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Journal of Biomedicine and Biotechnology
Volume 2010, Article ID 786078, 9 pages
http://dx.doi.org/10.1155/2010/786078
Research Article

Reduction of Foxp Cells by Depletion with the PC61 mAb Induces Mortality in Resistant BALB/c Mice Infected with Toxoplasma gondii

Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Apartado Postal 70228, C.U., CP 04510, Mexico City, Mexico

Received 30 June 2009; Revised 9 September 2009; Accepted 14 September 2009

Academic Editor: Luis I. Terrazas

Copyright © 2010 Eda Patricia Tenorio 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. P. Hughes, “Toxoplasmosis: the need for improved diagnostic techniques and accurate risk assessment,” Current Topics in Microbiology and Immunology, vol. 120, pp. 105–139, 1985. View at Google Scholar · View at Scopus
  2. J. G. Montoya and O. Liesenfeld, “Toxoplasmosis,” The Lancet, vol. 363, no. 9425, pp. 1965–1976, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. R. McCabe and J. S. Remington, “Toxoplasmosis: the time has come,” The New England Journal of Medicine, vol. 318, no. 5, pp. 313–315, 1988. View at Google Scholar · View at Scopus
  4. J. S. Remington and J. L. Krahenbuhl, “Immunology of Toxoplasma gondii,” in Immunology of Human Infection, Part II, p. 327, Plenum, New York, NY, USA, 1982. View at Google Scholar
  5. S.-Y. Wong and J. S. Remington, “Toxoplasmosis in pregnancy,” Clinical Infectious Diseases, vol. 18, no. 6, pp. 853–861, 1994. View at Google Scholar · View at Scopus
  6. J. K. Frenkel, “Adoptive immunity to intracellular infection,” The Journal of Immunology, vol. 98, no. 6, pp. 1309–1319, 1967. View at Google Scholar · View at Scopus
  7. J. Aliberti, “Host persistence: exploitation of anti-inflammatory pathways by Toxoplasma gondii,” Nat.Rev.Immunol., vol. 5, no. 2, pp. 162–170, 2005. View at Google Scholar
  8. R. T. Gazzinelli, F. T. Hakim, S. Hieny, G. M. Shearer, and A. Sher, “Synergistic role of CD4+CD8+ T lymphocytes in IFN-γ production and protective immunity induced by an attenuated Toxoplasma gondii vaccine,” The Journal of Immunology, vol. 146, no. 1, pp. 286–292, 1991. View at Google Scholar · View at Scopus
  9. Y. Suzuki and J. S. Remington, “Dual regulation of resistance against Toxoplasma gondii infection by Lyt-2+ and Lyt-1+, L3T4+ T cells in mice,” The Journal of Immunology, vol. 140, no. 11, pp. 3943–3946, 1988. View at Google Scholar · View at Scopus
  10. R. T. Gazzinelli, D. Amichay, T. Sharton-Kersten, E. Grunwald, J. M. Farber, and A. Sher, “Role of macrophage-derived cytokines in the induction and regulation of cell-mediated immunity to Toxoplasma gondii,” Current Topics in Microbiology and Immunology, vol. 219, pp. 127–139, 1996. View at Google Scholar · View at Scopus
  11. R. T. Gazzinelli, M. Wysocka, S. Hayashi et al., “Parasite-induced IL-12 stimulates early IFN-? synthesis and resistance during acute infection with Toxoplasma gondii,” The Journal of Immunology, vol. 153, no. 6, pp. 2533–2543, 1994. View at Google Scholar · View at Scopus
  12. C.-H. Liu, Y.-T. Fan, A. Dias et al., “Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice,” The Journal of Immunology, vol. 177, no. 1, pp. 31–35, 2006. View at Google Scholar · View at Scopus
  13. Y. Suzuki, M. A. Orellana, R. D. Schreiber, and J. S. Remington, “Interferon-γ: the major mediator of resistance against Toxoplasma gondii,” Science, vol. 240, no. 4851, pp. 516–518, 1988. View at Google Scholar · View at Scopus
  14. Y. Suzuki and J. S. Remington, “The effect of anti-IFN-γ antibody on the protective effect of Lyt-2+ immune T cells against toxoplasmosis in mice,” The Journal of Immunology, vol. 144, no. 5, pp. 1954–1956, 1990. View at Google Scholar · View at Scopus
  15. E. Y. Denkers and R. T. Gazzinelli, “Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection,” Clinical Microbiology Reviews, vol. 11, no. 4, pp. 569–588, 1998. View at Google Scholar · View at Scopus
  16. Y. Suzuki, A. Sher, G. Yap et al., “IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma gondii,” The Journal of Immunology, vol. 164, no. 10, pp. 5375–5382, 2000. View at Google Scholar · View at Scopus
  17. D. K. Sojka, Y.-H. Huang, and D. J. Fowell, “Mechanisms of regulatory T-cell suppression—a diverse arsenal for a moving target,” Immunology, vol. 124, no. 1, pp. 13–22, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. D. A. A. Vignali, L. W. Collison, and C. J. Workman, “How regulatory T cells work,” Nature Reviews Immunology, vol. 8, no. 7, pp. 523–532, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. Q. Tang and J. A. Bluestone, “The Foxp3+ regulatory T cell: a jack of all trades, master of regulation,” Nature Immunology, vol. 9, no. 3, pp. 239–244, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S. Sakaguchi, N. Sakaguchi, M. Asano, M. Itoh, and M. Toda, “Immunologic self-tolerance maintained by activated T cells expressing IL- 2 receptor alpha-chains (CD25): breakdown of a single mechanism of self- tolerance causes various autoimmune diseases,” The Journal of Immunology, vol. 155, no. 3, pp. 1151–1164, 1995. View at Google Scholar · View at Scopus
  21. T. Takahashi, T. Tagami, S. Yamazaki et al., “Immunologic self-tolerance maintained by CD25+CD4+ regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4,” The Journal of Experimental Medicine, vol. 192, no. 2, pp. 303–310, 2000. View at Publisher · View at Google Scholar · View at Scopus
  22. J. D. Fontenot, M. A. Gavin, and A. Y. Rudensky, “Foxp3 programs the development and function of CD4+CD25+ regulatory T cells,” Nature Immunology, vol. 4, no. 4, pp. 330–336, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. R. Khattri, T. Cox, S.-A. Yasayko, and F. Ramsdell, “An essential role for Scurfin in CD4+CD25+ T regulatory cells,” Nature Immunology, vol. 4, no. 4, pp. 337–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Sakaguchi, T. Yamaguchi, T. Nomura, and M. Ono, “Regulatory T cells and immune tolerance,” Cell, vol. 133, no. 5, pp. 775–787, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Kim, J. P. Rasmussen, and A. Y. Rudensky, “Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice,” Nature Immunology, vol. 8, no. 2, pp. 191–197, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. B. T. Rouse and S. Suvas, “Regulatory cells and infectious agents: détentes cordiale and contraire,” The Journal of Immunology, vol. 173, no. 4, pp. 2211–2215, 2004. View at Google Scholar · View at Scopus
  27. Y. Belkaid and K. Tarbell, “Regulatory T cells in the control of host-microorganism interactions,” Annual Review of Immunology, vol. 27, pp. 551–589, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Belkaid and B. T. Rouse, “Natural regulatory T cells in infectious disease,” Nature Immunology, vol. 6, no. 4, pp. 353–360, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. K. H. G. Mills, “Regulatory T cells: friend or foe in immunity to infection?” Nature Reviews Immunology, vol. 4, no. 11, pp. 841–855, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Cambos, B. Bélanger, A. Jacques, A. Roulet, and T. Scorza, “Natural regulatory (CD4+CD25+FOXP+) T cells control the production of pro-inflammatory cytokines during Plasmodium chabaudi adami infection and do not contribute to immune evasion,” International Journal for Parasitology, vol. 38, no. 2, pp. 229–238, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Guilliams, G. Oldenhove, W. Noel et al., “African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation,” The Journal of Immunology, vol. 179, no. 5, pp. 2748–2757, 2007. View at Google Scholar · View at Scopus
  32. J. J. Taylor, M. Mohrs, and E. J. Pearce, “Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population,” The Journal of Immunology, vol. 176, no. 10, pp. 5839–5847, 2006. View at Google Scholar · View at Scopus
  33. F. H. Amante, A. C. Stanley, L. M. Randall et al., “A role for natural regulatory T cells in the pathogenesis of experimental cerebral malaria,” The American Journal of Pathology, vol. 171, no. 2, pp. 548–559, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. M. D. Taylor, L. LeGoff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels, “Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo,” The Journal of Immunology, vol. 174, no. 8, pp. 4924–4933, 2005. View at Google Scholar · View at Scopus
  35. C. Piña-Vázquez, R. Saavedra, and P. Hérion, “A quantitative competitive PCR method to determine the parasite load in the brain of Toxoplasma gondii-infected mice,” Parasitology International, vol. 57, no. 3, pp. 347–353, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. K. M. Quinn, R. S. McHugh, F. J. Rich et al., “Inactivation of CD4+CD25+ regulatory T cells during early mycobacterial infection increases cytokine production but does not affect pathogen load,” Immunology & Cell Biology, vol. 84, no. 5, pp. 467–474, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. A. McNeill, E. Spittle, and B. T. Bäckström, “Partial depletion of CD69low-expressing natural regulatory T cells with the anti-CD25 monoclonal antibody PC61,” Scandinavian Journal of Immunology, vol. 65, no. 1, pp. 63–69, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. T. T. A. Long, S. Nakazawa, S. Onizuka, M. C. Huaman, and H. Kanbara, “Influence of CD4+CD25+ T cells on Plasmodium berghei NK65 infection in BALB/c mice,” International Journal for Parasitology, vol. 33, no. 2, pp. 175–183, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. A. M. Vigário, O. Gorgette, H. C. Dujardin et al., “Regulatory CD4+CD25+Foxp3+ T cells expand during experimental Plasmodium infection but do not prevent cerebral malaria,” International Journal for Parasitology, vol. 37, no. 8-9, pp. 963–973, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. K. N. Couper, D. G. Blount, J. B. de Souza, I. Suffia, Y. Belkaid, and E. M. Riley, “Incomplete depletion and rapid regeneration of Foxp3+ regulatory T cells following anti-CD25 treatment in malaria-infected mice,” The Journal of Immunology, vol. 178, no. 7, pp. 4136–4146, 2007. View at Google Scholar · View at Scopus
  41. K. N. Couper, P. A. Lanthier, G. Perona-Wright et al., “Anti-CD25 antibody-mediated depletion of effector T cell populations enhances susceptibility of mice to acute but not chronic Toxoplasma gondii infection,” The Journal of immunology, vol. 182, no. 7, pp. 3985–3994, 2009. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Q. Nie, N. J. Bernard, L. Schofield, and D. S. Hansen, “CD4+CD25+ regulatory T cells suppress CD4+ T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis,” Infection and Immunity, vol. 75, no. 5, pp. 2275–2282, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Y. Ge, L. Zhang, G. Zhang et al., “In pregnant mice, the infection of Toxoplasma gondii causes the decrease of CD4+CD25+-regulatory T cells,” Parasite Immunology, vol. 30, no. 9, pp. 471–481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. C. A. M. Finney, M. D. Taylor, M. S. Wilson, and R. M. Maizels, “Expansion and activation of CD4+CD25+ regulatory T cells in Heligmosomoides polygyrus infection,” European Journal of Immunology, vol. 37, no. 7, pp. 1874–1886, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. J. P. Scott-Browne, S. Shafiani, G. Tucker-Heard et al., “Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis,” The Journal of Experimental Medicine, vol. 204, no. 9, pp. 2159–2169, 2007. View at Publisher · View at Google Scholar · View at Scopus
  46. K. N. Couper, D. G. Blount, M. S. Wilson et al., “IL-10 from CD4+CD25+Foxp3-CD127- adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection,” PLoS Pathogens, vol. 4, no. 2, Article ID e1000004, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. H. J. McSorley, Y. M. Harcus, J. Murray, M. D. Taylor, and R. M. Maizels, “Expansion of Foxp3+ regulatory T cells in mice infected with the filarial parasite Brugia malayi,” The Journal of Immunology, vol. 181, no. 9, pp. 6456–6466, 2008. View at Google Scholar · View at Scopus
  48. M. D. Taylor, N. van der Werf, A. Harris et al., “Early recruitment of natural CD4+Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection,” European Journal of Immunology, vol. 39, no. 1, pp. 192–206, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Zenner, F. Darcy, A. Capron, and M.-F. Cesbron-Delauw, “Toxoplasma gondii: kinetics of the dissemination in the host tissues during the acute phase of infection of mice and rats,” Experimental Parasitology, vol. 90, no. 1, pp. 86–94, 1998. View at Publisher · View at Google Scholar · View at Scopus
  50. M. H. Sumyuen, Y. J. F. Garin, and F. Derouin, “Early kinetics of Toxoplasma gondii infection in mice infected orally with cysts of an avirulent strain,” Journal of Parasitology, vol. 81, no. 2, pp. 327–329, 1995. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Hisaeda, Y. Maekawa, D. Iwakawa et al., “Escape of malaria parasites from host immunity requires CD4+CD25+ regulatory T cells,” Nature Medicine, vol. 10, no. 1, pp. 29–30, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. A. P. Kohm, J. S. McMahon, J. R. Podojil et al., “Cutting edge: anti-CD25 monoclonal antibody injection results in the functional inactivation, not depletion, of CD4+CD25+ T regulatory cells,” The Journal of Immunology, vol. 176, no. 6, pp. 3301–3305, 2006. View at Google Scholar · View at Scopus
  53. E. Y. Denkers and R. T. Gazzinelli, “Regulation and function of T-cell-mediated immunity during Toxoplasma gondii infection,” Clinical Microbiology Reviews, vol. 11, no. 4, pp. 569–588, 1998. View at Google Scholar · View at Scopus