1887

Abstract

Immature or B capsids of herpes simplex virus type 1 (HSV-1) are composed of seven proteins encoded by six viral genes. The proteins encoded by UL18 (VP23), UL19 (VP5), UL35 (VP26) and UL38 (VP19C) are components of the outer capsid shell whereas those specified by UL26 (VP21 and VP24) and UL26.5 (VP22a), are involved in scaffold formation. We have used a panel of recombinant baculoviruses, each expressing one of the capsid protein genes, to examine the requirements for capsid assembly. Coexpression of the six genes in insect cells resulted in the formation of capsids that were indistinguishable in appearance and protein composition from those made during HSV-1 infection of mammalian cells. This demonstrates that the proteins encoded by the known capsid genes contain all the structural information necessary for capsid assembly and that other virus-encoded proteins are not required for this process. Omission of single recombinant baculo-viruses from this system allowed the role of individual HSV-1 proteins in capsid assembly to be determined. Thus, capsid assembly did not take place in the absence of VP23, VP5 or VP19C, whereas lack of VP26 had no discernible effect on capsid formation. Capsids assembled in the absence of the UL26 gene products had a large-cored phenotype resembling that previously described for the HSV-1 mutant 1201 which has a lesion in this gene. Some apparently intact capsid shells were also made in the absence of the major scaffolding protein, VP22a, whereas the omission of both UL26 and UL26.5 resulted in the appearance of large numbers of partial and deformed capsid shells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-75-5-1101
1994-05-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/75/5/JV0750051101.html?itemId=/content/journal/jgv/10.1099/0022-1317-75-5-1101&mimeType=html&fmt=ahah

References

  1. Baker T. S., Newcomb W. W., Booy F. P., Brown J. C., Steven A. C. 1990; Three-dimensional structures of maturable and abortive capsids of equine herpesvirus 1 from cryoelectron microscopy. Journal of Virology 64:563–573
    [Google Scholar]
  2. Bishop D. H. L. 1992; Baculovirus expression vectors. Seminars in Virology 3:253–264
    [Google Scholar]
  3. Booy F. P., Newcomb W. W., Trus B. L., Brown J. C., Baker T. S., Steven A. C. 1991; Liquid-crystalline, phage-like packing of encapsidated DNA in herpes simplex virus. Cell 64:1007–1015
    [Google Scholar]
  4. Brown M., Faulkner P. 1977; A plaque assay for nuclear polyhedrosis virus using a solid overlay. Journal of General Virology 36:361–364
    [Google Scholar]
  5. Brown S. M., Ritchie D. A., Subak-Sharpe J. H. 1973; Genetic studies with herpes simplex virus type 1: the isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. Journal of General Virology 18:329–346
    [Google Scholar]
  6. Davison M. D., Rixon F. J., Davison A. J. 1992; Identification of genes encoding two capsid proteins (VP24 and VP26) of herpes simplex virus type 1. Journal of General Virology 73:2709–2713
    [Google Scholar]
  7. Deckman I. C., Hagen M., Mccann P. J. 1992; Herpes simplex type 1 protease expressed in Escherichia coli exhibits autoprocessing and specific cleavage of the ICP35 assembly protein. Journal of Virology 66:7362–7367
    [Google Scholar]
  8. Desai P., Deluca N. A., Glorioso J. C., Person S. 1993; Mutations in herpes simplex virus type 1 genes encoding VP5 and VP23 abrogate capsid formation and cleavage of replicated DNA. Journal of Virology 67:1357–1364
    [Google Scholar]
  9. Diianni C. L., Drier D. A., Deckman I. C., Mccann P. J., Liu F., Roizman B., Colonno R. J., Cordingly M. G. 1993; Identification of the herpes simplex virus-1 protease cleavage sites. Journal of Biological Chemistry 268:2048–2051
    [Google Scholar]
  10. Earnshaw W., King J. 1978; Structure of phage P22 coat protein aggregates formed in the absence of scaffolding protein. Journal of Molecular Biology 126:721–747
    [Google Scholar]
  11. Fuller M. T., King J. 1981; Purification of the coat and scaffolding proteins from procapsids of bacteriophage P22. Virology 112:529–547
    [Google Scholar]
