1887

Abstract

The most highly conserved glycoproteins in herpesviruses, homologues of glycoprotein B (gB) of herpes simplex virus, have been shown to play essential roles in membrane fusion during penetration and direct cell-to-cell spread of herpes virions. In studies aimed at assessing whether sequence conservation is reflected in the conservation of functional properties, we previously showed that bovine herpesvirus 1 (BHV-1) gB was able to functionally complement a gB PrV mutant. To analyse in detail the function of gB in BHV-1, and to be able to test for reciprocal complementation between pseudorabies virus (PrV) and BHV-1 gB, we isolated a gB BHV-1 mutant on a cell line stably expressing BHV-1 gB. Functional analysis showed that BHV-1 gB was essential for penetration as well as for direct cell-to-cell spread of BHV-1, indicating similar functions for PrV and BHV-1 gB. However, PrV gB was unable to complement plaque formation, i.e. direct cell-to-cell spread, or penetration of gB BHV-1 virions despite its incorporation into the virion envelope. Analysis of cell lines expressing chimeric gB molecules composed of PrV and BHV-1 gB showed that plaque formation of both gB mutants was complemented when the carboxy-terminal half of the chimeric gB was derived from BHV-1 gB and the amino-terminal half from PrV gB. In the opposite case, unidirectional complementation occurred. Although the chimeric molecules were generally less efficient in complementing infectivity of free virions, a similar complementation pattern was observed. In summary, our data show a unidirectional pattern of transcomplementation between the gB glycoproteins of PrV and BHV-1. This indicates that these proteins are functionally related but not identical. The unidirectional transcomplementation pattern was determined by the provenance of the carboxy-terminal half in chimeric gB proteins indicating that regions which are important for gB function but differ between PrV and BHV-1 reside in this part of gB.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-76-7-1623
1995-07-01
2024-12-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/76/7/JV0760071623.html?itemId=/content/journal/jgv/10.1099/0022-1317-76-7-1623&mimeType=html&fmt=ahah

