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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Jun 15;88(12):5087–5091. doi: 10.1073/pnas.88.12.5087

Infection of polarized MDCK cells with herpes simplex virus 1: two asymmetrically distributed cell receptors interact with different viral proteins.

A E Sears 1, B S McGwire 1, B Roizman 1
PMCID: PMC51816  PMID: 1647025

Abstract

Herpes simplex virus 1 attaches to at least two cell surface receptors. In polarized epithelial (Madin-Darby canine kidney; MDCK) cells one receptor is located in the apical surface and attachment to the cells requires the presence of glycoprotein C in the virus. The second receptor is located in the basal surface and does not require the presence of glycoprotein C. Exposure of MDCK cells at either the apical or basal surface to wild-type virus yields plaques and viral products whereas infection by a glycoprotein C-negative mutant yields identical results only after exposure of MDCK cells to virus at the basal surface. Multiple receptors for viral entry into cells expand the host range of the virus. The observation that glycoprotein C-negative mutants are infectious in many nonpolarized cell lines suggests that cells in culture may express more than one receptor and explains why genes that specify the viral proteins that recognize redundant receptors, like glycoprotein C, are expendable.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. AURELIAN L., ROIZMAN B. ABORTIVE INFECTION OF CANINE CELLS BY HERPES SIMPLEX VIRUS. II. ALTERNATIVE SUPPRESSION OF SYNTHESIS OF INTERFERON AND VIRAL CONSTITUENTS. J Mol Biol. 1965 Mar;11:539–548. doi: 10.1016/s0022-2836(65)80009-2. [DOI] [PubMed] [Google Scholar]
  2. Ackermann M., Braun D. K., Pereira L., Roizman B. Characterization of herpes simplex virus 1 alpha proteins 0, 4, and 27 with monoclonal antibodies. J Virol. 1984 Oct;52(1):108–118. doi: 10.1128/jvi.52.1.108-118.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Campadelli-Fiume G., Stirpe D., Boscaro A., Avitabile E., Foá-Tomasi L., Barker D., Roizman B. Glycoprotein C-dependent attachment of herpes simplex virus to susceptible cells leading to productive infection. Virology. 1990 Sep;178(1):213–222. doi: 10.1016/0042-6822(90)90396-9. [DOI] [PubMed] [Google Scholar]
  4. Caplan M. J., Stow J. L., Newman A. P., Madri J., Anderson H. C., Farquhar M. G., Palade G. E., Jamieson J. D. Dependence on pH of polarized sorting of secreted proteins. Nature. 1987 Oct 15;329(6140):632–635. doi: 10.1038/329632a0. [DOI] [PubMed] [Google Scholar]
  5. Draper K. G., Costa R. H., Lee G. T., Spear P. G., Wagner E. K. Molecular basis of the glycoprotein-C-negative phenotype of herpes simplex virus type 1 macroplaque strain. J Virol. 1984 Sep;51(3):578–585. doi: 10.1128/jvi.51.3.578-585.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ejercito P. M., Kieff E. D., Roizman B. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J Gen Virol. 1968 May;2(3):357–364. doi: 10.1099/0022-1317-2-3-357. [DOI] [PubMed] [Google Scholar]
  7. HOGGAN M. D., ROIZMAN B., ROANE P. R., Jr Further studies of variants of herpes simplex virus that produce syncytia or pocklike lesions in cell cultures. Am J Hyg. 1961 Jan;73:114–122. doi: 10.1093/oxfordjournals.aje.a120162. [DOI] [PubMed] [Google Scholar]
  8. Heine J. W., Honess R. W., Cassai E., Roizman B. Proteins specified by herpes simplex virus. XII. The virion polypeptides of type 1 strains. J Virol. 1974 Sep;14(3):640–651. doi: 10.1128/jvi.14.3.640-651.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Kaner R. J., Baird A., Mansukhani A., Basilico C., Summers B. D., Florkiewicz R. Z., Hajjar D. P. Fibroblast growth factor receptor is a portal of cellular entry for herpes simplex virus type 1. Science. 1990 Jun 15;248(4961):1410–1413. doi: 10.1126/science.2162560. [DOI] [PubMed] [Google Scholar]
  11. Kousoulas K. G., Pellett P. E., Pereira L., Roizman B. Mutations affecting conformation or sequence of neutralizing epitopes identified by reactivity of viable plaques segregate from syn and ts domains of HSV-1(F) gB gene. Virology. 1984 Jun;135(2):379–394. doi: 10.1016/0042-6822(84)90194-6. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Langeland N., Moore L. J., Holmsen H., Haarr L. Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. J Gen Virol. 1988 Jun;69(Pt 6):1137–1145. doi: 10.1099/0022-1317-69-6-1137. [DOI] [PubMed] [Google Scholar]
  15. Longnecker R., Roizman B. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science. 1987 May 1;236(4801):573–576. doi: 10.1126/science.3033823. [DOI] [PubMed] [Google Scholar]
  16. Longnecker R., Roizman B. Generation of an inverting herpes simplex virus 1 mutant lacking the L-S junction a sequences, an origin of DNA synthesis, and several genes including those specifying glycoprotein E and the alpha 47 gene. J Virol. 1986 May;58(2):583–591. doi: 10.1128/jvi.58.2.583-591.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mavromara-Nazos P., Ackermann M., Roizman B. Construction and properties of a viable herpes simplex virus 1 recombinant lacking coding sequences of the alpha 47 gene. J Virol. 1986 Nov;60(2):807–812. doi: 10.1128/jvi.60.2.807-812.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McGeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., McNab D., Perry L. J., Scott J. E., Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol. 1988 Jul;69(Pt 7):1531–1574. doi: 10.1099/0022-1317-69-7-1531. [DOI] [PubMed] [Google Scholar]
  19. Pogue-Geile K. L., Spear P. G. The single base pair substitution responsible for the Syn phenotype of herpes simplex virus type 1, strain MP. Virology. 1987 Mar;157(1):67–74. doi: 10.1016/0042-6822(87)90314-x. [DOI] [PubMed] [Google Scholar]
  20. Post L. E., Roizman B. A generalized technique for deletion of specific genes in large genomes: alpha gene 22 of herpes simplex virus 1 is not essential for growth. Cell. 1981 Jul;25(1):227–232. doi: 10.1016/0092-8674(81)90247-6. [DOI] [PubMed] [Google Scholar]
  21. ROIZMAN B., AURELIAN L. ABORTIVE INFECTION OF CANINE CELLS BY HERPES SIMPLEX VIRUS. I. CHARACTERIZATION OF VIRAL PROGENY FROM CO-OPERATIVE INFECTION WITH MUTANTS DIFFERING IN CAPACITY TO MULTIPLY IN CANINE CELLS. J Mol Biol. 1965 Mar;11:528–538. doi: 10.1016/s0022-2836(65)80008-0. [DOI] [PubMed] [Google Scholar]
  22. Ruyechan W. T., Morse L. S., Knipe D. M., Roizman B. Molecular genetics of herpes simplex virus. II. Mapping of the major viral glycoproteins and of the genetic loci specifying the social behavior of infected cells. J Virol. 1979 Feb;29(2):677–697. doi: 10.1128/jvi.29.2.677-697.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Spring S. B., Roizman B., Schwartz J. Herpes simplex virus products in productive and abortive infection. II. Electron microscopic and immunological evidence for failure of virus envelopment as a cause of abortive infection. J Virol. 1968 Apr;2(4):384–392. doi: 10.1128/jvi.2.4.384-392.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Weber P. C., Levine M., Glorioso J. C. Rapid identification of nonessential genes of herpes simplex virus type 1 by Tn5 mutagenesis. Science. 1987 May 1;236(4801):576–579. doi: 10.1126/science.3033824. [DOI] [PubMed] [Google Scholar]
  25. 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]

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