Table of Contents Author Guidelines Submit a Manuscript
Journal of Parasitology Research
Volume 2011, Article ID 316067, 10 pages
http://dx.doi.org/10.1155/2011/316067
Research Article

Trypanosoma congolense Infections: Induced Nitric Oxide Inhibits Parasite Growth In Vivo

1College of Animal Science and Technology, Jilin Agricultural University, Changchun 130118, China
2Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK, Canada S7N 5B4

Received 20 September 2010; Accepted 7 February 2011

Academic Editor: Ana Maria Jansen

Copyright © 2011 Wenfa Lu 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. H. W. Mulligan and W. H. Potts, The African Trypanosomiases, John Wiley & Sons, New York, NY, USA, 1970.
  2. P. Gerold, B. Striepen, B. Reitter et al., “Glycosyl-phosphatidylinositols of Trypanosoma congolense: two common precursors but a new protein-anchor,” Journal of Molecular Biology, vol. 261, no. 2, pp. 181–194, 1996. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Aderem and D. M. Underhill, “Mechanisms of phagocytosis in macrophages,” Annual Review of Immunology, vol. 17, pp. 593–623, 1999. View at Publisher · View at Google Scholar · View at Scopus
  4. S. A. Linehan, L. Martínez-Pomares, and S. Gordon, “Macrophage lectins in host defence,” Microbes and Infection, vol. 2, no. 3, pp. 279–288, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. W. L. Dempsey and J. M. Mansfield, “Lymphocyte function in experimental African trypanosomiasis. V. Role of antibody and the mononuclear phagocyte system in variant-specific immunity,” Journal of Immunology, vol. 130, no. 1, pp. 405–411, 1983. View at Google Scholar · View at Scopus
  6. J. A. Macaskill, P. H. Holmes, D. D. Whitelaw, I. McConnell, F. W. Jennings, and G. M. Urquhart, “Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. II. Mechanisms in immune animals,” Immunology, vol. 40, pp. 629–635, 1980. View at Google Scholar
  7. W. Pan, O. Ogunremi, G. Wei, M. Shi, and H. Tabel, “CR3 (CD11b/CD18) is the major macrophage receptor for IgM antibody-mediated phagocytosis of African trypanosomes: diverse effect on subsequent synthesis of tumor necrosis factor alpha and nitric oxide,” Microbes and Infection, vol. 8, pp. 1209–1218, 2006. View at Google Scholar
  8. M. Shi, G. Wei, W. Pan, and H. Tabel, “Trypanosoma congolense infections: antibody-mediated phagocytosis by Kupffer cells,” Journal of Leukocyte Biology, vol. 76, no. 2, pp. 399–405, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. H. Tabel, R. S. Kaushik, and J. E. Uzonna, “Susceptibility and resistance to Trypanosoma congolense infections,” Microbes and Infection, vol. 2, no. 13, pp. 1619–1629, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. A. E. Balber, J. D. Bangs, S. M. Jones, and R. L. Proia, “Inactivation or elimination of potentially trypanolytic, complement-activating immune complexes by pathogenic trypanosomes,” Infection and Immunity, vol. 24, no. 3, pp. 617–627, 1979. View at Google Scholar · View at Scopus
  11. B. Flemmings and C. Diggs, “Antibody-dependent cytotoxicity against Trypanosoma rhodesiense mediated through an alternative complement pathway,” Infection and Immunity, vol. 19, no. 3, pp. 928–933, 1978. View at Google Scholar · View at Scopus
  12. U. Frevert and E. Reinwald, “Trypanosoma congolense bloodstream forms evade complement lysis in vitro by shedding of immune complexes,” European Journal of Cell Biology, vol. 52, no. 2, pp. 264–269, 1990. View at Google Scholar · View at Scopus
  13. M. Pinder, P. Chassin, and F. Fumoux, “Mechanisms of self-cure from Trypanosoma congolense infection in mice,” Journal of Immunology, vol. 136, no. 4, pp. 1427–1434, 1986. View at Google Scholar · View at Scopus
