1887

Abstract

The alphaherpesvirus glycoproteins gE and gI form a hetero-oligomeric complex involved in cell-to-cell transmission. The gI-deficient recombinant feline herpesvirus (FHV), FHVdeltagI-LZ, produces plaques that are only 15% the size of those of wild-type FHV. Here, we have complemented FHV(delta)gI-LZ allotopically by expressing intact gI and C-terminally truncated gI derivatives from the thymidine kinase locus. The effect on gE-gI-mediated cell-to-cell spread was assessed by plaque assay employing computer-assisted image analysis (software available at http://www.androclus.vet.uu.nl/spotter/spotter.htm). Allotopic complementation with intact gI fully restored plaque size. Deletion of the C-terminal 11 residues of gI did not affect cell-to-cell spread, whereas deletion of the complete cytoplasmic tail reduced plaque size by only 35%. Mutants expressing gI166, roughly corresponding to the N-terminal half of the ectodomain, displayed a small-plaque phenotype. Nevertheless, their plaques were reproducibly larger than those of matched gI-deficient controls, indicating that the gE-gI166 hetero-oligomer, though crippled, is still able to mediate cell-to-cell spread. Our data demonstrate that plaque analysis provides a reliable and convenient tool to measure and quantitate gE-gI function in vitro.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-80-7-1799
1999-07-01
2022-05-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/80/7/0801799a.html?itemId=/content/journal/jgv/10.1099/0022-1317-80-7-1799&mimeType=html&fmt=ahah

