Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 563425, 17 pages
http://dx.doi.org/10.1155/2015/563425
Research Article

Extraintestinal Helminth Infection Limits Pathology and Proinflammatory Cytokine Expression during DSS-Induced Ulcerative Colitis: A Role for Alternatively Activated Macrophages and Prostaglandins

1Unidad de Biomedicina, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México, Avenida De Los Barrios 1, Los Reyes Iztacala, 54090 Tlalnepantla, MEX, Mexico
2Department of Pathology, Medical Center, The Ohio State University, Columbus, OH 43221, USA
3Department of Physiology and Pharmacology, Faculty of Medicine, University of Calgary, Calgary, AB, Canada T2N 4N1
4Departamento de Inmunología, Instituto de Investigaciones Biomédicas, UNAM, 04510 Mexico, DF, Mexico

Received 8 August 2014; Revised 14 October 2014; Accepted 20 October 2014

Academic Editor: Abraham Landa

Copyright © 2015 Yadira Ledesma-Soto 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. J. E. Allen and R. M. Maizels, “Diversity and dialogue in immunity to helminths,” Nature Reviews Immunology, vol. 11, no. 6, pp. 375–388, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. K. J. Mylonas, M. A. Hoeve, A. S. MacDonald, and J. E. Allen, “Alternative activation of macrophages by filarial nematodes is MyD88-independent,” Immunobiology, vol. 218, no. 4, pp. 570–578, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. 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, pp. 89–116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. D. E. Elliott and J. V. Weinstock, “Helminth-host immunological interactions: prevention and control of immune-mediated diseases,” Annals of the New York Academy of Sciences, vol. 1247, no. 1, pp. 83–96, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. D. Kappelman, S. L. Rifas-Shiman, K. Kleinman et al., “The prevalence and geographic distribution of Crohn's disease and ulcerative colitis in the United States,” Clinical Gastroenterology and Hepatology, vol. 5, no. 12, pp. 1424–1429, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Burisch, T. Jess, M. Martinato, and P. L. Lakatos, “The burden of inflammatory bowel disease in Europe,” Journal of Crohn's and Colitis, vol. 7, no. 4, pp. 322–337, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. V. Valatas, M. Vakas, and G. Kolios, “The value of experimental models of colitis in predicting efficacy of biological therapies for inflammatory bowel diseases,” American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 305, no. 11, pp. G763–G785, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Donskow-Łysoniewska, P. Majewski, K. Brodaczewska, K. Jóźwicka, and M. Doligalska, “Heligmosmoides polygyrus fourth stages induce protection against DSS-induced colitis and change opioid expression in the intestine,” Parasite Immunology, vol. 34, no. 11, pp. 536–546, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Melon, A. Wang, V. Phan, and D. M. McKay, “Infection with Hymenolepis diminuta is more effective than daily corticosteroids in blocking chemically induced colitis in mice,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 384523, 7 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. N. A. Braus and D. E. Elliott, “Advances in the pathogenesis and treatment of IBD,” Clinical Immunology, vol. 132, no. 1, pp. 1–9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. J. V. Weinstock and D. E. Elliott, “Helminths and the IBD hygiene hypothesis,” Inflammatory Bowel Diseases, vol. 15, no. 1, pp. 128–133, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. R. W. Summers, D. E. Elliott, J. F. Urban Jr., R. A. Thompson, and J. V. Weinstock, “Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial,” Gastroenterology, vol. 128, no. 4, pp. 825–832, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. A. Wang, M. Fernando, G. Leung, V. Phan, D. Smyth, and D. M. McKay, “Exacerbation of oxazolone colitis by infection with the helminth Hymenolepis diminuta: involvement of IL-5 and eosinophils,” The American Journal of Pathology, vol. 177, no. 6, pp. 2850–2859, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Heylen, N. E. Ruyssers, E. M. Gielis