1887

Abstract

Summary

The genes of herpes simplex virus type 1 (HSV-1) can be divided into at least three temporally regulated groups termed immediate early (IE), early and late. We have studied in detail the expression of a member of the late class of genes, US11, which encodes a polypeptide of apparent molecular weight 21K. Highly specific and sensitive probes were used to monitor US11 RNA and protein synthesis during HSV-1 infection of tissue culture cells in the presence and absence of phosphonoacetic acid, an inhibitor of viral DNA replication. The results were compared with a similar study of the products of a delayed early gene, US6, encoding glycoprotein D (gD). It was found that the patterns of RNA and protein synthesis from US11 were significantly different to those of gD. US11 products appeared later and accumulated until late in infection, while gD RNA was significantly reduced at late times. In the presence of the inhibitor of DNA synthesis, US11 gene expression was reduced 50- to 100-fold while gD expression was reduced five- to tenfold. We conclude that US11 behaves as a true late gene during HSV-1 infection. However, the use of sensitive assays, which allowed the detection of very low levels of US11 gene products under conditions designed to eliminate DNA replication, brings into question the absolute requirement for DNA replication for the expression of a true late HSV-1 gene. These results are discussed in terms of current models for the regulation of late gene expression.

Keyword(s): expression , HSV-1 and late gene
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-67-5-871
1986-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/67/5/JV0670050871.html?itemId=/content/journal/jgv/10.1099/0022-1317-67-5-871&mimeType=html&fmt=ahah

References

  1. Anderson K. P., Frink R. J., Devi G. B., Gaylord B. H., Costa R. H., Wagner E. K. 1981; Detailed characterization of the mRNA mapping in the Hind III fragment K region of the herpes simplex virus type 1 genome. Journal of Virology 37:1011–1027
    [Google Scholar]
  2. Bassiri R. M., Dvorak J., Utiger R. D. 1979; Thyrotropin-releasing hormone. In Methods of Hormone Radioimmunoassay pp 46–47 Edited by Jaffe B. M., Behrman H. R. New York: Academic Press;
    [Google Scholar]
  3. Bayliss G. J., Marsden H. S., Hay J. 1975; Herpes simplex virus proteins: DNA-binding proteins in infected cells and in the virus structure. Virology 68:124–134
    [Google Scholar]
  4. 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]
  5. Campbell M. E. M., Palfreyman J. W., Preston C. M. 1984; Identification of herpes simplex virus DNA sequences which encode a trans-acting polypeptide responsible for stimulation of immediate early transcription. Journal of Molecular Biology 180:1–19
    [Google Scholar]
  6. Conley A. J., Knipe D. M., Jones P. C., Roizman B. 1981; Molecular genetics of herpes simplex virus. VII. Characterization of a temperature-sensitive mutant produced by in vitro mutagenesis and defective in DNA synthesis and accumulation of γ polypeptides. Journal of Virology 37:191–206
    [Google Scholar]
  7. Crumpacker C. S., Chartrand P., Subak-Sharpe J. H., Wilkie N. M. 1980; Resistance of herpes simplex virus to acycloguanosine – genetic and physical analysis. Virology 105:171–184
    [Google Scholar]
  8. Dalziel R. G., Marsden H. S. 1984; Identification of two herpes simplex virus type 1-induced proteins (21K and 22K) which interact specifically with the a sequence of herpes simplex virus DNA. Journal of General Virology 65:1467–1475
    [Google Scholar]
  9. Everett R. D. 1983; DNA sequence elements required for regulated expression of the HSV-1 glycoprotein D gene lie within 83 bp of the RNA capsites. Nucleic Acids Research 11:6647–6666
    [Google Scholar]
  10. Everett R. D. 1984a; Trans activation of transcription by herpes virus products: requirement for two HSV-1 immediate-early polypeptides for maximum activity. EMBO Journal 3:3135–3141
    [Google Scholar]
  11. Everett R. D. 1984b; A detailed analysis of an HSV-1 early promoter: sequences involved in trans-activation by viral immediate-early gene products are not early-gene specific. Nucleic Acids Research 12:3037–3056
    [Google Scholar]
  12. Godowski P. J., Knipe D. M. 1985; Identification of a herpes simplex virus function that represses late gene expression from parental viral genomes. Journal of Virology 55:357–365
    [Google Scholar]
  13. Hall L. M., Draper K. G., Frink R. J., Costa R. H., Wagner E. K. 1982; Herpes simplex virus mRNA species mapping in Eco RI fragment I. Journal of Virology 43:594–607
    [Google Scholar]
  14. Hartzell S. W., Byrne B. J., Subramanian K. N. 1984; Mapping of the late promoter of simian virus 40. Proceedings of the National Academy of Sciences, U,. S,. A. 81:23–27
    [Google Scholar]
  15. Hay J., Subak-Sharpe J. H. 1976; Mutants of herpes simplex virus types 1 and 2 that are resistant to phosphonoacetic acid induce altered DNA polymerase activities in infected cells. Journal of General Virology 31:145–148
    [Google Scholar]
  16. Holland L. E., Anderson K. P., Shipman C. Jr, Wagner E. K. 1980; Viral DNA synthesis is required for the efficient expression of specific herpes simplex virus type 1 mRNA species. Virology 101:10–24
    [Google Scholar]
  17. Honess R. W., Roizman B. 1974; Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. Journal of Virology 14:8–19
    [Google Scholar]
  18. Honess R. W., Roizman B. 1975; Regulation of herpes virus macromolecular synthesis: sequential transition of polypeptide synthesis requires functional viral polypeptides. Proceedings of the National Academy of Sciences, U,. S,. A 72:1276–1280
    [Google Scholar]
  19. Honess R. W., Watson D. H. 1977; Herpes simplex virus resistance and sensitivity to phosphonoacetic acid. Journal of Virology 21:584–600
    [Google Scholar]
  20. Hunter W. M., Greenwood F. C. 1962; Preparation of iodine-131 labelled human growth hormone of high specific activity. Nature, London 194:495–496
    [Google Scholar]
  21. Jat P., Roberts J. W., Cowie A., Kamen R. 1982; Comparison of the polyoma virus early and late promoters by transcription in vitro. Nucleic Acids Research 10:871–887
    [Google Scholar]
  22. Johnson D. C., Spear P. G. 1984; Evidence for translational regulation of herpes simplex virus type 1 gD expression. Journal of Virology 51:389–394
    [Google Scholar]
  23. Jones P. C., Roizman B. 1979; Regulation of herpes virus macromolecular synthesis. VIII. The transcription program consists of three phases during which both extent of transcription and accumulation of RNA in the cytoplasm are regulated. Journal of Virology 31:299–314
    [Google Scholar]
