1887

Abstract

We demonstrated previously that immunization with a DNA vaccine expressing the Japanese encephalitis virus (JEV) envelope (E) protein conferred a high level of protection through a poorly neutralizing antibody response. Here, we further investigated the role of the IgG subclass in this antibody-dependent protection using cytokine co-immunization and cytokine-deficient mice. A significant difference in IgG2a/c but not IgG1 was observed between mice that survived or died following a lethal challenge. Correspondingly, the IgG2a/c response and protection increased in IL-4-deficient mice but decreased in IFN-γ-deficient mice, highlighting the importance of IgG2a/c. In addition, the restoration of protection and E-specific IgG2a/c production in IFN-γ-deficient mice by a T helper (Th) type 1-biased intramuscular immunization suggested that IgG2a/c but not IFN-γ was the major component for protection. The failure of protection against a direct intracranial challenge indicated that IgG2a/c-mediated protection was restricted to outside the central nervous system. Consistent with this conclusion, passive transfer of E-specific antisera conferred protection only pre-exposure to JEV. Therefore, our data provided evidence that the IgG subclass plays an important role in protection against JEV, particular in poorly neutralizing E-specific antibodies, and Th1-biased IgG2a/c confers better protection than Th2-biased IgG1 against JEV.

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2014-09-01
2020-10-25
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References

  1. Baldridge J. R., Buchmeier M. J. 1992; Mechanisms of antibody-mediated protection against lymphocytic choriomeningitis virus infection: mother-to-baby transfer of humoral protection. J Virol 66:4252–4257[PubMed]
    [Google Scholar]
  2. Barr T. A., Brown S., Mastroeni P., Gray D. 2009; B cell intrinsic MyD88 signals drive IFN-gamma production from T cells and control switching to IgG2c. J Immunol 183:1005–1012 [CrossRef][PubMed]
    [Google Scholar]
  3. Burke D. S., Leake C. J. 1988 Japanese Encephalitis Boca Raton, FL: CRC Press;
    [Google Scholar]
  4. Chen H. W., Pan C. H., Liau M. Y., Jou R., Tsai C. J., Wu H. J., Lin Y. L., Tao M. H. 1999; Screening of protective antigens of Japanese encephalitis virus by DNA immunization: a comparative study with conventional viral vaccines. J Virol 73:10137–10145[PubMed]
    [Google Scholar]
  5. Chow Y. H., Chiang B. L., Lee Y. L., Chi W. K., Lin W. C., Chen Y. T., Tao M. H. 1998; Development of Th1 and Th2 populations and the nature of immune responses to hepatitis B virus DNA vaccines can be modulated by codelivery of various cytokine genes. J Immunol 160:1320–1329[PubMed]
    [Google Scholar]
  6. Chung K. M., Nybakken G. E., Thompson B. S., Engle M. J., Marri A., Fremont D. H., Diamond M. S. 2006; Antibodies against West Nile Virus nonstructural protein NS1 prevent lethal infection through Fc gamma receptor-dependent and -independent mechanisms. J Virol 80:1340–1351 [CrossRef][PubMed]
    [Google Scholar]
  7. Chung K. M., Thompson B. S., Fremont D. H., Diamond M. S. 2007; Antibody recognition of cell surface-associated NS1 triggers Fc-gamma receptor-mediated phagocytosis and clearance of West Nile virus-infected cells. J Virol 81:9551–9555 [CrossRef][PubMed]
    [Google Scholar]
  8. Clynes R., Takechi Y., Moroi Y., Houghton A., Ravetch J. V. 1998; Fc receptors are required in passive and active immunity to melanoma. Proc Natl Acad Sci U S A 95:652–656 [CrossRef][PubMed]
    [Google Scholar]
  9. Coutelier J. P., van der Logt J. T., Heessen F. W., Warnier G., Van Snick J. 1987; IgG2a restriction of murine antibodies elicited by viral infections. J Exp Med 165:64–69 [CrossRef][PubMed]
    [Google Scholar]
  10. Ding D., Kilgore P. E., Clemens J. D., Wei L., Zhi-Yi X. 2003; Cost-effectiveness of routine immunization to control Japanese encephalitis in Shanghai, China. Bull World Health Organ 81:334–342[PubMed]
    [Google Scholar]
  11. Engle M. J., Diamond M. S. 2003; Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J Virol 77:12941–12949 [CrossRef][PubMed]
    [Google Scholar]