et al., “Of worms, mice and man: an overview of experimental and clinical helminth-based therapy for inflammatory bowel disease,” Pharmacology & Therapeutics, vol. 143, no. 2, pp. 153–167, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. H. J. van Kruiningen and A. B. West, “Potential danger in the medical use of Trichuris suis for the treatment of inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 11, no. 5, p. 515, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. A. N. Peón, A. Espinoza-Jiménez, and L. I. Terrazas, “Immunoregulation by Taenia crassiceps and its antigens,” BioMed Research International, vol. 2013, Article ID 498583, 13 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Espinoza-Jiménez, I. Rivera-Montoya, R. Cárdenas-Arreola, L. Morán, and L. I. Terrazas, “Taenia crassiceps infection attenuates multiple low-dose streptozotocin-induced diabetes,” Journal of Biomedicine and Biotechnology, vol. 2010, Article ID 850541, 11 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. J. L. Reyes, A. F. Espinoza-Jiménez, M. I. González, L. Verdin, and L. I. Terrazas, “Taenia crassiceps infection abrogates experimental autoimmune encephalomyelitis,” Cellular Immunology, vol. 267, no. 2, pp. 77–87, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. A. M. Ortiz-Flores, Y. Ledesma-Soto, E. A. Calleja, M. Rodríguez-Sosa, I. Juárez, and L. I. Terrazas, “Taenia crassiceps infection does not influence the development of experimental rheumatoid arthritis,” BioMed Research International, vol. 2013, Article ID 316980, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. C. E. Matisz, J. J. McDougall, K. A. Sharkey, and D. M. McKay, “Helminth parasites and the modulation of joint inflammation,” Journal of Parasitology Research, vol. 2011, Article ID 942616, 8 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. J. H. Niess and S. Danese, “Anti-TNF and skin inflammation in IBD: a new paradox in gastroenterology?” Gut, vol. 63, no. 4, pp. 533–535, 2014. View at Google Scholar
  22. F. Tao, C. Qian, W. Guo, Q. Luo, Q. Xu, and Y. Sun, “Inhibition of Th1/Th17 responses via suppression of STAT1 and STAT3 activation contributes to the amelioration of murine experimental colitis by a natural flavonoid glucoside icariin,” Biochemical Pharmacology, vol. 85, no. 6, pp. 798–807, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. X. Yang, Y. Yang, Y. Wang et al., “Excretory/secretory products from Trichinella spiralis adult worms ameliorate DSS-induced colitis in mice,” PLoS ONE, vol. 9, no. 5, Article ID e96454, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Leung, L. Hang, A. Blum, T. Setiawan, K. Stoyanoff, and J. Weinstock, “Heligmosomoides polygyrus abrogates antigen-specific gut injury in a murine model of inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 18, no. 8, pp. 1447–1455, 2012. View at Publisher · View at Google Scholar · View at Scopus
  25. H.-M. Mo, W.-Q. Liu, J.-H. Lei, Y.-L. Cheng, C.-Z. Wang, and Y.-L. Li, “Schistosoma japonicum eggs modulate the activity of CD4+ CD25+ Tregs and prevent development of colitis in mice,” Experimental Parasitology, vol. 116, no. 4, pp. 385–389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. L. Hang, A. M. Blum, T. Setiawan, J. P. Urban Jr., K. M. Stoyanoff, and J. V. Weinstock, “Heligmosomoides polygyrus bakeri infection activates colonic Foxp3+ T cells enhancing their capacity to prevent colitis,” The Journal of Immunology, vol. 191, no. 4, pp. 1927–1934, 2013. View at Publisher · View at Google Scholar · View at Scopus
  27. V. B. L. Moura, M. M. Silva, L. F. Batista et al., “Arginase activity is associated with fibrosis in experimental infection with Taenia crassiceps, but does not play a major role in resistance to infection,” Experimental Parasitology, vol. 135, no. 3, pp. 599–605, 2013. View at Publisher · View at Google Scholar · View at Scopus
  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 Scopus
