About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2010 (2010), Article ID 795210, 11 pages
http://dx.doi.org/10.1155/2010/795210
Research Article

Immune Modulation by Schistosoma mansoni Antigens in NOD Mice: Effects on Both Innate and Adaptive Immune Systems

Department of Pathology, University of Cambridge, Tennis Court Road, CB2 1QP Cambridge, UK

Received 2 September 2009; Accepted 10 November 2009

Academic Editor: Luis I. Terrazas

Copyright © 2010 Paola Zaccone 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. B. Everts, G. Perona-Wright, H. H. Smits, et al., “Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses,” The Journal of Experimental Medicine, vol. 206, no. 8, pp. 1673–1680, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. S. Steinfelder, J. F. Andersen, J. L. Cannons, et al., “The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1),” The Journal of Experimental Medicine, vol. 206, no. 8, pp. 1681–1690, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. S. Makino, K. Kunimoto, Y. Muraoka, Y. Mizushima, K. Katagiri, and Y. Tochino, “Breeding of a non-obese, diabetic strain of mice,” Jikken Dobutsu, vol. 29, no. 1, pp. 1–13, 1980. View at Scopus
  4. A. Cooke, P. Tonks, F. M. Jones, et al., “Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice,” Parasite Immunology, vol. 21, no. 4, pp. 169–176, 1999. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Zaccone, Z. Fehérvári, F. M. Jones, et al., “Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes,” European Journal of Immunology, vol. 33, no. 5, pp. 1439–1449, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  6. P. Zaccone, O. Burton, N. Miller, F. M. Jones, D. W. Dunne, and A. Cooke, “Schistosoma mansoni egg antigens induce Treg that participate in diabetes prevention in NOD mice,” European Journal of Immunology, vol. 39, no. 4, pp. 1098–1107, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. D. Bending, H. De La Pena, M. Veldhoen, et al., “Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice,” The Journal of Clinical Investigation, vol. 119, no. 3, pp. 565–572, 2009. View at Publisher · View at Google Scholar · View at PubMed
  8. E. Sgouroudis and C. A. Piccirillo, “Control of type 1 diabetes by CD4+Foxp3+ regulatory T cells: lessons from mouse models and implications for human disease,” Diabetes/Metabolism Research and Reviews, vol. 25, no. 3, pp. 208–218, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. J. M. Phillips, N. M. Parish, M. Drage, and A. Cooke, “Cutting edge: interactions through the IL-10 receptor regulate autoimmune diabetes,” The Journal of Immunology, vol. 167, no. 11, pp. 6087–6091, 2001. View at Scopus
  10. A. S. MacDonald, A. D. Straw, B. Bauman, and E. J. Pearce, “CD8- dendritic cell activation status plays an integral role in influencing Th2 response development,” The Journal of Immunology, vol. 167, no. 4, pp. 1982–1988, 2001. View at Scopus
  11. E. J. Pearce, C. M. Kane, and J. Sun, “Regulation of dendritic cell function by pathogen-derived molecules plays a key role in dictating the outcome of the adaptive immune response,” Chemical Immunology and Allergy, vol. 90, pp. 82–90, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. A. W. Thomson and P. D. Robbins, “Tolerogenic dendritic cells for autoimmune disease and transplantation,” Annals of the Rheumatic Diseases, vol. 67, supplement 3, pp. iii90–iii96, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. D. W. Dunne, A. E. Butterworth, A. J. Fulford, et al., “Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection,” European Journal of Immunology, vol. 22, no. 6, pp. 1483–1494, 1992. View at Publisher · View at Google Scholar · View at PubMed
  14. C. M. Kane, L. Cervi, J. Sun, et al., “Helminth antigens modulate TLR-initiated dendritic cell activation,” The Journal of Immunology, vol. 173, no. 12, pp. 7454–7461, 2004.
  15. C. M. Kane, E. Jung, and E. J. Pearce, “Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88,” Infection and Immunity, vol. 76, no. 12, pp. 5754–5759, 2008. View at Publisher · View at Google Scholar · View at PubMed
  16. F. Trottein, N. Pavelka, C. Vizzardelli, et al., “A type I IFN-dependent pathway induced by Schistosoma mansoni eggs in mouse myeloid dendritic cells generates an inflammatory signature,” The Journal of Immunology, vol. 172, no. 5, pp. 3011–3017, 2004.
  17. A. S. MacDonald, A. D. Straw, N. M. Dalto, and E. J. Pearce, “Cutting edge: Th2 response induction by dendritic cells: a role for CD401,” The Journal of Immunology, vol. 168, no. 2, pp. 537–540, 2002.
