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PMID: 12388707 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Antibody to a lytic cycle viral protein decreases gammaherpesvirus latency in B-cell-deficient mice.

Journal of virology ·Vol. 76 ·No. 22 ·2002-11-00 ·Pages 11460-8

Gangappa S, Kapadia SB, Speck SH, Virgin HW

Abstract

While antiviral antibody plays a key role in resistance to acute viral infection, the contribution of antibody to the control of latent virus infection is less well understood. Gammaherpesvirus 68 (gammaHV68) infection of mice provides a model well suited to defining contributions of specific immune system components to the control of viral latency. B cells play a critical role in regulating gammaHV68 latency, but the mechanism(s) by which B cells regulate latency is not known. In the experiments reported here, we determined the effect of passively transferred antibody on established gammaHV68 latency in B-cell-deficient (B-cell(-/-)) mice. Immune antibody decreased the frequency of cells reactivating ex vivo from latency in splenocytes (>10-fold) and peritoneal cells (>100-fold) and the frequency of cells carrying latent viral genome in splenocytes (>5-fold) and peritoneal cells (>50-fold). This effect required virus-specific antibody and was observed when total and virus-specific serum antibody concentrations in recipient B-cell(-/-) mice were <8% of those in normal mice during latent infection. Passive transfer of antibody specific for the lytic cycle gammaHV68 RCA protein, but not passive transfer of antibody specific for the v-cyclin protein or the latent protein M2, decreased both the frequency of cells reactivating ex vivo from latency and the frequency of cells carrying the latent viral genome. Therefore, antibody specific for lytic cycle viral antigens can play an important role in the control of gammaherpesvirus latency in immunocompromised hosts. Based on these findings, we propose a model in which ongoing productive replication is essential for maintaining high levels of latently infected cells in immunocompromised hosts. We confirmed this model by the treatment of latently infected B-cell(-/-) mice with the antiviral drug cidofovir.

