The herpes simplex virus 1 IgG Fc receptor blocks antibody-mediated complement activation and antibody-dependent cellular cytotoxicity in vivo

Journal of Virology

Volumn 85, Issue 7, 2011, Pages 3239-3249

  Lubinski, John M ^a   Lazear, Helen M ^a,b   Awasthi, Sita ^a   Wang, Fushan ^a   Friedman, Harvey M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Campus Box 8051 ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; CYTOTOXICITY; DISEASE SEVERITY; HERPES SIMPLEX VIRUS 1; HERPES ZOSTER; HUMAN; HUMAN CELL; IMMUNE EVASION; IN VIVO STUDY; MOUSE; NONHUMAN; PASSIVE IMMUNIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; RECEPTOR BINDING; SPINAL GANGLION; VIRUS MUTANT; WILD TYPE;

ANIMALS; ANTIBODIES, VIRAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; COMPLEMENT ACTIVATION; COMPLEMENT C3; DISEASE MODELS, ANIMAL; HERPES ZOSTER; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNE EVASION; KILLER CELLS, NATURAL; LEUKOCYTE REDUCTION PROCEDURES; MICE; MICE, INBRED BALB C; SEVERITY OF ILLNESS INDEX; VIRAL ENVELOPE PROTEINS; VIRULENCE FACTORS;

HUMAN HERPESVIRUS 1; MURINAE; MUS; SIMPLEXVIRUS;

EID: 79952608357     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02509-10     Document Type: Article

References (58)

