IgG fc receptors provide an alternative infection route for murine gamma-herpesvirus-68.

[en] BACKGROUND: Herpesviruses can be neutralized in vitro but remain infectious in immune hosts. One difference between these settings is the availability of immunoglobulin Fc receptors. The question therefore arises whether a herpesvirus exposed to apparently neutralizing antibody can still infect Fc receptor(+) cells. PRINCIPAL FINDINGS: Immune sera blocked murine gamma-herpesvirus-68 (MHV-68) infection of fibroblasts, but failed to block and even enhanced its infection of macrophages and dendritic cells. Viral glycoprotein-specific monoclonal antibodies also enhanced infection. MHV-68 appeared to be predominantly latent in macrophages regardless of whether Fc receptors were engaged, but the infection was not abortive and new virus production soon overwhelmed infected cultures. Lytically infected macrophages down-regulated MHC class I-restricted antigen presentation, endocytosis and their response to LPS. CONCLUSIONS: IgG Fc receptors limit the neutralization of gamma-herpesviruses such as MHV-68.

Disciplines :

Microbiology

Author, co-author :

Rosa, Gustavo T

Gillet, Laurent ; Université de Liège - ULiège > Immunologie et vaccinologie

Smith, Christopher M

de Lima, Brigitte D

Stevenson, Philip G

Language :

English

Title :

IgG fc receptors provide an alternative infection route for murine gamma-herpesvirus-68.

Publication date :

2007

Journal title :

PLoS ONE

eISSN :

1932-6203

Publisher :

Public Library of Science, San Franscisco, United States - California

Volume :

Issue :

Pages :

e560

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 20 November 2010

Statistics

Number of views

135 (3 by ULiège)

