1887

Abstract

All herpesviruses have a post-transcriptional regulatory protein that prevents precursor mRNA splicing and leads to the shutting off of host protein synthesis. The ICP27 protein of herpes simplex virus 1 (HSV-1) is the prototype of these proteins. Marek’s disease virus (MDV-1), an alphaherpesvirus that induces lymphoma in birds, also has an ICP27 protein that is produced in lytic MDV-1-infected cells. We characterized this protein. We demonstrated ICP27 production in latently infected MSB-1 cells, but only on MDV-1 reactivation. ICP27 was found predominantly in specific structures within the nucleus. The ICP27 of MDV-1 colocalized and interacted with SR proteins. We demonstrated inhibitory effects of MDV-1 ICP27 on the splicing of both the viral and cellular (telomerase reverse transcriptase) genes. Thus, the ICP27 of MDV-1 plays a similar role to the ICP27 of HSV-1 and may be involved in MDV-1 replication and the development of Marek’s disease.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.028969-0
2011-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/6/1273.html?itemId=/content/journal/jgv/10.1099/vir.0.028969-0&mimeType=html&fmt=ahah

References

  1. Akiyama Y., Kato S. 1974; Two cell lines from lymphomas of Marek’s disease. Biken J 17:105–116[PubMed]
    [Google Scholar]
  2. Amor S., Remy S., Dambrine G., Le Vern Y., Rasschaert D., Laurent S. 2010; Alternative splicing and nonsense-mediated decay regulate telomerase reverse transcriptase (TERT) expression during virus-induced lymphomagenesis in vivo. BMC Cancer 10:571 [View Article][PubMed]
    [Google Scholar]
  3. Debba-Pavard M., Ait-Lounis A., Soubieux D., Rasschaert D., Dambrine G. 2008; Vaccination against Marek’s disease reduces telomerase activity and viral gene transcription in peripheral blood leukocytes from challenged chickens. Vaccine 26:4904–4912 [View Article][PubMed]
    [Google Scholar]
  4. Escudero-Paunetto L., Li L., Hernandez F. P., Sandri-Goldin R. M. 2010; SR proteins SRp20 and 9G8 contribute to efficient export of herpes simplex virus 1 mRNAs. Virology 401:155–164 [View Article][PubMed]
    [Google Scholar]
  5. Hardwicke M. A., Sandri-Goldin R. M. 1994; The herpes simplex virus regulatory protein ICP27 contributes to the decrease in cellular mRNA levels during infection. J Virol 68:4797–4810[PubMed]
    [Google Scholar]
  6. Hardy W. R., Sandri-Goldin R. M. 1994; Herpes simplex virus inhibits host cell splicing, and regulatory protein ICP27 is required for this effect. J Virol 68:7790–7799[PubMed]
    [Google Scholar]
  7. Himly M., Foster D. N., Bottoli I., Iacovoni J. S., Vogt P. K. 1998; The DF-1 chicken fibroblast cell line: transformation induced by diverse oncogenes and cell death resulting from infection by avian leukosis viruses. Virology 248:295–304 [View Article][PubMed]
    [Google Scholar]
  8. Laurent S., Vautherot J. F., Le Gall G., Madelaine M. F., Rasschaert D. 1997; Structural, antigenic and immunogenic relationships between European brown hare syndrome virus and rabbit haemorrhagic disease virus. J Gen Virol 78:2803–2811[PubMed]
    [Google Scholar]
  9. Laurent A. M., Madjar J. J., Greco A. 1998; Translational control of viral and host protein synthesis during the course of herpes simplex virus type 1 infection: evidence that initiation of translation is the limiting step. J Gen Virol 79:2765–2775[PubMed]
    [Google Scholar]
  10. Long J. C., Caceres J. F. 2009; The SR protein family of splicing factors: master regulators of gene expression. Biochem J 417:15–27 [View Article][PubMed]
    [Google Scholar]
  11. Majerciak V., Yamanegi K., Allemand E., Kruhlak M., Krainer A. R., Zheng Z. M. 2008; Kaposi’s sarcoma-associated herpesvirus ORF57 functions as a viral splicing factor and promotes expression of intron-containing viral lytic genes in spliceosome-mediated RNA splicing. J Virol 82:2792–2801 [View Article][PubMed]
    [Google Scholar]
  12. Malik P., Schirmer E. C. 2006; The Kaposi’s sarcoma-associated herpesvirus ORF57 protein: a pleurotropic regulator of gene expression. Biochem Soc Trans 34:705–710 [View Article][PubMed]
    [Google Scholar]
  13. Mettenleiter T. C., Klupp B. G., Granzow H. 2009; Herpesvirus assembly: an update. Virus Res 143:222–234 [View Article][PubMed]