1. Atalay, R., et al. 2002. Identification and expression of human cytomegalovirus transcription units coding for two distinct Fcγ receptor homologs. J. Virol. 76:8596-8608. (Pubitemid 34864054)
2. Basu, S., G. Dubin, M. Basu, V. Nguyen, and H. M. Friedman. 1995. Characterization of regions of herpes simplex virus type 1 glycoprotein E involved in binding the Fc domain of monomeric IgG and in forming a complex with glycoprotein I. J. Immunol. 154:260-267.
3. Basu, S., et al. 1997. Mapping regions of herpes simplex virus type 1 glycoprotein I required for formation of the viral Fc receptor for monomeric IgG. J. Immunology 158:209-215. (Pubitemid 127483858)
4. Baucke, R. B., and P. G. Spear. 1979. Membrane proteins specified by herpes simplex viruses. V. Identification of an Fc-binding glycoprotein. J. Virol. 32:779-789.
5. Bell, S., M. Cranage, L. Borysiewicz, and T. Minson. 1990. Induction of immunoglobulin G Fc receptors by recombinant vaccinia viruses expressing glycoproteins E and I of herpes simplex virus type 1. J. Virol. 64:2181-2186. (Pubitemid 20148464)
6. Berman, E. J., and J. M. Hill. 1985. Spontaneous ocular shedding of HSV-1 in latently infected rabbits. Invest. Ophthalmol. Vis. Sci. 26:587-590.
7. Brittle, E. E., F. Wang, J. M. Lubinski, R. M. Bunte, and H. M. Friedman. 2008. A replication-competent, neuronal spread-defective, live attenuated herpes simplex virus type 1 vaccine. J. Virol. 82:8431-8441.
8. Carroll, M. C. 2000. The role of complement in B cell activation and tolerance. Adv. Immunol. 74:61-88.
9. Chapman, T. L., et al. 1999. Characterization of the interaction between the herpes simplex virus type I Fc receptor and immunoglobulin G. J. Biol. Chem. 274:6911-6919.
10. Ch'ng, T. H., E. A. Flood, and L. W. Enquist. 2005. Culturing primary and transformed neuronal cells for studying pseudorabies virus infection. Methods Mol. Biol. 292:299-316.
11. Ch'ng, T. H., and L. W. Enquist. 2005. Neuron-to-cell spread of pseudorabies virus in a compartmented neuronal culture system. J. Virol. 79:10875-10889.
12. Cohen, G. H., et al. 1980. Structural analysis of the capsid polypeptides of herpes simplex virus types 1 and 2. J. Virol. 34:521-531. (Pubitemid 10104055)
13. Crnkovic-Mertens, I., et al. 1998. Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control. J. Virol. 72:1377-1382. (Pubitemid 28116923)
14. Dingwell, K. S., et al. 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. (Pubitemid 24022186)
15. Dingwell, K. S., L. C. Doering, and D. C. Johnson. 1995. Glycoproteins E and I facilitate neuron-to-neuron spread of herpes simplex virus. J. Virol. 69:7087-7098.
16. Dubin, G., et al. 1994. Characterization of domains of herpes simplex virus type 1 glycoprotein E involved in Fc binding activity for immunoglobulin G aggregates. J. Virol. 68:2478-2485.
17. Dubin, G., I. Frank, and H. M. Friedman. 1990. Herpes simplex virus type 1 encodes two Fc receptors which have different binding characteristics for monomeric immunoglobulin G (IgG) and IgG complexes. J. Virol. 64:2725-2731.
18. Dubin, G., E. Socolof, I. Frank, and H. M. Friedman. 1991. Herpes simplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity. J. Virol. 65:7046-7050.
19. Favoreel, H. W., H. J. Nauwynck, P. Van Oostveldt, T. C. Mettenleiter, and M. B. Pensaert. 1997. Antibody-induced and cytoskeleton-mediated redistribution and shedding of viral glycoproteins, expressed on pseudorabies virus-infected cells. J. Virol. 71:8254-8261.
20. Frank, I., and H. M. Friedman. 1989. A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G. J. Virol. 63:4479-4488.
21. Friedman, H. M., E. J. Macarak, R. R. MacGregor, J. Wolfe, and N. A. Kefalides. 1981. Virus infection of endothelial cells. J. Infect. Dis. 143:266-273.
22. Hook, L. M., J. Huang, M. Jiang, R. Hodinka, and H. M. Friedman. 2008. Blocking antibody access to neutralizing domains on glycoproteins involved in entry as a novel mechanism of immune evasion by herpes simplex virus type 1 glycoproteins C and E. J. Virol. 82:6935-6941.
23. Janeway, C. A., P. Travers, M. Walport, and J. D. Capra. 1999. Immunobiology. The immune system in health and disease, 4th ed. Elsevier Scence Ltd./Garland Publishing, New York, NY.
24. Johansson, P. J., E. B. Myhre, and J. Blomberg. 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. (Pubitemid 16192336)
25. Johnson, D. C., and V. Feenstra. 1987. Identification of a novel herpes simplex virus type 1-induced glycoprotein which complexes with gE and binds immunoglobulin. J. Virol. 61:2208-2216. (Pubitemid 17088934)
26. Johnson, D. C., M. C. Frame, M. W. Ligas, A. M. Cross, and N. D. Stow. 1988. Herpes simplex virus immunoglobulin G Fc receptor activity depends on a complex of two viral glycoproteins, gE and gI. J. Virol. 62:1347-1354.
27. Kitaichi, N., et al. 2002. Diminution of experimental autoimmune uveoretinitis (EAU) in mice depleted of NK cells. J. Leukoc. Biol. 72:1117-1121.
28. Kopf, M., B. Abel, A. Gallimore, M. Carroll, and M. F. Bachmann. 2002. Complement component C3 promotes T-cell priming and lung migration to control acute influenza virus infection. Nat. Med. 8:373-378.
29. Lenac, T., et al. 2006. The herpesviral Fc receptor Fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203:1843-1850.
