Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1987 Sep;61(9):2896–2901. doi: 10.1128/jvi.61.9.2896-2901.1987

Herpes simplex virus 1 protein kinase is encoded by open reading frame US3 which is not essential for virus growth in cell culture.

F C Purves, R M Longnecker, D P Leader, B Roizman
PMCID: PMC255814  PMID: 3039176

Abstract

Earlier reports have described a novel protein kinase in cells infected with herpes simplex or pseudorabies viruses. These novel enzymes were characterized by their acceptance of protamine as a substrate and by their differential chromatographic behavior in anion-exchange chromatography. We report that this activity was not present in extracts of uninfected cells or of cells infected with a mutant constructed so as to contain a deletion in the US3 open reading frame mapping in the small component of herpes simplex virus 1 DNA. The activity was present in extracts of cells infected with wild-type virus and with a recombinant in which the US3 open reading frame had been rescued. Our results are consistent with the observation reported earlier that the coding sequences predict an amino acid motif common to protein kinases and lead to the conclusion that the US3 open reading frame encodes a virus-specific protein kinase that is not required for virus growth in cells in culture.

Full text

PDF
2896

Images in this article

2899Image
on p.2899

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ackermann M., Longnecker R., Roizman B., Pereira L. Identification, properties, and gene location of a novel glycoprotein specified by herpes simplex virus 1. Virology. 1986 Apr 15;150(1):207–220. doi: 10.1016/0042-6822(86)90280-1. [DOI] [PubMed] [Google Scholar]
  2. Barker W. C., Dayhoff M. O. Viral src gene products are related to the catalytic chain of mammalian cAMP-dependent protein kinase. Proc Natl Acad Sci U S A. 1982 May;79(9):2836–2839. doi: 10.1073/pnas.79.9.2836. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blue W. T., Stobbs D. G. Isolation of a protein kinase induced by herpes simplex virus type 1. J Virol. 1981 Apr;38(1):383–388. doi: 10.1128/jvi.38.1.383-388.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cohen P. The role of protein phosphorylation in the hormonal control of enzyme activity. Eur J Biochem. 1985 Sep 16;151(3):439–448. doi: 10.1111/j.1432-1033.1985.tb09121.x. [DOI] [PubMed] [Google Scholar]
  5. Collett M. S., Erikson R. L. Protein kinase activity associated with the avian sarcoma virus src gene product. Proc Natl Acad Sci U S A. 1978 Apr;75(4):2021–2024. doi: 10.1073/pnas.75.4.2021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Courtneidge S. A., Smith A. E. Polyoma virus transforming protein associates with the product of the c-src cellular gene. Nature. 1983 Jun 2;303(5916):435–439. doi: 10.1038/303435a0. [DOI] [PubMed] [Google Scholar]
  7. Davison A. J., Scott J. E. The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986 Sep;67(Pt 9):1759–1816. doi: 10.1099/0022-1317-67-9-1759. [DOI] [PubMed] [Google Scholar]
  8. Ejercito P. M., Kieff E. D., Roizman B. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J Gen Virol. 1968 May;2(3):357–364. doi: 10.1099/0022-1317-2-3-357. [DOI] [PubMed] [Google Scholar]
  9. Flockhart D. A., Corbin J. D. Regulatory mechanisms in the control of protein kinases. CRC Crit Rev Biochem. 1982 Feb;12(2):133–186. doi: 10.3109/10409238209108705. [DOI] [PubMed] [Google Scholar]
  10. Hunter T., Cooper J. A. Protein-tyrosine kinases. Annu Rev Biochem. 1985;54:897–930. doi: 10.1146/annurev.bi.54.070185.004341. [DOI] [PubMed] [Google Scholar]
  11. Kamata T., Watanabe Y. Role for nucleocapsid protein phosphorylation in the transcription of influenza virus genome. Nature. 1977 Jun 2;267(5610):460–462. doi: 10.1038/267460a0. [DOI] [PubMed] [Google Scholar]
  12. Katan M., McGarvey M. J., Stevely W. S., Leader D. P. The phosphorylation of ribosomal protein S6 by protein kinases from cells infected with pseudorabies virus. Biochem J. 1986 Oct 1;239(1):205–211. doi: 10.1042/bj2390205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Katan M., Stevely W. S., Leader D. P. Partial purification and characterization of a new phosphoprotein kinase from cells infected with pseudorabies virus. Eur J Biochem. 1985 Oct 1;152(1):57–65. doi: 10.1111/j.1432-1033.1985.tb09163.x. [DOI] [PubMed] [Google Scholar]
  14. Kennedy I. M., Stevely W. S., Leader D. P. Phosphorylation of ribosomal proteins in hamster fibroblasts infected with pseudorabies virus or herpes simplex virus. J Virol. 1981 Aug;39(2):359–366. doi: 10.1128/jvi.39.2.359-366.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kingsford L., Emerson S. U. Transcriptional activities of different phosphorylated species of NS protein purified from vesicular stomatitis virions and cytoplasm of infected cells. J Virol. 1980 Mar;33(3):1097–1105. doi: 10.1128/jvi.33.3.1097-1105.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Krebs E. G. Historical perspectives on protein phosphorylation and a classification system for protein kinases. Philos Trans R Soc Lond B Biol Sci. 1983 Jul 5;302(1108):3–11. doi: 10.1098/rstb.1983.0033. [DOI] [PubMed] [Google Scholar]
