1887

Abstract

Sub-neutralizing concentrations of antibody to dengue virus (DENV) enhance DENV infection of Fc receptor-expressing cells. This phenomenon, referred to as antibody-dependent enhancement (ADE), has been hypothesized to be responsible for the severe form of DENV infection, including dengue haemorrhagic fever and dengue shock syndrome. To analyse further the mechanisms of ADE , this study introduced a series of cytoplasmic mutants into human FcRIIA. The mutated FcRIIA was then expressed on COS-7 cells to see whether these mutants could enhance DENV infection. Wild-type FcRIIA enhanced DENV infection, consistent with previous reports using FcR-positive monocytes. Disruption of the immune tyrosine activation motif (ITAM) in the cytoplasmic domain of FcRIIA or removing the sequences between the two ITAM regions eliminated ADE. These findings suggest that the specific structure of the FcRIIA cytoplasmic domain is essential for the ability of FcRIIA to mediate ADE.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.014829-0
2010-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/1/103.html?itemId=/content/journal/jgv/10.1099/vir.0.014829-0&mimeType=html&fmt=ahah

References

  1. Abdel Shakor, A. B., Kwiatkowska, K. & Sobota, A.(2004). Cell surface ceramide generation precedes and controls FcγRII clustering and phosphorylation in rafts. J Biol Chem 279, 36778–36787.[CrossRef] [Google Scholar]
  2. An, T.(1982). Rapid endocytosis of soluble immune complexes by Fc receptors of normal human neutrophils. Immunology 45, 413–422. [Google Scholar]
  3. Anderson, K. B., Chunsuttiwat, S., Nisalak, A., Mammen, M. P., Libraty, D. H., Rothman, A. L., Green, S., Vaughn, D. W., Ennis, F. A. & Endy, T. P.(2007). Burden of symptomatic dengue infection in children at primary school in Thailand: a prospective study. Lancet 369, 1452–1459.[CrossRef] [Google Scholar]
  4. Barabé, F., Rollet-Labelle, E., Gilbert, C., Fernandes, M. J., Naccache, S. N. & Naccache, P. H.(2002). Early events in the activation of FcγRIIA in human neutrophils: stimulated insolubilization, translocation to detergent-resistant domains, and degradation of FcγRIIA. J Immunol 168, 4042–4049.[CrossRef] [Google Scholar]
  5. Barnes, N. C., Powell, M. S., Trist, H. M., Gavin, A. L., Wines, B. D. & Hogarth, P. M.(2006). Raft localisation of FcγRIIA and efficient signaling are dependent on palmitoylation of cysteine 208. Immunol Lett 104, 118–123.[CrossRef] [Google Scholar]
  6. Booth, J. W., Kim, M., Jankowski, A., Schreiber, A. D. & Grinstein, S.(2002). Contrasting requirements for ubiquitylation during Fc receptor-mediated endocytosis and phagocytosis. EMBO J 21, 251–258.[CrossRef] [Google Scholar]
  7. Brooks, D. G., Qiu, W. Q., Luster, A. D. & Ravetch, J. V.(1989). Structure and expression of human IgG FcRII (CD32). J Exp Med 170, 1369–1385.[CrossRef] [Google Scholar]
  8. Davis, W., Harrison, P. T., Hutchinson, M. J. & Allen, J. M.(1995). Two distinct regions of FcγRI initiate separate signalling pathways involved in endocytosis and phagocytosis. EMBO J 14, 432–441. [Google Scholar]
  9. García-García, E. & Rosales, C.(2002). Signal transduction during Fc receptor-mediated phagocytosis. J Leukoc Biol 72, 1092–1108. [Google Scholar]
  10. Gessner, J. E., Heiken, H., Tamm, A. & Schmidt, R. E.(1998). The IgG Fc receptor family. Ann Hematol 76, 231–248.[CrossRef] [Google Scholar]
  11. Graham, R. R., Juffrie, M., Tan, R., Hayes, C. G., Laksono, I., Ma'roef, C., Erlin, Sutaryo, Porter, K. R. & Halstead, S. B.(1999). A prospective seroepidemiologic study on dengue in children four to nine years of age in Yogyakarta, Indonesia. I. Studies in 1995–1996. Am J Trop Med Hyg 61, 412–419. [Google Scholar]
  12. Huang, M. M., Indik, Z., Brass, L. F., Hoxie, J. A., Schreiber, A. D. & Brugge, J. S.(1992). Activation of FcγRII induces tyrosine phosphorylation of multiple proteins including FcγRII. J Biol Chem 267, 5467–5473. [Google Scholar]
  13. Indik, Z., Kelly, C., Chien, P., Levinson, A. I. & Schreiber, A. D.(1991). Human FcγRII, in the absence of other Fcγ receptors, mediates a phagocytic signal. J Clin Invest 88, 1766–1771.[CrossRef] [Google Scholar]
  14. Indik, Z. K., Park, J. G., Hunter, S. & Schreiber, A. D.(1995a). Structure/function relationships of Fcγ receptors in phagocytosis. Semin Immunol 7, 45–54.[CrossRef] [Google Scholar]
  15. Indik, Z. K., Park, J. G., Hunter, S. & Schreiber, A. D.(1995b). The molecular dissection of Fcγ receptor mediated phagocytosis. Blood 86, 4389–4399. [Google Scholar]