30. Lilley, B. N., H. L. Ploegh, and R. S. Tirabassi. 2001. Human cytomegalovirus open reading frame TRL11/IRL11 encodes an immunoglobulin G Fc-binding protein. J. Virol. 75:11218-11221.
31. Lin, X., J. M. Lubinski, and H. M. Friedman. 2004. Immunization strategies to block the herpes simplex virus type 1 immunoglobulin G Fc receptor. J. Virol. 78:2562-2571.
32. Litwin, V., W. Jackson, and C. Grose. 1992. Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J. Virol. 66:3643-3651.
33. Lopez, C. 1975. Genetics of natural resistance to herpesvirus infections in mice. Nature 258:152-153.
34. Lubinski, J. M., et al. 2002. Herpes simplex virus type 1 evades the effects of antibody and complement in vivo. J. Virol. 76:9232-9241. (Pubitemid 34919882)
35. Lubinski, J. M., et al. 1998. Herpes simplex virus type 1 glycoprotein gC mediates immune evasion in vivo. J. Virol. 72:8257-8263. (Pubitemid 28421823)
36. Lundberg, P., et al. 2003. A locus on mouse chromosome 6 that determines resistance to herpes simplex virus also influences reactivation, while an unlinked locus augments resistance of female mice. J. Virol. 77:11661-11673. (Pubitemid 37271665)
37. Maillard, P., et al. 2004. Fcγ receptor-like activity of hepatitis C virus core protein. J. Biol. Chem. 279:2430-2437.
38. McGraw, H. M., S. Awasthi, J. A. Wojcechowskyj, and H. M. Friedman. 2009. Anterograde spread of herpes simplex virus type 1 requires glycoprotein E and glycoprotein I but not Us9. J. Virol. 83:8315-8326.
39. McGraw, H. M., and H. M. Friedman. 2009. Herpes simplex virus type 1 glycoprotein E mediates retrograde spread from epithelial cells to neurites. J. Virol. 83:4791-4799.
40. Metcalf, J. F., S. Chatterjee, J. Koga, and R. J. Whitley. 1988. Protection against herpetic ocular disease by immunotherapy with monoclonal antibodies to herpes simplex virus glycoproteins. Intervirology 29:39-49.
41. Mintern, J. D., et al. 2006. Viral interference with B7-1 costimulation: a new role for murine cytomegalovirus Fc receptor-1. J. Immunol. 177:8422-8431. (Pubitemid 44893804)
42. Nagashunmugam, T., et al. 1998. In vivo immune evasion mediated by the herpes simplex virus type 1 immunoglobulin G Fc receptor. J. Virol. 72:5351-5359.
43. Pandey, J. P., et al. 2008. Genetic markers of IgG influence the outcome of infection with hepatitis C virus. J. Infect. Dis. 198:1334-1336.
44. Para, M. F., R. B. Baucke, and P. G. Spear. 1982. Glycoprotein gE of herpes simplex virus type 1: effects of anti-gE on virion infectivity and on virus-induced Fc-binding receptors. J. Virol. 41:129-136.
45. Para, M. F., R. B. Baucke, and P. G. Spear. 1980. Immunoglobulin G (Fc)-binding receptors on virions of herpes simplex virus type 1 and transfer of these receptors to the cell surface by infection. J. Virol. 34:512-520.
46. Para, M. F., L. Goldstein, and P. G. Spear. 1982. Similarities and differences in the Fc-binding glycoprotein (gE) of herpes simplex virus types 1 and 2 and tentative mapping of the viral gene for this glycoprotein. J. Virol. 41:137-144. (Pubitemid 12197306)
47. Polcicova, K., K. Goldsmith, B. L. Rainish, T. W. Wisner, and D. C. Johnson. 2005. The extracellular domain of herpes simplex virus gE is indispensable for efficient cell-to-cell spread: evidence for gE/gI receptors. J. Virol. 79:11990-12001.
48. Rizvi, S. M., and M. Raghavan. 2001. An N-terminal domain of herpes simplex virus type Ig E is capable of forming stable complexes with gI. J. Virol. 75:11897-11901. (Pubitemid 33063283)
49. Saldanha, C. E., et al. 2000. Herpes simplex virus type 1 glycoprotein E domains involved in virus spread and disease. J. Virol. 74:6712-6719. (Pubitemid 30470652)
50. Sen, D. K., and G. S. Sarin. 1979. Immunoglobulin concentrations in human tears in ocular diseases. Br. J. Ophthalmol. 63:297-300.
51. Simmons, A., and A. A. Nash. 1985. Role of antibody in primary and recurrent herpes simplex virus infection. J. Virol. 53:944-948.
52. Simova, J., J. Bubenik, J. Bieblova, and T. Jandlova. 2004. The role of NK1.1+ cells in the protection against MHC class I+ HPV16-associated tumours. Folia Biol. (Praha) 50:200-202.
53. Sprague, E. R., C. Wang, D. Baker, and P. J. Bjorkman. 2006. Crystal structure of the HSV-1 Fc receptor bound to Fc reveals a mechanism for antibody bipolar bridging. PLoS Biol. 4:e148.
54. Van de Walle, G. R., H. W. Favoreel, H. J. Nauwynck, and M. B. Pensaert. 2003. Antibody-induced internalization of viral glycoproteins and gE-gI Fc receptor activity protect pseudorabies virus-infected monocytes from efficient complement-mediated lysis. J. Gen. Virol. 84:939-947.
55. Van Vliet, K. E., L. A. De Graaf-Miltenburg, J. Verhoef, and J. A. Van Strijp. 1992. Direct evidence for antibody bipolar bridging on herpes simplex virusinfected cells. Immunology 77:109-115.
56. Wang, F., et al. 2005. Herpes simplex virus type 1 glycoprotein E is required for axonal localization of capsid, tegument, and membrane glycoproteins. J. Virol. 79:13362-13372. (Pubitemid 41508150)
57. Watkins, J. F. 1964. Adsorption of sensitized sheep erythrocytes to HeLa cells infected with herpes simplex virus. Nature 202:1364-1365.
58. Weeks, B. S., P. Sundaresan, T. Nagashunmugam, E. Kang, and H. M. Friedman. 1997. The herpes simplex virus-1 glycoprotein E (gE) mediates IgG binding and cell-to-cell spread through distinct gE domains. Biochem. Biophys. Res. Commun. 235:31-35.