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Journal of Immunology Research
Volume 2015 (2015), Article ID 840842, 13 pages
http://dx.doi.org/10.1155/2015/840842
Research Article

Downmodulation of Vaccine-Induced Immunity and Protection against the Intracellular Bacterium Francisella tularensis by the Inhibitory Receptor FcγRIIB

1Center for Immunology and Microbial Disease, Albany Medical College, Albany, NY 12208, USA
2Regeneron Pharmaceuticals, 81 Columbia Turnpike, Rensselaer, NY 12144, USA
3Department of Biological Sciences, Seton Hall University, South Orange, NJ 07079, USA
4Regeneron Pharmaceuticals, 777 Old Saw Mill River Road, Tarrytown, NY 10591, USA
5Pfizer, 610 Main Street, Cambridge, MA 02139, USA

Received 25 September 2014; Revised 5 January 2015; Accepted 6 January 2015

Academic Editor: Oscar Bottasso

Copyright © 2015 Brian J. Franz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. Nimmerjahn and J. V. Ravetch, “Fcγ receptors as regulators of immune responses,” Nature Reviews Immunology, vol. 8, no. 1, pp. 34–47, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. G. C. Smith and M. R. Clatworthy, “FcγRIIB in autoimmunity and infection: evolutionary and therapeutic implications,” Nature Reviews Immunology, vol. 10, no. 5, pp. 328–343, 2010. View at Publisher · View at Google Scholar
  3. E. J. Gosselin, C. Bitsaktsis, Y. Li, and B. V. Iglesias, “Fc receptor-targeted mucosal vaccination as a novel strategy for the generation of enhanced immunity against mucosal and non-mucosal pathogens,” Archivum Immunologiae et Therapiae Experimentalis, vol. 57, no. 5, pp. 311–323, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. T. L. McGaha, B. Sorrentino, and J. V. Ravetch, “Restoration of tolerance in lupus by targeted inhibitory receptor expression,” Science, vol. 307, no. 5709, pp. 590–593, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Boross, V. L. Arandhara, J. Martin-Ramirez et al., “The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility,” Journal of Immunology, vol. 187, no. 3, pp. 1304–1313, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. R. J. Brownlie, K. E. Lawlor, H. A. Niederer et al., “Distinct cell-specific control of autoimmunity and infection by FcγRIIb,” Journal of Experimental Medicine, vol. 205, no. 4, pp. 883–895, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. Z. Xiang, A. J. Cutler, R. J. Brownlie et al., “FcγRllb controls bone marrow plasma cell persistence and apoptosis,” Nature Immunology, vol. 8, no. 4, pp. 419–429, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. J. V. Ravetch and J.-P. Kinet, “Fc receptors,” Annual Review of Immunology, vol. 9, pp. 457–492, 1991. View at Publisher · View at Google Scholar · View at Scopus
  9. P. J. Maglione, J. Xu, A. Casadevall, and J. Chan, “Fcγ receptors regulate immune activation and susceptibility during Mycobacterium tuberculosis infection,” Journal of Immunology, vol. 180, no. 5, pp. 3329–3338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. I. Gjertsson, S. Kleinau, and A. Tarkowski, “The impact of Fcgamma receptors on Staphylococcus aureus infection,” Microbial Pathogenesis, vol. 33, no. 4, pp. 145–152, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. R. Clatworthy and K. G. C. Smith, “FcγRIIb balances efficient pathogen clearance and the cytokine-mediated consequences of sepsis,” Journal of Experimental Medicine, vol. 199, no. 5, pp. 717–723, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. A. L. Goodman, E. K. Forbes, A. R. Williams et al., “The utility of Plasmodium berghei as a rodent model for anti-merozoite malaria vaccine assessment,” Scientific Reports, vol. 3, article 1706, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. D. B. Rawool, C. Bitsaktsis, Y. Li et al., “Utilization of Fc receptors as a mucosal vaccine strategy against an intracellular bacterium, Francisella tularensis,” Journal of Immunology, vol. 180, no. 8, pp. 5548–5557, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. D. T. Dennis, T. V. Inglesby, D. A. Henderson et al., “Tularemia as a biological weapon: medical and public health management,” Journal of the American Medical Association, vol. 285, no. 21, pp. 2763–2773, 2001. View at Publisher · View at Google Scholar · View at Scopus
  15. J. W. Conlan and P. C. F. Oyston, “Vaccines against Francisella tularensis,” Annals of the New York Academy of Sciences, vol. 1105, pp. 325–350, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Bolland and J. V. Ravetch, “Spontaneous autoimmune disease in FcγRIIB-deficient mice results from strain-specific epistasis,” Immunity, vol. 13, no. 2, pp. 277–285, 2000. View at Publisher · View at Google Scholar · View at Scopus
  17. L. E. Cole, Y. Yang, K. L. Elkins et al., “Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 11, pp. 4343–4348, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. T. Takai, M. Ono, M. Hikida, H. Ohmori, and J. V. Ravetch, “Augmented humoral and anaphylactic responses in FcγRII-deficient mice,” Nature, vol. 379, no. 6563, pp. 346–349, 1996. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Getahun, J. Dahlström, S. Wernersson, and B. Heyman, “IgG2a-mediated enhancement of antibody and T cell responses and its relation to inhibitory and activating Fc-γ receptors,” Journal of Immunology, vol. 172, no. 9, pp. 5269–5276, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Wernersson, M. C. I. Karlsson, J. Dahlström, R. Mattsson, J. S. Verbeek, and B. Heyman, “IgG-mediated enhancement of antibody responses is low in Fc receptor γ chain-deficient mice and increased in FcγRII-deficient mice,” The Journal of Immunology, vol. 163, no. 2, pp. 618–622, 1999. View at Google Scholar · View at Scopus