  18. D. Artis, C. M. Kane, J. Fiore, et al., “Dendritic cell-intrinsic expression of NF-κ B1 is required to promote optimal Th2 cell differentiation,” The Journal of Immunology, vol. 174, no. 11, pp. 7154–7159, 2005.
  19. E. van Riet, B. Everts, K. Retra, et al., “Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization,” BMC Immunology, vol. 10, article 9, 2009.
  20. T. K. van den Berg, H. Honing, N. Franke, et al., “LacdiNAc-glycans constitute a parasite pattern for galectin-3-mediated immune recognition,” The Journal of Immunology, vol. 173, pp. 1902–1907, 2004.
  21. E. van Liempt, A. Imberty, C. M. Bank, et al., “Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and Schistosoma mansoni egg antigens,” The Journal of Biological Chemistry, vol. 279, pp. 33161–33167, 2004. View at Publisher · View at Google Scholar · View at PubMed
  22. E. van Liempt, S. J. van Vliet, A. Engering, et al., “Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation,” Molecular Immunology, vol. 44, no. 10, pp. 2605–2615, 2007.
  23. S. S. Saunders, C. M. Walsh, J. L. Barlow, et al., “The C-type lectin SIGNR1 binds Schistosoma mansoni antigens in vitro but SIGNR1-deficient mice have normal responses during schistosome infection,” Infection and Immunity, vol. 77, no. 1, pp. 399–404, 2008. View at Publisher · View at Google Scholar · View at PubMed
  24. F. L. Oliveira, P. Frazão, R. Chammas, et al., “Kinetics of mobilization and differentiation of lymphohematopoietic cells during experimental murine schistosomiasis in galectin-3-/- mice,” Journal of Leukocyte Biology, vol. 82, no. 2, pp. 300–310, 2007. View at Publisher · View at Google Scholar · View at PubMed
  25. L. Breuilh, F. Vanhoutte, J. Fontaine, et al., “Galectin-3 modulates immune and inflammatory responses during helminthic infection: impact of galectin-3 deficiency on the functions of dendritic cells,” Infection and Immunity, vol. 75, no. 11, pp. 5148–5157, 2007. View at Publisher · View at Google Scholar · View at PubMed
  26. P. J. Wipff and B. Hinz, “Integrins and the activation of latent transforming growth factor β1—an intimate relationship,” European Journal of Cell Biology, vol. 87, no. 8-9, pp. 601–615, 2008. View at Publisher · View at Google Scholar · View at PubMed
  27. A. C. MacKinnon, S. L. Farnworth, P. S. Hodkinson, et al., “Regulation of alternative macrophage activation by galectin-3,” The Journal of Immunology, vol. 180, no. 4, pp. 2650–2658, 2008.
  28. L. I. Terrazas, D. Montero, C. A. Terrazas, J. L. Reyes, and M. Rodríguez-Sosa, “Role of the programmed Death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis,” International Journal for Parasitology, vol. 35, no. 13, pp. 1349–1358, 2005. View at Publisher · View at Google Scholar · View at PubMed
  29. E. J. Pearce, C. M. Kane, J. Sun, J. J. Taylor, A. S. McKee, and L. Cervi, “Th2 response polarization during infection with die helminth parasite Schistosoma mansoni,” Immunological Reviews, vol. 201, pp. 117–126, 2004. View at Publisher · View at Google Scholar · View at PubMed
  30. A. S. McKee and E. J. Pearce, “CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development,” The Journal of Immunology, vol. 173, no. 2, pp. 1224–1231, 2004.
  31. M. Baumgart, F. Tompkins, J. Leng, and M. Hesse, “Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation,” The Journal of Immunology, vol. 176, no. 9, pp. 5374–5387, 2006.
  32. L. E. Layland, R. Rad, H. Wagner, and C. U. Prazeres da Costa, “Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2,” European Journal of Immunology, vol. 37, no. 8, pp. 2174–2184, 2007. View at Publisher · View at Google Scholar · View at PubMed
  33. E. A. Partridge, C. Le Roy, G. M. Di Guglielmo, et al., “Regulation of cytokine receptors by Golgi N-glycan processing and endocytosis,” Science, vol. 306, no. 5693, pp. 120–124, 2004.
  34. A. M. Cooper and S. A. Khader, “IL-12p40: an inherently agonistic cytokine,” Trends in Immunology, vol. 28, no. 1, pp. 33–38, 2007. View at Publisher · View at Google Scholar · View at PubMed
  35. M. J. I. Ansari, A. D. Salama, T. Chitnis, et al., “The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice,” The Journal of Experimental Medicine, vol. 198, no. 1, pp. 63–69, 2003. View at Publisher · View at Google Scholar · View at PubMed
  36. Y. Belkaid, “Regulatory T cells and infection: a dangerous necessity,” Nature Reviews Immunology, vol. 7, no. 11, pp. 875–888, 2007. View at Publisher · View at Google Scholar · View at PubMed
  37. Y. Belkaid, K. F. Hoffmann, S. Mendez, et al., “The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure,” The Journal of Experimental Medicine, vol. 194, no. 10, pp. 1497–1506, 2001. View at Publisher · View at Google Scholar