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Journal of Tropical Medicine
Volume 2012, Article ID 639304, 7 pages
http://dx.doi.org/10.1155/2012/639304
Review Article

Differential Regulation of the Immune Response in the Spleen and Liver of Mice Infected with Leishmania donovani

1Department of Molecular and Comparative Pathobiology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA
2Institut National de la Recherche Scientifique, Institut Armand-Frappier, Laval, QC, Canada

Received 12 April 2011; Accepted 21 May 2011

Academic Editor: Christian Engwerda

Copyright © 2012 Rashmi Bankoti and Simona Stäger. 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. J. J. Stern, M. J. Oca, B. Y. Rubin, S. L. Anderson, and H. W. Murray, “Role of L3T4+ and Lyt-2+ cells in experimental visceral leishmaniasis,” Journal of Immunology, vol. 140, no. 11, pp. 3971–3977, 1988. View at Google Scholar · View at Scopus
  2. M. Ato, S. Stäger, C. R. Engwerda, and P. M. Kaye, “Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis,” Nature Immunology, vol. 3, no. 12, pp. 1185–1191, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Joshi, S. Rodriguez, V. Perovic, I. A. Cockburn, and S. Stäge, “B7-H1 blockade increases survival of dysfunctional CD8(+) T cells and confers protection against Leishmania donovani infections,” PLoS Pathogens, vol. 5, no. 5, Article ID e1000431, 2009. View at Google Scholar
  4. M. Ato, A. Maroof, S. Zubairi, H. Nakano, T. Kakiuchi, and P. M. Kaye, “Loss of dendritic cell migration and impaired resistance to Leishmania donovani infection in mice deficient in CCL19 and CCL21,” Journal of Immunology, vol. 176, no. 9, pp. 5486–5493, 2006. View at Google Scholar · View at Scopus
  5. C. R. Engwerda, M. Ato, S. E. J. Cotterell et al., “A role for tumor necrosis factor-α in remodeling the splenic marginal zone during Leishmania donovani infection,” American Journal of Pathology, vol. 161, no. 2, pp. 429–437, 2002. View at Google Scholar · View at Scopus
  6. A. C. Stanley and C. R. Engwerda, “Balancing immunity and pathology in visceral leishmaniasis,” Immunology and Cell Biology, vol. 85, no. 2, pp. 138–147, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. P. M. Kaye, M. Svensson, M. Ato et al., “The immunopathology of experimental visceral leishmaniasis,” Immunological Reviews, vol. 201, pp. 239–253, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. C. R. Engwerda and P. M. Kaye, “Organ-specific immune responses associated with infectious disease,” Immunology Today, vol. 21, no. 2, pp. 73–78, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. P. M. Gorak, C. R. Engwerda, and P. M. Kaye, “Dendritic cells, but not macrophages, produce IL-12 immediately following Leishmania donovani infection,” European Journal of Immunology, vol. 28, no. 2, pp. 687–695, 1998. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Stager, A. Maroof, S. Zubairi, S. L. Sanos, M. Kopf, and P. M. Kaye, “Distinct roles for IL-6 and IL-12p40 in mediating protection against Leishmania donovani and the expansion of IL-CD4+CD25+ T cells,” European Journal of Immunology, vol. 36, no. 7, pp. 1764–1771, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. S. C. Smelt, C. R. Engwerda, M. McCrossen, and P. M. Kaye, “Destruction of follicular dendritic cells during chronic visceral leishmaniasis,” Journal of Immunology, vol. 158, no. 8, pp. 3813–3821, 1997. View at Google Scholar · View at Scopus
  12. J. E. Dalton, A. Maroof, B. M. J. Owens et al., “Inhibition of receptor tyrosine kinases restores immunocompetence and improves immune-dependent chemotherapy against experimental leishmaniasis in mice,” Journal of Clinical Investigation, vol. 120, no. 4, pp. 1204–1216, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. R. J. Greenwald, G. J. Freeman, and A. H. Sharpe, “The B7 family revisited,” Annual Review of Immunology, vol. 23, pp. 515–548, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Chen, “Co-inhibitory molecules of the B7-CD28 family in the control of T-cell immunity,” Nature Reviews Immunology, vol. 4, no. 5, pp. 336–347, 2004. View at Google Scholar · View at Scopus
