About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 719361, 8 pages
http://dx.doi.org/10.1155/2010/719361
Review Article

The Prominent Role of Neutrophils during the Initial Phase of Infection by Leishmania Parasites

WHO Immunology Research and Training Center, Department of Biochemistry, University of Lausanne, 1066 Epalinges, Switzerland

Received 6 July 2009; Accepted 6 August 2009

Academic Editor: Abhay R. Satoskar

Copyright © 2010 Mélanie Charmoy 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. D. Sacks and N. Noben-Trauth, “The immunology of susceptibility and resistance to Leishmania major in mice,” Nature Reviews Immunology, vol. 2, no. 11, pp. 845–858, 2002. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Louis, H. Himmelrich, C. Parra-Lopez, et al., “Regulation of protective immunity against Leishmania major in mice,” Current Opinion in Immunology, vol. 10, no. 4, pp. 459–464, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. W. J. Beil, G. Meinardus-Hager, D. C. Neugebauer, et al., “Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice,” Journal of Leukocyte Biology, vol. 52, no. 2, pp. 135–142, 1992. View at Scopus
  4. F. Tacchini-Cottier, C. Zweifel, Y. Belkaid, et al., “An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major,” Journal of Immunology, vol. 165, no. 5, pp. 2628–2636, 2000. View at Scopus
  5. N. C. Peters, J. G. Egen, N. Secundino, et al., “In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies,” Science, vol. 321, no. 5891, pp. 970–974, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Laufs, K. Muller, J. Fleischer, et al., “Intracellular survival of Leishmania major in neutrophil granulocytes after uptake in the absence of heat-labile serum factors,” Infection and Immunity, vol. 70, no. 2, pp. 826–835, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Gueirard, A. Laplante, C. Rondeau, et al., “Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages,” Cellular Microbiology, vol. 10, no. 1, pp. 100–111, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Aga, D. M. Katschinski, G. van Zandbergen, et al., “Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major,” Journal of Immunology, vol. 169, no. 2, pp. 898–905, 2002. View at Scopus
  9. G. van Zandbergen, M. Klinger, A. Mueller, et al., “Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages,” Journal of Immunology, vol. 173, no. 11, pp. 6521–6525, 2004.
  10. C. Allenbach, C. Zufferey, C. Perez, et al., “Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major,” Journal of Immunology, vol. 176, no. 11, pp. 6656–6664, 2006. View at Scopus
  11. C. Allenbach, P. Launois, C. Mueller, et al., “An essential role for transmembrane TNF in the resolution of the inflammatory lesion induced by Leishmania major infection,” European Journal of Immunology, vol. 38, no. 3, pp. 720–731, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. F. L. Ribeiro-Gomes, A. C. Otero, N. A. Gomes, et al., “Macrophage interactions with neutrophils regulate Leishmania major Infection,” Journal of Immunology, vol. 172, no. 7, pp. 4454–4462, 2004. View at Scopus
  13. T. Laskay, G. van Zandbergen, and W. Solbach, “Neutrophil granulocytes as host cells and transport vehicles for intracellular pathogens: apoptosis as infection-promoting factor,” Immunobiology, vol. 213, no. 3-4, pp. 183–191, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Rousseau, S. Demartino, B. Ferrua, et al., “In vivo involvement of polymorphonuclear neutrophils in Leishmania infantum infection,” BMC Microbiol, vol. 117, 2001.
  15. S. C. Smelt, S. E. Cotterell, C. R. Engwerda, et al., “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 Scopus
  16. E. McFarlane, C. Perez, M. Charmoy, et al., “Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani,” Infection and Immunity, vol. 76, no. 2, pp. 532–541, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. C. Nathan, “Neutrophils and immunity: challenges and opportunities,” Nature Reviews Immunology, vol. 6, no. 3, pp. 173–182, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Romani, A. Mencacci, E. Cenci, et al., “An immunoregulatory role for neutrophils in CD4+ T helper subset selection in mice with candidiasis,” Journal of Immunology, vol. 158, no. 5, pp. 2356–2362, 1997. View at Scopus
  19. K. Tateda, T. A. Moore, J. C. Deng, et al., “Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia,” Journal of Immunology, vol. 166, no. 5, pp. 3355–3361, 2001. View at Scopus
  20. A. Easton, A. Haque, K. Chu, et al., “A critical role for neutrophils in resistance to experimental infection with Burkholderia pseudomallei,” Journal of Infectious Diseases, vol. 195, no. 1, pp. 99–107, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Tsuda, H. Takahashi, M. Kobayashi, et al., “Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus,” Immunity, vol. 21, no. 2, pp. 215–226, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. G. van Zandbergen, N. Hermann, H. Laufs, et al., “Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes,” Infection and Immunity, vol. 70, no. 8, pp. 4177–4184, 2002.
  23. K. Muller, G. van Zandbergen, B. Hansen, et al., “Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice,” Medical Microbiology and Immunology, vol. 190, no. 1-2, pp. 73–76, 2001. View at Scopus
  24. C. T. Weaver, R. D. Hatton, P. R. Mangan, et al., “IL-17 family cytokines and the expanding diversity of effector T cell lineages,” Annual Review of Immunology, pp. 25821–25852, 2007.
  25. S. Lopez Kostka, S. Dinges, K. Griewank, et al., “IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice,” Journal of Immunology, vol. 182, no. 5, pp. 3039–3046, 2009.
  26. L. Q. Vieira, M. Goldschmidt, M. Nashleanas, et al., “Mice lacking the TNF receptor p55 fail to resolve lesions caused by infection with Leishmania major, but control parasite replication,” Journal of Immunology, vol. 157, no. 2, pp. 827–835, 1996. View at Scopus
  27. M. Nashleanas, S. Kanaly, and P. Scott, “Control of Leishmania major infection in mice lacking TNF receptors,” Journal of Immunology, vol. 160, no. 11, pp. 5506–5513, 1998. View at Scopus
  28. S. T. Kanaly, M. Nashleanas, B. Hondowicz, et al., “TNF receptor p55 is required for elimination of inflammatory cells following control of intracellular pathogens,” Journal of Immunology, vol. 163, no. 7, pp. 3883–3889, 1999. View at Scopus
  29. R. Chakour, R. Guler, M. Bugnon, et al., “Both the fas ligand and inducible nitric oxide synthase are needed for control of parasite replication within lesions in mice infected with Leishmania major whereas the contribution of tumor necrosis factor is minimal,” Infection and Immunity, vol. 71, no. 9, pp. 5287–5295, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. U. Ritter, J. Mattner, J. S. Rocha, et al., “The control of Leishmania (Leishmania) major by TNF in vivo is dependent on the parasite strain,” Microbes and Infection, vol. 6, no. 6, pp. 559–565, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Wilhelm, U. Ritter, S. Labbow, et al., “Rapidly fatal Leishmaniasis in resistant C57BL/6 mice lacking TNF,” Journal of Immunology, vol. 166, no. 6, pp. 4012–4019, 2001. View at Scopus
  32. B. K. Wershil and S. J. Galli, “The analysis of mast cell function in vivo using mast cell-deficient mice,” Advances in Experimental Medicine and Biology, pp. 34739–34754, 1994.
  33. M. Maurer, S. Lopez Kostka, F. Siebenhaar, et al., “Skin mast cells control T cell-dependent host defense in Leishmania major infections,” FASEB Journal, vol. 20, no. 14, pp. 2460–2467, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Jacobs, J. Andra, I. Gaworski, et al., “Complement C3 is required for the progression of cutaneous lesions and neutrophil attraction in Leishmania major infection,” Medical Microbiology and Immunology, vol. 194, no. 3, pp. 143–149, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. P. Scapini, J. A. Lapinet-Vera, S. Gasperini, et al., “The neutrophil as a cellular source of chemokines,” Immunological Reviews, pp. 177195–177203, 2000.
  36. R. I. Tepper, R. L. Coffman, and P. Leder, “An eosinophil-dependent mechanism for the antitumor effect of interleukin-4,” Science, vol. 257, no. 5069, pp. 548–551, 1992. View at Scopus
  37. A. F. Lopez, M. Strath, and C. J. Sanderson, “Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies,” British Journal of Haematology, vol. 57, no. 3, pp. 489–494, 1984. View at Scopus
  38. T. J. Fleming, M. L. Fleming, and T. R. Malek, “Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow: RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family,” Journal of Immunology, vol. 151, no. 5, pp. 2399–2408, 1993. View at Scopus
  39. J. M. Daley, A. A. Thomay, M. D. Connolly, et al., “Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice,” Journal of Leukocyte Biology, vol. 83, no. 1, pp. 64–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. G. M. Lima, A. L. Vallochi, U. R. Silva, et al., “The role of polymorphonuclear leukocytes in the resistance to cutaneous Leishmaniasis,” Immunology Letters, vol. 64, no. 2-3, pp. 145–151, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Chen, Z. H. Zhang, T. Watanabe, et al., “The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice,” Parasitology International, vol. 54, no. 2, pp. 109–118, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Charmoy, R. Megnekou, C. Allenbach, et al., “Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection,” Journal of Leukocyte Biology, vol. 82, no. 2, pp. 288–299, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. F. L. Ribeiro-Gomes, M. C. A. Moniz-de-Souza, M. S. Alexandre-Moreira, et al., “Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase,” Journal of Immunology, vol. 179, no. 6, pp. 3988–3994, 2007. View at Scopus
  44. N. C. Peters, N. Kimblin, N. Secundino, et al., “Vector transmission of Leishmania abrogates vaccine-induced protective immunity,” PLoS Pathogens, vol. 5, no. 6, article e1000484, 2009. View at Publisher · View at Google Scholar · View at Scopus