1887

Abstract

Herpes simplex virus type 1 (HSV-1) interaction with glycoprotein D (gD) receptors facilitates virus entry into cells. Chinese hamster ovary (CHO-K1) cells lacking cellular receptors allow virus to attach, but not to enter, implying a role for receptors during the post-attachment (entry) phase of HSV-1 infection. Here, it is shown that the presence of soluble heparan sulfate (HS) modified by 3--sulfotransferase-3 (3-ST-3), but not by 3-ST-1, triggered HSV-1 entry into resistant CHO-K1 cells. It was further demonstrated that a CHO-K1 mutant deficient in glycosaminoglycan synthesis became susceptible to entry when spinoculated in the presence of 3-ST-3-modified soluble HS, indicating that the role of the gD receptor is to trigger entry rather than cell attachment. In separate experiments, 3-ST-3-modified soluble HS also triggered fusion of HSV-1 glycoprotein-expressing cells with CHO-K1 cells. Taken together, these results show that association of gD with cell surface-bound receptor is not essential for HSV-1 entry and spread.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82476-0
2007-04-01
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/4/1075.html?itemId=/content/journal/jgv/10.1099/vir.0.82476-0&mimeType=html&fmt=ahah

References

  1. Allan J. S., Strauss J., Buck D. W. 1990; Enhancement of SIV infection with soluble receptor molecules. Science 247:1084–1088 [CrossRef]
    [Google Scholar]
  2. Browne H., Bruun B., Minson T. 2001; Plasma membrane requirements for cell fusion induced by herpes simplex virus type 1 glycoproteins gB, gD, gH and gL. J Gen Virol 82:1419–1422
    [Google Scholar]
  3. Campadelli-Fiume G., Cocchi F., Menotti L., Lopez M. 2000; The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev Med Virol 10:305–319 [CrossRef]
    [Google Scholar]
  4. Clement C., Tiwari V., Scanlan P. M., Valyi-Nagy T., Yue B. Y., Shukla D. 2006; A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol 174:1009–1021 [CrossRef]
    [Google Scholar]
  5. Cocchi F., Menotti L., Dubreuil P., Lopez M., Campadelli-Fiume G. 2000; Cell-to-cell spread of wild-type herpes simplex virus type-1, but not of syncytial strains, is mediated by the immunoglobulin-like receptors that mediate virion entry, nectin1 (PRR1/HveC/HIgR) and nectin2 (PRR2/HveB). J Virol 74:3909–3917 [CrossRef]
    [Google Scholar]
  6. Damico R., Bates P. 2000; Soluble receptor-induced retroviral infection of receptor-deficient cells. J Virol 74:6469–6475 [CrossRef]
    [Google Scholar]
  7. Esko J. D., Lindahl U. 2001; Molecular diversity of heparan sulfate. J Clin Invest 108:169–173 [CrossRef]
    [Google Scholar]
  8. Geraghty R. J., Krummenacher C., Cohen G. H., Eisenberg R. J., Spear P. G. 1998; Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618–1620 [CrossRef]
    [Google Scholar]
  9. Herold B. C., WuDunn D., Soltys N., Spear P. G. 1991; Glycoprotein C of herpes simplex virus type 1 plays a principle role in the adsorption of virus to cells and in infectivity. J Virol 65:1090–1098
    [Google Scholar]
  10. Knauss D. J., Young J. A. 2002; A fifteen-amino-acid TVB peptide serves as a minimal soluble receptor for subgroup B avian leukosis and sarcoma viruses. J Virol 76:5404–5410 [CrossRef]
    [Google Scholar]
  11. Krummenacher C., Nicola A. V., Whitbeck J. C., Lou H., Hou W., Lambris J. D., Geraghty R. J., Spear P. G., Cohen G. H., Eisenberg R. J. 1998; Herpes simplex virus glycoprotein D can bind to poliovirus receptor-related protein 1 or herpesvirus entry mediator, two structurally unrelated mediators of virus entry. J Virol 72:7064–7074
    [Google Scholar]
  12. Kwon H., Bai Q., Baek H. J., Felmet K., Burton E. A., Goins W. F., Cohen J. B., Glorioso J. C. 2006; Soluble V domain of Nectin-1/HveC enables entry of herpes simplex virus type 1 (HSV-1) into HSV-resistant cells by binding to viral glycoprotein D. J Virol 80:138–148 [CrossRef]
    [Google Scholar]
  13. Lindahl U., Kusche-Gullberg M., Kjellen L. 1998; Regulated diversity of heparan sulfate. J Biol Chem 273:24979–24982 [CrossRef]
    [Google Scholar]
  14. Liu J., Rosenberg R. D. 2002; Heparan sulfate d-glucosaminyl 3- O -sulfotransferase-1, -2, -3, and -4. In Handbook of Glycosyltransferases and Related Genes pp 475–483 Edited by Taniguchi N., Honke K., Fukuda M. Tokyo: Springer-Verlag;
    [Google Scholar]
  15. Liu J., Shworak N. W., Sinaÿ P., Schwartz J. J., Zhang L., Fritze L. M., Rosenberg R. D. 1999; Expression of heparan sulfate d-glucosaminyl 3- O -sulphotransferase isoforms reveals novel substrate specificities. J Biol Chem 274:5185–5192 [CrossRef]
    [Google Scholar]
  16. Montgomery R. I., Warner M. S., Lum B. J., Spear P. G. 1996; Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427–436 [CrossRef]
    [Google Scholar]
  17. O'Donnell C. D., Tiwari V., Oh M. J., Shukla D. 2006; A role for heparan sulfate 3- O -sulfotransferase isoform 2 in herpes simplex virus type 1 entry and spread. Virology 346:452–459 [CrossRef]
    [Google Scholar]
  18. Pertel P. E., Fridberg A., Parish M. L., Spear P. G. 2001; Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH–gL requires a gD receptor but not necessarily heparan sulfate. Virology 279:313–324 [CrossRef]
    [Google Scholar]
  19. Richart S. M., Simpson S. A., Krummenacher C., Whitbeck J. C., Pizer L. I., Cohen G. H., Eisenberg R. J., Wilcox C. L. 2003; Entry of herpes simplex virus type 1 into primary sensory neurons in vitro is mediated by nectin-1/HveC. J Virol 77:3307–3311 [CrossRef]
    [Google Scholar]
  20. Rosenberg R. D., Showrak N. W., Liu J., Schwartz J. J., Zhang L. 1997; Heparan sulfate proteoglycans of the cardiovascular system: specific structures emerge but how is synthesis regulated?. J Clin Invest 99:2062–2070 [CrossRef]
    [Google Scholar]
  21. Scanlan P. M., Tiwari V., Bommireddy S., Shukla D. 2005; Spinoculation of heparan sulfate deficient cells enhances HSV-1 entry, but does not abolish the need for essential glycoproteins in viral fusion. J Virol Methods 128:104–112 [CrossRef]
    [Google Scholar]
  22. 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. J Cell Biol 116:1273–1281 [CrossRef]
    [Google Scholar]
  23. Shukla D., Spear P. G. 2001; Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J Clin Invest 108:503–510 [CrossRef]
    [Google Scholar]
  24. Shukla D., Liu J., Blaiklock P., Shworak N. W., Bai X., Esko J. D., Cohen G. H., Eisenberg R. J., Rosenberg R. D., Spear P. G. 1999; A novel role for 3- O -sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13–22 [CrossRef]
    [Google Scholar]
  25. Shukla D., Dal Canto M. C., Rowe C. L., Spear P. G. 2000; Striking similarity of murine nectin-1alpha to human nectin-1alpha (HveC) in sequence and activity as a glycoprotein D receptor for alphaherpesvirus entry. J Virol 74:11773–11781 [CrossRef]
    [Google Scholar]
  26. Shworak N. W., Liu J., Petros L. M., Schwartz J. J., Zhang L., Kobayashi M., Copeland N. G., Jenkins N. A., Rosenberg R. D. 1999; Multiple isoforms of heparan sulfate d-glucosaminyl 3- O -sulfotransferase. Isolation, characterization, and expression of human cDNAs and identification of distinct genomic loci. J Biol Chem 274:5170–5184 [CrossRef]
    [Google Scholar]
  27. Spear P. G., Longnecker R. 2003; Herpesvirus entry: an update. J Virol 77:10179–10185 [CrossRef]
    [Google Scholar]
  28. Tiwari V., Clement C., Duncan M. B., Chen J., Liu J., Shukla D. 2004; A role for 3- O -sulfated heparan sulfate in cell fusion induced by herpes simplex virus type 1. J Gen Virol 85:805–809 [CrossRef]
    [Google Scholar]
  29. Tiwari V., O'Donnell C. D., Oh M. J., Valyi-Nagy T., Shukla D. 2005a; A role for 3- O -sulfotransferase isoform-4 in assisting HSV-1 entry and spread. Biochem Biophys Res Commun 338:930–937 [CrossRef]
    [Google Scholar]
  30. Tiwari V., Clement C., Scanlan P. M., Yue B. Y. J. T., Shukla D. 2005b; A role for HVEM as the receptor for herpes simplex virus-1 entry into primary human trabecular meshwork cells. J Virol 79:13173–13179 [CrossRef]
    [Google Scholar]
  31. Tiwari V., Clement C., Xu D., Valyi-Nagy T., Yue B. Y. J. T., Liu J., Shukla D. 2006; Role for 3- O -sulfated heparan sulfate as a receptor for herpes simplex virus type-1 entry into primary human corneal fibroblasts. J Virol 80:8970–8980 [CrossRef]
    [Google Scholar]
  32. Turner A., Bruun B., Minson T., Browne H. 1998; Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J Virol 72:873–875
    [Google Scholar]
  33. Warner M. S., Geraghty R. J., Martinez W. M., Montgomery R. I., Whitbeck J. C., Xu R., Eisenberg R. J., Cohen G. H., Spear P. G. 1998; A cell surface protein with herpesvirus entry activity (HveB) confers susceptibility to infection by mutants of herpes simplex virus type 1, herpes simplex virus type 2 and pseudorabies virus. Virology 246:179–189 [CrossRef]
    [Google Scholar]
  34. Werner A., Winskowsky G., Kurth R. 1990; Soluble CD4 enhances simian immunodeficiency virus SIVagm infection. J Virol 64:6252–6256
    [Google Scholar]
  35. WuDunn D., Spear P. G. 1989; Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol 63:52–58
    [Google Scholar]
  36. Xia G., Chen J., Tiwari V., Ju W., Li J. P., Malmström A., Shukla D., Liu J. 2002; Heparan sulfate 3- O -sulfotransferase isoform 5 generates both an antithrombin-binding site and an entry receptor for herpes simplex virus, type 1. J Biol Chem 277:37912–37919 [CrossRef]
    [Google Scholar]
  37. Xu D., Tiwari V., Xia G., Clement C., Shukla D., Liu J. 2005; Characterization of heparan sulphate 3- O -sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem J 385:451–459 [CrossRef]
    [Google Scholar]
  38. Yoon M., Zago A., Shukla D., Spear P. G. 2003; Mutations in the N termini of herpes simplex virus type 1 and 2 gDs alter functional interactions with the entry/fusion receptors HVEM, nectin-2, and 3- O -sulfated heparan sulfate but not with nectin-1. J Virol 77:9221–9231 [CrossRef]
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.82476-0
Loading
/content/journal/jgv/10.1099/vir.0.82476-0
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