1887

Abstract

Translation elongation factor 1δ (EF-1δ) is hyperphosphorylated in various mammalian cells infected with alpha-, beta- and gammaherpesviruses and EF-1δ modification is mediated by viral protein kinases, including UL13 of herpes simplex virus type 1 and UL97 of human cytomegalovirus. In this study, the following is reported. (i) BGLF4 encoded by the prototype gammaherpesvirus Epstein–Barr virus was purified as a fusion protein that was labelled with [γ-P]ATP and labelling was eliminated by phosphatase. (ii) The ratio of the hyperphosphorylated form of human EF-1δ was increased both in Sf9 cells after infection with baculoviruses expressing GST–BGLF4 fusion proteins and in COS-7 cells after transfection with a BGLF4 expression plasmid. These results indicate that purified BGLF4 possesses protein kinase activity and mediates EF-1δ hyperphosphorylation. These data also support the hypothesis that the protein kinases that are conserved by herpesviruses universally mediate EF-1δ modification in mammalian cells.

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2001-06-01
2024-04-27
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References

  1. Cannon J. S., Hamzeh F., Moore S., Nicholas J., Ambinder R. F. 1999; Human herpesvirus 8-encoded thymidine kinase and phosphotransferase homologues confer sensitivity to ganciclovir. Journal of Virology 73:4786–4793
    [Google Scholar]
  2. Chee M. S., Lawrence G. L., Barrell B. G. 1989; Alpha-, beta- and gammaherpesviruses encode a putative phosphotransferase. Journal of General Virology 70:1151–1160
    [Google Scholar]
  3. Chen M. R., Chang S. J., Huang H., Chen J. Y. 2000; A protein kinase activity associated with Epstein–Barr virus BGLF4 phosphorylates the viral early antigen EA-D in vitro . Journal of Virology 74:3093–3104
    [Google Scholar]
  4. Das T., Mathur M., Gupta A. K., Janssen G. M., Banerjee A. K. 1998; RNA polymerase of vesicular stomatitis virus specifically associates with translation elongation factor-1 alphabetagamma for its activity. Proceedings of the National Academy of Sciences, USA 95:1449–1454
    [Google Scholar]
  5. Edelman A. M., Blumenthal D. K., Krebs E. G. 1987; Protein serine/threonine kinases. Annual Review of Biochemistry 56:567–613
    [Google Scholar]
  6. Everett R. D., Preston C. M., Stow N. D. 1991; Functional and genetic analysis of the role of Vmw 110 in herpes simplex virus replication. In Herpesvirus Transcription and its Replication pp 50–76 Edited by Wagner E. K. Boston, MA: CRC Press;
    [Google Scholar]
  7. He Z., He Y.-S., Kim Y., Chu L., Ohmstede C., Biron K. K., Coen D. M. 1997; The human cytomegalovirus UL97 protein is a protein kinase that autophosphorylates on serines and threonine. Journal of Virology 71:405–411
    [Google Scholar]
  8. Heineman T. C., Cohen J. I. 1995; The varicella-zoster virus (VZV) open reading frame 47 (ORF47) protein kinase is dispensable for viral replication and is not required for phosphorylation of ORF63 protein, the VZV homolog of herpes simplex virus ICP22. Journal of Virology 69:7367–7370
    [Google Scholar]
  9. Horimoto T., Limcumpao J. A., Xuan X., Ono M., Maeda K., Kawaguchi Y., Kai C., Takahashi E., Mikami T. 1992; Heterogeneity of feline herpesvirus type 1 strains. Archives of Virology 126:283–292
    [Google Scholar]
  10. Kawaguchi Y., Bruni R., Roizman B. 1997a; Interaction of herpesvirus simplex virus 1 alpha regulatory protein ICP0 with elongation factor 1delta: ICP0 affects translational machinery. Journal of Virology 71:1019–1024
    [Google Scholar]
  11. Kawaguchi Y., Van Sant C., Roizman B. 1997b; Herpesvirus simplex virus 1α regulatory protein ICP0 interacts with and stabilized the cell cycle regulator cyclin D3. Journal of Virology 71:7328–7336
    [Google Scholar]
  12. Kawaguchi Y., Van Sant C., Roizman B. 1998; Eukaryotic elongation factor 1δ is hyperphosphorylated by the protein kinase encoded by the UL13 gene of herpes simplex virus 1. Journal of Virology 72:1731–1736
    [Google Scholar]
  13. Kawaguchi Y., Matsumura T., Roizman B., Hirai K. 1999; Cellular elongation factor 1δ is modified in cells infected with representative alpha-, beta-, or gammaherpesvirus. Journal of Virology 73:4456–4460
    [Google Scholar]
  14. Kawaguchi Y., Nakajima K., Igarashi M., Morita T., Tanaka M., Suzuki M., Yokoyama A., Matsuda G., Kato K., Hirai K. 2000; Interaction of Epstein–Barr virus nuclear antigen leader protein (EBNA-LP) with HS1-associated protein X-1: implication of cytoplasmic function of EBNA-LP. Journal of Virology 74:10104–10111
    [Google Scholar]
