1887

Abstract

Antibody-dependent enhancement (ADE) of dengue virus infection occurs when neutralizing antibodies at sub-neutralizing concentrations or non-neutralizing antibodies form complexes with the virus. These virus-antibody complexes can then attach to a Fcγ receptor-bearing cell, via the Fc portion of the immunoglobulin, resulting in an increased number of infected cells. ADE may be responsible in part for the most severe clinical manifestations of dengue virus infection which include haemorrhage and shock. Three classes of human Fcγ receptors exist, FcγRI, FcγRII and FcγRIII. In this study, we examined the effects of neuraminidase on ADE of dengue virus infection mediated by the low-affinity FcγRII. K562 cells, which express only FcγRII, treated with neuraminidase resulted in augmentation of ADE of dengue virus infection by human anti-dengue antibodies. This augmented ADE of infection could be blocked by anti-FcγRII monoclonal antibody IV.3. Incubation of neuraminidase-treated K562 cells with IgG-coated human red blood cells resulted in an increase in the percentage of rosette formations compared with the untreated K562 cells. A bispecific antibody directed against FcγRII and dengue virus (IV.3 × 2H2) enhanced virus infection. Neuraminidase also augmented ADE mediated by this antibody, but to a much lesser degree (by 50%) compared with that seen using conventional human anti-dengue antibody (by 200 to 300%). Fluorescence-activated cell sorting analysis of neuraminidase-treated K562 cells showed that the number of FcγRII-specific antibodies that bind to FcγRII increases by 15 to 20% after treatment with neuraminidase. These results indicate that neuraminidase augments ADE of dengue virus infection and that the augmented ADE is mediated through FcγRII.

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1993-05-01
2024-03-28
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References