References

  1. Alconada A., Bauer U., Hoflack B. 1996; A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO Journal 15:6096–6110
    [Google Scholar]
  2. Alconada A., Bauer U., Baudoux L., Piette J., Hoflack B. 1998; Intracellular transport of the glycoproteins gE and gI of the varicella-zoster virus. Journal of Biological Chemistry 273:13430–13436
    [Google Scholar]
  3. Alconada A., Bauer U., Sodeik B., Hoflack B. 1999; Intracellular traffic of herpes simplex virus glycoprotein E: characterization of the sorting signals required for its trans-Golgi network localization. Journal of Virology 73:377–387
    [Google Scholar]
  4. Audonnet J.-C., Winslow J., Allen G., Paoletti E. 1990; Equine herpesvirus type 1 unique short fragment encodes glycoproteins with homology to herpes simplex virus type 1 gD, gI and gE. Journal ofGeneral Virology 71:2969–2978
    [Google Scholar]
  5. 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 ofGeneral Virology 75:1245–1258
    [Google Scholar]
  6. Cassady K. A., Gross M., Roizman B. 1998; The second-site mutation in the herpes simplex virus recombinants lacking the gamma134.5 genes precludes shutoff ofprotein synthesis by blocking the phosphorylation of eIF-2alpha. Journal of Virology 72:7005–7011
    [Google Scholar]
  7. Dingwell K. S., Brunetti C. R., Hendricks R. L., Tang Q., Tang M., Rainbow A. J., Johnson D. C. 1994; Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. Journal of Virology 68:834–845
    [Google Scholar]
  8. Johnson D. C., Feenstra V. 1987; Identification of a novel herpes simplex virus type 1-induced glycoprotein which complexes with gE and binds immunoglobulin. Journal of Virology 61:2208–2216
    [Google Scholar]
  9. Kimman T. G., de Wind N., Oei-Lie N., Pol J. M. A., Berns A. J. M., Gielkens A. L. J. 1992; Contribution of single genes within the unique short region of Aujeszky’s disease virus (suid herpesvirus type 1) to virulence, pathogenesis and immunogenicity. Journal of General Virology 73:243–251
    [Google Scholar]
  10. Kimura H., Straus S. E., Williams R. K. 1997; Varicella-zoster virus glycoproteins E and I expressed in insect cells form a heterodimer that requires the N-terminal domain of glycoprotein I. Virology 233:382–391
    [Google Scholar]
  11. Kost T. A., Jones E. V., Smith K. M., Reed A. P., Brown A. L., Miller T. J. 1989; Biological evaluation of glycoproteins mapping to two distinct mRNAs within the Bam HI fragment 7 of pseudorabies virus: expression of the coding regions by vaccinia virus. Virology 171:365–376
    [Google Scholar]
  12. Leung-Tack P., Audonnet J. C., Riviere M. 1994; The complete DNA sequence and the genetic organization of the short unique region (US) of the bovine herpesvirus type 1 (ST strain). Virology 199:409–421
    [Google Scholar]
  13. Liang X., Pyne C., Li Y., Babiuk L. A., Kowalski J. 1995; Delineation of the essential function of bovine herpesvirus 1 gD: an indication for the modulatory role of gD in virus entry. Virology 207:429–441
    [Google Scholar]
  14. Litwin V., Jackson W., Grose C. 1992; Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. Journal of Virology 66:3643–3651
    [Google Scholar]
  15. McGeoch D. J. 1990; Evolutionary relationships of virion glycoprotein genes in the S regions of alphaherpesvirus genomes. Journal of General Virology 71:2361–2367
    [Google Scholar]
  16. 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]
  17. Mettenleiter T. C. 1994; Pseudorabies (Aujeszky’s disease) virus: state of the art. August 1993. Acta Veterinaria Hungarica 42:153–177
    [Google Scholar]
  18. Mijnes J. D. F. 1999 Structure–function analysis of the feline herpesvirus virulence factors gE and gI PhD thesis University of Utrecht; The Netherlands:
    [Google Scholar]
  19. Mijnes J. D. F., van der Horst L. M., van Anken E., Horzinek M. C., Rottier P. J. M., 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]
  20. Mijnes J. D. F., Lutters B. C., Vlot A. C., van Anken E., Horzinek M. C., Rottier P. J. M., deGroot R. J. 1997; Structure–functionanalysisof the gE–gI complex of feline herpesvirus: mapping of gI domains required for gE–gI interaction, intracellular transport, and cell-to-cell spread. Journal of Virology 71:8397–8404
    [Google Scholar]
  21. Mohr I., Gluzman Y. 1996; A herpesvirus genetic element which affects translation in the absence of the viral GADD34 function. EMBO Journal 15:4759–4766
    [Google Scholar]
  22. 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]
  23. Nunberg J. H., Wright D. K., Cole G. E., Petrovskis E. A., Post L. E., Compton T., Gilbert J. H. 1989; Identification of the thymidine kinase gene of feline herpesvirus: use of degenerate oligonucleotides in the polymerase chain reaction to isolate herpesvirus gene homologs. Journal of Virology 63:3240–3249
    [Google Scholar]
  24. Olson J. K., Grose C. 1997; Endocytosis and recycling of varicella-zoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. Journal of Virology 71:4042–4054
    [Google Scholar]
  25. Olson J. K., Grose C. 1998; Compl ex formation facilitates endocytosis of the varicella-zoster virus gE: gI Fc receptor. Journal of Virology 72:1542–1551
    [Google Scholar]
  26. Peeters B., de Wind N., Hooisma M., Wagenaar F., Gielkens A., Moormann R. 1992; Pseudorabies virus envelope glycoproteins gp50 and gII are essential for virus penetration, but only gII is involved in membrane fusion. Journal of Virology 66:894–905
    [Google Scholar]
  27. Rauh I., Mettenleiter T. C. 1991; Pseudorabies virus glycoproteins gII and gp50 are essential for virus penetration. Journal of Virology 65:5348–5356
    [Google Scholar]
  28. Rebordosa X., Piñol J., Pérez Pons J. A., Lloberas J., Naval J., Serra-Hartmann X., Espuña E., Querol E. 1996; Glycoprotein E of bovine herpesvirus type 1 is involved in virus transmission by direct cell-to-cell spread. Virus Research 45:59–68
    [Google Scholar]
  29. Sanders P. G., Wilkie N. M., Davison A. J. 1982; Thymidine kinase deletion mutants of herpes simplex virus type 1. Journal of General Virology 63:277–295
    [Google Scholar]
  30. Schmidt J., Klupp B. G., Karger A., Mettenleiter T. C. 1997; Adaptability in herpesviruses: glycoprotein D-independent infectivity of pseudorabies virus. Journal of Virology 71:17–24
    [Google Scholar]
  31. Schröder C., Linde G., Fehler F., Keil G. M. 1997; From essential to beneficial: glycoprotein D loses importance for replication of bovine herpesvirus 1 in cell culture. Journal of Virology 71:25–33
    [Google Scholar]
  32. Spear P. G. 1993; Entry of alphaherpesviruses into cells. Seminars in Virology 4:167–180
    [Google Scholar]
  33. Tirabassi R. S., Enquist L. W. 1998; Role of envelope protein gE endocytosis in the pseudorabies virus life cycle. Journal of Virology 72:4571–4579
    [Google Scholar]
  34. Whealy M. E., Card J. P., Robbins A. K., Dubin J. R., Rziha H. J., Enquist L. W. 1993; Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. Journal of Virology 67:3786–3797
    [Google Scholar]
  35. Whitbeck J. C., Knapp A. C., Enquist L. W., Lawrence W. C., Bello L. J. 1996; Synthesis, processing, and oligomerization of bovine herpesvirus 1 gE and gI membrane proteins. Journal of Virology 70:7878–7884
    [Google Scholar]
  36. Willemse M. J., Strijdveen I. G., van Schooneveld S. H., van den Berg M. C., Sondermeijer P. J. 1995; Transcriptional analysis of the short segment of the feline herpesvirus type 1 genome and insertional mutagenesis of a unique reading frame. Virology 208:704–711
    [Google Scholar]
  37. Yao Z., Grose C. 1994; Unusual phosphorylation sequence in the gpIV (gI) component of the varicella-zoster virus gpI–gpIV glycoprotein complex (VZV gE–gI complex). Journal of Virology 68:4204–4211
    [Google Scholar]
  38. Yao Z., Jackson W., Forghani B., Grose C. 1993; Varicella-zoster virus glycoprotein gpI/gpIV receptor: expression, complex formation, and antigenicity within the vaccinia virus-T7 RNA polymerase transfection system. Journal of Virology 67:305–314
    [Google Scholar]
  39. 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]
  40. Zhu Z., Gershon M. D., Hao Y., Ambron R. T., Gabel C. A., Gershon A. A. 1995; Envelopment of varicella-zoster virus: targeting of viral glycoproteins to the trans-Golgi network. Journal of Virology 69:7951–7959
    [Google Scholar]
  41. Zsak L., Zuckermann F., Sugg N., Ben Porat T. 1992; Glycoprotein gI of pseudorabies virus promotes cell fusion and virus spread via direct cell-to-cell transmission. Journal of Virology 66:2316–2325
    [Google Scholar]
  42. Zuckermann F. A., Mettenleiter T. C., Schreurs C., Sugg N., Ben Porat T. 1988; Compl ex 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/10.1099/0022-1317-80-7-1799
Loading
/content/journal/jgv/10.1099/0022-1317-80-7-1799
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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