  14. R. S. Kaushik, J. E. Uzonna, J. R. Gordon, and H. Tabel, “Innate resistance to Trypanosoma congolense infections: differential production of nitric oxide by macrophages from susceptible BALB/c and resistant C57B1/6 mice,” Experimental Parasitology, vol. 92, no. 2, pp. 131–143, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Duleu, P. Vincendeau, P. Courtois et al., “Mouse strain susceptibility to Trypanosome infection: an arginase-dependent effect,” Journal of Immunology, vol. 172, no. 10, pp. 6298–6303, 2004. View at Google Scholar · View at Scopus
  16. A. P. Gobert, S. Semballa, S. Daulouede et al., “Murine macrophages use oxygen- and nitric oxide-dependent mechanisms to synthesize S-nitroso-albumin and to kill extracellular trypanosomes,” Infection and Immunity, vol. 66, no. 9, pp. 4068–4072, 1998. View at Google Scholar · View at Scopus
  17. P. Vincendeau, S. Daulouède, B. Veyret, M. L. Darde, B. Bouteille, and J. L. Lemesre, “Nitric oxide-mediated cytostatic activity on Trypanosoma brucei gambiense and Trypanosoma brucei brucei,” Experimental Parasitology, vol. 75, no. 3, pp. 353–360, 1992. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Sternberg, N. Mabbott, I. Sutherland, and F. Y. Liew, “Inhibition of nitric oxide synthesis leads to reduced parasitemia in murine Trypanosoma brucei infection,” Infection and Immunity, vol. 62, no. 5, pp. 2135–2137, 1994. View at Google Scholar · View at Scopus
  19. C. J. Hertz and J. M. Mansfield, “IFN-γ-dependent nitric oxide production is not linked to resistance in experimental African trypanosomiasis,” Cellular Immunology, vol. 192, no. 1, pp. 24–32, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Sternberg and F. McGuigan, “Nitric oxide mediates suppression of T cell responses in murine Trypanosoma brucei infection,” European Journal of Immunology, vol. 22, no. 10, pp. 2741–2744, 1992. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Magez, M. Radwanska, M. Drennan et al., “Interferon-γ and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 infections,” Journal of Infectious Diseases, vol. 193, no. 11, pp. 1575–1583, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Wei and H. Tabel, “Regulatory T cells prevent control of experimental African trypanosomiasis,” Journal of Immunology, vol. 180, no. 4, pp. 2514–2521, 2008. View at Google Scholar · View at Scopus
  23. H. Tabel, “Activation of the alternative pathway of bovine complement by Trypanosoma congolense,” Parasite Immunology, vol. 4, no. 5, pp. 329–335, 1982. View at Google Scholar · View at Scopus
  24. S. M. Lanham and D. G. Godfrey, “Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose,” Experimental Parasitology, vol. 28, no. 3, pp. 521–534, 1970. View at Google Scholar · View at Scopus
  25. W. M. Moore, R. K. Webber, G. M. Jerome, F. S. Tjoeng, T. P. Misko, and M. G. Currie, “L-N6-(1-Iminoethyl)lysine: a selective inhibitor of inducible nitric oxide synthase,” Journal of Medicinal Chemistry, vol. 37, no. 23, pp. 3886–3888, 1994. View at Google Scholar · View at Scopus
  26. G. A. Morgan, H. B. Laufman, F. P. Otieno-Omondi, and S. J. Black, “Control of G1 to S cell cycle progression of Trypanosoma brucei S427c11 organisms under axenic conditions,” Molecular and Biochemical Parasitology, vol. 57, no. 2, pp. 241–252, 1993. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Noguchi, “Use of flow cytometry for DNA analysis,” in Current Protocols in Immunology, R. Coico, Ed., vol. 1, pp. 571–576, John Wiley & Sons, New York, NY, USA, 1994. View at Google Scholar
  28. E. B. Otesile, M. Lee, and H. Tabel, “Plasma levels of proteins of the alternative complement pathway in inbred mice that differ in resistance to Trypanosoma congolense infections,” Journal of Parasitology, vol. 77, no. 6, pp. 958–964, 1991. View at Google Scholar · View at Scopus