  12. Fuller M. T., King J. 1982; Assembly in vitro of bacteriophage P22 procapsids from purified coat and scaffolding subunits. Journal of Molecular Biology 156:633–665
    [Google Scholar]
  13. Gibson W., Roizman B. 1972; Proteins specified by herpes simplex virus. VIII. Characterization and composition of multiple capsid forms of subtypes 1 and 2. Journal of Virology 10:1044–1052
    [Google Scholar]
  14. King J., Lenk E. V., Botstein D. 1973; Mechanism of head assembly and DNA encapsulation in Salmonella phage P22 II. Morphogenetic pathway. Journal of Molecular Biology 80:697–731
    [Google Scholar]
  15. King L. A., Possee R. D. 1992 The Baculovirus Expression System: A Laboratory Guide London: Chapman & Hall;
    [Google Scholar]
  16. Kuhn A., Keller B., Maeder M., Traub F. 1987; Prohead core of bacteriophage T4 can act as an intermediate in the T4 head assembly pathway. Journal of Virology 61:113–118
    [Google Scholar]
  17. Lenk E., Casjens S., Weeks J., King J. 1975; Intracellular visualisation of precursor capsids in phage P22 mutant infected cells. Virology 68:182–199
    [Google Scholar]
  18. Liu F., Roizman B. 1991a; The promoter, transcriptional unit, and coding sequences of the herpes simplex virus 1 family 35 proteins are contained within and in frame with the UL26 open reading frame. Journal of Virology 65:206–212
    [Google Scholar]
  19. Liu F., Roizman B. 1991b; The herpes simplex virus 1 gene encoding a protease also contains within its coding domain the gene encoding the more abundant substrate. Journal of Virology 65:5149–5156
    [Google Scholar]
  20. Liu F., Roizman B. 1992; Differentiation of multiple domains in the herpes simplex virus 1 protease encoded by the UL26 gene. Proceedings of the National Academy of Sciences U.S.A: 892076–2080
    [Google Scholar]
  21. Livingstone C., Jones I. 1989; Baculovirus expression vectors with single strand capability. Nucleic Acids Research 17:2366
    [Google Scholar]
  22. Mcgeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., Mcnab D., Perry L. J., Scott J. E., Taylor P. 1988; The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. Journal of General Virology 69:1531–1574
    [Google Scholar]
  23. Mcnabb D. S., Courtney R. J. 1992; Identification and characterization of the herpes simplex virus type 1 virion protein encoded by the UL35 open reading frame. Journal of Virology 66:2653–2663
    [Google Scholar]
  24. Marsden H. S., Crombie I. K., Subak-Sharpe J. H. 1976; Control of protein synthesis in herpesvirus-infected cells: analysis of the polypeptides induced by wild type and sixteen temperature-sensitive mutants of HSV strain 17. Journal of General Virology 31:347–372
    [Google Scholar]
  25. Matsuura Y., Possee R. D., Overton H. A., Bishop D. H. L. 1987; Baculovirus expression vectors: the requirements for high level expression of proteins, including glycoproteins. Journal of General Virology 68:1233–1250
    [Google Scholar]
  26. Newcomb W. W., Brown J. C. 1989; Use of Ar+ plasma etching to localize structural proteins in the capsid of herpes simplex virus type 1. Journal of Virology 63:4697–4702
    [Google Scholar]
  27. Newcomb W. W., Brown J. C. 1991; Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. Journal of Virology 65:613–620
    [Google Scholar]
  28. Newcomb W. W., Brown J. C., Booy F. P., Steven A. C. 1989; Nucleocapsid mass and protein stoichiometry in equine herpesvirus 1: scanning transmission electron microscopic study. Journal of Virology 63:3777–3783
    [Google Scholar]
  29. Newcomb W. W., Trus B. L., Booy F. P., Steven A. C., Wall J. S., Brown J. C. 1993; Structure of the herpes simplex virus capsid: molecular composition of the pentons and triplexes. Journal of Molecular Biology 232:499–511
    [Google Scholar]
  30. Nicholson P. 1992 Analysis of four capsid protein genes of HSV-1 Ph.D. Thesis University of Glasgow:
    [Google Scholar]
  31. Nicholson P., Addison C., Cross A. M., Kennard J., Preston V. G., Rixon F. J. 1994; Localization of the herpes simplex virus type 1 major capsid protein VP5 to the cell nucleus requires the abundant scaffolding protein VP22a. Journal of General Virology 75:1091–1099
    [Google Scholar]