Number of downloads

117 (0 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Zinkernagel RM, 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.
Knossow M, Skehel JJ (2006) Variation and infectivity neutralization in influenza. Immunology 119: 1-7.
Pantophlet R, Burton DR. GP120: target for neutralizing HIV-1 antibodies. Annu Rev Immunol 24: 739-769.
Yao QY, Rickinson AB, Epstein MA (1985) A re-examination of the Epstein-Barr virus carrier state in healthy seropositive individuals. Int J Cancer 35: 35-42.
Yoshino K, Taniguchi S (1965) Studies on the neutralization of herpes simplex virus. i. appearance of neutralizing antibodies having different grades of complement requirement. Virology 26: 44-53.
Martos LM, Ablashi DV, Gilden RV, Siguenza RF, Hampar B (1970) Preparation of immune rabbit sera with neutralizing activity against human cytomegalovirus and varicella-zoster virus. J Gen Virol 7: 169-171.
Miller G, Niederman JC, Stitt DA (1972) Infectious mononucleosis: appearance of neutralizing antibody to Epstein-Barr virus measured by inhibition of formation of lymphoblastoid cell lines. J Infect Dis 125: 403-406.
Dialyna U, Graham- D, Rezaee R, Blue CE, Stavrianeas NG, et al. (2004) Anti-HHV-8/KSHV antibodies in infected individuals inhibit infection in vitro. AIDS 18: 1263-1270.
Blaskovic D, Stancekova M; Svobodova J, Mistrikova J (1980) Isolation of five strains of herpesviruses, from two species of free living small rodents. Acta Virol 24: 468.
Speck SH, Virgin HW (1999) Host and viral genetics of chronic infection: a mouse model of gamma-herpesvirus pathogenesis. Curr Opin Microbiol 2: 403-409.
Flano E, Woodland DL, Blackman MA (2002) A mouse model for infectious mononucleosis. Immunol Res 25: 201-217.
Stevenson PG, Boname JM, de Lima B, Efstathiou S (2002) A battle for survival: immune control and immune' evasion in- murine gammna-herpesvius-68 infection- Microbes Infect 4: 1177-1182.
Cardin RD, Brooks JW, Sarawar SR, Doherty PC (1996) Progressive loss of CD8+ T cell-mediated control of a gamma-herpesvirus in the absence of CD4+ T cells. J Exp Med 184: 863-871.
Dal Canto AJ, Virgin HW, Speck SH (2000) Ongoing viral replication is required for gammaherpesvirus 68-induced vascular damage. J Virol 74: 11304-11310.
Christensen JP, Cardin RD, Branum KC, Doherty PC (1999) CD4(+) T cell-mediated control of a gamma-herpesvirus in B cell-deficient mice is mediated by IFN-gamma. Proc Natl Acad Sci U S A 96: 5135-5140.
Stevenson PG, Cardin RD, Christensen JP, Doherty PC (1999) Immunological control of a murine gammaherpesvirus independent of CD8+ T cells. J Gen Virol 80: 477-483.
Ehtisham S, Sunil-Chandra NP, Nash AA (1993) Pathogenesis of murine gammaherpesvirus infection in mice deficient in CD4 and CDR T cells. J Virol 67: 5247-5252.
Stewart JP, Usherwood EJ, Ross A, Dyson H, Nash T (1998) Lung epithelial cells are a major site of routine gammaherpesvirus persistence. J Exp Med 187: 1941-1951.
Kim IJ, Flano E, Woodland DL, Blackman MA (2002) Antibody-mediated control of persistent gamma-herpevirus infection. J Immunol 168: 3958-3964.
Gangappa S, Kapadia SB, Speck SH, Virgin HW (2000) Antibody to a lytic cycle viral protein decreases gammaherpesvirus latency in B-cell-deficient mice. J Virol 76: 11460-11468.
Stevenson PG, May JS, Smith XG, Marques S, Adler H, et al. (2002) K3-mediated evasion of CD8(+) T cells aids amplification of a latent gamma-herpesvirus. Nat Immunol 3: 733-740.
Stevenson PG (2004) Immune evasion by gamma-herpesviruses. Curr Opin Immunol 16: 456-462.
Kohl S, Loo LS (1982) Protection of neonatal mice against herpes simplex virus infection probable in vivo antibody-dependent cellular cytotoxicity. J Immunol 129: 370-376.
Sissons JG, Oldstone MB (1980) Killing of virus antiviral antibody and complement in limiting virus infection. J Infect Dis 142: 442-448.
tevenson PG, Doherty PC (1998) Kinetic analysis of the specific host response to a murine gammaherpesvirus. J Virol 72: 943-949.
Stevenson PG, Doherty PC (1999) Non-antigen-specific B-cell activation following murine gammaherpesvirus infection is CD4 independent in vitro but CD4 dependent in vivo. J Virol 73: 1075-1079.
Gill MB, Gillet L, Colaco S, May JS, de Lima BD, et al. (2006) Murine gmmaherpesvirus-68 glycoprotein H-glycoprotein L complex is a major target for neutralizing monoclonal antibodies. J Gen Virol 87: 1465-1475.
Peiris JS, Porterfield JS (1979) Antibody-mediated enhancement of Flavivirus replication in macrophage-like cell lines. Nature 282: 509-511.
Iankov ID, Pandey M, Harvey M, Griesmann GE, Federspiel MJ, et al. (2006) Immunoglobulin g. antibody-mediated enhancement of measles virus infection can bypass the protective antiviral immune response. J Virol 80: 8530-8540.
Weck KE, Kim SS, Virgin HW, Speck SH (1999) Macrophages are the major repervoir of latent murine gammaherpesvirus 68 in peritoneal cells. J Virol 73: 3213-3283.
