et al. The effects of radiation damage on the structure of frozen hydrated HSV-1 capsids. J. struct. Biol. 111, 222–233 (1993).

    Article  CAS  PubMed  Google Scholar 

  26. Crowther, R.A. Procedures for three-dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Phil. Trans. R. Soc.B 261, 221–230 (1971).

    Article  CAS  PubMed  Google Scholar 

  27. Fuller, S.D. The T=4 envelope of Sindbis virus is organized by interactions with a complementary T=3 capsid. Cell 48, 923–934 (1987).

    Article  CAS  PubMed  Google Scholar 

  28. Baker, T.S., Newcomb, W.W., Booy, F.P., Brown, J.C. & Steven, A.C. Three-dimensional structures of maturable and abortive capsids of equine herpesvirus 1 from cryoelectron microscopy. J. Virol. 64, 563–573 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Crowther, R.A., et al. Three-dimensional structure of hepatitis B virus core particles determined by electron cryomicroscopy. Cell 77, 943–950 (1994).

    Article  CAS  PubMed  Google Scholar 

  30. Zhou, Z.H. High resolution three-dimensional electron cryomicroscopy and reconstruction of herpes simplex virus capsids. Ph.D. thesis, Baylor College of Medicine (1995).

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Authors and Affiliations

  1. Texas Center for Advanced Molecular Computation, University of Houston, Houston, Texas, 77204-3476, USA

    Z. Hong Zhou

  2. Program of Structural and Computational Biology and Molecular Biophysics, Baylor College of Medicine, Houston, Texas, 77030, USA

    Jing He & Wah Chiu

  3. Verna & Marrs McLean Department of Biochemistry, W.M. Keck Center for Computational Biology, Baylor College of Medicine, Houston, Texas, 77030, USA

    Joanita Jakana & Wah Chiu

  4. MRC Virology Unit, Institute of Virology, Glasgow, G11 5JR, Scotland

    Jacqueline D. Tatman & Frazer J. Rixon

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  1. Z. Hong Zhou
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  2. Jing He
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  4. Jacqueline D. Tatman
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  5. Frazer J. Rixon
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  6. Wah Chiu
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Zhou, Z., He, J., Jakana, J. et al. Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat Struct Mol Biol 2, 1026–1030 (1995). https://doi.org/10.1038/nsb1195-1026

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  • DOI: https://doi.org/10.1038/nsb1195-1026

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