  15. G. J. Freeman, A. J. Long, Y. Iwai et al., “Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation,” Journal of Experimental Medicine, vol. 192, no. 7, pp. 1027–1034, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Dong, S. E. Strome, D. R. Salomao et al., “Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion,” Nature Medicine, vol. 8, no. 8, pp. 793–800, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. J. Hernández-Ruiz, N. Salaiza-Suazo, G. Carrada et al., “CD8 cells of patients with diffuse cutaneous leishmaniasis display functional exhaustion: the latter is reversed, in vitro, by TLR2 agonists,” PLoS Neglected Tropical Diseases, vol. 4, no. 11, article e871, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. F. Grosso, M. V. Goldberg, D. Getnet et al., “Functionally distinct LAG-3 and PD-1 subsets on activated and chronically stimulated CD8 T cells,” Journal of Immunology, vol. 182, no. 11, pp. 6659–6669, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. C. J. Workman, L. S. Cauley, I. J. Kim, M. A. Blackman, D. L. Woodland, and D. A. A. Vignali, “Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo,” Journal of Immunology, vol. 172, no. 9, pp. 5450–5455, 2004. View at Google Scholar · View at Scopus
  20. C. J. Workman and D. A. A. Vignali, “The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T cells,” European Journal of Immunology, vol. 33, no. 4, pp. 970–979, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Favali, D. Costa, L. Afonso et al., “Role of costimulatory molecules in immune response of patients with cutaneous leishmaniasis,” Microbes and Infection, vol. 7, no. 1, pp. 86–92, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. S. Khan, D. J. Burt, C. Ralph, F. C. Thistlethwaite, R. E. Hawkins, and E. Elkord, “Tremelimumab (anti-CTLA4) mediates immune responses mainly by direct activation of T effector cells rather than by affecting T regulatory cells,” Clinical Immunology, vol. 138, no. 1, pp. 85–96, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. L. Murphy, C. R. Engwerda, P. M. A. Gorak, and P. M. Kaye, “B7-2 blockade enhances T cell responses to Leishmania donovani,” Journal of Immunology, vol. 159, no. 9, pp. 4460–4466, 1997. View at Google Scholar · View at Scopus
  24. S. Zubairi, S. L. Sanos, S. Hill, and P. M. Kaye, “Immunotherapy with OX40L-Fc or anti-CTLA-4 enhances local tissue responses and killing of Leishmania donovani,” European Journal of Immunology, vol. 34, no. 5, pp. 1433–1440, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. M. L. Murphy, S. E. J. Cotterell, P. M. A. Gorak, C. R. Engwerda, and P. M. Kaye, “Blockade of CTLA-4 enhances host resistance to the intracellular pathogen, Leishmania donovani,” Journal of Immunology, vol. 161, no. 8, pp. 4153–4160, 1998. View at Google Scholar · View at Scopus
  26. H. W. Murray, C. M. Lu, S. Mauze et al., “Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy,” Infection and Immunity, vol. 70, no. 11, pp. 6284–6293, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. M. L. Murphy, U. Wille, E. N. Villegas, C. A. Hunter, and J. P. Farrell, “IL-10 mediates susceptibility to Leishmania donovani infection,” European Journal of Immunology, vol. 31, no. 10, pp. 2848–2856, 2001. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Belkaid, C. A. Piccirillo, S. Mendez, E. M. Shevach, and D. L. Sacks, “CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity,” Nature, vol. 420, no. 6915, pp. 502–507, 2002. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Nylén and D. Sacks, “Interleukin-10 and the pathogenesis of human visceral leishmaniasis,” Trends in Immunology, vol. 28, no. 9, pp. 378–384, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Ranatunga, C. M. Hedrich, W. Fengying et al., “A human IL10 BAC transgene reveals tissue-specific control of IL-10 expression and alters disease outcome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 40, pp. 17123–17128, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Maroof, L. Beattie, S. Zubairi, M. Svensson, S. Stager, and P. M. Kaye, “Posttranscriptional regulation of II10 gene expression allows natural killer cells to express immunoregulatory function,” Immunity, vol. 29, no. 2, pp. 295–305, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Svensson, A. Maroof, M. Ato, and P. M. Kaye, “Stromal cells direct local differentiation of regulatory dendritic cells,” Immunity, vol. 21, no. 6, pp. 805–816, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. D. L. Sacks, P. A. Scott, R. Asofsky, and F. A. Sher, “Cutaneous leishmaniasis in anti-IgM-treated mice: enhanced resistance due to functional depletion of a B cell-dependent T cell involved in the suppressor pathway,” Journal of Immunology, vol. 132, no. 4, pp. 2072–2077, 1984. View at Google Scholar · View at Scopus
  34. E. Deak, A. Jayakumar, K. W. Cho et al., “Murine visceral leishmaniasis: IgM and polyclonal B-cell activation lead to disease exacerbation,” European Journal of Immunology, vol. 40, no. 5, pp. 1355–1368, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. S. C. Smelt, S. E. J. Cotterell, C. R. Engwerda, and P. M. Kaye, “B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology,” Journal of Immunology, vol. 164, no. 7, pp. 3681–3688, 2000. View at Google Scholar · View at Scopus
  36. C. Ronet, Y. Hauyon-La Torre, M. Revaz-Breton et al., “Regulatory B cells shape the development of Th2 immune responses in BALB/c mice infected with Leishmania major through IL-10 production,” Journal of Immunology, vol. 184, no. 2, pp. 886–894, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Miles, S. M. Conrad, R. G. Alves, S. M. B. Jeronimo, and D. M. Mosser, “A role for IgG immune complexes during infection with the intracellular pathogen Leishmania,” Journal of Experimental Medicine, vol. 201, no. 5, pp. 747–754, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. M. M. Kane and D. M. Mosser, “The role of IL-10 in promoting disease progression in Leishmaniasis,” Journal of Immunology, vol. 166, no. 2, pp. 1141–1147, 2001. View at Google Scholar · View at Scopus
  39. F. Martin and J. F. Kearney, “Marginal-zone B cells,” Nature Reviews Immunology, vol. 2, no. 5, pp. 323–335, 2002. View at Google Scholar · View at Scopus
  40. T. Lopes-Carvalho and J. F. Kearney, “Development and selection of marginal zone B cells,” Immunological Reviews, vol. 197, pp. 192–205, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Balazs, F. Martin, T. Zhou, and J. F. Kearney, “Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses,” Immunity, vol. 17, no. 3, pp. 341–352, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. A. M. Oliver, F. Martin, and J. F. Kearney, “IgM(high)CD21(high) lymphocytes enriched in the splenic marginal zone generate effector cells more rapidly than the bulk of follicular B cells,” Journal of Immunology, vol. 162, no. 12, pp. 7198–7207, 1999. View at Google Scholar · View at Scopus
  43. G. Cinamon, M. A. Zachariah, O. M. Lam, F. W. Foss, and J. G. Cyster, “Follicular shuttling of marginal zone B cells facilitates antigen transport,” Nature Immunology, vol. 9, no. 1, pp. 54–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. E. C. Whipple, R. S. Shanahan, A. H. Ditto, R. P. Taylor, and M. A. Lindorfer, “Analyses of the in vivo trafficking of stoichiometric doses of an anti-complement receptor 1/2 monoclonal antibody infused intravenously in mice,” Journal of Immunology, vol. 173, no. 4, pp. 2297–2306, 2004. View at Google Scholar · View at Scopus