  15. Knipe D. K. 1996; Virus–host cell interactions. In Fields Virology pp 273–299 Edited by Fields B. N., Knipe D. M., Howley P. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  16. Litter E., Stuart A. D., Chee M. S. 1992; Human cytomegalovirus UL97 open reading frame encodes a protein that phosphorylates the antiviral nucleoside analogue ganciclovir. Nature 358:160–162
    [Google Scholar]
  17. Merrick W. C. 1992; Mechanism and regulation of eukaryotic protein synthesis. Microbiological Reviews 56:291–315
    [Google Scholar]
  18. Miller L. K. 1996; Insect viruses. In Fields Virology pp 533–556 Edited by Fields B. N., Knipe D. M., Howley P. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  19. Moffat J. F., Zerboni L., Sommer M. H., Heineman T. C., Cohen J. I., Kaneshima H., Arvin A. M. 1998; The ORF47 and ORF66 putative protein kinases of varicella-zoster virus determine tropism for human T cells and skin in the SCID-hu mouse. Proceedings of the National Academy of Sciences, USA 95:11969–11974
    [Google Scholar]
  20. Morales J., Corminer P., Mulner-Lorillon O., Poulhe R., Belle R. 1992; Molecular cloning of a new guanine-nucleotide exchange protein. Nucleic Acids Research 20:4091
    [Google Scholar]
  21. Ng T. I., Keenan L., Kinchington P. R., Grose C. 1994; Phosphorylation of varicella-zoster virus open reading frame (ORF) 62 regulatory product by viral ORF47-associated protein kinase. Journal of Virology 68:1350–1359
    [Google Scholar]
  22. Ng T. I., Talarico C., Burnette T. C., Biron K., Roizman B. 1996; Partial substitution of the functions of the herpes simplex virus 1 UL13 gene by the human cytomegalovirus UL97 gene. Virology 225:347–358
    [Google Scholar]
  23. Ng T. I., Ogle W. O., Roizman B. 1998; UL13 protein kinase of herpes simplex virus 1 complexes with glycoprotein E and mediates the phosphorylation of the viral Fc receptor: glycoproteins E and I. Virology 241:37–48
    [Google Scholar]
  24. Ogle W. O., Ng T. I., Carter K. L., Roizman B. 1997; The UL13 protein kinase and the infected cell type are determinants of posttranslational modification of ICP0. Virology 235:406–413
    [Google Scholar]
  25. Prichard M. N., Gao N., Jairath S., Mulamba G., Krosky P., Coen D. M., Parker B. O., Pari G. S. 1999; A recombinant human cytomegalovirus with a large deletion in UL97 has a severe replication deficiency. Journal of Virology 73:5663–5670
    [Google Scholar]
  26. Purves F. C., Roizman B. 1992; The UL13 gene of herpes simplex virus 1 encodes the functions for posttranslational processing associated with phosphorylation of the regulatory protein α22. Proceedings of the National Academy of Sciences, USA 89:7310–7314
    [Google Scholar]
  27. Purves F. C., Ogle W. O., Roizman B. 1993; Processing of the herpes simplex virus regulatory protein α22 mediated by the UL13 protein kinase determines the accumulation of a subset of α and γ mRNAs and proteins in infected cells. Proceedings of the National Academy of Sciences, USA 90:6701–6705
    [Google Scholar]
  28. Riis B., Rattan S. I. S., Clark B. F. C., Merrick W. C. 1990; Eukaryotic protein elongation factors. Trends in Biochemical Sciences 15:420–424
    [Google Scholar]
  29. Roizman B., Sears A. E. 1996; The replication of the herpes simplex viruses. In Fields Virology pp 2231–2295 Edited by Fields B. N., Knipe D. M., Howley P. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  30. Smith R. F., Smith T. F. 1989; Identification of new protein kinase-related genes in three herpesviruses, herpes simplex virus, Varicella-Zoster virus, and Epstein–Barr virus. Journal of Virology 63:450–455
    [Google Scholar]
  31. Sullivan V., Talarico C. L., Stanat S. C., Davis M., Coen D. M., Biron K. K. 1992; A protein kinase homologue controls phosphorylation of ganciclovir in human cytomegalovirus-infected cells. Nature 358:162–164
    [Google Scholar]
  32. Takebe Y., Seiki M., Fujisawa J., Hoy P., Yokota K., Arai K., Yoshida M., Arai N. 1988; SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat. Molecular and Cellular Biology 8:466–472
    [Google Scholar]
  33. Van Damme H. T. F., Amons R., Karssie R., Timmers C. J., Janssen G. M. C., Moller W. 1990; Elongation factor EF-1β of artemia: localization of functional sites and homology to elongation factor 1δ. Biochimica et Biophysica Acta 1050:241–247
    [Google Scholar]
  34. Xiao H., Neuveut C., Benkirane M., Jeang K. T. 1998; Interaction of the second coding exon of Tat with human EF-1 delta delineates a mechanism for HIV-1-mediated shut-off of host mRNA translation. Biochemical and Biophysical Research Communications 244:384–389
    [Google Scholar]
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