  29. M. Rodríguez-Sosa, A. R. Satoskar, R. Calderón et al., “Chronic helminth infection induces alternatively activated macrophages expressing high levels of CCR5 with low interleukin-12 production and Th2-biasing ability,” Infection and Immunity, vol. 70, no. 7, pp. 3656–3664, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Chinen, K. Komai, G. Muto et al., “Prostaglandin E2 and SOCS1 have a role in intestinal immune tolerance,” Nature Communications, vol. 2, no. 1, article 190, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Burisch, N. Pedersen, S. Cukovic-Cavka et al., “Environmental factors in a population-based inception cohort of inflammatory bowel disease patients in Europe—an ECCO-EpiCom study,” Journal of Crohn's and Colitis, vol. 8, no. 7, pp. 607–616, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Adalid-Peralta, G. Fragoso, A. Fleury, and E. Sciutto, “Mechanisms underlying the induction of regulatory T cells and its relevance in the adaptive immune response in parasitic infections,” International Journal of Biological Sciences, vol. 7, no. 9, pp. 1412–1426, 2011. View at Google Scholar · View at Scopus
  33. K. Yasukawa, H. Tokuda, X. Tun, H. Utsumi, and K.-I. Yamada, “The detrimental effect of nitric oxide on tissue is associated with infl ammatory events in the vascular endothelium and neutrophils in mice with dextran sodium sulfate-induced colitis,” Free Radical Research, vol. 46, no. 12, pp. 1427–1436, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Yamagata, T. Mikami, T. Tsuruta et al., “Submucosal fibrosis and basic-fibroblast growth factor-positive neutrophils correlate with colonic stenosis in cases of ulcerative colitis,” Digestion, vol. 84, no. 1, pp. 12–21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. C. C. Bain and A. M. Mowat, “Macrophages in intestinal homeostasis and inflammation,” Immunological Reviews, vol. 260, no. 1, pp. 102–117, 2014. View at Publisher · View at Google Scholar
  36. C. C. Bain and A. M. Mowat, “The monocyte-macrophage axis in the intestine,” Cellular Immunology, vol. 291, no. 1-2, pp. 41–48, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. Y. Takada, T. Hisamatsu, N. Kamada et al., “Monocyte chemoattractant protein-1 contributes to gut homeostasis and intestinal inflammation by composition of IL-10-producing regulatory macrophage subset,” The Journal of Immunology, vol. 184, no. 5, pp. 2671–2676, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. S. Bao, P. Zhang, R. J. Xie et al., “The regulation of CD4+ T cell immune responses toward Th2 cell development by prostaglandin E2,” International Immunopharmacology, vol. 11, no. 10, pp. 1599–1605, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. 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
  40. S. Koyasu and K. Moro, “Type 2 innate immune responses and the natural helper cell,” Immunology, vol. 132, no. 4, pp. 475–481, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Leon-Cabrera, M. Cruz-Rivera, F. Mendlovic et al., “Immunological mechanisms involved in the protection against intestinal taeniosis elicited by oral immunization with Taenia solium calreticulin,” Experimental Parasitology, vol. 132, no. 3, pp. 334–340, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Kurashima, Y. Goto, and H. Kiyono, “Mucosal innate immune cells regulate both gut homeostasis and intestinal inflammation,” European Journal of Immunology, vol. 43, no. 12, pp. 3108–3115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. M. van der Sluis, B. A. E. de Koning, A. C. J. M. de Bruijn et al., “Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection,” Gastroenterology, vol. 131, no. 1, pp. 117–129, 2006. View at Publisher · View at Google Scholar · View at Scopus
  44. X. O. Yang, S. H. Chang, H. Park et al., “Regulation of inflammatory responses by IL-17F,” The Journal of Experimental Medicine, vol. 205, no. 5, pp. 1063–1075, 2008. View at Publisher · View at Google Scholar
  45. C. Tang and Y. Iwakura, “IL-23 in Colitis: targeting the Progenitors,” Immunity, vol. 37, no. 6, pp. 957–959, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Becerra-Díaz and L. I. Terrazas, “Taenia crassiceps infection and its excreted/secreted products inhibit STAT1 activation in response to IFN-γ,” International Journal for Parasitology, vol. 44, no. 9, pp. 613–623, 2014. View at Publisher · View at Google Scholar · View at Scopus