  29. D. Salvemini, P. T. Manning, B. S. Zweifel et al., “Dual inhibition of nitric oxide and prostaglandin production contributes to the antiinflammatory properties of nitric oxide synthase inhibitors,” Journal of Clinical Investigation, vol. 96, no. 1, pp. 301–308, 1995. View at Google Scholar · View at Scopus
  30. A. Diefenbach, H. Schindler, N. Donhauser et al., “Type 1 interferon (IFNα/β) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite,” Immunity, vol. 8, no. 1, pp. 77–87, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. C. Lagneux, D. Godin-Ribuot, P. Demenge, and C. Ribuot, “Nitric oxide and its role in the induction of kinin B-receptors after heat stress in the rat,” Immunopharmacology, vol. 48, no. 1, pp. 43–49, 2000. View at Publisher · View at Google Scholar · View at Scopus
  32. E. B. Otesile and H. Tabel, “Enhanced resistance of highly susceptible Balb/c mice to infection with Trypanosoma congolense after infection and cure,” Journal of Parasitology, vol. 73, no. 5, pp. 947–953, 1987. View at Google Scholar · View at Scopus
  33. M. Shi, W. Pan, and H. Tabel, “Experimental African trypanosomiasis: IFN-γ mediates early mortality,” European Journal of Immunology, vol. 33, no. 1, pp. 108–118, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Tabel, G. Wei, and M. Shi, “T cells and immunopathogenesis of experimental African trypanosomiasis,” Immunological Reviews, vol. 225, no. 1, pp. 128–139, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. N. A. Mabbott, I. A. Sutherland, and J. M. Sternberg, “Trypanosoma brucei is protected from the cytostatic effects of nitric oxide under in vivo conditions,” Parasitology Research, vol. 80, no. 8, pp. 687–690, 1994. View at Google Scholar · View at Scopus
  36. J. E. Uzonna, R. S. Kaushik, J. R. Gordon, and H. Tabel, “Cytokines and antibody responses during Trypanosoma congolense infections in two inbred mouse strains that differ in resistance,” Parasite Immunology, vol. 21, no. 2, pp. 57–71, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. R. E. Mebius, M. A. Nolte, and G. Kraal, “Development and function of the splenic marginal zone,” Critical Reviews in Immunology, vol. 24, no. 6, pp. 449–464, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. J. E. Strickler and C. L. Patton, “Adenosine 3',5' monophosphate in reproducing and differentiated trypanosomes,” Science, vol. 190, no. 4219, pp. 1110–1112, 1975. View at Google Scholar · View at Scopus
  39. D. S. Wechsler and P. A. L. Kongshavn, “Characterization of antibodies mediating protection and cure of Trypanosoma musculi infection in mice,” Infection and Immunity, vol. 48, no. 3, pp. 787–794, 1985. View at Google Scholar · View at Scopus
  40. V. Le Cabec, S. Carréno, A. Moisand, C. Bordier, and I. Maridonneau-Parini, “Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively,” Journal of Immunology, vol. 169, no. 4, pp. 2003–2009, 2002. View at Google Scholar · View at Scopus
  41. B. P. Thornton, V. Větvička, M. Pitman, R. C. Goldman, and G. D. Ross, “Analysis of the sugar specificity and molecular location of the β-glucan-binding lectin site of complement receptor type 3 (CD11D/CD18),” Journal of Immunology, vol. 156, no. 3, pp. 1235–1246, 1996. View at Google Scholar · View at Scopus
  42. J. Yan, V. Větvička, YU. Xia, M. Hanikýřová, T. N. Mayadas, and G. D. Ross, “Critical role of Kupffer cell CR3 (CD11b/CD18) in the clearance of IgM-opsonized erythrocytes or soluble β-glucan,” Immunopharmacology, vol. 46, no. 1, pp. 39–54, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. S. P. Coller, J. M. Mansfield, and D. M. Paulnock, “Glycosylinositolphosphate soluble variant surface glycoprotein inhibits IFN-γ-induced nitric oxide production via reduction in STAT1 phosphorylation in African trypanosomiasis,” Journal of Immunology, vol. 171, no. 3, pp. 1466–1472, 2003. View at Google Scholar · View at Scopus