1887

Journal of General Virology header logo

Volume 83, Issue 9

Glycoprotein B plays a predominant role in mediating herpes simplex virus type 2 attachment and is required for entry and cell-to-cell spread Free

Abstract

Heparan sulfate moieties serve as receptors for initial binding of herpes simplex virus types 1 and 2 (HSV-1 and -2) to cells. Deletion of HSV-1 glycoprotein C (gC-1) but not HSV-2 gC (gC-2) results in virions with reduced specific binding activity (virus particles bound per cell) and specific infectivity (p.f.u. per particle), suggesting that for HSV-1, but not HSV-2, gC plays a major role in mediating virus attachment. To test the hypothesis that glycoprotein B (gB), the other heparin-binding glycoprotein, mediates HSV-2 attachment, HSV-2 viruses deleted in gB-2 alone or deleted in both gB-2 and gC-2 were constructed. These viruses were grown on complementing or non-complementing cells and were compared with parental HSV-2(G) or a gC-2-deleted HSV-2 mutant (with respect to ability to bind and infect cells). At equivalent input concentrations of purified virions, significantly fewer gB-2-deleted virions bound to cells compared to parental HSV-2(G) or virus grown on complementing cells. In addition, viruses deleted in gB-2 were non-infectious. No immediate early proteins were detected in cells infected with gB-2-deleted virus harvested from non-complementing Vero cells, whereas these proteins were readily detected 4 h post-infection in cells infected with virus grown on complementing cells or with parental viruses. Viruses deleted in gB-2 failed to spread cell to cell, as evidenced by the inability to form plaques. Together these studies demonstrate that gB-2 plays a key role in mediating HSV-2 attachment and is required for entry and cell-to-cell spread. This glycoprotein is an important target for development of novel antiviral drugs.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-9-2247
2002-09-01
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/9/0832247a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-9-2247&mimeType=html&fmt=ahah

