Table of Contents Author Guidelines Submit a Manuscript
Journal of Biomedicine and Biotechnology
Volume 2010, Article ID 850541, 11 pages
http://dx.doi.org/10.1155/2010/850541
Research Article

Taenia crassiceps Infection Attenuates Multiple Low-Dose Streptozotocin-Induced Diabetes

1Unidad de Biomedicina, Facultad de Estudios Superiores-Iztacala, Universidad Nacional Autónoma de México, Tlalnepantla, México 54090, Mexico
2Centro Médico Nacional Siglo XXI, IMSS, Mexico City, Mexico

Received 29 August 2009; Accepted 12 October 2009

Academic Editor: Abhay R. Satoskar

Copyright © 2010 Arlett Espinoza-Jiménez 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. R. M. Maizels, “Parasite immunomodulation and polymorphisms of the immune system,” Journal of Biology, vol. 8, article 62, pp. 1–4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. R. M. Maizels, A. Balic, N. Gomez-Escobar, M. Nair, M. D. Taylor, and J. E. Allen, “Helminth parasites—masters of regulation,” Immunological Reviews, vol. 201, no. 1, pp. 89–116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. J. P. Hewitson, J. R. Grainger, and R. M. Maizels, “Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity,” Molecular and Biochemical Parasitology, vol. 167, no. 1, pp. 1–11, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. R. D'Elia, J. M. Behnke, J. E. Bradley, and K. J. Else, “Regulatory T cells: a role in the control of helminth-driven intestinal pathology and worm survival,” Journal of Immunology, vol. 182, no. 4, pp. 2340–2348, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. 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
  6. 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,” Journal of immunology, vol. 181, no. 9, pp. 6456–6466, 2008. View at Google Scholar · View at Scopus
  7. D. P. Beiting, L. F. Gagliardo, M. Hesse, S. K. Bliss, D. Meskill, and J. A. Appleton, “Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-β,” Journal of Immunology, vol. 178, no. 2, pp. 1039–1047, 2007. View at Google Scholar · View at Scopus
  8. S. Rausch, J. Huehn, D. Kirchhoff et al., “Functional analysis of effector and regulatory T cells in a parasitic nematode infection,” Infection and Immunity, vol. 76, no. 5, pp. 1908–1919, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. L. Carvalho, J. Sun, C. Kane, F. Marshall, C. Krawczyk, and E. J. Pearce, “Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function,” Immunology, vol. 126, no. 1, pp. 28–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. T. Kreider, R. M. Anthony, J. F. Urban Jr., and W. C. Gause, “Alternatively activated macrophages in helminth infections,” Current Opinion in Immunology, vol. 19, no. 4, pp. 448–453, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. J. L. Reyes and L. I. Terrazas, “The divergent roles of alternatively activated macrophages in helminthic infections,” Parasite Immunology, vol. 29, no. 12, pp. 609–619, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Zaccone, O. T. Burton, and A. Cooke, “Interplay of parasite-driven immune responses and autoimmunity,” Trends in Parasitology, vol. 24, no. 1, pp. 35–42, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Vercelli, “Mechanisms of the hygiene hypothesis—molecular and otherwise,” Current Opinion in Immunology, vol. 18, no. 6, pp. 733–737, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Cooke, P. Zaccone, T. Raine, J. M. Phillips, and D. W. Dunne, “Infection and autoimmunity: are we winning the war, only to lose the peace?” Trends in Parasitology, vol. 20, no. 7, pp. 316–321, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. M. C. Denis, U. Mahmood, C. Benoist, D. Mathis, and R. Weissleder, “Imaging inflammation of the pancreatic islets in type 1 diabetes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 34, pp. 12634–12639, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. T. Szkudelski, “The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas,” Physiological Research, vol. 50, no. 6, pp. 537–546, 2001. View at Google Scholar · View at Scopus
  17. M. Cetkovic-Cvrlje and F. M. Uckun, “Effect of targeted disruption of signal transducer and activator of transcription (Stat)4 and Stat6 genes on the autoimmune diabetes development induced by multiple low doses of streptozotocin,” Clinical Immunology, vol. 114, no. 3, pp. 299–306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Rodríguez-Sosa, I. Rivera-Montoya, A. Espinoza et al., “Acute cysticercosis favours rapid and more severe lesions caused by Leishmania major and Leishmania mexicana infection, a role for alternatively activated macrophages,” Cellular Immunology, vol. 242, no. 2, pp. 61–71, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. D. M. McKay, “The beneficial helminth parasite?” Parasitology, vol. 132, no. 1, pp. 1–12, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. 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 Scopus
  21. M. Rodríguez, L. I. Terrazas, R. Márquez, and R. Bojalil, “Susceptibility to Trypanosoma cruzi is modified by a previous non-related infection,” Parasite Immunology, vol. 21, no. 4, pp. 177–185, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. R. J. Spolski, J. Corson, P. G. Thomas, and R. E. Kuhn, “Parasite-secreted products regulate the host response to larval Taenia crassiceps,” Parasite Immunology, vol. 22, no. 6, pp. 297–305, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Nookala, S. Srinivasan, P. Kaliraj, R. B. Narayanan, and T. B. Nutman, “Impairment of tetanus-specific cellular and humoral responses following tetanus vaccination in human lymphatic filariasis,” Infection and Immunity, vol. 72, no. 5, pp. 2598–2604, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Müller, P. Schott-Ohly, C. Dohle, and H. Gleichmann, “Differential regulation of Th1-type and Th2-type cytokine profiles in pancreatic islets of C57BL/6 and BALB/c mice by multiple low doses of streptozotocin,” Immunobiology, vol. 205, no. 1, pp. 35–50, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. E. Sciutto, G. Fragoso, M. L. Diaz et al., “Murine Taenia crassiceps cysticercosis: H-2 complex and sex influence on susceptibility,” Parasitology Research, vol. 77, no. 3, pp. 243–246, 1991. View at Google Scholar · View at Scopus
