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Journal of Virology logoLink to Journal of Virology
. 1990 Oct;64(10):4866–4872. doi: 10.1128/jvi.64.10.4866-4872.1990

Bovine cells expressing bovine herpesvirus 1 (BHV-1) glycoprotein IV resist infection by BHV-1, herpes simplex virus, and pseudorabies virus.

C C Chase 1, K Carter-Allen 1, C Lohff 1, G J Letchworth 3rd 1
PMCID: PMC247976  PMID: 2168973

Abstract

We expressed the bovine herpesvirus 1 (BHV-1) glycoprotein IV (gIV) in bovine cells. The protein expressed was identical in molecular mass and antigenic reactivity to the native gIV protein but was localized in the cytoplasm. Expressing cells were partially resistant to BHV-1, herpes simplex virus, and pseudorabies virus, as shown by a 10- to 1,000-fold-lower number of plaques forming on these cells than on control cells. The level of resistance depended on the level of gIV expression and the type and amount of challenge virus. These data are consistent with previous reports by others that cellular expression of the BHV-1 gIV homologs, herpes simplex virus glycoprotein D, and pseudorabies virus glycoprotein gp50 provide partial resistance against infection with these viruses. We have extended these findings by showing that once BHV-1 enters gIV-expressing cells, it replicates and spreads normally, as shown by the normal size of BHV-1 plaques and the delayed but vigorous synthesis of viral proteins. Our data are consistent with the binding of BHV-1 gIV to a cellular receptor required for initial penetration by all three herpesviruses and interference with the function of that receptor molecule.

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Selected References

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  1. Arsenakis M., Campadelli-Fiume G., Roizman B. Regulation of glycoprotein D synthesis: does alpha 4, the major regulatory protein of herpes simplex virus 1, regulate late genes both positively and negatively? J Virol. 1988 Jan;62(1):148–158. doi: 10.1128/jvi.62.1.148-158.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. Chase C. C., Carter-Allen K., Letchworth G. J., 3rd The effect of bovine herpesvirus type 1 glycoproteins gI and gIII on herpesvirus infections. J Gen Virol. 1989 Jun;70(Pt 6):1561–1569. doi: 10.1099/0022-1317-70-6-1561. [DOI] [PubMed] [Google Scholar]
  6. Eiden M., Newman M., Fisher A. G., Mann D. L., Howley P. M., Reitz M. S. Type 1 human T-cell leukemia virus small envelope protein expressed in mouse cells by using a bovine papilloma virus-derived shuttle vector. Mol Cell Biol. 1985 Nov;5(11):3320–3324. doi: 10.1128/mcb.5.11.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Godowski P. J., Knipe D. M. Transcriptional control of herpesvirus gene expression: gene functions required for positive and negative regulation. Proc Natl Acad Sci U S A. 1986 Jan;83(2):256–260. doi: 10.1073/pnas.83.2.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. 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]
  12. Kawamura I., Koga Y., Oh-Hori N., Onodera K., Kimura G., Nomoto K. Depletion of the surface CD4 molecule by the envelope protein of human immunodeficiency virus expressed in a human CD4+ monocytoid cell line. J Virol. 1989 Sep;63(9):3748–3754. doi: 10.1128/jvi.63.9.3748-3754.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Marshall R. L., Israel B. A., Letchworth G. J., 3rd Monoclonal antibody analysis of bovine herpesvirus-1 glycoprotein antigenic areas relevant to natural infection. Virology. 1988 Aug;165(2):338–347. doi: 10.1016/0042-6822(88)90578-8. [DOI] [PubMed] [Google Scholar]
  16. Marshall R. L., Rodriguez L. L., Letchworth G. J., 3rd Characterization of envelope proteins of infectious bovine rhinotracheitis virus (bovine herpesvirus 1) by biochemical and immunological methods. J Virol. 1986 Mar;57(3):745–753. doi: 10.1128/jvi.57.3.745-753.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Matthias P. D., Bernard H. U., Scott A., Brady G., Hashimoto-Gotoh T., Schütz G. A bovine papilloma virus vector with a dominant resistance marker replicates extrachromosomally in mouse and E. coli cells. EMBO J. 1983;2(9):1487–1492. doi: 10.1002/j.1460-2075.1983.tb01612.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McGeoch D. J., Dolan A., Donald S., Rixon F. J. Sequence determination and genetic content of the short unique region in the genome of herpes simplex virus type 1. J Mol Biol. 1985 Jan 5;181(1):1–13. doi: 10.1016/0022-2836(85)90320-1. [DOI] [PubMed] [Google Scholar]
  19. Noble A. G., Lee G. T., Sprague R., Parish M. L., Spear P. G. Anti-gD monoclonal antibodies inhibit cell fusion induced by herpes simplex virus type 1. Virology. 1983 Aug;129(1):218–224. doi: 10.1016/0042-6822(83)90409-9. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. van Drunen Littel-van den Hurk S., van den Hurk J. V., Babiuk L. A. Topographical analysis of bovine herpesvirus type-1 glycoproteins: use of monoclonal antibodies to identify and characterize functional epitopes. Virology. 1985 Jul 15;144(1):216–227. doi: 10.1016/0042-6822(85)90319-8. [DOI] [PubMed] [Google Scholar]
  22. van Drunen Littel-van den Hurk S., van den Hurk J. V., Gilchrist J. E., Misra V., Babiuk L. A. Interactions of monoclonal antibodies and bovine herpesvirus type 1 (BHV-1) glycoproteins: characterization of their biochemical and immunological properties. Virology. 1984 Jun;135(2):466–479. doi: 10.1016/0042-6822(84)90201-0. [DOI] [PubMed] [Google Scholar]

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