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Interactions between Trichinella spiralis infection and induced colitis in mice

Published online by Cambridge University Press:  12 February 2013

D.S. Ashour ,
A.A. Othman ,
M.M. Shareef ,
H.H. Gaballah  and
W.W. Mayah
D.S. Ashour
Affiliation:
Department of Medical Parasitology, Tanta Faculty of Medicine, Egypt
A.A. Othman*
Affiliation:
Department of Medical Parasitology, Tanta Faculty of Medicine, Egypt
M.M. Shareef
Affiliation:
Department of Pathology, Tanta Faculty of Medicine, Egypt
H.H. Gaballah
Affiliation:
Department of Biochemistry, Tanta Faculty of Medicine, Egypt
W.W. Mayah
Affiliation:
Department of Tropical Medicine, Tanta Faculty of Medicine, Egypt
*
*Fax: 002 40 34 07734 E-mail: ahmed_ali44@hotmail.com
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Abstract

Inflammatory bowel disease (IBD) is a chronic relapsing inflammation afflicting any part of the bowel wall as a result of a deregulated and inappropriate immune response. In recent years, experimental and clinical evidence has demonstrated that infection with parasitic worms could protect hosts from IBD. The aims of this study were to determine if the underlying mechanism of the host immune regulation inherent to Trichinella spiralis infection involves Foxp3-expressing regulatory T cells, and to gain insight about time-related interactions between intestinal nematode infection and induced colitis using an experimental model for ulcerative colitis. Mice were experimentally subjected to acetic acid-induced colitis, which was either preceded or followed by T. spiralis infection. Assessment of colitis was done by histopathological examination of the colon and determination of pentraxin 3 levels. Immunohistochemistry was done for demonstration of Foxp3-expressing regulatory T cells in colonic tissues. It was evident that T. spiralis infection ameliorated the severe inflammation induced by acetic acid, evidenced by amelioration of histopathological changes and diminution of pentraxin 3 levels. The amelioration was more pronounced when T. spiralis infection preceded the induction of colitis. Regarding the immunohistochemical staining of regulatory T cells, T. spiralis infection induced recruitment of Foxp3-expressing regulatory T cells to areas of inflammation. In conclusion, T. spiralis regulatory mechanism can improve inflammation of the colon through the ‘inflammatory–regulatory’ axis. