1887

Abstract

Antibody is an important antiviral defence. However, it is considered to do little against human gamma-herpesviruses, which establish predominantly latent infections regulated by T cells. One limitation on analysing these infections has been that latency is already well-established at clinical presentation; early infection may still be accessible to antibody. Here, using murid herpesvirus-4 (MuHV-4), we tested the impact of adoptively transferred antibody on early gamma-herpesvirus infection. Immune sera and neutralizing and non-neutralizing monoclonal antibodies (mAbs) all reduced acute lytic MuHV-4 replication. The reductions, even by neutralizing mAbs, were largely or completely dependent on host IgG Fc receptors. Therefore, passive antibody can blunt acute gamma-herpesvirus lytic infection, and does this principally by IgG Fc-dependent functions rather than by neutralization.

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2009-11-01
2024-04-19
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References

  1. Adler H., Messerle M., Wagner M., Koszinowski U. H. 2000; Cloning and mutagenesis of the murine gammaherpesvirus 68 genome as an infectious bacterial artificial chromosome. J Virol 74:6964–6974 [CrossRef]
    [Google Scholar]
  2. Balachandran N., Bacchetti S., Rawls W. E. 1982; Protection against lethal challenge of BALB/c mice by passive transfer of monoclonal antibodies to five glycoproteins of herpes simplex virus type 2. Infect Immun 37:1132–1137
    [Google Scholar]
  3. Beisel C., Tanner J., Matsuo T., Thorley-Lawson D., Kezdy F., Kieff E. 1985; Two major outer envelope glycoproteins of Epstein–Barr virus are encoded by the same gene. J Virol 54:665–674
    [Google Scholar]
  4. Callan M. F., Steven N., Krausa P., Wilson J. D., Moss P. A., Gillespie G. M., Bell J. I., Rickinson A. B., McMichael A. J. 1996; Large clonal expansions of CD8+ T cells in acute infectious mononucleosis. Nat Med 2:906–911 [CrossRef]
    [Google Scholar]
  5. Carneiro-Sampaio M., Coutinho A. 2007; Immunity to microbes: lessons from primary immunodeficiencies. Infect Immun 75:1545–1555 [CrossRef]
    [Google Scholar]
  6. Chu C. F., Meador M. G., Young C. G., Strasser J. E., Bourne N., Milligan G. N. 2008; Antibody-mediated protection against genital herpes simplex virus type 2 disease in mice by Fc gamma receptor-dependent and -independent mechanisms. J Reprod Immunol 78:58–67 [CrossRef]
    [Google Scholar]
  7. de Lima B. D., May J. S., Stevenson P. G. 2004; Murine gammaherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo . J Virol 78:5103–5112 [CrossRef]
    [Google Scholar]
  8. Dingwell K. S., Brunetti C. R., Hendricks R. L., Tang Q., Tang M., Rainbow A. J., Johnson D. C. 1994; Herpes simplex virus glycoproteins E and I facilitate cell-to-cell spread in vivo and across junctions of cultured cells. J Virol 68:834–845
    [Google Scholar]
  9. Faulkner G. C., Burrows S. R., Khanna R., Moss D. J., Bird A. G., Crawford D. H. 1999; X-linked agammaglobulinemia patients are not infected with Epstein–Barr virus: implications for the biology of the virus. J Virol 73:1555–1564
    [Google Scholar]
  10. Gangappa S., Kapadia S. B., Speck S. H., Virgin H. W. 2002; Antibody to a lytic cycle viral protein decreases gammaherpesvirus latency in B-cell-deficient mice. J Virol 76:11460–11468 [CrossRef]
    [Google Scholar]
  11. Gill M. B., Gillet L., Colaco S., May J. S., de Lima B. D., Stevenson P. G. 2006; Murine gammaherpesvirus-68 glycoprotein H–glycoprotein L complex is a major target for neutralizing monoclonal antibodies. J Gen Virol 87:1465–1475 [CrossRef]
    [Google Scholar]
  12. Gill M. B., Edgar R., May J. S., Stevenson P. G. 2008; A gamma-herpesvirus glycoprotein complex manipulates actin to promote viral spread. PLoS ONE 3:e1808 [CrossRef]
    [Google Scholar]
  13. Gillet L., Stevenson P. G. 2007a; Antibody evasion by the N terminus of murid herpesvirus-4 glycoprotein B. EMBO J 26:5131–5142 [CrossRef]
    [Google Scholar]
  14. Gillet L., Stevenson P. G. 2007b; Evidence for a multi-protein gamma-2-herpesvirus entry complex. J Virol 81:13082–13091 [CrossRef]
    [Google Scholar]
  15. Gillet L., Gill M. B., Colaco S., Smith C. M., Stevenson P. G. 2006; Murine gammaherpesvirus-68 glycoprotein B presents a difficult neutralization target to monoclonal antibodies derived from infected mice. J Gen Virol 87:3515–3527 [CrossRef]
    [Google Scholar]
  16. Gillet L., May J. S., Stevenson P. G. 2007a; Post-exposure vaccination improves gammaherpesvirus neutralization. PLoS One 2:e899 [CrossRef]
    [Google Scholar]
  17. Gillet L., May J. S., Colaco S., Stevenson P. G. 2007b; The murine gammaherpesvirus-68 gp150 acts as an immunogenic decoy to limit virion neutralization. PLoS One 2:e705 [CrossRef]
    [Google Scholar]
  18. Gillet L., Adler H., Stevenson P. G. 2007c; Glycosaminoglycan interactions in murine gammaherpesvirus-68 infection. PLoS One 2:e347 [CrossRef]
    [Google Scholar]
  19. Gillet L., May J. S., Colaco S., Stevenson P. G. 2007d; Glycoprotein L disruption reveals two functional forms of the murine gammaherpesvirus 68 glycoprotein H. J Virol 81:280–291 [CrossRef]
    [Google Scholar]
  20. Gillet L., Colaco S., Stevenson P. G. 2008a; The murid herpesvirus-4 gL regulates an entry-associated conformation change in gH. PLoS One 3:e2811 [CrossRef]
    [Google Scholar]
  21. Gillet L., Colaco S., Stevenson P. G. 2008b; Glycoprotein B switches conformation during murid herpesvirus 4 entry. J Gen Virol 89:1352–1363 [CrossRef]
    [Google Scholar]
  22. Gillet L., Colaco S., Stevenson P. G. 2008c; The murid herpesvirus-4 gH/gL binds to glycosaminoglycans. PLoS One 3:e1669 [CrossRef]
    [Google Scholar]
  23. Gillet L., Alenquer M., Glauser D. L., Colaco S., May J. S., Stevenson P. G. 2009; Glycoprotein L sets the neutralization profile of murid herpesvirus-4. J Gen Virol 90:1202–1214 [CrossRef]
    [Google Scholar]
  24. Hoagland R. J. 1964; The incubation period of infectious mononucleosis. Am J Public Health Nations Health 54:1699–1705 [CrossRef]
    [Google Scholar]
  25. Hooks J. J., Burns W., Hayashi K., Geis S., Notkins A. L. 1976; Viral spread in the presence of neutralizing antibody: mechanisms of persistence in foamy virus infection. Infect Immun 14:1172–1178
    [Google Scholar]
  26. Ishizaka S. T., Piacente P., Silva J., Mishkin E. M. 1995; IgG subtype is correlated with efficiency of passive protection and effector function of anti-herpes simplex virus glycoprotein D monoclonal antibodies. J Infect Dis 172:1108–1111 [CrossRef]
    [Google Scholar]
  27. Johansson P. J. H., Myhre E. B., Blomberg J. 1985; Specificity of Fc receptors induced by herpes simplex virus type 1: comparison of immunoglobulin G from different animal species. J Virol 56:489–494
    [Google Scholar]
  28. Julenius K., Mølgaard A., Gupta R., Brunak S. 2005; Prediction, conservation analysis and structural characterization of mammalian mucin-type O -glycosylation sites. Glycobiology 15:153–164
    [Google Scholar]
  29. Kapadia S. B., Molina H., van Berkel V., Speck S. H., Virgin H. W. 1999; Murine gammaherpesvirus 68 encodes a functional regulator of complement activation. J Virol 73:7658–7670
    [Google Scholar]
  30. Kim I. J., Flaño E., Woodland D. L., Blackman M. A. 2002; Antibody-mediated control of persistent gamma-herpesvirus infection. J Immunol 168:3958–3964 [CrossRef]
    [Google Scholar]
  31. Köhler G., Milstein C. 1975; Continuous cultures of fused cells secreting antibody of predefined specificity. Nature 256:495–497 [CrossRef]
    [Google Scholar]
  32. Kozuch O., Reichel M., Lesso J., Remenová A., Labuda M., Lysy J., Mistríková J. 1993; Further isolation of murine herpesviruses from small mammals in southwestern Slovakia. Acta Virol 37:101–105
    [Google Scholar]
  33. Kümel G., Kaerner H. C., Levine M., Schröder C. H., Glorioso J. C. 1985; Passive immune protection by herpes simplex virus-specific monoclonal antibodies and monoclonal antibody-resistant mutants altered in pathogenicity. J Virol 56:930–937
    [Google Scholar]
  34. Mancini G., Carbonara A. O., Heremans J. F. 1965; Immunochemical quantitation of antigens by single radial immunodiffusion. Immunochemistry 2:235–254 [CrossRef]
    [Google Scholar]
  35. May J. S., Colaco S., Stevenson P. G. 2005a; Glycoprotein M is an essential lytic replication protein of the murine gammaherpesvirus 68. J Virol 79:3459–3467 [CrossRef]
    [Google Scholar]
  36. May J. S., Coleman H. M., Boname J. M., Stevenson P. G. 2005b; Murine gammaherpesvirus-68 ORF28 encodes a non-essential virion glycoprotein. J Gen Virol 86:919–928 [CrossRef]
    [Google Scholar]
  37. May J. S., Walker J., Colaco S., Stevenson P. G. 2005c; The murine gammaherpesvirus 68 ORF27 gene product contributes to intercellular viral spread. J Virol 79:5059–5068 [CrossRef]
    [Google Scholar]
  38. McKendall R. R. 1985; IgG-mediated viral clearance in experimental infection with herpes simplex virus type 1: role for neutralization and Fc-dependent functions but not C′ cytolysis and C5 chemotaxis. J Infect Dis 151:464–470 [CrossRef]
    [Google Scholar]
  39. Milho R., Smith C. M., Marques S., Alenquer M., May J. S., Gillet L., Gaspar M., Efstathiou S., Simas J. P., Stevenson P. G. 2009; In vivo imaging of murid herpesvirus-4 infection. J Gen Virol 90:21–32 [CrossRef]
    [Google Scholar]
  40. Minson A. C., Hodgman T. C., Digard P., Hancock D. C., Bell S. E., Buckmaster E. A. 1986; An analysis of the biological properties of monoclonal antibodies against glycoprotein D of herpes simplex virus and identification of amino acid substitutions that confer resistance to neutralization. J Gen Virol 67:1001–1013 [CrossRef]
    [Google Scholar]
  41. Nash A. A., Dutia B. M., Stewart J. P., Davison A. J. 2001; Natural history of murine gamma-herpesvirus infection. Philos Trans R Soc Lond B Biol Sci 356:569–579 [CrossRef]
    [Google Scholar]
  42. Nimmerjahn F., Ravetch J. V. 2008; Fc γ receptors as regulators of immune responses. Nat Rev Immunol 8:34–47 [CrossRef]
    [Google Scholar]
  43. Ogilvie M. M. 1998; Antiviral prophylaxis and treatment in chickenpox. A review prepared for the UK Advisory Group on Chickenpox on behalf of the British Society for the Study of Infection. J Infect 36:Suppl. 131–38 [CrossRef]
    [Google Scholar]
  44. Peeters B., Pol J., Gielkens A., Moormann R. 1993; Envelope glycoprotein gp50 of pseudorabies virus is essential for virus entry but is not required for viral spread in mice. J Virol 67:170–177
    [Google Scholar]
  45. Rickinson A. B., Moss D. J. 1997; Human cytotoxic T lymphocyte responses to Epstein–Barr virus infection. Annu Rev Immunol 15:405–431 [CrossRef]
    [Google Scholar]
  46. Rosa G. T., Gillet L., Smith C. M., de Lima B. D., Stevenson P. G. 2007; IgG Fc receptors provide an alternative infection route for murine gamma-herpesvirus-68. PLoS One 2:e560 [CrossRef]
    [Google Scholar]
  47. Smith C. M., Gill M. B., May J. S., Stevenson P. G. 2007; Murine gammaherpesvirus-68 inhibits antigen presentation by dendritic cells. PLoS One 2:e1048 [CrossRef]
    [Google Scholar]
  48. Sokal E. M., Hoppenbrouwers K., Vandermeulen C., Moutschen M., Léonard P., Moreels A., Haumont M., Bollen A., Smets F., Denis M. 2007; Recombinant gp350 vaccine for infectious mononucleosis: a phase 2, randomized, double-blind, placebo-controlled trial to evaluate the safety, immunogenicity, and efficacy of an Epstein–Barr virus vaccine in healthy young adults. J Infect Dis 196:1749–1753 [CrossRef]
    [Google Scholar]
  49. Stevenson P. G., Doherty P. C. 1998; Kinetic analysis of the specific host response to a murine gammaherpesvirus. J Virol 72:943–949
    [Google Scholar]
  50. Stevenson P. G., Efstathiou S. 2005; Immune mechanisms in murine gammaherpesvirus-68 infection. Viral Immunol 18:445–456 [CrossRef]
    [Google Scholar]
  51. Stevenson P. G., Cardin R. D., Christensen J. P., Doherty P. C. 1999; Immunological control of a murine gammaherpesvirus independent of CD8+ T cells. J Gen Virol 80:477–483
    [Google Scholar]
  52. Stewart J. P., Usherwood E. J., Ross A., Dyson H., Nash T. 1998; Lung epithelial cells are a major site of murine gammaherpesvirus persistence. J Exp Med 187:1941–1951 [CrossRef]
    [Google Scholar]
  53. Thorley-Lawson D. A., Geilinger K. 1980; Monoclonal antibodies against the major glycoprotein (gp350/220) of Epstein–Barr virus neutralize infectivity. Proc Natl Acad Sci U S A 77:5307–5311 [CrossRef]
    [Google Scholar]
  54. Virgin H. W., Speck S. H. 1999; Unraveling immunity to γ -herpesviruses: a new model for understanding the role of immunity in chronic virus infection. Curr Opin Immunol 11:371–379 [CrossRef]
    [Google Scholar]
  55. Walker R. C., Paya C. V., Marshall W. F., Strickler J. G., Wiesner R. H., Velosa J. A., Habermann T. M., Daly R. C., McGregor C. G. 1995; Pretransplantation seronegative Epstein–Barr virus status is the primary risk factor for posttransplantation lymphoproliferative disorder in adult heart, lung, and other solid organ transplantations. J Heart Lung Transplant 14:214–221
    [Google Scholar]
  56. Whitley R. J. 1994; Neonatal herpes simplex virus infections: is there a role for immunoglobulin in disease prevention and therapy?. Pediatr Infect Dis J 13:432–438 [CrossRef]
    [Google Scholar]
  57. Yao Q. Y., Ogan P., Rowe M., Wood M., Rickinson A. B. 1989; The Epstein–Barr virus : host balance in acute infectious mononucleosis patients receiving acyclovir anti-viral therapy. Int J Cancer 43:61–66 [CrossRef]
    [Google Scholar]
  58. Zinkernagel R. M., Hengartner H. 2006; Protective ‘immunity’ by pre-existent neutralizing antibody titers and preactivated T cells but not by so-called ‘immunological memory’. Immunol Rev 211:310–319 [CrossRef]
    [Google Scholar]
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