  26. J. L. Reyes, C. A. Terrazas, L. Vera-Arias, and L. I. Terrazas, “Differential response of antigen presenting cells from susceptible and resistant strains of mice to Taenia crassiceps infection,” Infection, Genetics and Evolution, vol. 9, no. 6, pp. 1115–1127, 2009. View at Publisher · View at Google Scholar
  27. A. Rabinovitch and W. L. Suarez-Pinzon, “Cytokines and their roles in pancreatic islet β-cell destruction and insulin-dependent diabetes mellitus,” Biochemical Pharmacology, vol. 55, no. 8, pp. 1139–1149, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. 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,” Journal of Immunology, vol. 176, no. 10, pp. 5839–5847, 2006. View at Google Scholar · View at Scopus
  29. A. S. McKee and E. J. Pearce, “CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development,” Journal of Immunology, vol. 173, no. 2, pp. 1224–1231, 2004. View at Google Scholar · View at Scopus
  30. E. Biros, M. A. Jordan, and A. G. Baxter, “Genes mediating environment interactions in type 1 diabetes,” The Review of Diabetic Studies, vol. 2, no. 4, pp. 192–207, 2005. View at Google Scholar
  31. S. A. Toenjes, R. J. Spolski, K. A. Mooney, and R. E. Kuhn, “The systemic immune response of BALB/c mice infected with larval Taenia crassiceps is a mixed Th1/Th2-type response,” Parasitology, vol. 118, no. 6, pp. 623–633, 1999. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Dahlén, K. Dawe, L. Ohlsson, and G. Hedlund, “Dendritic cells and macrophages are the first and major producers of TNF-α in pancreatic islets in the nonobese diabetic mouse,” Journal of Immunology, vol. 160, no. 7, pp. 3585–3593, 1998. View at Google Scholar · View at Scopus
  33. C. Chen, W.-H. Lee, P. Yun, P. Snow, and C.-P. Liu, “Induction of autoantigen-specific Th2 and Tr1 regulatory T cells and modulation of autoimmune diabetes,” Journal of Immunology, vol. 171, no. 2, pp. 733–744, 2003. View at Google Scholar · View at Scopus
  34. 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
  35. 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 Scopus
  36. 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 Scopus
  37. K. A. Saunders, T. Raine, A. Cooke, and C. E. Lawrence, “Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection,” Infection and Immunity, vol. 75, no. 1, pp. 397–407, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. A. C. La Flamme, K. Ruddenklau, and B. T. Bäckström, “Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis,” Infection and Immunity, vol. 71, no. 9, pp. 4996–5004, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Sewell, Z. Qing, E. Reinke et al., “Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization,” International Immunology, vol. 15, no. 1, pp. 59–69, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. W. I. Khan, P. A. Blennerhasset, A. K. Varghese et al., “Intestinal nematode infection ameliorates experimental colitis in mice,” Infection and Immunity, vol. 70, no. 11, pp. 5931–5937, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. D. E. Elliott, J. Li, A. Blum et al., “Exposure to schistosome eggs protects mice from TNBS-induced colitis,” American Journal of Physiology, vol. 284, no. 3, pp. G385–G391, 2003. View at Google Scholar · View at Scopus
  42. P. Smith, N. E. Mangan, C. M. Walsh et al., “Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism,” Journal of Immunology, vol. 178, no. 7, pp. 4557–4566, 2007. View at Google Scholar · View at Scopus
  43. T. G. Moreels, R. J. Nieuwendijk, J. G. De Man et al., “Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats,” Gut, vol. 53, no. 1, pp. 99–107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. D. E. Elliott, T. Setiawan, A. Metwali, A. Blum, J. F. Urban Jr., and J. V. Weinstock, “Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice,” European Journal of Immunology, vol. 34, no. 10, pp. 2690–2698, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. C. Reardon, A. Sanchez, C. M. Hogaboam, and D. M. McKay, “Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis,” Infection and Immunity, vol. 69, no. 7, pp. 4417–4423, 2001. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Tominaga, M. Nagata, H. Yasuda et al., “Administration of IL-4 prevents autoimmune diabetes but enhances pancreatic insulitis in NOD mice,” Clinical Immunology and Immunopathology, vol. 86, no. 2, pp. 209–218, 1998. View at Publisher · View at Google Scholar · View at Scopus
  47. M. J. Rapoport, A. Jaramillo, D. Zipris et al., “Interleukin 4 reverses T cell proliferative unresponsiveness and prevents the onset of diabetes in nonobese diabetic mice,” Journal of Experimental Medicine, vol. 178, no. 1, pp. 87–99, 1993. View at Google Scholar · View at Scopus
  48. O. Grip, S. Janciauskiene, and S. Lindgren, “Macrophages in inflammatory bowel disease,” Current Drug Targets—Inflammation & Allergy, vol. 2, no. 2, pp. 155–160, 2003. View at Publisher · View at Google Scholar · View at Scopus