  32. Perdue M. L., Cohen J. C., Randall C. C., O’Callaghan D. J. 1976; Biochemical studies on the maturation of herpesvirus nucleocapsid species. Virology 74:194–208
    [Google Scholar]
  33. Person S., Laquerre S., Desai P., Hempel J. 1993; Herpes simplex virus type 1 capsid protein, VP21, originates within the UL26 open reading frame. Journal of General Virology 74:2269–2273
    [Google Scholar]
  34. Pertuiset B., Boccara M., Cebrian J., Berthelot N., Chouster-Man S., Puvion-Dutilleul F., Sisman J., Sheldrick P. 1989; Physical mapping and nucleotide sequence of a herpes simplex virus type 1 gene required for capsid assembly. Journal of Virology 63:2169–2179
    [Google Scholar]
  35. Preston V. G., Coates J. A. V., Rixon F. J. 1983; Identification and characterization of a herpes simplex virus gene product required for encapsidation of virus DNA. Journal of Virology 45:1056–1064
    [Google Scholar]
  36. Preston V. G., Rixon F. J., Mcdougall I. M., Mcgregor M., Alkobaisi M. F. 1992; Processing of the herpes simplex virus assembly protein ICP35 near its carboxy terminal end requires the product of the whole UL26 open reading frame. Virology 186:87–98
    [Google Scholar]
  37. Rixon F. J. 1993; Structure and assembly of herpesviruses. Seminars in Virology 4:135–144
    [Google Scholar]
  38. Rixon F. J., Cross A. M., Addison C., Preston V. G. 1988; The products of herpes simplex virus type 1 gene UL26 which are involved in DNA packaging are strongly associated with empty but not with full capsids. Journal of General Virology 69:2879–2891
    [Google Scholar]
  39. Rixon F. J., Davison M. D., Davison A. J. 1990; Identification of the genes encoding two capsid proteins of herpes simplex virus type 1 by direct amino acid sequencing. Journal of General Virology 71:1211–1214
    [Google Scholar]
  40. Rose J. K., Buonocore L., Whitt M. A. 1991; A new cationic liposome reagent mediating nearly quantitative transfection of animal cells. Biotechniques 10:520–525
    [Google Scholar]
  41. Schaffer P. A., Brunschwig J. P., Mccombs R. M., Benyesh-Melnick M. 1974; Electron microscopic studies of temperature-sensitive mutants of herpes simplex virus type 1. Virology 62:444–457
    [Google Scholar]
  42. Schrag J. D., Prasad B. V. V., Rixon F. J., Chiu W. 1989; Three-dimensional structure of the HSV-1 nucleocapsid. Cell 56:651–660
    [Google Scholar]
  43. Sherman G., Bachenheimer S. L. 1988; Characterization of intranuclear capsids made by ts morphogenic mutants of HSV-1. Virology 163:471–480
    [Google Scholar]
  44. Traub F., Maeder M. 1984; Formation of the prohead core of bacteriophage T4 in vivo. Journal of Virology 49:892–901
    [Google Scholar]
  45. Traub F., Keller B., Kuhn A., Maeder M. 1984; Isolation of the prohead core of bacteriophage T4 after cross-linking and determination of protein composition. Journal of Virology 49:902–908
    [Google Scholar]
  46. Trus B. L., Newcomb W. W., Booy F. P., Brown J. C., Steven A. C. 1992; Distinct monoclonal antibodies separately label the hexons or the pentons of herpes simplex virus capsid. Proceedings of the National Academy of Sciences U.S.A: 8911508–11512
    [Google Scholar]
  47. Weinheimer S. P., Mccann P. J., O’Boyle D. R., Stevens J. T., Boyd B. A., Drier D. A., Yamanaka G. A., Diianni C. L., Deckman I. C., Cordingly M. G. 1993; Autoproteolysis of herpes simplex virus type 1 protease releases an active catalytic domain found in intermediate capsid particles. Journal of Virology 67:5813–5822
    [Google Scholar]
  48. Welch A. R., Woods A. S., Mcnally L. M., Cotter R. J., Gibson W. 1991; A herpesvirus maturational proteinase, assem-blin: identification of its gene, putative active site domain, and cleavage site. Proceedings of the National Academy of Sciences U.S.A: 8810792–10796
    [Google Scholar]
  49. Weller S. K., Carmichael E. P., Aschman D. P., Goldstein D. J., Schaffer P. A. 1987; Genetic and phenotypic characterization of mutants in four essential genes that map to the left half of HSV-1 UL DNA. Virology 161:198–210
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-75-5-1101
Loading
/content/journal/jgv/10.1099/0022-1317-75-5-1101
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error