  45. K. Suzuki, I. Grigorova, T. G. Phan, L. M. Kelly, and J. G. Cyster, “Visualizing B cell capture of cognate antigen from follicular dendritic cells,” Journal of Experimental Medicine, vol. 206, no. 7, pp. 1485–1493, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. A. R. Ferguson, M. E. Youd, and R. B. Corley, “Marginal zone B cells transport and deposit IgM-containing immune complexes onto follicular dendritic cells,” International Immunology, vol. 16, no. 10, pp. 1411–1422, 2004. View at Publisher · View at Google Scholar · View at Scopus
  47. M. E. Youd, A. R. Ferguson, and R. B. Corley, “Synergistic roles of IgM and complement in antigen trapping and follicular localization,” European Journal of Immunology, vol. 32, no. 8, pp. 2328–2337, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Rajewsky, “Clonal selection and learning in the antibody system,” Nature, vol. 381, no. 6585, pp. 751–758, 1996. View at Publisher · View at Google Scholar · View at Scopus
  49. A. C. Ghose, J. P. Haldar, and S. C. Pal, “Serological investigations on Indian kala-azar,” Clinical & Experimental Immunology, vol. 40, no. 2, pp. 318–326, 1980. View at Google Scholar · View at Scopus
  50. L. C. Pontes de Carvalho, R. Badaro, and E. M. Carvalho, “Nature and incidence of erythrocyte-bound IgG and some aspects of the physiopathogenesis of anaemia in American visceral leishmaniasis,” Clinical & Experimental Immunology, vol. 64, no. 3, pp. 495–502, 1986. View at Google Scholar · View at Scopus
  51. H. Louzir, L. Belal-Kacemi, A. Sassi, D. Laouini, R. B. Ismail, and K. Dellagi, “Natural autoantibodies, IgG antibodies to tetanus toxoid and CD5+ B cells in patients with Mediterranean visceral leishmaniasis. The Leishmania study group,” Clinical & Experimental Immunology, vol. 95, no. 3, pp. 479–484, 1994. View at Google Scholar
  52. B. Galvao-Castro, J. A. Sa Ferreira, and K. F. Marzochi, “Polyclonal B cell activation, circulating immune complexes and autoimmunity in human American visceral leishmaniasis,” Clinical & Experimental Immunology, vol. 56, no. 1, pp. 58–66, 1984. View at Google Scholar · View at Scopus
  53. C. Ronet, H. Voigt, H. Himmelrich et al., “Leishmania major-specific B cells are necessary for Th2 cell development and susceptibility to L. major LV39 in BALB/c mice,” Journal of Immunology, vol. 180, no. 7, pp. 4825–4835, 2008. View at Google Scholar · View at Scopus
  54. H. W. Murray, “Tissue granuloma structure-function in experimental visceral leishmaniasis,” International Journal of Experimental Pathology, vol. 82, no. 5, pp. 249–267, 2001. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Scharton-Kersten, L. C. C. Afonso, M. Wysocka, G. Trinchieri, and P. Scott, “IL-12 is required for natural killer cell activation and subsequent T helper 1 cell development in experimental Leishmaniasis,” Journal of Immunology, vol. 154, no. 10, pp. 5320–5330, 1995. View at Google Scholar · View at Scopus
  56. H. W. Murray, “Endogenous interleukin-12 regulates acquired resistance in experimental visceral leishmaniasis,” Journal of Infectious Diseases, vol. 175, no. 6, pp. 1477–1479, 1997. View at Google Scholar · View at Scopus
  57. H. W. Murray and J. Hariprashad, “Interleukin 12 is effective treatment for an established systemic intracellular infection: experimental visceral leishmaniasis,” Journal of Experimental Medicine, vol. 181, no. 1, pp. 387–391, 1995. View at Publisher · View at Google Scholar · View at Scopus
  58. H. W. Murray, K. E. Squires, C. D. Miralles et al., “Acquired resistance and granuloma formation in experimental visceral leishmaniasis. Differential T cell and lymphokine roles in initial versus established immunity,” Journal of Immunology, vol. 148, no. 6, pp. 1858–1863, 1992. View at Google Scholar · View at Scopus
  59. H. W. Murray and F. Nathan, “Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani,” Journal of Experimental Medicine, vol. 189, no. 4, pp. 741–746, 1999. View at Publisher · View at Google Scholar · View at Scopus