  21. M. E. Weksler, “Changes in the B-cell repertoire with age,” Vaccine, vol. 18, no. 16, pp. 1624–1628, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. J. T. Schwartz, J. H. Barker, M. E. Long, J. Kaufman, J. McCracken, and L.-A. H. Allen, “Natural IgM mediates complement-dependent uptake of Francisella tularensis by human neutrophils via complement receptors 1 and 3 in nonimmune serum,” Journal of Immunology, vol. 189, no. 6, pp. 3064–3077, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. E. J. Gosselin, D. R. Gosselin, and S. A. Lotz, “Natural killer and CD8 T cells dominate the response by human peripheral blood mononuclear cells to inactivated Francisella tularensis live vaccine strain,” Human Immunology, vol. 66, no. 10, pp. 1039–1049, 2005. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Baumgarth, “The double life of a B-1 cell: self-reactivity selects for protective effector functions,” Nature Reviews Immunology, vol. 11, no. 1, pp. 34–46, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Baumgarth, J. W. Tung, and L. A. Herzenberg, “Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion,” Springer Seminars in Immunopathology, vol. 26, no. 4, pp. 347–362, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. G. S. Kirimanjeswara, J. M. Golden, C. S. Bakshi, and D. W. Metzger, “Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis,” The Journal of Immunology, vol. 179, no. 1, pp. 532–539, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. A. A. I. Kostiala, D. D. McGregor, and P. S. Logie, “Tularaemia in the rat. I. The cellular basis of host resistance to infection,” Immunology, vol. 28, no. 5, pp. 855–869, 1975. View at Google Scholar · View at Scopus
  28. R. KuoLee, X. Zhao, J. Austin, G. Harris, J. W. Conlan, and W. Chen, “Mouse model of oral infection with virulent type A Francisella tularensis,” Infection and Immunity, vol. 75, no. 4, pp. 1651–1660, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. S. D. Baron, R. Singh, and D. W. Metzger, “Inactivated Francisella tularensis live vaccine strain protects against respiratory tularemia by intranasal vaccination in an immunoglobulin A-dependent fashion,” Infection and Immunity, vol. 75, no. 5, pp. 2152–2162, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. G. S. Kirimanjeswara, S. Olmos, C. S. Bakshi, and D. W. Metzger, “Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis,” Immunological Reviews, vol. 225, no. 1, pp. 244–255, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. S. R. Slight, L. Monin, R. Gopal et al., “IL-10 restrains IL-17 to limit lung pathology characteristics following pulmonary infection with Francisella tularensis live vaccine strain,” The American Journal of Pathology, vol. 183, no. 5, pp. 1397–1404, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. S. C. Cowley and K. L. Elkins, “Immunity to Francisella,” Frontiers in Microbiology, vol. 2, p. 26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Bitsaktsis, D. B. Rawool, Y. Li, N. V. Kurkure, B. Iglesias, and E. J. Gosselin, “Differential requirements for protection against mucosal challenge with Francisella tularensis in the presence versus absence of cholera toxin B and inactivated F. tularensis,” The Journal of Immunology, vol. 182, no. 8, pp. 4899–4909, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. T. R. Rhinehart-Jones, A. H. Fortier, and K. L. Elkins, “Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells,” Infection and Immunity, vol. 62, no. 8, pp. 3129–3137, 1994. View at Google Scholar · View at Scopus
  35. V. C. Dreisbach, S. Cowley, and K. L. Elkins, “Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon,” Infection and Immunity, vol. 68, no. 4, pp. 1988–1996, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Mara-Koosham, J. A. Hutt, C. R. Lyons, and T. H. Wu, “Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains,” Infection and Immunity, vol. 79, no. 4, pp. 1770–1778, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Kubelkova, Z. Krocova, L. Balonova, J. Pejchal, J. Stulik, and A. Macela, “Specific antibodies protect gamma-irradiated mice against Francisella tularensis infection,” Microbial Pathogenesis, vol. 53, no. 5-6, pp. 259–268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  38. G. R. Klimpel, T. Eaves-Pyles, S. T. Moen et al., “Levofloxacin rescues mice from lethal intra-nasal infections with virulent Francisella tularensis and induces immunity and production of protective antibody,” Vaccine, vol. 26, no. 52, pp. 6874–6882, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. A. A. Melillo, O. Foreman, C. M. Bosio, and K. L. Elkins, “T-bet regulates immunity to Francisella tularensis live vaccine strain infection, particularly in lungs,” Infection and Immunity, vol. 82, no. 4, pp. 1477–1490, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Bitsaktsis, B. V. Iglesias, Y. Li et al., “Mucosal immunization with an unadjuvanted vaccine that targets Streptococcus pneumoniae PspA to human fcγ receptor type I protects against pneumococcal infection through complement- and lactoferrin-mediated bactericidal activity,” Infection and Immunity, vol. 80, no. 3, pp. 1166–1180, 2012. View at Publisher · View at Google Scholar · View at Scopus