  12. Fossati-Jimack L., Ioan-Facsinay A., Reininger L., Chicheportiche Y., Watanabe N., Saito T., Hofhuis F. M., Gessner J. E., Schiller C.other authors 2000; Markedly different pathogenicity of four immunoglobulin G isotype-switch variants of an antierythrocyte autoantibody is based on their capacity to interact in vivo with the low-affinity Fcγ receptor III. J Exp Med 191:1293–1302 [CrossRef][PubMed]
    [Google Scholar]
  13. Hamaguchi Y., Xiu Y., Komura K., Nimmerjahn F., Tedder T. F. 2006; Antibody isotype-specific engagement of Fcγ receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 203:743–753 [CrossRef][PubMed]
    [Google Scholar]
  14. Hawkes R. A., Roehrig J. T., Hunt A. R., Moore G. A. 1988; Antigenic structure of the Murray Valley encephalitis virus E glycoprotein. J Gen Virol 69:1105–1109 [CrossRef][PubMed]
    [Google Scholar]
  15. Heusser C. H., Anderson C. L., Grey H. M. 1977; Receptors for IgG: subclass specificity of receptors on different mouse cell types and the definition of two distinct receptors on a macrophage cell line. J Exp Med 145:1316–1327 [CrossRef][PubMed]
    [Google Scholar]
  16. Hoke C. H., Nisalak A., Sangawhipa N., Jatanasen S., Laorakapongse T., Innis B. L., Kotchasenee S., Gingrich J. B., Latendresse J.other authors 1988; Protection against Japanese encephalitis by inactivated vaccines. N Engl J Med 319:608–614 [CrossRef][PubMed]
    [Google Scholar]
  17. Hombach J., Solomon T., Kurane I., Jacobson J., Wood D. 2005; Report on a WHO consultation on immunological endpoints for evaluation of new Japanese encephalitis vaccines, WHO, Geneva, 2–3 September, 2004. Vaccine 23:5205–5211 [CrossRef][PubMed]
    [Google Scholar]
  18. Huber V. C., Lynch J. M., Bucher D. J., Le J., Metzger D. W. 2001; Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol 166:7381–7388 [CrossRef][PubMed]
    [Google Scholar]
  19. Kaufman B. M., Summers P. L., Dubois D. R., Cohen W. H., Gentry M. K., Timchak R. L., Burke D. S., Eckels K. H. 1989; Monoclonal antibodies for dengue virus prM glycoprotein protect mice against lethal dengue infection. Am J Trop Med Hyg 41:576–580[PubMed]
    [Google Scholar]
  20. Kimura-Kuroda J., Yasui K. 1988; Protection of mice against Japanese encephalitis virus by passive administration with monoclonal antibodies. J Immunol 141:3606–3610[PubMed]
    [Google Scholar]
  21. Kipps T. J., Parham P., Punt J., Herzenberg L. A. 1985; Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J Exp Med 161:1–17 [CrossRef][PubMed]
    [Google Scholar]
  22. Konishi E., Mason P. W. 1993; Proper maturation of the Japanese encephalitis virus envelope glycoprotein requires cosynthesis with the premembrane protein. J Virol 67:1672–1675[PubMed]
    [Google Scholar]
  23. Kreil T. R., Eibl M. M. 1997; Pre- and postexposure protection by passive immunoglobulin but no enhancement of infection with a flavivirus in a mouse model. J Virol 71:2921–2927[PubMed]
    [Google Scholar]
  24. Larena M., Regner M., Lee E., Lobigs M. 2011; Pivotal role of antibody and subsidiary contribution of CD8+ T cells to recovery from infection in a murine model of Japanese encephalitis. J Virol 85:5446–5455 [CrossRef][PubMed]
    [Google Scholar]
  25. Larena M., Regner M., Lobigs M. 2013; Cytolytic effector pathways and IFN-γ help protect against Japanese encephalitis. Eur J Immunol 43:1789–1798 [CrossRef][PubMed]
    [Google Scholar]
  26. Li Y., Counor D., Lu P., Duong V., Yu Y., Deubel V. 2012; Protective immunity to Japanese encephalitis virus associated with anti-NS1 antibodies in a mouse model. Virol J 9:135 [CrossRef][PubMed]
    [Google Scholar]
  27. Mackenzie J. S., Gubler D. J., Petersen L. R. 2004; Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10:SupplS98–S109 [CrossRef][PubMed]
    [Google Scholar]
  28. Markine-Goriaynoff D., Coutelier J. P. 2002; Increased efficacy of the immunoglobulin G2a subclass in antibody-mediated protection against lactate dehydrogenase-elevating virus-induced polioencephalomyelitis revealed with switch mutants. J Virol 76:432–435 [CrossRef][PubMed]
    [Google Scholar]
  29. Miyajima I., Dombrowicz D., Martin T. R., Ravetch J. V., Kinet J. P., Galli S. J. 1997; Systemic anaphylaxis in the mouse can be mediated largely through IgG1 and Fc gammaRIII. Assessment of the cardiopulmonary changes, mast cell degranulation, and death associated with active or IgE- or IgG1-dependent passive anaphylaxis. J Clin Invest 99:901–914 [CrossRef][PubMed]