  60. J. S. Cervia, H. Rosen, and H. W. Murray, “Effector role of blood monocytes in experimental visceral leishmaniasis,” Infection and Immunity, vol. 61, no. 4, pp. 1330–1333, 1993. View at Google Scholar · View at Scopus
  61. B. J. Barnes, J. Richards, M. Mancl, S. Hanash, L. Beretta, and P. M. Pitha, “Global and distinct targets of IRF-5 and IRF-7 during innate response to viral infection,” Journal of Biological Chemistry, vol. 279, no. 43, pp. 45194–45207, 2004. View at Publisher · View at Google Scholar · View at Scopus
  62. B. J. Barnes, P. A. Moore, and P. M. Pitha, “Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon α genes,” Journal of Biological Chemistry, vol. 276, no. 26, pp. 23382–23390, 2001. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Paun, J. T. Reinert, Z. Jiang et al., “Functional characterization of murine interferon regulatory factor 5 (IRF-5) and its role in the innate antiviral response,” Journal of Biological Chemistry, vol. 283, no. 21, pp. 14295–14308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. H. Yanai, H. M. Chen, T. Inuzuka et al., “Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 9, pp. 3402–3407, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Takaoka, H. Yanai, S. Kondo et al., “Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors,” Nature, vol. 434, no. 7030, pp. 243–249, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Paun, R. Bankoti, T. Joshi, P. M. Pitha, and S. Stäger, “Critical role of IRF-5 in the development of T helper 1 responses to Leishmania donovani infection,” PLoS Pathogens, vol. 7, no. 1, Article ID e1001246, 2011. View at Google Scholar
  67. T. Krausgruber, K. Blazek, T. Smallie et al., “IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses,” Nature Immunology, vol. 12, no. 3, pp. 231–238, 2011. View at Publisher · View at Google Scholar
  68. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. D. C. Dale, L. Boxer, and W. Conrad Liles, “The phagocytes: neutrophils and monocytes,” Blood, vol. 112, no. 4, pp. 935–945, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Thoma-Uszynski, S. Stenger, O. Takeuchi et al., “Induction of direct antimicrobial activity through mammalian toll-like receptors,” Science, vol. 291, no. 5508, pp. 1544–1547, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Bogdan, “Nitric oxide and the immune response,” Nature Immunology, vol. 2, no. 10, pp. 907–916, 2001. View at Publisher · View at Google Scholar · View at Scopus
  72. H. D. Brightbill, D. H. Libraty, S. R. Krutzik et al., “Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors,” Science, vol. 285, no. 5428, pp. 732–736, 1999. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Schoenemeyer, B. J. Barnes, M. E. Mancl et al., “The interferon regulatory factor, IRF5, is a central mediator of toll-like receptor 7 signaling,” Journal of Biological Chemistry, vol. 280, no. 17, pp. 17005–17012, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Balaraman, P. Tewary, V. K. Singh, and R. Madhubala, “Leishmania donovani induces interferon regulatory factor in murine macrophages: a host defense response,” Biochemical and Biophysical Research Communications, vol. 317, no. 2, pp. 639–647, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. R. Phillips, M. Svensson, N. Aziz et al., “Innate killing of Leishmania donovani by macrophages of the splenic marginal zone requires IRF-7,” PLoS Pathogens, vol. 6, no. 3, Article ID e1000813, 2010. View at Publisher · View at Google Scholar · View at Scopus
  76. C. Matte and A. Descoteaux, “Leishmania donovani amastigotes impair gamma interferon-induced STAT1α nuclear translocation by blocking the interaction between STAT1α and importin-α5,” Infection and Immunity, vol. 78, no. 9, pp. 3736–3743, 2010. View at Publisher · View at Google Scholar · View at Scopus