  16. Ito, M., Yamada, K., Takasaki, T., Pandey, B., Nerome, R., Tajima, S., Morita, K. & Kurane, I.(2007). Phylogenetic analysis of dengue viruses isolated from imported dengue patients: possible aid for determining the countries where infections occurred. J Travel Med 14, 233–244.[CrossRef] [Google Scholar]
  17. Kim, M.-K., Huang, Z.-Y., Hwang, P.-H., Jones, B. A., Sato, N., Hunter, S., Kim-Han, T.-H., Worth, R. G., Indik, Z. K. & Schreiber, A. D.(2003). Fcγ receptor transmembrane domains: role in cell surface expression, γ chain interaction, and phagocytosis. Blood 101, 4479–4484.[CrossRef] [Google Scholar]
  18. Kindzelskii, A. L., Xue, W., Todd, R. F., III, Boxer, L. A. & Petty, H. R.(1994). Abberant capping of membrane proteins on neutrophils from patients with leukocyte adhesion deficiency. Blood 83, 1650–1655. [Google Scholar]
  19. Kontny, U., Kurane, I. & Ennis, F. A.(1988). Gamma interferon augments Fcγ receptor-mediated dengue virus infection of human monocytic cells. J Virol 62, 3928–3933. [Google Scholar]
  20. Kurane, I. & Ennis, F.(1992). Immunity and immunopathology in dengue virus infections. Semin Immunol 4, 121–127. [Google Scholar]
  21. Kwiatkowska, K., Frey, J. & Sobota, A.(2003). Phosphorylation of FcγRIIA is required for the receptor-induced actin rearrangement and capping: the role of membrane rafts. J Cell Sci 116, 537–550.[CrossRef] [Google Scholar]
  22. Littaua, R., Kurane, I. & Ennis, F. A.(1990). Human IgG Fc receptor II mediates antibody-dependent enhancement of dengue virus infection. J Immunol 144, 3183–3186. [Google Scholar]
  23. Mady, B. J., 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 Fcγ receptors. J Immunol 147, 3139–3144. [Google Scholar]
  24. Mero, P., Zhang, C. Y., Huang, Z., Kim, M., Schreiber, A. D., Grinstein, S. & Booth, J. W.(2006). Phosphorylation-independent ubiquitylation and endocytosis of FcγRIIA. J Biol Chem 281, 33242–33249.[CrossRef] [Google Scholar]
  25. Mitchell, M. A., Huang, M. M., Chien, P., Indik, Z. K., Pan, X. Q. & Schreiber, A. D.(1994). Substitutions and deletions in the cytoplasmic domain of the phagocytic receptor FcγRIIA: effect on receptor tyrosine phosphorylation and phagocytosis. Blood 84, 1753–1759. [Google Scholar]
  26. Noisakran, S. & Perng, G. C.(2008). Alternate hypothesis on the pathogenesis of dengue hemorrhagic fever (DHF)/dengue shock syndrome (DSS) in dengue virus infection. Exp Biol Med (Maywood) 233, 401–408.[CrossRef] [Google Scholar]
  27. Okanurak, K., Sornmani, S. & Indaratna, K.(1997). The cost of dengue hemorrhagic fever in Thailand. Southeast Asian J Trop Med Public Health 28, 711–717. [Google Scholar]
  28. Ravetch, J. V. & Kinet, J. P.(1991). Fc receptors. Annu Rev Immunol 9, 457–492.[CrossRef] [Google Scholar]
  29. Rodrigo, W. W., Jin, X., Blackley, S. D., Rose, R. C. & Schlesinger, J. J.(2006). Differential enhancement of dengue virus immune complex infectivity mediated by signaling-competent and signaling-incompetent human FcγRIA (CD64) or FcγRIIA (CD32). J Virol 80, 10128–10138.[CrossRef] [Google Scholar]
  30. Ruangjirachuporn, W., Boonpucknavig, S. & Nimmanitya, S.(1979). Circulating immune complexes in serum from patients with dengue haemorrhagic fever. Clin Exp Immunol 36, 46–53. [Google Scholar]
  31. Sangkawibha, N., Rojanasuphot, S., Ahandrik, S., Viriyapongse, S., Jatanasen, S., Salitul, V., Phanthumachinda, B. & Halstead, S. B.(1984). Risk factors in dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120, 653–669. [Google Scholar]
  32. Schlesinger, J. J. & Chapman, S. E.(1999). Influence of the human high-affinity IgG receptor FcγRI (CD64) on residual infectivity of neutralized dengue virus. Virology 260, 84–88.[CrossRef] [Google Scholar]
  33. Sobota, A., Strzelecka-Kiliszek, A., Gładkowska, E., Yoshida, K., Mrozińska, K. & Kwiatkowska, K.(2005). Binding of IgG-opsonized particles to FcγR is an active stage of phagocytosis that involves receptor clustering and phosphorylation. J Immunol 175, 4450–4457.[CrossRef] [Google Scholar]
  34. Vaughn, D. W., Green, S., Kalayanarooj, S., Innis, B. L., Nimmannitya, S., Suntayakorn, S., Endy, T. P., Raengsakulrach, B., Rothman, A. L. & other authors(2000). Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181, 2–9.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.014829-0
Loading
/content/journal/jgv/10.1099/vir.0.014829-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error