1887

Abstract

Pseudorabies virus (PRV)-infected blood monocytes are able to transport virus throughout the body of vaccination-immune pigs. PRV-infected monocytes express viral glycoproteins in their plasma membrane that can be recognized by virus-specific antibodies. Recently, it has been shown that addition of PRV-specific polyclonal immunoglobulins to PRV-infected monocytes at 37 °C induces internalization of the majority of plasma membrane-expressed viral glycoproteins. This study investigated whether this process may interfere with efficient antibody-dependent complement-mediated lysis (ADCML) of infected monocytes. Therefore, an ADCML assay was set up . A significant decrease in the percentage of cells lysed by ADCML was observed when antibody-induced internalization of PRV glycoproteins occurred (<0·005). Furthermore, it is shown (i) that the PRV gE–gI complex, which, like certain other alphaherpesvirus orthologues, possesses IgG-binding capacity, aids in avoiding efficient ADCML of PRV-infected monocytes and (ii) that the efficiency of PRV gE–gI-mediated evasion of ADCML can be decreased by the presence of gE–gI-specific antibodies.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18663-0
2003-04-01
2020-06-01
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/4/vir840939.html?itemId=/content/journal/jgv/10.1099/vir.0.18663-0&mimeType=html&fmt=ahah

References

  1. Albrecht J. C., Fleckenstein B.. 1992; New member of the multigene family of complement control proteins in herpesvirus saimiri. J Virol66:3937–3940
    [Google Scholar]
  2. Bitsch V., Eskildsen M.. 1982; Complement dependent neutralization of Aujeszky's disease virus by antibody. Curr Top Vet Med Anim Sci17:41–49
    [Google Scholar]
  3. Fanger N. A., Fanger M. W., Guyre P. M.. 1998; Fc receptors. In Encyclopedia of Immunology , 2nd edn. pp 886–891 Edited by Delves P. J., Roitt I. M.. San Diego: Academic Press;
    [Google Scholar]
  4. Favoreel H. W., Nauwynck H. J., Van Oostveldt P., Mettenleiter T. C., Pensaert M. B.. 1997; Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J Virol71:8254–8261
    [Google Scholar]
  5. Favoreel H. W., Nauwynck H. J., Halewyck H. M., Van Oostveldt P., Mettenleiter T. C., Pensaert M. B.. 1999; Antibody-induced endocytosis of viral glycoproteins and major histocompatibility complex class I on pseudorabies virus-infected monocytes. J Gen Virol80:1283–1291
    [Google Scholar]
  6. Favoreel H. W., Van Minnebruggen G., Nauwynck H. J., Enquist L. W., Pensaert M. B.. 2002; A tyrosine-based motif in the cytoplasmic tail of pseudorabies virus glycoprotein B is important for both antibody-induced internalization of viral glycoproteins and efficient cell-to-cell spread. J Virol76:6845–6851
    [Google Scholar]
  7. Frank I., Friedman H. M.. 1989; A novel function of the herpes simplex virus type I Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J Virol63:4479–4488
    [Google Scholar]
  8. Friedman H. M., Cohen G. H., Eisenberg R. J., Seidel C. A., Cines D. B.. 1984; Glycoprotein C of herpes simplex virus 1 acts as a receptor for the C3b complement component on infected cells. Nature309:633–635
    [Google Scholar]
  9. Friedman H. M., Wang L., Fishman N. O., Lambris J. D., Eisenberg R. J., Cohen G. H., Lubinski J.. 1996; Immune evasion properties of herpes simplex virus type I glycoprotein gC. J Virol70:4253–4260
    [Google Scholar]
  10. Friedman H. M., Wang L., Pangburn M. K., Lambris J. D., Lubinski J.. 2000; Novel mechanism of antibody-independent complement neutralization of herpes simplex virus type 1. J Immunol15:4528–4536
    [Google Scholar]
  11. Fries L. F., Friedman H. M., Cohen G. H., Eisenberg R. J., Hammer C. H., Frank M. M.. 1986; Glycoprotein C of herpes simplex virus 1 is an inhibitor of the complement cascade. J Immunol137:1636–1641
    [Google Scholar]
  12. Friguet B., Djavadi-Ohaniance L., Goldberg M. E.. 1998; Affinity. In Encyclopedia of Immunology , 2nd edn. pp 43–46 Edited by Delves P. J., Roitt I. M.. San Diego: Academic Press;
    [Google Scholar]
  13. Huemer H. P., Larcher C., van Drunen Littel-van den Hurk S., Babiuk L. A.. 1993; Species selective interaction of Alphaherpesvirinae with the ‘unspecific’ immune system of the host. Arch Virol130:353–364
    [Google Scholar]
  14. Isaacs S. N., Kotwal G. J., Moss B.. 1992; Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence. Proc Natl Acad Sci U S A89:628–632
    [Google Scholar]
  15. Johnson D. C., Frame M. C., Ligas M. W., Cross A. M., Stow N. D.. 1988; Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J Virol62:1347–1354
    [Google Scholar]
  16. Joseph B. S., Cooper N. R., Oldstone M. B. A.. 1975; Immunologic injury of cultured cells infected with measles virus. I. Role of IgG antibody and the alternative complement pathway. J Exp Med141:761–774
    [Google Scholar]
  17. Kapadia S. B., Molina H., van Berkel V., Speck S. H., Virgin H. W. IV. 1999; Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J Virol73:7658–7670
    [Google Scholar]
  18. Kaplan A. S., Vatter A. E.. 1959; A comparison of herpes simplex and pseudorabies virus. Virology7:394–407
    [Google Scholar]
  19. Kimman T. G., Brouwers R. A. M., Daus F. J., van Oirschot J. T., van Zaane D.. 1992; Measurement of isotype-specific antibody responses to Aujeszky's disease virus in sera and mucosal secretions of pigs. Vet Immunol Immunopathol31:95–113
    [Google Scholar]
  20. Litwin V., Jackson W., Grose C.. 1992; Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J Virol66:3643–3651
    [Google Scholar]
  21. Lubinski J., Wang L., Mastellos D., Sahu A., Lambris J. D., Friedman H. M.. 1999; In vivo role of complement-interacting domains of herpes simplex virus type 1 glycoprotein gC. J Exp Med190:1637–1646
    [Google Scholar]
  22. McFerran J. B., Dow C.. 1975; Studies on immunisation of pigs with the Bartha strain of Aujeszky's disease virus. Res Vet Sci19:17–22
    [Google Scholar]
  23. Mettenleiter T. C., Schreurs C., Zuckermann F., Ben-Porat T.. 1987; Role of pseudorabies virus glycoprotein gI in virus release from infected cells. J Virol61:2764–2769
    [Google Scholar]
  24. Mold C., Bradt B. M., Nemerow G. R., Cooper N. R.. 1988; Epstein–Barr virus regulates activation and processing of the third component of complement. J Exp Med168:949–969
    [Google Scholar]
  25. Müller-Eberhard H. J.. 1984; The membrane attack complex. Springer Semin Immunopathol7:93–141
    [Google Scholar]
  26. Nagashunmugam T., Lubinski J., Wang L., Goldstein L. T., Weeks B. S., Sundaresan P., Kang E. H., Dubin G., Friedman H. M.. 1998; In vivo immune evasion mediated by the herpes simplex virus type I immunoglobulin G Fc receptor. J Virol72:5351–5359
    [Google Scholar]
  27. Nauwynck H. J., Pensaert M. B.. 1992; Abortion induced by cell-associated pseudorabies virus in vaccinated sows. Am J Vet Res53:489–493
    [Google Scholar]
  28. Nauwynck H. J., Pensaert M. B.. 1995a; Cell-free and cell-associated viremia in pigs after oronasal infection with Aujeszky's disease virus. Vet Microbiol43:307–314
    [Google Scholar]
  29. Nauwynck H. J., Pensaert M. B.. 1995b; Effect of specific antibodies on the cell-associated spread of pseudorabies virus in monolayers of different cell types. Arch Virol140:1137–1146
    [Google Scholar]
  30. Pangburn M. K., Müller-Eberhard H. J.. 1984; The alternative pathway of complement. Springer Semin Immunopathol7:163–192
    [Google Scholar]
  31. Pensaert M. B., Kluge J. P.. 1989; Pseudorabies virus (Aujeszky's Disease). In Virus Infections of Porcines pp 39–64 Edited by Pensaert M. B.. Oxford: Elsevier Science;
    [Google Scholar]
  32. Pescovitz M. D., Lunney J. K., Sachs D. H.. 1984; Preparation and characterization of monoclonal antibodies reactive with porcine PBL. J Immunol133:368–375
    [Google Scholar]
  33. Russo J. J., Bohenzky R. A., Chien M. C.. 8 other authors 1996; Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A93:14862–14867
    [Google Scholar]
  34. Saifuddin M., Hedayati T., Atkinson J. P., Holguin M. H., Parker C. J., Spear G. T.. 1997; Human immunodeficiency virus type 1 incorporates both glycosyl phosphatidylinositol-anchored CD55 and CD59 and integral membrane CD64 at levels that protect from complement-mediated destruction. J Gen Virol78:1907–1911
    [Google Scholar]
  35. Sim R. B., Dodds A. W.. 1997; Complement A Practical Approach. pp 1–18 Edited by Dodds A. W., Sim R. B.. Oxford: IRL;
  36. Sissons J. G., Oldstone M. B.. 1980; Antibody-mediated destruction of virus-infected cells. Adv Immunol29:209–260
    [Google Scholar]
  37. Spiller O. B., Morgan B. P., Tufaro F., Devine D. V.. 1996; Altered expression of host-encoded complement regulators on human cytomegalovirus-infected cells. Eur J Immunol26:1532–1538
    [Google Scholar]
  38. Van de Walle G. R., Favoreel H. W., Nauwynck H. J., Van Oostveldt P., Pensaert M. B.. 2001; Involvement of cellular cytoskeleton components in antibody-induced internalization of viral glycoproteins in pseudorabies virus-infected monocytes. Virology288:129–138
    [Google Scholar]
  39. Whealy M. E., Card J. P., Robbins A. K., Dubin J. R., Rziha H. J., Enquist L. W.. 1993; Specific pseudorabies virus infection of the rat visual system requires both gI and gp63 glycoproteins. J Virol67:3786–3797
    [Google Scholar]
  40. Wittmann G., Jakubik J., Ahl R.. 1980; Multiplication and distribution of Aujeszky's disease (pseudorabies) virus in vaccinated and non-vaccinated pigs after intranasal infection. Arch Virol66:227–240
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18663-0
Loading
/content/journal/jgv/10.1099/vir.0.18663-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error