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. 1993 Sep;67(9):5088–5097. doi: 10.1128/jvi.67.9.5088-5097.1993

Herpes simplex virus type 1 and pseudorabies virus bind to a common saturable receptor on Vero cells that is not heparan sulfate.

W C Lee 1, A O Fuller 1
PMCID: PMC237906  PMID: 8394437

Abstract

Herpes simplex virus type 1 (HSV-1) and pseudorabies virus (PRV) infect different natural hosts but are very similar in structure, replicative cycle, and entry into cultured cells. We determined whether HSV-1 and PRV use the same cellular components during entry into Vero cells, which are highly susceptible to each virus but are not from native hosts for either. UV-inactivated virions of either HSV-1 or PRV could saturate cell surfaces to block infection of challenge HSV-1 or PRV. In the presence of saturating levels for infection of either virus, radiolabeled virus bound well and in a heparin-sensitive manner. This result shows that heparan sulfate proteoglycans on Vero cells are not the limiting cellular component. To identify the virus component required for blocking, we used an HSV-1 null mutant virus lacking gB, gD, or gH as blocking virus. Virions lacking gB were able to block infection of challenge virus to the same level as did virus containing gB. In contrast, virions lacking gD lost all and most of the ability to block infection of HSV-1 and PRV, respectively. HSV-1 lacking gH and PRV lacking gp50 also were less competent in blocking infection of challenge virus. We conclude that HSV-1 and PRV bind to a common receptor for infection of Vero cells. Although both viruses bind a heparin-like cell component on many cells, including Vero cells, they also attach to a different and limited cell surface component that is bound at least by HSV-1 gD and possibly gH and to some degree by PRV gp50 but not gB. These results clearly demonstrate binding of both HSV-1 and PRV to a common cell receptor that is not heparan sulfate and demonstrate that several types of attachment occur for both viruses during infectious entry.

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Selected References

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  1. Ben-Porat T., Demarchi J. M., Kaplan A. S. Characterization of defective interfering viral particles present in a population of pseudorabies virions. Virology. 1974 Sep;61(1):29–37. doi: 10.1016/0042-6822(74)90239-6. [DOI] [PubMed] [Google Scholar]
  2. Bzik D. J., Fox B. A., DeLuca N. A., Person S. Nucleotide sequence of a region of the herpes simplex virus type 1 gB glycoprotein gene: mutations affecting rate of virus entry and cell fusion. Virology. 1984 Aug;137(1):185–190. doi: 10.1016/0042-6822(84)90022-9. [DOI] [PubMed] [Google Scholar]
  3. Cai W. H., Gu B., Person S. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J Virol. 1988 Aug;62(8):2596–2604. doi: 10.1128/jvi.62.8.2596-2604.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Campadelli-Fiume G., Arsenakis M., Farabegoli F., Roizman B. Entry of herpes simplex virus 1 in BJ cells that constitutively express viral glycoprotein D is by endocytosis and results in degradation of the virus. J Virol. 1988 Jan;62(1):159–167. doi: 10.1128/jvi.62.1.159-167.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Campadelli-Fiume G., Qi S., Avitabile E., Foà-Tomasi L., Brandimarti R., Roizman B. Glycoprotein D of herpes simplex virus encodes a domain which precludes penetration of cells expressing the glycoprotein by superinfecting herpes simplex virus. J Virol. 1990 Dec;64(12):6070–6079. doi: 10.1128/jvi.64.12.6070-6079.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DeLuca N., Bzik D. J., Bond V. C., Person S., Snipes W. Nucleotide sequences of herpes simplex virus type 1 (HSV-1) affecting virus entry, cell fusion, and production of glycoprotein gb (VP7). Virology. 1982 Oct 30;122(2):411–423. doi: 10.1016/0042-6822(82)90240-9. [DOI] [PubMed] [Google Scholar]
  7. Desai P. J., Schaffer P. A., Minson A. C. Excretion of non-infectious virus particles lacking glycoprotein H by a temperature-sensitive mutant of herpes simplex virus type 1: evidence that gH is essential for virion infectivity. J Gen Virol. 1988 Jun;69(Pt 6):1147–1156. doi: 10.1099/0022-1317-69-6-1147. [DOI] [PubMed] [Google Scholar]
  8. Forrester A., Farrell H., Wilkinson G., Kaye J., Davis-Poynter N., Minson T. Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted. J Virol. 1992 Jan;66(1):341–348. doi: 10.1128/jvi.66.1.341-348.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fuller A. O., Lee W. C. Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. J Virol. 1992 Aug;66(8):5002–5012. doi: 10.1128/jvi.66.8.5002-5012.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fuller A. O., Santos R. E., Spear P. G. Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. J Virol. 1989 Aug;63(8):3435–3443. doi: 10.1128/jvi.63.8.3435-3443.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fuller A. O., Spear P. G. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5454–5458. doi: 10.1073/pnas.84.15.5454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fuller A. O., Spear P. G. Specificities of monoclonal and polyclonal antibodies that inhibit adsorption of herpes simplex virus to cells and lack of inhibition by potent neutralizing antibodies. J Virol. 1985 Aug;55(2):475–482. doi: 10.1128/jvi.55.2.475-482.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goodman J. L., Engel J. P. Altered pathogenesis in herpes simplex virus type 1 infection due to a syncytial mutation mapping to the carboxy terminus of glycoprotein B. J Virol. 1991 Apr;65(4):1770–1778. doi: 10.1128/jvi.65.4.1770-1778.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  15. HUANG A. S., WAGNER R. R. PENETRATION OF HERPES SIMPLEX VIRUS INTO HUMAN EPIDERMOID CELLS. Proc Soc Exp Biol Med. 1964 Aug-Sep;116:863–869. doi: 10.3181/00379727-116-29392. [DOI] [PubMed] [Google Scholar]
  16. Herold B. C., WuDunn D., Soltys N., Spear P. G. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J Virol. 1991 Mar;65(3):1090–1098. doi: 10.1128/jvi.65.3.1090-1098.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Highlander S. L., Sutherland S. L., Gage P. J., Johnson D. C., Levine M., Glorioso J. C. Neutralizing monoclonal antibodies specific for herpes simplex virus glycoprotein D inhibit virus penetration. J Virol. 1987 Nov;61(11):3356–3364. doi: 10.1128/jvi.61.11.3356-3364.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hutchinson L., Browne H., Wargent V., Davis-Poynter N., Primorac S., Goldsmith K., Minson A. C., Johnson D. C. A novel herpes simplex virus glycoprotein, gL, forms a complex with glycoprotein H (gH) and affects normal folding and surface expression of gH. J Virol. 1992 Apr;66(4):2240–2250. doi: 10.1128/jvi.66.4.2240-2250.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hutchinson L., Goldsmith K., Snoddy D., Ghosh H., Graham F. L., Johnson D. C. Identification and characterization of a novel herpes simplex virus glycoprotein, gK, involved in cell fusion. J Virol. 1992 Sep;66(9):5603–5609. doi: 10.1128/jvi.66.9.5603-5609.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Johnson D. C., Burke R. L., Gregory T. Soluble forms of herpes simplex virus glycoprotein D bind to a limited number of cell surface receptors and inhibit virus entry into cells. J Virol. 1990 Jun;64(6):2569–2576. doi: 10.1128/jvi.64.6.2569-2576.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Johnson D. C., Ligas M. W. Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors. J Virol. 1988 Dec;62(12):4605–4612. doi: 10.1128/jvi.62.12.4605-4612.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Johnson R. M., Spear P. G. Herpes simplex virus glycoprotein D mediates interference with herpes simplex virus infection. J Virol. 1989 Feb;63(2):819–827. doi: 10.1128/jvi.63.2.819-827.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Karger A., Mettenleiter T. C. Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology. 1993 Jun;194(2):654–664. doi: 10.1006/viro.1993.1305. [DOI] [PubMed] [Google Scholar]
