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. 1993 Aug;67(8):4492–4496. doi: 10.1128/jvi.67.8.4492-4496.1993

Involvement of membrane-bound viral glycoproteins in adhesion of pseudorabies virus-infected cells.

F P Hanssens 1, H J Nauwynck 1, M B Pensaert 1
PMCID: PMC237832  PMID: 8392594

Abstract

Cell-associated spread of pseudorabies virus (PrV) plays an important role in the pathogenesis of the disease. Besides the already known direct cell-to-cell spread of the virus in monolayers, adhesion and subsequent fusion of suspended PrV infected cells to monolayers of uninfected cells are thought to occur. To study the adhesion of PrV-infected cells, an in vitro model was developed in SK-6 cells. Specific adhesion of PrV-infected cells to an uninfected monolayer started 5 h after infection of the cells and reached a maximum 6 h later. A correlation was found between the surface expression of PrV glycoproteins on the infected cells and the adhesion of these cells. PrV hyperimmune serum completely inhibited binding of the infected cells. To investigate which PrV envelope glycoproteins were responsible for the cell adhesion, the infected cells were incubated with antisera against glycoproteins gII, gIII, and gp50. Antiserum against either gII or gIII inhibited cell adhesion, and antisera against gII and gIII together had a cooperative effect. Antiserum against gp50 had no effect on binding when used alone but enhanced the inhibition induced by gII and gIII antisera. Heparin and neomycin inhibited adhesion, showing that the receptor for adhesion was a heparinlike substance. SK-6 cells infected with a gIII deletion mutant of PrV exhibited a much lower adhesion. This binding was heparin and neomycin independent and was not blocked by anti-gII serum. Nevertheless, it was completely inhibited with PrV hyperimmune serum and with anti-gp50 serum. This finding demonstrates that the ligand for adhesion of gIII(-)-infected cells is glycoprotein gp50. These results strongly suggest that the mechanism for adhesion of a PrV-infected cell to an uninfected monolayer is similar to the mechanism of adsorption and penetration of a PrV virion to a host cell.

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Selected References

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  1. Ben-Porat T., DeMarchi J. M., Lomniczi B., Kaplan A. S. Role of glycoproteins of pseudorabies virus in eliciting neutralizing antibodies. Virology. 1986 Oct 30;154(2):325–334. doi: 10.1016/0042-6822(86)90458-7. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Campadelli-Fiume G., Avitabile E., Fini S., Stirpe D., Arsenakis M., Roizman B. Herpes simplex virus glycoprotein D is sufficient to induce spontaneous pH-independent fusion in a cell line that constitutively expresses the glycoprotein. Virology. 1988 Oct;166(2):598–602. doi: 10.1016/0042-6822(88)90533-8. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Eloit M., Bouzghaia H., Toma B. Identification of antigenic sites on pseudorabies virus glycoprotein gp50 implicated in virus penetration of the host cell. J Gen Virol. 1990 Sep;71(Pt 9):2179–2183. doi: 10.1099/0022-1317-71-9-2179. [DOI] [PubMed] [Google Scholar]
  6. Gompels U., Minson A. The properties and sequence of glycoprotein H of herpes simplex virus type 1. Virology. 1986 Sep;153(2):230–247. doi: 10.1016/0042-6822(86)90026-7. [DOI] [PubMed] [Google Scholar]
  7. Heine J. W., Spear P. G., Roizman B. Proteins specified by herpes simplex virus. VI. Viral proteins in the plasma membrane. J Virol. 1972 Mar;9(3):431–439. doi: 10.1128/jvi.9.3.431-439.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Keller P. M., Davison A. J., Lowe R. S., Riemen M. W., Ellis R. W. Identification and sequence of the gene encoding gpIII, a major glycoprotein of varicella-zoster virus. Virology. 1987 Apr;157(2):526–533. doi: 10.1016/0042-6822(87)90295-9. [DOI] [PubMed] [Google Scholar]
  9. Klupp B. G., Visser N., Mettenleiter T. C. Identification and characterization of pseudorabies virus glycoprotein H. J Virol. 1992 May;66(5):3048–3055. doi: 10.1128/jvi.66.5.3048-3055.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Langeland N., Holmsen H., Lillehaug J. R., Haarr L. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J Virol. 1987 Nov;61(11):3388–3393. doi: 10.1128/jvi.61.11.3388-3393.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Mettenleiter T. C., Lukàcs N., Rziha H. J. Pseudorabies virus avirulent strains fail to express a major glycoprotein. J Virol. 1985 Oct;56(1):307–311. doi: 10.1128/jvi.56.1.307-311.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mettenleiter T. C., Lukàcs N., Thiel H. J., Schreurs C., Rziha H. J. Location of the structural gene of pseudorabies virus glycoprotein complex gII. Virology. 1986 Jul 15;152(1):66–75. doi: 10.1016/0042-6822(86)90372-7. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Nauwynck H. J., Pensaert M. B. Abortion induced by cell-associated pseudorabies virus in vaccinated sows. Am J Vet Res. 1992 Apr;53(4):489–493. [PubMed] [Google Scholar]
  16. Peeters B., de Wind N., Broer R., Gielkens A., Moormann R. Glycoprotein H of pseudorabies virus is essential for entry and cell-to-cell spread of the virus. J Virol. 1992 Jun;66(6):3888–3892. doi: 10.1128/jvi.66.6.3888-3892.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. Petrovskis E. A., Timmins J. G., Armentrout M. A., Marchioli C. C., Yancey R. J., Jr, Post L. E. DNA sequence of the gene for pseudorabies virus gp50, a glycoprotein without N-linked glycosylation. J Virol. 1986 Aug;59(2):216–223. doi: 10.1128/jvi.59.2.216-223.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Petrovskis E. A., Timmins J. G., Gierman T. M., Post L. E. Deletions in vaccine strains of pseudorabies virus and their effect on synthesis of glycoprotein gp63. J Virol. 1986 Dec;60(3):1166–1169. doi: 10.1128/jvi.60.3.1166-1169.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Petrovskis E. A., Timmins J. G., Post L. E. Use of lambda gt11 to isolate genes for two pseudorabies virus glycoproteins with homology to herpes simplex virus and varicella-zoster virus glycoproteins. J Virol. 1986 Oct;60(1):185–193. doi: 10.1128/jvi.60.1.185-193.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Rea T. J., Timmins J. G., Long G. W., Post L. E. Mapping and sequence of the gene for the pseudorabies virus glycoprotein which accumulates in the medium of infected cells. J Virol. 1985 Apr;54(1):21–29. doi: 10.1128/jvi.54.1.21-29.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Robbins A. K., Dorney D. J., Wathen M. W., Whealy M. E., Gold C., Watson R. J., Holland L. E., Weed S. D., Levine M., Glorioso J. C. The pseudorabies virus gII gene is closely related to the gB glycoprotein gene of herpes simplex virus. J Virol. 1987 Sep;61(9):2691–2701. doi: 10.1128/jvi.61.9.2691-2701.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robbins A. K., Watson R. J., Whealy M. E., Hays W. W., Enquist L. W. Characterization of a pseudorabies virus glycoprotein gene with homology to herpes simplex virus type 1 and type 2 glycoprotein C. J Virol. 1986 May;58(2):339–347. doi: 10.1128/jvi.58.2.339-347.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robbins A. K., Whealy M. E., Watson R. J., Enquist L. W. Pseudorabies virus gene encoding glycoprotein gIII is not essential for growth in tissue culture. J Virol. 1986 Sep;59(3):635–645. doi: 10.1128/jvi.59.3.635-645.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Spear P. G., Kellejmroian B. Proteins spcified by herpes simplex virus. II. Viral glycoprotins associated with cellular membranes. J Virol. 1970 Feb;5(2):123–131. doi: 10.1128/jvi.5.2.123-131.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vandeputte J., Chappuis G., Fargeaud D., Précausta P., Guillemin F., Brun A., Desmettre P., Stellmann C. Vaccination against pseudorabies with glycoprotein gI+ or glycoprotein gI- vaccine. Am J Vet Res. 1990 Jul;51(7):1100–1106. [PubMed] [Google Scholar]
  30. Wathen M. W., Wathen L. M. Isolation, characterization, and physical mapping of a pseudorabies virus mutant containing antigenically altered gp50. J Virol. 1984 Jul;51(1):57–62. doi: 10.1128/jvi.51.1.57-62.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wittmann G., Jakubik J., Ahl R. Multiplication and distribution of Aujeszky's disease (pseudorabies) virus in vaccinated and non-vaccinated pigs after intranasal infection. Arch Virol. 1980;66(3):227–240. doi: 10.1007/BF01314736. [DOI] [PubMed] [Google Scholar]
  32. Zsak L., Zuckermann F., Sugg N., Ben-Porat T. Glycoprotein gI of pseudorabies virus promotes cell fusion and virus spread via direct cell-to-cell transmission. J Virol. 1992 Apr;66(4):2316–2325. doi: 10.1128/jvi.66.4.2316-2325.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Zuckermann F., Zsak L., Reilly L., Sugg N., Ben-Porat T. Early interactions of pseudorabies virus with host cells: functions of glycoprotein gIII. J Virol. 1989 Aug;63(8):3323–3329. doi: 10.1128/jvi.63.8.3323-3329.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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