References

  1. Akula S. M., Pramod N. P., Wang F. Z., Chandran B. 2001; Human herpesvirus 8 envelope-associated glycoprotein B interacts with heparan sulfate-like moieties. Virology 284:235–249
     [Google Scholar]
  2. Boyle K. A., Compton T. 1998; Receptor-binding properties of a soluble form of human cytomegalovirus glycoprotein B. Journal of Virology 72:1826–1833
     [Google Scholar]
  3. Bzik D. J., Debroy C., Fox B. A., Pederson N. E., Person S. 1986; The nucleotide sequence of the gB glycoprotein gene of HSV-2 and comparison with the corresponding gene of HSV-1. Virology 155:322–333
     [Google Scholar]
  4. Cai W. H., 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]
  5. Campadelli-Fiume G., Stirpe D., Boscaro A., Avitabile E., Foa-Tomasi L., Barker D., Roizman B. 1990; Glycoprotein C-dependent attachment of herpes simplex virus to susceptible cells leading to productive infection. Virology 178:213–222
     [Google Scholar]
  6. Dowbenko D. J., Lasky L. A. 1984; Extensive homology between the herpes simplex virus type 2 glycoprotein F gene and the herpes simplex virus type 1 glycoprotein C gene. Journal of Virology 52:154–163
     [Google Scholar]
  7. Frink R. J., Eisenberg R., Cohen G., Wagner E. K. 1983; Detailed analysis of the portion of the herpes simplex virus type 1 genome encoding glycoprotein C. Journal of Virology 45:634–647
     [Google Scholar]
  8. Gerber S. I., Belval B. J., Herold B. C. 1995; Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism. Virology 214:29–39
     [Google Scholar]
  9. Griffiths A., Renfrey S., Minson T. 1998; Glycoprotein C-deficient mutants of two strains of herpes simplex virus type 1 exhibit unaltered adsorption characteristics on polarized or non- polarized cells. Journal of General Virology 79:807–812
     [Google Scholar]
  10. Herold B. C., Spear P. G. 1994; Neomycin inhibits glycoprotein C (gC)-dependent binding of herpes simplex virus type 1 to cells and also inhibits postbinding events in entry. Virology 203:166–171
     [Google Scholar]
  11. Herold B. C., WuDunn D., Soltys N., Spear P. G. 1991; Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. Journal of Virology 65:1090–1098
     [Google Scholar]
  12. 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]
  13. Herold B. C., Gerber S. I., Belval B. J., Siston A. M., Shulman N. 1996; Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. Journal of Virology 70:3461–3469
     [Google Scholar]
  14. Herold B. C., Bourne N., Marcellino D., Kirkpatrick R., Strauss D. M., Zaneveld L. J., Waller D. P., Anderson R. A., Chany C. J., Barham B. J., Stanberry L. R., Cooper M. D. 2000; Poly(sodium 4-styrene sulfonate): an effective candidate topical antimicrobial for the prevention of sexually transmitted diseases. Journal of Infectious Diseases 181:770–773
     [Google Scholar]
  15. Immergluck L. C., Domowicz M. S., Schwartz N. B., Herold B. C. 1998; Viral and cellular requirements for entry of herpes simplex virus type 1 into primary neuronal cells. Journal of General Virology 79:549–559
     [Google Scholar]
  16. Karger A., Saalmuller A., Tufaro F., Banfield B. W., Mettenleiter T. C. 1995; Cell surface proteoglycans are not essential for infection by pseudorabies virus. Journal of Virology 69:3482–3489
     [Google Scholar]
  17. Klupp B. G., Karger A., Mettenleiter T. C. 1997; Bovine herpesvirus 1 glycoprotein B does not productively interact with cell surface heparan sulfate in a pseudorabies virion background. Journal of Virology 71:4838–4841
     [Google Scholar]
  18. Langeland N., Moore L. J., Holmsen H., Haarr L. 1988; Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. Journal of General Virology 69:1137–1145
     [Google Scholar]
  19. Langeland N., Oyan A. M., Marsden H. S., Cross A., Glorioso J. C., Moore L. J., Haarr L. 1990; Localization on the herpes simplex virus type 1 genome of a region encoding proteins involved in adsorption to the cellular receptor. Journal of Virology 64:1271–1277
     [Google Scholar]
  20. Laquerre S., Argnani R., Anderson D. B., Zucchini S., Manservigi R., Glorioso J. C. 1998; Heparan sulfate proteoglycan binding by herpes simplex virus type 1 glycoproteins B and C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread. Journal of Virology 72:6119–6130
     [Google Scholar]
  21. 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]
  22. 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]
  23. Okazaki K., Matsuzaki T., Sugahara Y., Okada J., Hasebe M., Iwamura Y., Ohnishi M., Kanno T., Shimizu M., Honda E. and others 1991; BHV 1 adsorption is mediated by the interaction of glycoprotein gIII with heparinlike moiety on the cell surface. Virology 181:666–670
     [Google Scholar]
  24. Oyan A. M., Dolter K. E., Langeland N., Goins W. F., Glorioso J. C., Haarr L., Crumpacker C. S. 1993; Resistance of herpes simplex virus type 2 to neomycin maps to the N-terminal portion of glycoprotein C. Journal of Virology 67:2434–2441
     [Google Scholar]
  25. Qie L., Marcellino D., Herold B. C. 1999; Herpes simplex virus entry is associated with tyrosine phosphorylation of cellular proteins. Virology 256:220–227
     [Google Scholar]
  26. Roller R. J., Herold B. C. 1997; Characterization of a BHK(TK-) cell clone resistant to postattachment entry by herpes simplex virus types 1 and 2. Journal of Virology 71:5805–5813
     [Google Scholar]
  27. Secchiero P., Sun D., De Vico A. L., Crowley R. W., Reitz M. S. Jr, Zauli G., Lusso P., Gallo R. C. 1997; Role of the extracellular domain of human herpesvirus 7 glycoprotein B in virus binding to cell surface heparan sulfate proteoglycans. Journal of Virology 71:4571–4580
     [Google Scholar]
  28. Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. 1992; Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. Journal of Cell Biology 116:1273–1281
     [Google Scholar]
  29. Spear P. 1993; Entry of alphaherpesviruses into cells. Seminars in Virology 4:167–180
     [Google Scholar]
  30. Spear P. G., Eisenberg R. J., Cohen G. H. 2000; Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275:1–8
     [Google Scholar]
  31. Stuve L. L., Brown-Shimer S., Pachl C., Najarian R., Dina D., Burke R. L. 1987; Structure and expression of the herpes simplex virus type 2 glycoprotein gB gene. Journal of Virology 61:326–335
     [Google Scholar]
  32. Swain M. A., Peet R. W., Galloway D. A. 1985; Characterization of the gene encoding herpes simplex virus type 2 glycoprotein C and comparison with the type 1 counterpart. Journal of Virology 53:561–569
     [Google Scholar]
  33. Tal-Singer R., Peng C., Ponce De Leon M., Abrams W. R., Banfield B. W., Tufaro F., Cohen G. H., Eisenberg R. J. 1995; Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. Journal of Virology 69:4471–4483
     [Google Scholar]
  34. Vahlne A., Svennerholm B., Lycke E. 1979; Evidence for herpes simplex virus type-selective receptors on cellular plasma membranes. Journal of General Virology 44:217–225
     [Google Scholar]
  35. Vahlne A., Svennerholm B., Sandberg M., Hamberger A., Lycke E. 1980; Differences in attachment between herpes simplex type 1 and type 2 viruses to neurons and glial cells. Infection and Immunity 28:675–680
     [Google Scholar]
  36. WuDunn D., Spear P. G. 1989; Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. Journal of Virology 63:52–58
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-9-2247
Loading
Glycoprotein B plays a predominant role in mediating herpes simplex virus type 2 attachment and is required for entry and cell-to-cell spread
J. Gen. Virol. 83, 2247 (2002); https://doi.org/10.1099/0022-1317-83-9-2247
/content/journal/jgv/10.1099/0022-1317-83-9-2247
/content/journal/jgv/10.1099/0022-1317-83-9-2247
Loading

Data & Media loading...

Most cited 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