1887

Abstract

T-lymphocytes are central targets of Marek's disease, a major chicken disease induced by the oncogenic alphaherpesvirus Marek's disease virus (MDV). T-lymphocyte infection is also associated with immunosuppression and virus latency. To decipher viral morphogenesis in T-lymphocytes, we used the recombinant vRB-1B 47EGFP marker virus to generate a new lymphoblastoid cell line, 3867K, that exhibited typical properties of other MDV-transformed chicken cell lines in term of cell markers, reactivation rate and infectivity. Examination of reactivating EGFP-positive 3867K cells by transmission electron microscopy revealed the presence of most types of herpesvirus particles inside the cells but no extracellular ones. Quantification of virion types indicated only 5 % cytoplasmic particles, with 0.5 % being mature. This study demonstrated that MDV morphogenesis is complete upon reactivation in T-lymphocytes, albeit with poor efficiency, with a defect in the exit of virions from the nucleus and secondary envelopment, as occurs in infected fibroblasts.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000354
2016-02-01
2019-10-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/480.html?itemId=/content/journal/jgv/10.1099/jgv.0.000354&mimeType=html&fmt=ahah

References

  1. Akiyama Y., Kato S.. ( 1974a;). Scanning electron microscopy of lymphoid cell lines and lymphocytes from thymus, bursa and blood of chickens. Biken J 17: 193–197 [PubMed].
    [Google Scholar]
  2. Akiyama Y., Kato S.. ( 1974b;). Two cell lines from lymphomas of Marek's disease. Biken J 17: 105–116 [PubMed].
    [Google Scholar]
  3. Blondeau C., Chbab N., Beaumont C., Courvoisier K., Osterrieder N., Vautherot J.-F., Denesvre C.. ( 2007;). A full UL13 open reading frame in Marek's disease virus (MDV) is dispensable for tumor formation and feather follicle tropism and cannot restore horizontal virus transmission of rRB-1B in vivo. Vet Res 38: 419–433 [CrossRef] [PubMed].
    [Google Scholar]
  4. Calnek B. W.. ( 2001;). Pathogenesis of Marek's disease virus infection. Curr Top Microbiol Immunol 255: 25–55 [PubMed].
    [Google Scholar]
  5. Denesvre C.. ( 2013;). Marek's disease virus morphogenesis. Avian Dis 57: 340–350 [CrossRef] [PubMed].
    [Google Scholar]
  6. Denesvre C., Blondeau C., Lemesle M., Le Vern Y., Vautherot D., Roingeard P., Vautherot J. F.. ( 2007;). Morphogenesis of a highly replicative EGFPVP22 recombinant Marek's disease virus in cell culture. J Virol 81: 12348–12359 [CrossRef] [PubMed].
    [Google Scholar]
  7. Deruelle M. J., Favoreel H. W.. ( 2011;). Keep it in the subfamily: the conserved alphaherpesvirus US3 protein kinase. J Gen Virol 92: 18–30 [CrossRef] [PubMed].
    [Google Scholar]
  8. Dienglewicz R. L., Parcells M. S.. ( 1999;). Establishment of a lymphoblastoid cell line using a mutant MDV containing a green fluorescent protein expression cassette. Acta Virol 43: 106–112 [PubMed].
    [Google Scholar]
  9. Frazier J. A., Powell P. C.. ( 1975;). The ultrastructure of lymphoblastoid cell lines from Marek's disease lymphomata. Br J Cancer 31: 7–14 [CrossRef] [PubMed].
    [Google Scholar]
  10. Jarosinski K. W., Arndt S., Kaufer B. B., Osterrieder N.. ( 2012;). Fluorescently tagged pUL47 of Marek's disease virus reveals differential tissue expression of the tegument protein in vivo. J Virol 86: 2428–2436 [CrossRef] [PubMed].
    [Google Scholar]
  11. Johnson D. C., Baines J. D.. ( 2011;). Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9: 382–394 [CrossRef] [PubMed].
    [Google Scholar]
  12. Klupp B. G., Granzow H., Fuchs W., Keil G. M., Finke S., Mettenleiter T. C.. ( 2007;). Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci U S A 104: 7241–7246 [CrossRef] [PubMed].
    [Google Scholar]
  13. Liu Z., Kato A., Shindo K., Noda T., Sagara H., Kawaoka Y., Arii J., Kawaguchi Y.. ( 2014;). Herpes simplex virus 1 UL47 interacts with viral nuclear egress factors UL31, UL34, and Us3 and regulates viral nuclear egress. J Virol 88: 4657–4667 [CrossRef] [PubMed].
    [Google Scholar]
  14. Mattila P. K., Lappalainen P.. ( 2008;). Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9: 446–454 [CrossRef] [PubMed].
    [Google Scholar]
