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Volume 97, Issue 2

Marek's disease virus undergoes complete morphogenesis after reactivation in a T-lymphoblastoid cell line transformed by recombinant fluorescent marker virus Open Access

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.

  • Received:
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© 2015 The Authors
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2016-02-01
2024-04-23
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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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  11. Johnson D. C., Baines J. D. 2011; Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9:382–394 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  14. Mattila P. K., Lappalainen P. 2008; Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9:446–454 [View Article][PubMed]
     [Google Scholar]
  15. Mettenleiter T. C. 2002; Herpesvirus assembly and egress. J Virol 76:1537–1547 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  19. Nazerian K. 1987; An updated list of avian cell lines and transplantable tumours. Avian Pathol 16:527–544 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
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Marek's disease virus undergoes complete morphogenesis after reactivation in a T-lymphoblastoid cell line transformed by recombinant fluorescent marker virus
J. Gen. Virol. 97, 480 (2016); https://doi.org/10.1099/jgv.0.000354
/content/journal/jgv/10.1099/jgv.0.000354
/content/journal/jgv/10.1099/jgv.0.000354
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