    [Google Scholar]
  14. Moriuchi H., Moriuchi M., Smith H. A., Cohen J. I. 1994; Varicella-zoster virus open reading frame 4 protein is functionally distinct from and does not complement its herpes simplex virus type 1 homolog, ICP27. J Virol 68:1987–1992[PubMed]
    [Google Scholar]
  15. Neugebauer K. M., Stolk J. A., Roth M. B. 1995; A conserved epitope on a subset of SR proteins defines a larger family of pre-mRNA splicing factors. J Cell Biol 129:899–908 [View Article][PubMed]
    [Google Scholar]
  16. Nojima T., Oshiro-Ideue T., Nakanoya H., Kawamura H., Morimoto T., Kawaguchi Y., Kataoka N., Hagiwara M. 2009; Herpesvirus protein ICP27 switches PML isoform by altering mRNA splicing. Nucleic Acids Res 37:6515–6527 [View Article][PubMed]
    [Google Scholar]
  17. Osterrieder N., Kamil J. P., Schumacher D., Tischer B. K., Trapp S. 2006; Marek’s disease virus: from miasma to model. Nat Rev Microbiol 4:283–294 [View Article][PubMed]
    [Google Scholar]
  18. Ote I., Piette J., Sadzot-Delvaux C. 2010; The varicella-zoster virus IE4 protein: a conserved member of the herpesviral mRNA export factors family and a potential alternative target in antiherpetic therapies. Biochem Pharmacol 80:1973–1980 [View Article][PubMed]
    [Google Scholar]
  19. Parcells M. S., Lin S. F., Dienglewicz R. L., Majerciak V., Robinson D. R., Chen H. C., Wu Z., Dubyak G. R., Brunovskis P. et al. 2001; Marek’s disease virus (MDV) encodes an interleukin-8 homolog (vIL-8): characterization of the vIL-8 protein and a vIL-8 deletion mutant MDV. J Virol 75:5159–5173 [View Article][PubMed]
    [Google Scholar]
  20. Petherbridge L., Brown A. C., Baigent S. J., Howes K., Sacco M. A., Osterrieder N., Nair V. K. 2004; Oncogenicity of virulent Marek’s disease virus cloned as bacterial artificial chromosomes. J Virol 78:13376–13380 [View Article][PubMed]
    [Google Scholar]
  21. Ren D., Lee L. F., Coussens P. M. 1994; Identification and characterization of Marek’s disease virus genes homologous to ICP27 and glycoprotein K of herpes simplex virus-1. Virology 204:242–250 [View Article][PubMed]
    [Google Scholar]
  22. Ruvolo V., Sun L., Howard K., Sung S., Delecluse H. J., Hammerschmidt W., Swaminathan S. 2004; Functional analysis of Epstein-Barr virus SM protein: identification of amino acids essential for structure, transactivation, splicing inhibition, and virion production. J Virol 78:340–352 [View Article][PubMed]
    [Google Scholar]
  23. Sandri-Goldin R. M., Hibbard M. K., Hardwicke M. A. 1995; The C-terminal repressor region of herpes simplex virus type 1 ICP27 is required for the redistribution of small nuclear ribonucleoprotein particles and splicing factor SC35; however, these alterations are not sufficient to inhibit host cell splicing. J Virol 69:6063–6076[PubMed]
    [Google Scholar]
  24. Sciabica K. S., Dai Q. J., Sandri-Goldin R. M. 2003; ICP27 interacts with SRPK1 to mediate HSV splicing inhibition by altering SR protein phosphorylation. EMBO J 22:1608–1619 [View Article][PubMed]
    [Google Scholar]
  25. Shkreli M., Dambrine G., Soubieux D., Kut E., Rasschaert D. 2007; Involvement of the oncoprotein c-Myc in viral telomerase RNA gene regulation during Marek’s disease virus-induced lymphomagenesis. J Virol 81:4848–4857 [View Article][PubMed]
    [Google Scholar]
  26. Smith R. W., Malik P., Clements J. B. 2005; The herpes simplex virus ICP27 protein: a multifunctional post-transcriptional regulator of gene expression. Biochem Soc Trans 33:499–501 [View Article][PubMed]
    [Google Scholar]
  27. Stik G., Laurent S., Coupeau D., Coutaud B., Dambrine G., Rasschaert D., Muylkens B. 2010; A p53-dependent promoter associated with polymorphic tandem repeats controls the expression of a viral transcript encoding clustered microRNAs. RNA 16:2263–2276 [View Article][PubMed]
    [Google Scholar]
  28. Zhi Y., Sandri-Goldin R. M. 1999; Analysis of the phosphorylation sites of herpes simplex virus type 1 regulatory protein ICP27. J Virol 73:3246–3257[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.028969-0
Loading
/content/journal/jgv/10.1099/vir.0.028969-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF
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