Flano E, Husain SM, Sample JF, Woodland DL, Blackman MA (2000) Latent murine gamma-herpesvirus infection is established in activated B cells, dendritic cells, and, macrophages. J Immunol 165: 1074-1081.
Niess JH, Brand S, Gu X, Landsman L, Jung S, et al. (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307: 254-258.
Qiao SW, Lencer WI, Blumberg RS (2007) How the controller is controlled-neonatal Fc receptor expression and immunoglobulin G homeostasis. Immunology 120: 145-147.
Maidji E, McDonagh S, Genbacev O, Tabata T, Pereira L (2006) Maternal antibodies enhance or prevent cytomegalovirus infection in the placenta by neonatal Fc receptor-mediated transcytosis. Am J Pathol 168: 1210-1226.
Adler H, Messerle M, Wagner M, Koszinowski UH (2000) Cloning and mutagenesis of the murine gammaherpesvirus 68 genome as an infectious bacterial artificial chromosome. J Virol 74: 6964-6974.
Gillet L, Gill MR, Colaco S, Smith CM, Stevenson PG (2006) Murine gammaherpesvirus-68 glycoprotein B presents a difficult neutralization target to monoclonal antibodies derived from infected mice. J Gen Virol 87: 3515-3527.
Coleman HM, Efstathiou S, Stevenson PG (2005) Transcription of the murine gammaherpesvirus 68 ORF73 from promoters in the viral terminal repeats. J Gen Virol 86: 561-574.
Bennett NJ, May JS, Stevenson PG (2005) Gamma-herpesvirus latency requires T cell evasion during episome maintenahce. PLoS Biol 3: e120.
Lee Y, Sohn WJ, Kim DS, Kwon HJ (2004) NF-kappaB- and c-Jun-dependent regulation of human cytomegalovirus immediate-early gene enhancer/ promoter in response to lipopolysaccharide and bacterial CpG-oligodeoxynucleotides in macrophage cell line RAW 264.7. Eur J Biochem 271: 1094-1105.
May JS, Colaco S, Stevenson PG (2005) Glycoprotein M is an essential lytic replication protein of the murine gammaherpesvirus 68. J Virol 79. 3459-3467.
Boname JM, de Lima BD, Lehner PJ, Stevenson PG (2004) Vital degradation of the MHC class I peptide loading complex. Immunity 20: 305-317.
Stevenson PG, Belz GT, Castrucci MR, Altman JD, Doherty PC (1999) A gamma-herpesvirus sneaks through a CD8(+) T cell response primed to a lytic-phase epitope. Proc Natl Acad Sci U S A. 96: 9281-9286.
Lubinski JM, Jiang M, Hook L, Chang Y, Sarver C, et al (2002) Herpes simplex virus type 1 evades the effects of antibody and complement in vivo. J Virol 76: 9232-9241.
Yao QY, Rowe M, Morgan AJ, Sam CK, Prasad U, et al. (1991) Salivary and serum IgA antibodies to the Epstein Barr virus glycoprotein gp340: incidence and potential for virus neutralization. Int J Cancer 40: 45-50.
Sangster MY, Topham , D'Costa S, Cardin RD, Marion TN, et al. (2000) Analysis of the virus-specific and nonspecific B cell response to a persisteut B-lymphotropic gammaherpesvirus. J Immunol 164: 1820-1828.
Mbopi-Keou FX, Legoff J, Piketty C, Hocini H, Malkin JE, et al (2004) Salivary produation of IgA and IgG to human herpes virus 8 latent and lytic antigens by patients in whom Kaposi's sarcoma has regres ed. AIDS. 18: 338-340.
Kraehenbuhl JP, Neutra MR (2000) Epithelial M cells: differentiation and function. Annu Rev Cell Dev Biol 16: 301-332.
van Montfort T, Nabatov AA, Geijtenbeek TB, Pollakis G, Paxton WA (2007) Efficient capture of antibody neutralized HIV-1 by cells expressing DC SIGN and tranfer to CD4+ T ymphocytes. J Immunol 178: 8177-3185.
Sunil-Chandra NP, Efstathiou S, Arno J, Nash AA (1992) Virological and pathological features of mice infected with murine gamma-herpesvirus 68. J Gen Virol 73: 2347-2856.
de Lima BD, May JS, Stevenson PG (2004) Murine gammaherpesvirus 68 lacking gp150 shows defective virion release but establishes normal latency in vivo. J Virol 78: 5103-5112.
Gillet L, May JS, Colaco S, Stevenson PG (2007) Glycoprotein L disruption reveals 2 functional forms of the murine gammaherpesvirus-68 glycoprotein H. J Virol 81: 280-291.
Galfre G, Milstein G (1981) Preparation of monoclonal antibodies: strategies and procedures. Methods Enzymol 73: 3-46.
Gillet L, Adler H. Stevenson PG (2007) Glycosaminoglycan interactions in murine gammaherpesvirus-68 infection. PLoS ONE 2: e347.
May JS, Walker J, Colaco S, Stevenson PG (2005) The murine gammaherpes-virus 68 ORF27 gene product contributes to intercellular viral spread. J Virol 79: 5059-5068.
May JS, de Lima BD, Colaco S, Stevenson PG (2005) Intercellular gamma-herpesvirus dissemination involves co-ordinated intracellular membrane protein transport. Traffic 6: 780-793.
Lopes FB, Colaco S, May JS, Stevenson PG (2004) Characterization of murine gammaherpesvirus 6B glycoprotein B. J Virol 78: 13370-13375.
Stevenson PG, Belz GT, Altman JD, Doherty PC (1999) Changing patterns of dominance in the CD8+ T cell response during acute and persistent murine gamma-herpesvirus infection. Eur J Immunol 29: 1059-1067.
Liu L, Flano E, Usherwood EJ, Surman S, Blackman MA, et al. (1999) Lytic cycle T cell epitopes are expressed in two distinct phases during MHV-68 infection. J Immunol 163: 868-874.