MeSH Terms
Animals Antibodies, Viral/administration & dosage,immunology Antigens, Viral/immunology B-Lymphocytes/immunology Cell Line Gammaherpesvirinae/immunology,physiology Herpesviridae Infections/immunology,virology Immunization, Passive Mice Mice, Inbred BALB C Viral Proteins/immunology Virus Activation Virus Latency/immunology Virus Replication
Chemicals
Antibodies, Viral Antigens, Viral Viral Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Gangappa Shivaprakash
Department of Pathology and Immunology, Washington University School of Medicine, Saint Louis, Missouri 63110, USA.
Kapadia Sharookh B
Speck Samuel H
Virgin Herbert W
References (47)
47 references, click to expand
  1. Identification of the in vivo role of a viral bcl-2.
    J Exp Med. 2002 Apr 1;195(7):931-40 PMID: 11927636
  2. Requirement for CD40 ligand, CD4(+) T cells, and B cells in an infectious mononucleosis-like syndrome.
    J Virol. 1999 Nov;73(11):9650-4 PMID: 10516078
  3. Immune control of the number and reactivation phenotype of cells latently infected with a gammaherpesvirus.
    J Virol. 2002 Jul;76(14):7125-32 PMID: 12072512
  4. Critical role of complement and viral evasion of complement in acute, persistent, and latent gamma-herpesvirus infection.
    Immunity. 2002 Aug;17(2):143-55 PMID: 12196286
  5. The B cell is the initiating antigen-presenting cell in peripheral lymph nodes.
    J Immunol. 1987 Feb 15;138(4):1051-5 PMID: 3100626
  6. T cell priming in vivo: a major role for B cells in presenting antigen to T cells in lymph nodes.
    J Immunol. 1987 May 1;138(9):2848-56 PMID: 2952725
  7. Herpes simplex virus glycoproteins gC-1 and gC-2 bind to the third component of complement and provide protection against complement-mediated neutralization of viral infectivity.
    J Exp Med. 1987 Nov 1;166(5):1525-35 PMID: 2824652
  8. Vaccinia virus complement-control protein prevents antibody-dependent complement-enhanced neutralization of infectivity and contributes to virulence.
    Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):628-32 PMID: 1731333
  9. Virological and pathological features of mice infected with murine gamma-herpesvirus 68.
    J Gen Virol. 1992 Sep;73 ( Pt 9):2347-56 PMID: 1328491
  10. Murine gammaherpesvirus 68 establishes a latent infection in mouse B lymphocytes in vivo.
    J Gen Virol. 1992 Dec;73 ( Pt 12):3275-9 PMID: 1469366
  11. Animal models of infection-mediated vasculitis: implications for human disease.
    Int J Cardiol. 2000 Aug 31;75 Suppl 1:S37-45; discussion S47-52 PMID: 10980335
  12. Role of cytotoxic T lymphocytes in Epstein-Barr virus-associated diseases.
    Annu Rev Microbiol. 2000;54:19-48 PMID: 11018123
  13. Control of gammaherpesvirus latency by latent antigen-specific CD8(+) T cells.
    J Exp Med. 2000 Oct 2;192(7):943-52 PMID: 11015436
  14. Ongoing viral replication is required for gammaherpesvirus 68-induced vascular damage.
    J Virol. 2000 Dec;74(23):11304-10 PMID: 11070030
  15. IFN-gamma action in the media of the great elastic arteries, a novel immunoprivileged site.
    J Clin Invest. 2001 Jan;107(2):R15-22 PMID: 11160143
  16. Virus-specific and bystander CD8+ T-cell proliferation in the acute and persistent phases of a gammaherpesvirus infection.
    J Virol. 2001 May;75(9):4435-8 PMID: 11287596
  17. Analysis of virus-specific CD4(+) t cells during long-term gammaherpesvirus infection.
    J Virol. 2001 Aug;75(16):7744-8 PMID: 11462049
  18. Disruption of the M2 gene of murine gammaherpesvirus 68 alters splenic latency following intranasal, but not intraperitoneal, inoculation.
    J Virol. 2002 Feb;76(4):1790-801 PMID: 11799175
  19. Herpes simplex virus.
    Front Biosci. 2002 Mar 1;7:d752-64 PMID: 11861220
  20. Lymphoproliferative disease in mice infected with murine gammaherpesvirus 68.
    Am J Pathol. 1994 Oct;145(4):818-26 PMID: 7943173
  21. Mature B cells are required for acute splenic infection, but not for establishment of latency, by murine gammaherpesvirus 68.
    J Virol. 1996 Oct;70(10):6775-80 PMID: 8794315
  22. Absence of splenic latency in murine gammaherpesvirus 68-infected B cell-deficient mice.
    J Gen Virol. 1996 Nov;77 ( Pt 11):2819-25 PMID: 8922476
  23. Pathogenesis of an infectious mononucleosis-like disease induced by a murine gamma-herpesvirus: role for a viral superantigen?
    J Exp Med. 1997 May 5;185(9):1641-50 PMID: 9151901
  24. Murine gamma-herpesvirus 68 causes severe large-vessel arteritis in mice lacking interferon-gamma responsiveness: a new model for virus-induced vascular disease.
