Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1989 Sep;63(9):3912–3918. doi: 10.1128/jvi.63.9.3912-3918.1989

Phosphorylation of varicella-zoster virus glycoprotein gpI by mammalian casein kinase II and casein kinase I.

C Grose 1, W Jackson 1, J A Traugh 1
PMCID: PMC250987  PMID: 2548005

Abstract

Varicella-zoster virus (VZV) glycoprotein gpI is the predominant viral glycoprotein within the plasma membranes of infected cells. This viral glycoprotein is phosphorylated on its polypeptide backbone during biosynthesis. In this report, we investigated the protein kinases which participate in the phosphorylation events. Under in vivo conditions, VZV gpI was phosphorylated on its serine and threonine residues by protein kinases present within lysates of either VZV-infected or uninfected cells. Because this activity was diminished by heparin, a known inhibitor of casein kinase II, isolated gpI was incubated with purified casein kinase II and shown to be phosphorylated in an in vitro assay containing [gamma-32P]ATP. The same glycoprotein was phosphorylated when [32P]GTP was substituted for [32P]ATP in the protein kinase assay. We also tested whether VZV gpI was phosphorylated by two other ubiquitous mammalian protein kinases--casein kinase I and cyclic AMP-dependent kinase--and found that only casein kinase I modified gpI. When the predicted 623-amino-acid sequence of gpI was examined, two phosphorylation sites known to be optimal for casein kinase II were observed. Immediately upstream from each of the casein kinase II sites was a potential casein kinase I phosphorylation site. In summary, this study showed that VZV gpI was phosphorylated by each of two mammalian protein kinases (casein kinase I and casein kinase II) and that potential serine-threonine phosphorylation sites for each of these two kinases were present in the viral glycoprotein.

Full text

PDF
3912

Images in this article

3914Image
on p.3914
3914Image
on p.3914
3914Image
on p.3914
3915Image
on p.3915
3915Image
on p.3915
3916Image
on p.3916
3916Image
on p.3916
3916Image
on p.3916
3917Image
on p.3917

Selected References

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

  1. 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]
  2. Dahmus M. E. Purification and properties of calf thymus casein kinases I and II. J Biol Chem. 1981 Apr 10;256(7):3319–3325. [PubMed] [Google Scholar]
  3. 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]
  4. Delpech M., Levy-Favatier F., Kruh J. Separation of nuclear cAMP independent protein kinases NI and NII from their chromosomal protein substrates and enzyme inhibitors by the use of a casein-phosvitin-Sepharose column. Anal Biochem. 1986 Jan;152(1):100–106. doi: 10.1016/0003-2697(86)90126-0. [DOI] [PubMed] [Google Scholar]
  5. Edelman A. M., Blumenthal D. K., Krebs E. G. Protein serine/threonine kinases. Annu Rev Biochem. 1987;56:567–613. doi: 10.1146/annurev.bi.56.070187.003031. [DOI] [PubMed] [Google Scholar]
  6. Edson C. M., Hosler B. A., Waters D. J. Varicella-zoster virus gpI and herpes simplex virus gE: phosphorylation and Fc binding. Virology. 1987 Dec;161(2):599–602. doi: 10.1016/0042-6822(87)90157-7. [DOI] [PubMed] [Google Scholar]
  7. Frame M. C., Purves F. C., McGeoch D. J., Marsden H. S., Leader D. P. Identification of the herpes simplex virus protein kinase as the product of viral gene US3. J Gen Virol. 1987 Oct;68(Pt 10):2699–2704. doi: 10.1099/0022-1317-68-10-2699. [DOI] [PubMed] [Google Scholar]
  8. Gravell M., Cromeans T. L. Viron-associated protein kinase and its involvement in nongenetic reactivation of frog polyhedral cytoplasmic deoxyribovirus. Virology. 1972 Jun;48(3):847–851. doi: 10.1016/0042-6822(72)90167-5. [DOI] [PubMed] [Google Scholar]
  9. Grose C. The synthesis of glycoproteins in human melanoma cells infected with varicella-zoster virus. Virology. 1980 Feb;101(1):1–9. doi: 10.1016/0042-6822(80)90478-x. [DOI] [PubMed] [Google Scholar]
  10. Grässer F. A., Scheidtmann K. H., Tuazon P. T., Traugh J. A., Walter G. In vitro phosphorylation of SV40 large T antigen. Virology. 1988 Jul;165(1):13–22. doi: 10.1016/0042-6822(88)90653-8. [DOI] [PubMed] [Google Scholar]
  11. Hathaway G. M., Lubben T. H., Traugh J. A. Inhibition of casein kinase II by heparin. J Biol Chem. 1980 Sep 10;255(17):8038–8041. [PubMed] [Google Scholar]
  12. Hathaway G. M., Traugh J. A. Casein kinase II. Methods Enzymol. 1983;99:317–331. doi: 10.1016/0076-6879(83)99067-5. [DOI] [PubMed] [Google Scholar]
  13. Hathaway G. M., Traugh J. A. Cyclic nucleotide-independent protein kinases from rabbit reticulocytes. Purification of casein kinases. J Biol Chem. 1979 Feb 10;254(3):762–768. [PubMed] [Google Scholar]
  14. 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]
  15. Jakubowicz T., Leader D. P. A major phosphoprotein of cells infected with pseudorabies virus is phosphorylated by cellular casein kinase II. J Gen Virol. 1987 Apr;68(Pt 4):1159–1163. doi: 10.1099/0022-1317-68-4-1159. [DOI] [PubMed] [Google Scholar]
  16. Jones F., Grose C. Role of cytoplasmic vacuoles in varicella-zoster virus glycoprotein trafficking and virion envelopment. J Virol. 1988 Aug;62(8):2701–2711. doi: 10.1128/jvi.62.8.2701-2711.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Krebs E. G., Eisenman R. N., Kuenzel E. A., Litchfield D. W., Lozeman F. J., Lüscher B., Sommercorn J. Casein kinase II as a potentially important enzyme concerned with signal transduction. Cold Spring Harb Symp Quant Biol. 1988;53(Pt 1):77–84. doi: 10.1101/sqb.1988.053.01.012. [DOI] [PubMed] [Google Scholar]
  19. Leader D. P., Katan M. Viral aspects of protein phosphorylation. J Gen Virol. 1988 Jul;69(Pt 7):1441–1464. doi: 10.1099/0022-1317-69-7-1441. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. 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]
  22. Montalvo E. A., Grose C. Varicella zoster virus glycoprotein gpI is selectively phosphorylated by a virus-induced protein kinase. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8967–8971. doi: 10.1073/pnas.83.23.8967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Montalvo E. A., Parmley R. T., Grose C. Structural analysis of the varicella-zoster virus gp98-gp62 complex: posttranslational addition of N-linked and O-linked oligosaccharide moieties. J Virol. 1985 Mar;53(3):761–770. doi: 10.1128/jvi.53.3.761-770.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Randall C. C., Rogers H. W., Downer D. N., Gentry G. A. Protein kinase activity in equine herpesvirus. J Virol. 1972 Feb;9(2):216–222. doi: 10.1128/jvi.9.2.216-222.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rubenstein A. S., Gravell M., Darlington R. Protein kinase in enveloped herpes simplex virions. Virology. 1972 Oct;50(1):287–290. doi: 10.1016/0042-6822(72)90374-1. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Strand M., August J. T. Protein kinase and phosphate acceptor proteins in Rauscher murine leukaemia virus. Nat New Biol. 1971 Sep 29;233(39):137–140. doi: 10.1038/newbio233137a0. [DOI] [PubMed] [Google Scholar]

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

RESOURCES