  24. Kühn J. E., Kramer M. D., Willenbacher W., Wieland U., Lorentzen E. U., Braun R. W. Identification of herpes simplex virus type 1 glycoproteins interacting with the cell surface. J Virol. 1990 Jun;64(6):2491–2497. doi: 10.1128/jvi.64.6.2491-2497.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ligas M. W., Johnson D. C. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells. J Virol. 1988 May;62(5):1486–1494. doi: 10.1128/jvi.62.5.1486-1494.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. doi: 10.1016/0092-8674(86)90590-8. [DOI] [PubMed] [Google Scholar]
  27. Martin L. B., Montgomery P. C., Holland T. C. Soluble glycoprotein D blocks herpes simplex virus type 1 infection of rat eyes. J Virol. 1992 Sep;66(9):5183–5189. doi: 10.1128/jvi.66.9.5183-5189.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
  29. Mettenleiter T. C. Molecular biology of pseudorabies (Aujeszky's disease) virus. Comp Immunol Microbiol Infect Dis. 1991;14(2):151–163. doi: 10.1016/0147-9571(91)90128-z. [DOI] [PubMed] [Google Scholar]
  30. Mettenleiter T. C., Zsak L., Zuckermann F., Sugg N., Kern H., Ben-Porat T. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J Virol. 1990 Jan;64(1):278–286. doi: 10.1128/jvi.64.1.278-286.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nemerow G. R., Wolfert R., McNaughton M. E., Cooper N. R. Identification and characterization of the Epstein-Barr virus receptor on human B lymphocytes and its relationship to the C3d complement receptor (CR2). J Virol. 1985 Aug;55(2):347–351. doi: 10.1128/jvi.55.2.347-351.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Peeters B., de Wind N., Hooisma M., Wagenaar F., Gielkens A., Moormann R. Pseudorabies virus envelope glycoproteins gp50 and gII are essential for virus penetration, but only gII is involved in membrane fusion. J Virol. 1992 Feb;66(2):894–905. doi: 10.1128/jvi.66.2.894-905.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Petrovskis E. A., Meyer A. L., Post L. E. Reduced yield of infectious pseudorabies virus and herpes simplex virus from cell lines producing viral glycoprotein gp50. J Virol. 1988 Jun;62(6):2196–2199. doi: 10.1128/jvi.62.6.2196-2199.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rauh I., Mettenleiter T. C. Pseudorabies virus glycoproteins gII and gp50 are essential for virus penetration. J Virol. 1991 Oct;65(10):5348–5356. doi: 10.1128/jvi.65.10.5348-5356.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sawitzky D., Hampl H., Habermehl K. O. Comparison of heparin-sensitive attachment of pseudorabies virus (PRV) and herpes simplex virus type 1 and identification of heparin-binding PRV glycoproteins. J Gen Virol. 1990 May;71(Pt 5):1221–1225. doi: 10.1099/0022-1317-71-5-1221. [DOI] [PubMed] [Google Scholar]
  36. Schreurs C., Mettenleiter T. C., Zuckermann F., Sugg N., Ben-Porat T. Glycoprotein gIII of pseudorabies virus is multifunctional. J Virol. 1988 Jul;62(7):2251–2257. doi: 10.1128/jvi.62.7.2251-2257.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Shieh M. T., WuDunn D., Montgomery R. I., Esko J. D., Spear P. G. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol. 1992 Mar;116(5):1273–1281. doi: 10.1083/jcb.116.5.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Staunton D. E., Merluzzi V. J., Rothlein R., Barton R., Marlin S. D., Springer T. A. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell. 1989 Mar 10;56(5):849–853. doi: 10.1016/0092-8674(89)90689-2. [DOI] [PubMed] [Google Scholar]
  39. Whealy M. E., Robbins A. K., Enquist L. W. Replacement of the pseudorabies virus glycoprotein gIII gene with its postulated homolog, the glycoprotein gC gene of herpes simplex virus type 1. J Virol. 1989 Sep;63(9):4055–4059. doi: 10.1128/jvi.63.9.4055-4059.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. WuDunn D., Spear P. G. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J Virol. 1989 Jan;63(1):52–58. doi: 10.1128/jvi.63.1.52-58.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Yeager C. L., Ashmun R. A., Williams R. K., Cardellichio C. B., Shapiro L. H., Look A. T., Holmes K. V. Human aminopeptidase N is a receptor for human coronavirus 229E. Nature. 1992 Jun 4;357(6377):420–422. doi: 10.1038/357420a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zsak L., Sugg N., Ben-Porat T., Robbins A. K., Whealy M. E., Enquist L. W. The gIII glycoprotein of pseudorabies virus is involved in two distinct steps of virus attachment. J Virol. 1991 Aug;65(8):4317–4324. doi: 10.1128/jvi.65.8.4317-4324.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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