    [Google Scholar]
  30. Neuberger M. S., Rajewsky K. 1981; Activation of mouse complement by monoclonal mouse antibodies. Eur J Immunol 11:1012–1016 [CrossRef][PubMed]
    [Google Scholar]
  31. Nimmerjahn F., Ravetch J. V. 2005; Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310:1510–1512 [CrossRef][PubMed]
    [Google Scholar]
  32. Nimmerjahn F., Bruhns P., Horiuchi K., Ravetch J. V. 2005; FcgammaRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23:41–51 [CrossRef][PubMed]
    [Google Scholar]
  33. Pan C. H., Chen H. W., Huang H. W., Tao M. H. 2001; Protective mechanisms induced by a Japanese encephalitis virus DNA vaccine: requirement for antibody but not CD8+ cytotoxic T-cell responses. J Virol 75:11457–11463 [CrossRef][PubMed]
    [Google Scholar]
  34. Peng S. L., Szabo S. J., Glimcher L. H. 2002; T-bet regulates IgG class switching and pathogenic autoantibody production. Proc Natl Acad Sci U S A 99:5545–5550 [CrossRef][PubMed]
    [Google Scholar]
  35. Phillpotts R. J., Stephenson J. R., Porterfield J. S. 1987; Passive immunization of mice with monoclonal antibodies raised against tick-borne encephalitis virus. Arch Virol 93:295–301 [CrossRef][PubMed]
    [Google Scholar]
  36. Pricop L., Redecha P., Teillaud J. L., Frey J., Fridman W. H., Sautès-Fridman C., Salmon J. E. 2001; Differential modulation of stimulatory and inhibitory Fc gamma receptors on human monocytes by Th1 and Th2 cytokines. J Immunol 166:531–537 [CrossRef][PubMed]
    [Google Scholar]
  37. Ravetch J. V. 2003 Fc Receptors Philadelphia, PA: Lippincott-Raven;
    [Google Scholar]
  38. Schlageter A. M., Kozel T. R. 1990; Opsonization of Cryptococcus neoformans by a family of isotype-switch variant antibodies specific for the capsular polysaccharide. Infect Immun 58:1914–1918[PubMed]
    [Google Scholar]
  39. Schlesinger J. J., Brandriss M. W., Walsh E. E. 1985; Protection against 17D yellow fever encephalitis in mice by passive transfer of monoclonal antibodies to the nonstructural glycoprotein gp48 and by active immunization with gp48. J Immunol 135:2805–2809[PubMed]
    [Google Scholar]
  40. Schmaljohn A. L., Johnson E. D., Dalrymple J. M., Cole G. A. 1982; Non-neutralizing monoclonal antibodies can prevent lethal alphavirus encephalitis. Nature 297:70–72 [CrossRef][PubMed]
    [Google Scholar]
  41. Schreier P. H., Bothwell A. L., Mueller-Hill B., Baltimore D. 1981; Multiple differences between the nucleic acid sequences of the IgG2aa and IgG2ab alleles of the mouse. Proc Natl Acad Sci U S A 78:4495–4499 [CrossRef][PubMed]
    [Google Scholar]
  42. Shresta S., Kyle J. L., Snider H. M., Basavapatna M., Beatty P. R., Harris E. 2004; Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J Virol 78:2701–2710 [CrossRef][PubMed]
    [Google Scholar]
  43. Shrestha B., Wang T., Samuel M. A., Whitby K., Craft J., Fikrig E., Diamond M. S. 2006; Gamma interferon plays a crucial early antiviral role in protection against West Nile virus infection. J Virol 80:5338–5348 [CrossRef][PubMed]
    [Google Scholar]
  44. Smythies L. E., Waites K. B., Lindsey J. R., Harris P. R., Ghiara P., Smith P. D. 2000; Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice. J Immunol 165:1022–1029 [CrossRef][PubMed]
    [Google Scholar]
  45. Srivastava A. K., Putnak J. R., Lee S. H., Hong S. P., Moon S. B., Barvir D. A., Zhao B., Olson R. A., Kim S. O.other authors 2001; A purified inactivated Japanese encephalitis virus vaccine made in Vero cells. Vaccine 19:4557–4565 [CrossRef][PubMed]
    [Google Scholar]
  46. van den Hurk A. F., Ritchie S. A., Mackenzie J. S. 2009; Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54:17–35 [CrossRef][PubMed]
    [Google Scholar]
  47. Vogt M. R., Dowd K. A., Engle M., Tesh R. B., Johnson S., Pierson T. C., Diamond M. S. 2011; Poorly neutralizing cross-reactive antibodies against the fusion loop of West Nile virus envelope protein protect in vivo via Fcgamma receptor and complement-dependent effector mechanisms. J Virol 85:11567–11580 [CrossRef][PubMed]
    [Google Scholar]
  48. Zhang Z., Goldschmidt T., Salter H. 2012; Possible allelic structure of IgG2a and IgG2c in mice. Mol Immunol 50:169–171 [CrossRef][PubMed]
    [Google Scholar]
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