  1. Anderson C. L. 1982; Isolation of the receptor for the IgG from a human monocyte cell line (U937) and from human peripheral blood monocytes. Journal of Experimental Medicine 156:1794–1805
    [Google Scholar]
  2. Brodsky F. M., Bodmer W. F., Parham P. 1979; Characterization of a monoclonal anti-β-microglobulin antibody and its use in the genetic and biochemical analysis of major histocompatibility antigens. European Journal of Immunology 9:536–545
    [Google Scholar]
  3. Burke D. S., Nisalak A., Johnson D. E., Scott R. M. 1988; A prospective study of dengue infections in Bangkok. American Journal of Tropical Medicine and Hygiene 38:172–180
    [Google Scholar]
  4. Debets J. M. H., Van de Winkel J. G. J., Ceuppens J. L., Dieterens I. E. M., Buurman W. A. 1990; Cross-linking of both FcγRI and FcγRII induces secretion of tumor necrosis factor by human monocytes requiring high affinity Fc-FcγR interactions. Journal of Immunology 144:1304–1310
    [Google Scholar]
  5. Guyre P. M., Morganelli P., Miller R. 1983; Recombinant immune interferon increases immunoglobulin G Fc receptors on cultured human mononuclear phagocytes. Journal of Clinical Investigation 72:393–397
    [Google Scholar]
  6. Halstead S. B. 1988; Pathogenesis of dengue. Challenges to molecular biology. Science 239:476–481
    [Google Scholar]
  7. Halstead S. B., Nimmannitya S., Cohen S. N. 1970; Observations related to pathogenesis of dengue hemorrhagic fever. IV. Relation of disease severity to antibody response and virus recovered. Yale Journal of Biology and Medicine 42:311–328
    [Google Scholar]
  8. Halstead S. B., O’Rourke E. J., Allison A. C. 1977; Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. Journal of Experimental Medicine 146:201–217
    [Google Scholar]
  9. Henchal E. A., McCown J. M., Burke D. S., Seguin M. C., Brandt W. E. 1985; Epitope analysis of antigenic determinants on the surface of dengue-2 virions using monoclonal antibodies. American Journal of Tropical Medicine and Hygiene 34:162–169
    [Google Scholar]
  10. Innis B. L., Eckels K. H., Kraiselburd E., Dubois D. R., Meadors G. F., Gubler D. J., Burke D. S., Bancroft W. H. 1988; Virulence of a live dengue virus vaccine candidate: a possible new marker of dengue virus attenuation. Journal of Infectious Diseases 158:876–880
    [Google Scholar]
  11. Kontny U., Kurane I., Ennis F. A. 1988; Interferon gamma augments Fey receptor-mediated dengue virus infection of human monocytic cells. Journal of Virology 62:3928–3933
    [Google Scholar]
  12. Kurane I., Hebblewaite D., Brandt W., Ennis F. A. 1984; Lysis of dengue-infected cells by natural cell-mediated cytotoxicity and antibody-dependent cell-mediated cytotoxicity. Journal of Virology 52:223–230
    [Google Scholar]
  13. LaMarco K. L., Diven W. F., Glew R. H. 1986; Experimental alteration of chinchilla middle ear mucosae by bacterial neuraminidase. Annals of Otology, Rhinology and Laryngology 95:304–308
    [Google Scholar]
  14. Liesveld J. L., Abboud C. N., Looney R. J., Ryan D. H., Brennan J. K. 1988; Expression of IgG Fc receptors in myeloid leukemic cell lines. Effect of colony-stimulating factors and cytokines. Journal of Immunology 140:1527–1533
    [Google Scholar]
  15. Littaua R., Kurane I., Ennis F. A. 1990; Human IgG FcγRII mediates antibody dependent enhancement of dengue virus infection. Journal of Immunology 144:3183–3186
    [Google Scholar]
  16. Looney R. J., Abraham G. N., Anderson C. L. 1986; Human monocytes and U937 cells bear two distinct Fc receptors for IgG. Journal of Immunology 136:1641–1647
    [Google Scholar]
  17. Lozzio C. B., Lozzio B. B. 1975; Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45:321–334
    [Google Scholar]
  18. Mady B. M., Erbe D. V., Kurane I., Fanger M. W., Ennis F. A. 1991; Antibody-dependent enhancement of dengue virus infection mediated by bispecific antibodies against cell surface molecules other than Fc receptors. Journal of Immunology 147:3139–3144
    [Google Scholar]
  19. Morens D. M., Venkateshan C. N., Halstead S. B. 1987; Dengue 4 virus monoclonal antibodies identify epitopes that mediate immune infection enhancement of dengue 2 viruses. Journal of General Virology 68:91–98
    [Google Scholar]
  20. Peiris J. S. M., Gordon S., Unkeless J. C., Porterfield J. S. 1981; Monoclonal anti-Fc receptor IgG blocks antibody enhancement of viral replication in macrophages. Nature, London 289:189–191
    [Google Scholar]
  21. Perussia B., Payton E. T., Lazarus R., Fanning U., Trincheri G. 1983; Immune interferon induces the receptor for monomeric IgGl on human monocytic and myeloid cells. Journal of Experimental Medicine 158:1092–1113
    [Google Scholar]
  22. Rosenfeld S. I., Looney R. J., Leddy J. P., Phipps D. C., Abraham G. N., Anderson C. L. 1985; Human platelet Fc receptor for immunoglobulin G. Identification as a 40000-molecular-weight membrane protein shared by monocytes. Journal of Clinical Investigation 76:2317–2322
    [Google Scholar]
  23. Sangkawibha N., Roujanasuphot S., Ahandrik S., Viriyapongse S., Jatanasen J., Salitul V., Phanthumachinda B., Halstead S. B. 1984; Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayond, Thailand. American Journal of Epidemiology 120:653–669
    [Google Scholar]
  24. Tax W. J. M., Van de Winkel J. 1990; Human Fey receptor II: a standby receptor activated by proteolysis. Immunology Today 11:308–310
    [Google Scholar]
  25. Unkeless J. C. 1989; Function and heterogenicity of human Fc receptors for immunoglobulin G. Journal of Clinical Investigation 83:355–361
    [Google Scholar]
  26. Van de Winkel J. G. J., Anderson C. L. 1991; Biology of human immunoglobulin G Fc receptors. Journal of Leukocyte Biology 49:511–524
    [Google Scholar]
  27. Van de Winkel J. G. J., Van Ommen R., Huizinga T. W. J., De Raad M. A. V. M., Tuijnman W. B., Grobnen P. J. T. A., Capel P. J. A., Koene R. A. P., Tax W. J. M. 1989; Proteolysis induces increased binding affinity of the monocyte type II FcR for human IgG. Journal of Immunology 143:571–578
    [Google Scholar]
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