References

  1. Blewett E., Misra V. 1991; Cleavage of the bovine herpesvirus glycoprotein B is not essential for its function. Journal of General Virology 72:2083–2090
    [Google Scholar]
  2. Bzik D. J., Fox B., DeLuca N., Person S. 1984; Nucleotide sequence specifying the glycoprotein gene, gB, of herpes simplex virus type 1. Virology 133:301–314
    [Google Scholar]
  3. Cai W., Gu B., Person S. 1988; Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. Journal of Virology 62:2596–2604
    [Google Scholar]
  4. Claesson-Welsh L., Spear P. G. 1986; Oligomerization of herpes simplex virus glycoprotein B. Journal of Virology 60:803–806
    [Google Scholar]
  5. Fehler F., Herrmann J., Saalmüaller A., Mettenleiter T. C., Keil G. M. 1992; Glycoprotein IV of bovine herpesvirus 1-expressing cell line complements and rescues a conditionally lethal viral mutant. Journal of Virology 66:831–839
    [Google Scholar]
  6. Fitzpatrick D., Zamb T., Parker M., Van Drunen Littel-van den Hurk S., Babiuk L., Lawman M. 1988; Expression of bovine herpesvirus 1 glycoproteins gI and gIII in transfected murine cells. Journal of Virology 62:4239–4248
    [Google Scholar]
  7. Gong M., Ooka T., Matsuo T., Kieff E. 1987; Epstein–Barr virus glycoprotein homologous to herpes simplex virus gB. Journal of Virology 61:499–508
    [Google Scholar]
  8. Graham F. L., Van der Eb A. J. 1973; A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52:456–467
    [Google Scholar]
  9. Hampl H., Ben-Porat T., Ehrlicher L., Habermehl K. O., Kaplan A. S. 1984; Characterization of the envelope proteins of pseudorabies virus. Journal of Virology 52:583–590
    [Google Scholar]
  10. Herold B. C., Visalli R. J., Susmarski N., Brandt C. R., Spear P. G. 1994; Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulphate and glycoprotein B. Journal of General Virology 75:1211–1222
    [Google Scholar]
  11. Kaplan A. S., Vatter A. E. 1959; A comparison of herpes simplex and pseudorabies viruses. Virology 7:394–407
    [Google Scholar]
  12. Kopp A., Mettenleiter T. C. 1992; Stable rescue of a glycoprotein gII deletion mutant of pseudorabies virus by glycoprotein gI of bovine herpesvirus 1. Journal of Virology 66:2754–2764
    [Google Scholar]
  13. Kopp A., Blewett E., Misra V., Mettenleiter T. C. 1994; Proteolytic cleavage of bovine herpesvirus 1 (BHV-1) glycoprotein gB is not necessary for its function in BHV-1 or pseudorabies virus. Journal of Virology 68:1667–1674
    [Google Scholar]
  14. Liang X., Babiuk L., Van Drunen Littel-van den Hurk S., Fitzpatrick D., Zamb T. 1991; Bovine herpesvirus 1 attachment to permissive cells is mediated by its major glycoproteins gI, gIII, and gIV. Journal of Virology 65:1124–1132
    [Google Scholar]
  15. Lukács N., Thiel H.-J., Mettenleiter T. C., Rziha H. J. 1985; Demonstration of three major species of pseudorabies virus glycoproteins and identification of a disulfide-linked glycoprotein complex. Journal of Virology 53:155–173
    [Google Scholar]
  16. Mayfield J. E., Good P. J., Vanoort H. J., Campbell A. R., Reed D. E. 1983; Cloning and cleavage site mapping of DNA from bovine herpesvirus 1 (Cooper strain). Journal of Virology 47:259–264
    [Google Scholar]
  17. Mettenleiter T. C. 1994; Initiation and spread of a-herpesvirus infections. Trends in Microbiology 2:2–4
    [Google Scholar]
  18. Mettenleiter T. C., Rauh I. 1990; A glycoprotein gX-β-galactosidase fusion gene as insertional marker for rapid identification of pseudorabies virus mutants. Journal of Virological Methods 30:55–66
    [Google Scholar]
  19. Mettenleiter T. C., Spear P. G. 1994; Glycoprotein gB (gII) of pseudorabies virus can functionally substitute for glycoprotein gB in herpes simplex virus type 1. Journal of Virology 68:500–504
    [Google Scholar]
  20. Mettenleiter T. C., Zsak L., Zuckermann F., Sugg N., Kern H., Ben-Porat T. 1990; Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. Journal of Virology 64:278–286
    [Google Scholar]
  21. Misra V., Nelson R., Smith M. 1988; Sequence of a bovine herpesvirus type 1 gene that is homologous to the herpes simplex gene for glycoprotein B. Virology 166:542–549
    [Google Scholar]
  22. Navarro D., Paz P., Pereira L. 1992; Domains of herpes simplex virus 1 glycoprotein B that function in virus penetration, cell-to-cell spread, and cell fusion. Virology 186:99–112
    [Google Scholar]
  23. 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]
  24. Pellet P., Kousoulas K., Pereira L., Roizman B. 1985; Anatomy of the herpes simplex virus 1 strain F glycoprotein B gene: primary sequence and predicted protein structure of the wild-type and of monoclonal antibody-resistant mutants. Journal of Virology 53:243–253
    [Google Scholar]
  25. 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]
  26. Rauh I., Weiland F., Fehler F., Keil G., Mettenleiter T. C. 1991; Pseudorabies virus mutants lacking the essential glycoprotein gll can be complemented by glycoprotein gl of bovine herpesvirus 1. Journal of Virology 65:621–631
    [Google Scholar]
  27. Robbins A. K., Dorney D., Wathen M. W., Whealy M. E., Gold C., Watson R. J., Holland L. E., Weed S. D., Levine M., Glorioso J., Enquist L. W. 1987; The pseudorabies virus gII gene is closely related to the gB glycoprotein gene of herpes simplex virus. Journal of Virology 61:2691–2701
    [Google Scholar]
  28. Roizman B., Desrosiers R., Fleckenstein B., Lopez C., Minson A. C., Studdert M. J. 1992; The family Herpesviridae: an update. Archives of Virology 123:425–149
    [Google Scholar]
  29. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: A Laboratory Manual 2nd edn New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Sarmiento M., Haffey M., Spear P. G. 1979; Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7(B2) in virion infectivity. Journal of Virology 29:1149–1158
    [Google Scholar]
  31. Schreurs C. 1988 Isolation and characterization of glycoprotein mutants of pseudorabies virus (suid herpesvirus 1) PhD thesis University of Tübingen; Germany:
    [Google Scholar]
  32. Southern P. J., Berg P. 1982; Transformation of mammalian cells to antibiotic resistance with a bacterial gene under control of the SV40 early region promoter. Journal of Molecular and Applied Genetics 1:327–341
    [Google Scholar]
  33. Spear P. G. 1993; Entry of alphaherpesviruses into cells. Seminars in Virology 4:167–180
    [Google Scholar]
  34. Stewart J. P., Janjua N., Sunil-Chandra N., Nash A., Arrand J. 1994; Characterization of murine gammaherpesvirus 68 glycoprotein B (gB) homolog: similarity to Epstein-Barr virus gB (gp110). Journal of Virology 68:6496–6504
    [Google Scholar]
  35. Van Drunen Littel-van den Hurk S., Babiuk L. 1986; Synthesis and processing of bovine herpesvirus 1 glycoproteins. Journal of Virology 59:401–410
    [Google Scholar]
  36. Whealy M. E., Robbins A. K., Enquist L. W. 1990; The export pathway of the pseudorabies virus gB homolog gII involves oligomer formation in the endoplasmic reticulum and protease processing in the Golgi apparatus. Journal of Virology 64:1946–1955
    [Google Scholar]
  37. Whitbeck J. C., Bello L., Lawrence W. 1988; Comparison of the bovine herpesvirus 1 gl gene and the herpes simplex virus type 1 gB gene. Journal of Virology 62:3319–3327
    [Google Scholar]
  38. Wölfer U., Kruft V., Sawitzky D., Hampl H., Wittmann-Liebold B., Habermehl K. O. 1990; Processing of pseudorabies virus glycoprotein gII. Journal of Virology 64:3122–3125
    [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-76-7-1623
Loading
/content/journal/jgv/10.1099/0022-1317-76-7-1623
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