    Nat Med. 1997 Dec;3(12):1346-53 PMID: 9396604
  25. Kinetic analysis of the specific host response to a murine gammaherpesvirus.
    J Virol. 1998 Feb;72(2):943-9 PMID: 9444986
  26. In vitro and in vivo inhibition of murine gamma herpesvirus 68 replication by selected antiviral agents.
    Antimicrob Agents Chemother. 1998 Jan;42(1):170-2 PMID: 9449280
  27. Lung epithelial cells are a major site of murine gammaherpesvirus persistence.
    J Exp Med. 1998 Jun 15;187(12):1941-51 PMID: 9625754
  28. Hierarchical and redundant lymphocyte subset control precludes cytomegalovirus replication during latent infection.
    J Exp Med. 1998 Sep 21;188(6):1047-54 PMID: 9743523
  29. Non-antigen-specific B-cell activation following murine gammaherpesvirus infection is CD4 independent in vitro but CD4 dependent in vivo.
    J Virol. 1999 Feb;73(2):1075-9 PMID: 9882308
  30. Analysis of murine gammaherpesvirus-68 transcription during lytic and latent infection.
    J Gen Virol. 1999 Jan;80 ( Pt 1):75-82 PMID: 9934687
  31. Three distinct regions of the murine gammaherpesvirus 68 genome are transcriptionally active in latently infected mice.
    J Virol. 1999 Mar;73(3):2321-32 PMID: 9971815
  32. Macrophages are the major reservoir of latent murine gammaherpesvirus 68 in peritoneal cells.
    J Virol. 1999 Apr;73(4):3273-83 PMID: 10074181
  33. Changing patterns of dominance in the CD8+ T cell response during acute and persistent murine gamma-herpesvirus infection.
    Eur J Immunol. 1999 Apr;29(4):1059-67 PMID: 10229071
  34. B cells regulate murine gammaherpesvirus 68 latency.
    J Virol. 1999 Jun;73(6):4651-61 PMID: 10233924
  35. The murine gammaherpesvirus 68 v-cyclin gene is an oncogene that promotes cell cycle progression in primary lymphocytes.
    J Virol. 1999 Jun;73(6):5110-22 PMID: 10233974
  36. Murine gammaherpesvirus M2 gene is latency-associated and its protein a target for CD8(+) T lymphocytes.
    Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7508-13 PMID: 10377445
  37. Apparent MHC-independent stimulation of CD8+ T cells in vivo during latent murine gammaherpesvirus infection.
    J Immunol. 1999 Aug 1;163(3):1481-9 PMID: 10415050
  38. Murine gammaherpesvirus 68 encodes a functional regulator of complement activation.
    J Virol. 1999 Sep;73(9):7658-70 PMID: 10438856
  39. Turnover of T cells in murine gammaherpesvirus 68-infected mice.
    J Virol. 1999 Sep;73(9):7866-9 PMID: 10438881
  40. Unraveling immunity to gamma-herpesviruses: a new model for understanding the role of immunity in chronic virus infection.
    Curr Opin Immunol. 1999 Aug;11(4):371-9 PMID: 10448140
  41. Host and viral genetics of chronic infection: a mouse model of gamma-herpesvirus pathogenesis.
    Curr Opin Microbiol. 1999 Aug;2(4):403-9 PMID: 10458986
  42. 2'-Deoxy-5-ethyl-beta-4'-thiouridine inhibits replication of murine gammaherpesvirus and delays the onset of virus latency.
    Antivir Chem Chemother. 1999 Nov;10(6):321-6 PMID: 10628807
  43. Disruption of the murine gammaherpesvirus 68 M1 open reading frame leads to enhanced reactivation from latency.
    J Virol. 2000 Feb;74(4):1973-84 PMID: 10644370
  44. Latent murine gamma-herpesvirus infection is established in activated B cells, dendritic cells, and macrophages.
    J Immunol. 2000 Jul 15;165(2):1074-81 PMID: 10878386
  45. The murine gammaherpesvirus 68 v-cyclin is a critical regulator of reactivation from latency.
    J Virol. 2000 Aug;74(16):7451-61 PMID: 10906198
  46. Requirement for CD4+ T cells in V beta 4+CD8+ T cell activation associated with latent murine gammaherpesvirus infection.
    J Immunol. 1999 Sep 15;163(6):3403-8 PMID: 10477611
  47. Antibody-mediated control of persistent gamma-herpesvirus infection.
    J Immunol. 2002 Apr 15;168(8):3958-64 PMID: 11937552
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2002-11-00
Pages
11460-8
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC136779
Subset
IM
Grants
NCI NIH HHS · R01 CA058524 · United States
NHLBI NIH HHS · R01 HL060090 · United States
NCI NIH HHS · R01 CA043143 · United States
NCI NIH HHS · CA96511 · United States
NCI NIH HHS · R01 CA052004 · United States
NCI NIH HHS · CA74730 · United States
NHLBI NIH HHS · HL60090 · United States
NCI NIH HHS · CA52004 · United States
NCI NIH HHS · CA43143 · United States
NCI NIH HHS · R01 CA074730 · United States
NCI NIH HHS · CA58524 · United States
NCI NIH HHS · R01 CA096511 · United States
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