  15. Mettenleiter T. C.. ( 2002;). Herpesvirus assembly and egress. J Virol 76: 1537–1547 [CrossRef] [PubMed].
    [Google Scholar]
  16. Mettenleiter T. C., Saalmüller A., Weiland F.. ( 1993;). Pseudorabies virus protein homologous to herpes simplex virus type 1 ICP18.5 is necessary for capsid maturation. J Virol 67: 1236–1245 [PubMed].
    [Google Scholar]
  17. Mettenleiter T. C., Klupp B. G., Granzow H.. ( 2009;). Herpesvirus assembly: an update. Virus Res 143: 222–234 [CrossRef] [PubMed].
    [Google Scholar]
  18. Mettenleiter T. C., Müller F., Granzow H., Klupp B. G.. ( 2013;). The way out: what we know and do not know about herpesvirus nuclear egress. Cell Microbiol 15: 170–178 [CrossRef] [PubMed].
    [Google Scholar]
  19. Nazerian K.. ( 1987;). An updated list of avian cell lines and transplantable tumours. Avian Pathol 16: 527–544 [CrossRef] [PubMed].
    [Google Scholar]
  20. Nazerian K., Witter R. L.. ( 1975;). Properties of a chicken lymphoblastoid cell line from Marek's disease tumor. J Natl Cancer Inst 54: 453–458 [PubMed].
    [Google Scholar]
  21. Nazerian K., Ackerson A., Hooper G.. ( 1976;). Scanning electron microscopy in the study of chicken T and B cells and cells from Marek's disease tumours. Avian Pathol 5: 135–145 [CrossRef] [PubMed].
    [Google Scholar]
  22. Nazerian K., Stephens E. A., Sharma J. M., Lee L. F., Gailitis M., Witter R. L.. ( 1977;). A nonproducer T lymphoblastoid cell line from Marek's disease transplantable tumor (JMV). Avian Dis 21: 69–76 [CrossRef] [PubMed].
    [Google Scholar]
  23. Owen D. J., Crump C. M., Graham S. C.. ( 2015;). Tegument assembly and secondary envelopment of alphaherpesviruses. Viruses 7: 5084–5114 [CrossRef] [PubMed].
    [Google Scholar]
  24. Pais-Correia A. M., Sachse M., Guadagnini S., Robbiati V., Lasserre R., Gessain A., Gout O., Alcover A., Thoulouze M. I.. ( 2010;). Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med 16: 83–89 [CrossRef] [PubMed].
    [Google Scholar]
  25. Parcells M. S., Dienglewicz R. L., Anderson A. S., Morgan R. W.. ( 1999;). Recombinant Marek's disease virus (MDV)-derived lymphoblastoid cell lines: regulation of a marker gene within the context of the MDV genome. J Virol 73: 1362–1373 [PubMed].
    [Google Scholar]
  26. Polliack A., Lampen N., Clarkson B. D., De Harven E., Bentwich Z., Siegal F. P., Kunkel H. G.. ( 1973;). Identification of human B and T lymphocytes by scanning electron microscopy. J Exp Med 138: 607–624 [CrossRef] [PubMed].
    [Google Scholar]
  27. Powell P. C., Payne L. N., Frazier J. A., Rennie M.. ( 1974;). T lymphoblastoid cell lines from Marek's disease lymphomas. Nature 251: 79–80 [CrossRef] [PubMed].
    [Google Scholar]
  28. Rémy S., Blondeau C., Le Vern Y., Lemesle M., Vautherot J.-F., Denesvre C.. ( 2013;). Fluorescent tagging of VP22 in N-terminus reveals that VP22 favors Marek's disease virus (MDV) virulence in chickens and allows morphogenesis study in MD tumor cells. Vet Res 44: 125 [CrossRef] [PubMed].
    [Google Scholar]
  29. Schat K. A., Chen C. L., Calnek B. W., Char D.. ( 1991;). Transformation of T-lymphocyte subsets by Marek's disease herpesvirus. J Virol 65: 1408–1413 [PubMed].
    [Google Scholar]
  30. Stinson R., Glick B.. ( 1978;). Scanning electron microscopy of chicken lymphocytes: a comparative study of thymic, bursal, and splenic lymphocytes. Dev Comp Immunol 2: 311–318 [CrossRef] [PubMed].
    [Google Scholar]
  31. Trapp-Fragnet L., Bencherit D., Chabanne-Vautherot D., Le Vern Y., Rémy S., Boutet-Robinet E., Mirey G., Vautherot J. F., Denesvre C.. ( 2014;). Cell cycle modulation by Marek's disease virus: the tegument protein VP22 triggers S-phase arrest and DNA damage in proliferating cells. PLoS One 9: e100004 [CrossRef] [PubMed].
    [Google Scholar]
  32. Zhao Y., Xu H., Yao Y., Smith L. P., Kgosana L., Green J., Petherbridge L., Baigent S. J., Nair V.. ( 2011;). Critical role of the virus-encoded microRNA-155 ortholog in the induction of Marek's disease lymphomas. PLoS Pathog 7: e1001305 [CrossRef] [PubMed].
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000354
Loading
/content/journal/jgv/10.1099/jgv.0.000354
Loading

Data & Media loading...

Most Cited This Month

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