  24. Kafatos F. C., Jones C. W., Efstratiadis A. 1979; Determination of nucleic acid sequence homologies and relative concentrations by dot hybridization procedure. Nucleic Acids Research 7:1541–1552
    [Google Scholar]
  25. Keller J. M., Alwine J. C. 1984; Activation of the SV401ate promoter: direct effects of T antigen in the absence of viral DNA replication. Cell 36:381–389
    [Google Scholar]
  26. Lonsdale D. M., Brown S. M., Subak-Sharpe J. H., Warren K. G., Koprowski H. 1979; The polypeptide and the DNA restriction enzyme profiles of spontaneous isolates of herpes simplex virus type 1 from explants of human trigeminal, superior cervical and vagus ganglia. Journal of General Virology 43:151–171
    [Google Scholar]
  27. McGeoch D. J., Dolan A., Donald S., Rixon F. J. 1985; Sequence determination and genetic content of the short unique region in the genome of herpes simplex virus type 1. Journal of Molecular Biology 181:1–13
    [Google Scholar]
  28. Macpherson I., Stoker M. G. 1962; Polyoma transformation of hamster cell clones – an investigation of genetic factors affecting cell competence. Virology 16:147–151
    [Google Scholar]
  29. 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]
  30. Marsden H. S., Stow N. D., Preston V. G., Timbury M. C., Wilkie N. M. 1978; Physical mapping of herpes simplex virus-induced polypeptides. Journal of Virology 28:624–642
    [Google Scholar]
  31. Maxam A. M., Gilbert W. 1980; Sequencing end-labeled DNA with base-specific chemical cleavages. Methods in Enzymology 65:499–560
    [Google Scholar]
  32. Murchie M.-J., McGeoch D. J. 1982; DNA sequence analysis of an immediate-early gene region of the herpes simplex virus type 1 genome (map coordinates 0.950 to 0.978). Journal of General Virology 62:1–15
    [Google Scholar]
  33. O’hare P., Hayward G. S. 1985; Evidence for a direct role for both the 175, 000- and 110, 000-molecular-weight immediate-early proteins of herpes simplex virus in the transactivation of delayed-early promoters. Journal of Virology 53:751–760
    [Google Scholar]
  34. Pedersen M., Talley-Brown S., Millette R. L. 1981; Gene expression of herpes simplex virus. III. Effect of arabinosyladenine on viral polypeptide synthesis. Journal of Virology 38:712–719
    [Google Scholar]
  35. Powell K. L., Purifoy D. J. M., Courtney R. J. 1975; The synthesis of herpes simplex virus proteins in the absence of virus DNA synthesis. Biochemical and Biophysical Research Communications 66:262–271
    [Google Scholar]
  36. Preston C. M., Cordingley M. G., Stow N. D. 1984; Analysis of DNA sequences which regulate the transcription of a herpes simplex virus immediate early gene. Journal of Virology 50:708–716
    [Google Scholar]
  37. Quinlan M. P., Knipe D. M. 1985; A genetic test for expression of a functional herpes simplex virus DNA-binding protein from a transfected plasmid. Journal of Virology 54:619–622
    [Google Scholar]
  38. Rigby P. W. J., Dieckmann M., Rhodes C., Berg P. 1977; Labelling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. Journal of Molecular Biology 113:237–251
    [Google Scholar]
  39. Rixon F. J., McGeoch D. J. 1984; A 3′ co-terminal family of mRNAs from the herpes simplex virus type 1 short region: two overlapping reading frames encode unrelated polypeptides one of which has a highly reiterated amino acid sequence. Nucleic Acids Research 12:2473–2487
    [Google Scholar]
  40. Silver S., Roizman B. 1985; γ 2, -Thymidine kinase chimeras are identically transcribed but regulated as γ 2 genes in herpes simplex virus genomes and as β genes in cell genomes. Molecular and Cellular Biology 5:518–528
    [Google Scholar]
  41. Stow N. D., McMonagle E. C. 1983; Characterization of the TRS/IRS origin of DNA replication of herpes simplex virus type 1. Virology 130:427–438
    [Google Scholar]
  42. Swanstrom R. I., Wagner E. K. 1974; Regulation of synthesis of herpes simplex type 1 virus mRNA during productive infection. Virology 60:522–533
    [Google Scholar]
  43. Towbin H., Staehelin T., Gordon J. 1979; Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, U,. S,. A. 76:4350–4354
    [Google Scholar]
  44. Wagner E. K. 1985; Individual HSV transcripts. In The Herpesviruses vol 3 pp 45–104 Edited by Roizman B. New York & London: Plenum Press;
    [Google Scholar]
  45. Watson R. G., Colberg-Poley A. M., Marcus-Sekura C. J., Carter B. J., Enquist L. W. 1983; Characterization of the herpes simplex virus type 1 glycoprotein D mRNA and expression of this protein in Xenopus oocytes. Nucleic Acids Research 11:1507–1522
    [Google Scholar]
  46. Zweig M., Heilman C. J. Jr, Rabin H., Hampar B. 1980; Shared antigenic determinants between two distinct classes of proteins in cells infected with herpes simplex virus. Journal of Virology 35:644–652
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-67-5-871
Loading
/content/journal/jgv/10.1099/0022-1317-67-5-871
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