  17. Krebs E. G. The phosphorylation of proteins: a major mechanism for biological regulation. Fourteenth Sir Frederick Gowland Hopkins memorial lecture. Biochem Soc Trans. 1985 Oct;13(5):813–820. doi: 10.1042/bst0130813. [DOI] [PubMed] [Google Scholar]
  18. Lemaster S., Roizman B. Herpes simplex virus phosphoproteins. II. Characterization of the virion protein kinase and of the polypeptides phosphorylated in the virion. J Virol. 1980 Sep;35(3):798–811. doi: 10.1128/jvi.35.3.798-811.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Longnecker R., Roizman B. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science. 1987 May 1;236(4801):573–576. doi: 10.1126/science.3033823. [DOI] [PubMed] [Google Scholar]
  20. Longnecker R., Roizman B. Generation of an inverting herpes simplex virus 1 mutant lacking the L-S junction a sequences, an origin of DNA synthesis, and several genes including those specifying glycoprotein E and the alpha 47 gene. J Virol. 1986 May;58(2):583–591. doi: 10.1128/jvi.58.2.583-591.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Marsden H. S., Stow N. D., Preston V. G., Timbury M. C., Wilkie N. M. Physical mapping of herpes simplex virus-induced polypeptides. J Virol. 1978 Nov;28(2):624–642. doi: 10.1128/jvi.28.2.624-642.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. McGeoch D. J., Davison A. J. Alphaherpesviruses possess a gene homologous to the protein kinase gene family of eukaryotes and retroviruses. Nucleic Acids Res. 1986 Feb 25;14(4):1765–1777. doi: 10.1093/nar/14.4.1765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. McGeoch D. J., Dolan A., Donald S., Rixon F. J. Sequence determination and genetic content of the short unique region in the genome of herpes simplex virus type 1. J Mol Biol. 1985 Jan 5;181(1):1–13. doi: 10.1016/0022-2836(85)90320-1. [DOI] [PubMed] [Google Scholar]
  24. Pereira L., Wolff M. H., Fenwick M., Roizman B. Regulation of herpesvirus macromolecular synthesis. V. Properties of alpha polypeptides made in HSV-1 and HSV-2 infected cells. Virology. 1977 Apr;77(2):733–749. doi: 10.1016/0042-6822(77)90495-0. [DOI] [PubMed] [Google Scholar]
  25. Post L. E., Conley A. J., Mocarski E. S., Roizman B. Cloning of reiterated and nonreiterated herpes simplex virus 1 sequences as BamHI fragments. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4201–4205. doi: 10.1073/pnas.77.7.4201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Post L. E., Roizman B. A generalized technique for deletion of specific genes in large genomes: alpha gene 22 of herpes simplex virus 1 is not essential for growth. Cell. 1981 Jul;25(1):227–232. doi: 10.1016/0092-8674(81)90247-6. [DOI] [PubMed] [Google Scholar]
  27. Purves F. C., Deana A. D., Marchiori F., Leader D. P., Pinna L. A. The substrate specificity of the protein kinase induced in cells infected with herpesviruses: studies with synthetic substrates [corrected] indicate structural requirements distinct from other protein kinases. Biochim Biophys Acta. 1986 Nov 28;889(2):208–215. doi: 10.1016/0167-4889(86)90106-0. [DOI] [PubMed] [Google Scholar]
  28. Purves F. C., Katan M., Stevely W. S., Leader D. P. Characteristics of the induction of a new protein kinase in cells infected with herpesviruses. J Gen Virol. 1986 Jun;67(Pt 6):1049–1057. doi: 10.1099/0022-1317-67-6-1049. [DOI] [PubMed] [Google Scholar]
  29. Sen A., Sherr C. J., Todaro G. J. Phosphorylation of murine type C viral p12 proteins regulates their extent of binding to the homologous viral RNA. Cell. 1977 Mar;10(3):489–496. doi: 10.1016/0092-8674(77)90036-8. [DOI] [PubMed] [Google Scholar]
  30. Stevely W. S., Katan M., Stirling V., Smith G., Leader D. P. Protein kinase activities associated with the virions of pseudorabies and herpes simplex virus. J Gen Virol. 1985 Apr;66(Pt 4):661–673. doi: 10.1099/0022-1317-66-4-661. [DOI] [PubMed] [Google Scholar]
  31. Takio K., Wade R. D., Smith S. B., Krebs E. G., Walsh K. A., Titani K. Guanosine cyclic 3',5'-phosphate dependent protein kinase, a chimeric protein homologous with two separate protein families. Biochemistry. 1984 Aug 28;23(18):4207–4218. doi: 10.1021/bi00313a030. [DOI] [PubMed] [Google Scholar]
  32. Walboomers J. M., Schegget J. T. A new method for the isolation of herpes simplex virus type 2 DNA. Virology. 1976 Oct 1;74(1):256–258. doi: 10.1016/0042-6822(76)90151-3. [DOI] [PubMed] [Google Scholar]
  33. Walser A., Deppert W. The kinase activity of SV40 large T antigen is mediated by a cellular kinase. EMBO J. 1986 May;5(5):883–889. doi: 10.1002/j.1460-2075.1986.tb04299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wilcox K. W., Kohn A., Sklyanskaya E., Roizman B. Herpes simplex virus phosphoproteins. I. Phosphate cycles on and off some viral polypeptides and can alter their affinity for DNA. J Virol. 1980 Jan;33(1):167–182. doi: 10.1128/jvi.33.1.167-182.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES