1887

Abstract

The role of the products of the UL10 and the UL49.5 homologous genes of Marek’s disease virus serotype 1 (MDV-1) in virus replication was investigated. Deletion of either open reading frame in an infectious bacterial artificial chromosome clone (BAC20) of MDV-1 resulted in progeny viruses that were unable to spread from cell to cell. After transfection of UL10- or UL49.5-negative BAC20 DNA into chicken or quail cells, only single infected cells were observed by indirect immunofluorescence analysis. In contrast, plaque formation was restored when mutant BAC DNAs were co-transfected with the corresponding expression plasmid encoding either the UL10-encoded gM or the UL49.5 gene product. These data demonstrate that gM and its putative complex partner, the UL49.5 homologous protein, are essential for MDV-1 growth in cultured cells. Thus, MDV-1 represents the first example of a member of the family for which the highly conserved membrane proteins are indispensable for cell-to-cell spread.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-5-997
2002-05-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/5/0830997a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-5-997&mimeType=html&fmt=ahah

References

  1. Baines J. D., Roizman B. 1991; The open reading frames UL3, UL4, UL10, and UL16 are dispensable for the replication of herpes simplex virus 1 in cell culture. Journal of Virology 65:938–944
    [Google Scholar]
  2. Balan P., Davis-Poynter N., Bell S., Atkinson H., Browne H., Minson T. 1994; An analysis of the in vitro and in vivo phenotypes of mutants of herpes simplex virus type 1 lacking glycoproteins gG, gE, gI or the putative gJ. Journal of General Virology 75:1245–1258
    [Google Scholar]
  3. Biggs P. M. 2001; The history and biology of Marek’s disease virus. Current Topics of Microbiology and Immunology 255:1–24
    [Google Scholar]
  4. Binns M. M., Ross N. L. 1989; Nucleotide sequence of the Marek’s disease virus (MDV) RB-1B A antigen gene and the identification of the MDV A antigen as the herpes simplex virus-1 glycoprotein C homologue. Virus Research 12:371–381
    [Google Scholar]
  5. Brack A. R., Dijkstra J. M., Granzow H., Klupp B. G., Mettenleiter T. C. 1999; Inhibition of virion maturation by simultaneous deletion of glycoproteins E, I, and M of pseudorabies virus. Journal of Virology 73:5364–5372
    [Google Scholar]
  6. Brack A. R., Klupp B. G., Granzow H., Tirabassi R., Enquist L. W., Mettenleiter T. C. 2000; Role of the cytoplasmic tail of pseudorabies virus glycoprotein E in virion formation. Journal of Virology 74:4004–4016
    [Google Scholar]
  7. Calnek B. W., Adldinger H. K., Kahn D. E. 1970; Feather follicle epithelium: a source of enveloped and infectious cell-free herpesvirus from Marek’s disease. Avian Diseases 14:219–233
    [Google Scholar]
  8. Cantello J. L., Anderson A. S., Francesconi A., Morgan R. W. 1991; Isolation of a Marek’s disease virus (MDV) recombinant containing the lacZ gene of Escherichia coli stably inserted within the MDV US2 gene. Journal of Virology 65:1584–1588
    [Google Scholar]
  9. Churchill A. E., Chubb R. C., Baxendale W. 1969; The attenuation, with loss of oncogenicity, of the herpes-type virus of Marek’s disease (strain HPRS-16) on passage in cell culture. Journal of General Virology 4:557–564
    [Google Scholar]
  10. Cohen J. I., Nguyen H. 1997; Varicella-zoster virus glycoprotein I is essential for growth of virus in Vero cells. Journal of Virology 71:6913–6920
    [Google Scholar]
  11. Cui Z. Z., Yan D., Lee L. F. 1990; Marek’s disease virus gene clones encoding virus-specific phosphorylated polypeptides and serological characterization of fusion proteins. Virus Genes 3:309–322
    [Google Scholar]
  12. Dijkstra J. M., Visser N., Mettenleiter T. C., Klupp B. G. 1996; Identification and characterization of pseudorabies virus glycoprotein gM as a nonessential virion component. Journal of Virology 70:5684–5688
    [Google Scholar]
  13. Dorange F., El Mehdaoui S., Pichon C., Coursaget P., Vautherot J.-F. 2000; Marek’s disease virus (MDV) homologues of herpes simplex virus type 1 UL49 (VP22) and UL48 (VP16) genes: high-level expression and characterization of MDV-1 VP22 and VP16. Journal of General Virology 81:2219–2230
    [Google Scholar]
  14. Dorange F., Tischer B. K., Vautherot J.-F., Osterrieder N. 2002; Characterization of Marek’s disease virus serotype 1 (MDV-1) deletion mutants that lack UL46 to UL49 genes: MDV-1 UL49 encoding VP22 is dispensable for virus growth. Journal of Virology 76:1959–1970
    [Google Scholar]
  15. Gershon M. D., Gershon A. A. 1999; Role of glycoproteins in varicella-zoster virus infection. Contributions to Microbiology 3:43–60
    [Google Scholar]
  16. Hobom U., Brune W., Messerle M., Hahn G., Koszinowski U. H. 2000; Fast screening procedures for random transposon libraries of cloned herpesvirus genomes: mutational analysis of human cytomegalovirus envelope glycoprotein genes. Journal of Virology 74:7720–7729
    [Google Scholar]
  17. Jöns A., Dijkstra J. M., Mettenleiter T. C. 1998; Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. Journal of Virology 72:550–557
    [Google Scholar]
  18. Lake C. M., Hutt-Fletcher L. M. 2000; Epstein–Barr virus that lacks glycoprotein gN is impaired in assembly and infection. Journal of Virology 74:11162–11172
    [Google Scholar]
  19. Lake C. M., Molesworth S. J., Hutt-Fletcher L. M. 1998; The Epstein–Barr virus (EBV) gN homolog BLRF1 encodes a 15-kilodalton glycoprotein that cannot be authentically processed unless it is coexpressed with the EBV gM homolog BBRF3. Journal of Virology 72:5559–5564
    [Google Scholar]
  20. Lee L. F., Wu P., Sui D., Ren D., Kamil J., Kung H. J., Witter R. L. 2000; The complete unique long sequence and the overall genomic organization of the GA strain of Marek’s disease virus. Proceedings of the National Academy of Sciences, USA 97:6091–6096
    [Google Scholar]
  21. Liang X., Tang M., Manns B., Babiuk L. A., Zamb T. J. 1993; Identification and deletion mutagenesis of the bovine herpesvirus 1 dUTPase gene and a gene homologous to herpes simplex virus UL49.5. Virology 195:42–50
    [Google Scholar]
  22. Mallory S., Sommer M., Arvin A. M. 1997; Mutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein E conformation and trafficking. Journal of Virology 71:8279–8288
    [Google Scholar]
  23. Mallory S., Sommer M., Arvin A. M. 1998; Analysis of the glycoproteins I and E of varicella-zoster virus (VZV) using deletional mutations of VZV cosmids. Journal of Infectious Diseases 178 (Suppl. 1):S22–S26
    [Google Scholar]
  24. Mijnes J. D., van der Horst L. M., van Anken E., Horzinek M. C., Rottier P. J., de Groot R. J. 1996; Biosynthesis of glycoproteins E and I of feline herpesvirus: gE–gI interaction is required for intracellular transport. Journal of Virology 70:5466–5475
    [Google Scholar]
  25. Morgan R. W., Cantello J. L., McDermott C. H. 1990; Transfection of chicken embryo fibroblasts with Marek’s disease virus DNA. Avian Diseases 34:345–351
    [Google Scholar]
  26. Muyrers J. P., Zhang Y., Testa G., Stewart A. F. 1999; Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Research 27:1555–1557
    [Google Scholar]
  27. Narayanan K., Williamson R., Zhang Y., Stewart A. F., Ioannou P. A. 1999; Efficient and precise engineering of a 200 kb β-globin human/bacterial artificial chromosome in E. coli DH10B using an inducible homologous recombination system. Gene Therapy 6:442–447
    [Google Scholar]
  28. Osterrieder N. 1999; Sequence and initial characterization of the UL10 (glycoprotein M) and UL11 homologous genes of serotype 1 Marek’s disease virus. Archives of Virology 144:1853–1863
    [Google Scholar]
  29. Osterrieder N., Neubauer A., Brandmüller C., Braun B., Kaaden O. R., Baines J. D. 1996; The equine herpesvirus 1 glycoprotein gp21/22a, the herpes simplex virus type 1 gM homolog, is involved in virus penetration and cell-to-cell spread of virions. Journal of Virology 70:4110–4115
    [Google Scholar]
  30. 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
    [Google Scholar]
  31. Ross L. J. N., Sanderson M., Scott S. D., Binns M. M., Doel T., Milne B. 1989; Nucleotide sequence and characterization of the Marek’s disease virus homologue of glycoprotein B of herpes simplex virus. Journal of General Virology 70:1789–1804
    [Google Scholar]
  32. Rudolph J., Seyboldt C., Granzow H., Osterrieder N. 2002; The gene 10 (UL49.5) product of equine herpesvirus type 1 (EHV-1) is necessary and sufficient for functional processing of glycoprotein M. Journal of Virology 76 (in press
    [Google Scholar]
  33. Schumacher D., Tischer B. K., Fuchs W., Osterrieder N. 2000; Reconstitution of Marek’s disease virus serotype 1 (MDV-1) from DNA cloned as a bacterial artificial chromosome and characterization of a glycoprotein B-negative MDV-1 mutant. Journal of Virology 74:11088–11098
    [Google Scholar]
  34. Schumacher D., Tischer B. K., Reddy S. M., Osterrieder N. 2001; Glycoproteins E and I of Marek’s disease virus serotype 1 are essential for virus growth in cultured cells. Journal of Virology 75:11307–11318
    [Google Scholar]
  35. Seyboldt C., Granzow H., Osterrieder N. 2000; Equine herpesvirus 1 (EHV-1) glycoprotein M: effect of deletions of transmembrane domains. Virology 278:477–489
    [Google Scholar]
  36. Tan X., Brunovskis P., Velicer L. F. 2001; Transcriptional analysis of Marek’s disease virus glycoprotein D, I, and E genes: gD expression is undetectable in cell culture. Journal of Virology 75:2067–2075
    [Google Scholar]
  37. Tulman E. R., Afonso C. L., Lu Z., Zsak L., Rock D. L., Kutish G. F. 2000; The genome of a very virulent Marek’s disease virus. Journal of Virology 74:7980–7988
    [Google Scholar]
  38. van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E., Estes M. K., Lemon S., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. (editors) 1999; Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses San Diego: Academic Press;
    [Google Scholar]
  39. Wilson M. R., Southwick R. A., Pulaski J. T., Tieber V. L., Hong Y., Coussens P. M. 1994; Molecular analysis of the glycoprotein C-negative phenotype of attenuated Marek’s disease virus. Virology 199:393–402
    [Google Scholar]
  40. Wu P., Reed W. M., Yoshida S., Sui D., Lee L. F. 1999; Identification and characterization of glycoprotein H of MDV-1 GA strain. Acta Virologica 43:152–158
    [Google Scholar]
  41. Yoshida S., Lee L. F., Yanagida N., Nazerian K. 1994; Identification and characterization of a Marek’s disease virus gene homologous to glycoprotein L of herpes simplex virus. Virology 204:414–419
    [Google Scholar]
  42. Yoshitake N., Xuan X., Otsuka H. 1997; Identification and characterization of bovine herpesvirus-1 glycoproteins E and I. Journal of General Virology 78:1399–1403
    [Google Scholar]
  43. Zhang Y., Buchholz F., Muyrers J. P., Stewart A. F. 1998; A new logic for DNA engineering using recombination in Escherichia coli . Nature Genetics 20:123–128
    [Google Scholar]
  44. Zuckermann F. A., Mettenleiter T. C., Schreurs C., Sugg N., Ben-Porat T. 1988; Complex between glycoproteins gI and gp63 of pseudorabies virus: its effect on virus replication. Journal of Virology 62:4622–4626
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-5-997
Loading
/content/journal/jgv/10.1099/0022-1317-83-5-997
Loading

Data & Media loading...

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