Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1997 Nov;71(11):8254–8261. doi: 10.1128/jvi.71.11.8254-8261.1997

Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells.

H W Favoreel 1, H J Nauwynck 1, P Van Oostveldt 1, T C Mettenleiter 1, M B Pensaert 1
PMCID: PMC192283  PMID: 9343177

Abstract

Fluorescein isothiocyanate-labeled porcine pseudorabies virus (PrV) polyclonal antibodies were added to PrV-infected swine kidney cells in vitro at 37 degrees C. In approximately 47% of the infected cells, the addition induced passive patching and subsequent energy- and microtubule-dependent capping of all viral envelope glycoproteins, expressed on the plasma membranes of the infected cells. Further contraction and extrusion of the capped viral glycoproteins occurred in approximately 30% of the capped cells 2 h after the addition of antibodies and was accompanied by a concentration of F-actin beneath the caps. At that time, about 18% of the extruded caps were shed spontaneously into the surrounding medium. Mechanical force released 85% of the extruded caps, leaving viable cells with no microscopically detectable levels of viral glycoproteins on their plasma membranes. Experiments with PrV deletion mutants showed that viral glycoproteins gE and gI are important in triggering viral glycoprotein redistribution. Since the PrV gE-gI complex exhibits Fc receptor activity which facilitates capping, the importance of gE and gI may be partially explained by antibody bipolar bridging.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Arhets P., Gounon P., Sansonetti P., Guillén N. Myosin II is involved in capping and uroid formation in the human pathogen Entamoeba histolytica. Infect Immun. 1995 Nov;63(11):4358–4367. doi: 10.1128/iai.63.11.4358-4367.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Banks T. A., Rouse B. T. Herpesviruses--immune escape artists? Clin Infect Dis. 1992 Apr;14(4):933–941. doi: 10.1093/clinids/14.4.933. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Bourguignon L. Y., Bourguignon G. J. Capping and the cytoskeleton. Int Rev Cytol. 1984;87:195–224. doi: 10.1016/s0074-7696(08)62443-2. [DOI] [PubMed] [Google Scholar]
  5. Calderón J., Avila E. E. Antibody-induced caps in Entamoeba histolytica: isolation and electrophoretic analysis. J Infect Dis. 1986 May;153(5):927–932. doi: 10.1093/infdis/153.5.927. [DOI] [PubMed] [Google Scholar]
  6. Calderón J., de Lourdes Muñoz M., Acosta H. M. Surface redistribution and release of antibody-induced caps in entamoebae. J Exp Med. 1980 Jan 1;151(1):184–193. doi: 10.1084/jem.151.1.184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chanh T. C., Alderete B. E. A rapid method for quantitating lymphocyte receptor capping: capping defect in AIDS patients. J Virol Methods. 1990 Sep;29(3):257–265. doi: 10.1016/0166-0934(90)90053-i. [DOI] [PubMed] [Google Scholar]
  8. Dijkstra J. M., Visser N., Mettenleiter T. C., Klupp B. G. Identification and characterization of pseudorabies virus glycoprotein gM as a nonessential virion component. J Virol. 1996 Aug;70(8):5684–5688. doi: 10.1128/jvi.70.8.5684-5688.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Edidin M., Kuo S. C., Sheetz M. P. Lateral movements of membrane glycoproteins restricted by dynamic cytoplasmic barriers. Science. 1991 Nov 29;254(5036):1379–1382. doi: 10.1126/science.1835798. [DOI] [PubMed] [Google Scholar]
  10. Espinosa-Cantellano M., Chávez B., Calderón J., Martínez-Palomo A. Entamoeba histolytica: electrophoretic analysis of isolated caps induced by several ligands. Arch Med Res. 1992;23(2):81–85. [PubMed] [Google Scholar]
  11. Espinosa-Cantellano M., Martínez-Palomo A. Entamoeba histolytica: mechanism of surface receptor capping. Exp Parasitol. 1994 Nov;79(3):424–435. doi: 10.1006/expr.1994.1104. [DOI] [PubMed] [Google Scholar]
  12. Frank I., Friedman H. M. A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J Virol. 1989 Nov;63(11):4479–4488. doi: 10.1128/jvi.63.11.4479-4488.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hanssens F. P., Nauwynck H. J., Pensaert M. B. Involvement of membrane-bound viral glycoproteins in adhesion of pseudorabies virus-infected cells. J Virol. 1993 Aug;67(8):4492–4496. doi: 10.1128/jvi.67.8.4492-4496.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Johnson D. C., Frame M. C., Ligas M. W., Cross A. M., Stow N. D. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol. 1988 Apr;62(4):1347–1354. doi: 10.1128/jvi.62.4.1347-1354.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson D. C., Spear P. G. Monensin inhibits the processing of herpes simplex virus glycoproteins, their transport to the cell surface, and the egress of virions from infected cells. J Virol. 1982 Sep;43(3):1102–1112. doi: 10.1128/jvi.43.3.1102-1112.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KAPLAN A. S., VATTER A. E. A comparison of herpes simplex and pseudorabies viruses. Virology. 1959 Apr;7(4):394–407. doi: 10.1016/0042-6822(59)90068-6. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Litwin V., Jackson W., Grose C. Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J Virol. 1992 Jun;66(6):3643–3651. doi: 10.1128/jvi.66.6.3643-3651.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Luton F., Buferne M., Davoust J., Schmitt-Verhulst A. M., Boyer C. Evidence for protein tyrosine kinase involvement in ligand-induced TCR/CD3 internalization and surface redistribution. J Immunol. 1994 Jul 1;153(1):63–72. [PubMed] [Google Scholar]
  20. Martin J., Sugden B. Transformation by the oncogenic latent membrane protein correlates with its rapid turnover, membrane localization, and cytoskeletal association. J Virol. 1991 Jun;65(6):3246–3258. doi: 10.1128/jvi.65.6.3246-3258.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Mettenleiter T. C., Schreurs C., Zuckermann F., Ben-Porat T., Kaplan A. S. Role of glycoprotein gIII of pseudorabies virus in virulence. J Virol. 1988 Aug;62(8):2712–2717. doi: 10.1128/jvi.62.8.2712-2717.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mettenleiter T. C., Schreurs C., Zuckermann F., Ben-Porat T. Role of pseudorabies virus glycoprotein gI in virus release from infected cells. J Virol. 1987 Sep;61(9):2764–2769. doi: 10.1128/jvi.61.9.2764-2769.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mettenleiter T. C., Zsak L., Kaplan A. S., Ben-Porat T., Lomniczi B. Role of a structural glycoprotein of pseudorabies in virus virulence. J Virol. 1987 Dec;61(12):4030–4032. doi: 10.1128/jvi.61.12.4030-4032.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Nauwynck H. J., Pensaert M. B. Effect of specific antibodies on the cell-associated spread of pseudorabies virus in monolayers of different cell types. Arch Virol. 1995;140(6):1137–1146. doi: 10.1007/BF01315422. [DOI] [PubMed] [Google Scholar]
  27. Nawynck H. J., Pensaert M. B. Cell-free and cell-associated viremia in pigs after oronasal infection with Aujeszky's disease virus. Vet Microbiol. 1995 Mar;43(4):307–314. doi: 10.1016/0378-1135(94)00103-4. [DOI] [PubMed] [Google Scholar]
  28. Olson J. K., Bishop G. A., Grose C. Varicella-zoster virus Fc receptor gE glycoprotein: serine/threonine and tyrosine phosphorylation of monomeric and dimeric forms. J Virol. 1997 Jan;71(1):110–119. doi: 10.1128/jvi.71.1.110-119.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Park J. G., Schreiber A. D. Determinants of the phagocytic signal mediated by the type IIIA Fc gamma receptor, Fc gamma RIIIA: sequence requirements and interaction with protein-tyrosine kinases. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7381–7385. doi: 10.1073/pnas.92.16.7381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Rauh I., Weiland F., Fehler F., Keil G. M., Mettenleiter T. C. Pseudorabies virus mutants lacking the essential glycoprotein gII can be complemented by glycoprotein gI of bovine herpesvirus 1. J Virol. 1991 Feb;65(2):621–631. doi: 10.1128/jvi.65.2.621-631.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Reth M. Antigen receptor tail clue. Nature. 1989 Mar 30;338(6214):383–384. doi: 10.1038/338383b0. [DOI] [PubMed] [Google Scholar]
  35. Schreiner G. F., Fujiwara K., Pollard T. D., Unanue E. R. Redistribution of myosin accompanying capping of surface Ig. J Exp Med. 1977 May 1;145(5):1393–1398. doi: 10.1084/jem.145.5.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Yakara I., Kakimoto-Sameshima F. Microtubule organization of lymphocytes and its modulation by patch and cap formation. Cell. 1978 Sep;15(1):251–259. doi: 10.1016/0092-8674(78)90100-9. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Zuckermann F. A., Mettenleiter T. C., Schreurs C., Sugg N., Ben-Porat T. Complex between glycoproteins gI and gp63 of pseudorabies virus: its effect on virus replication. J Virol. 1988 Dec;62(12):4622–4626. doi: 10.1128/jvi.62.12.4622-4626.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES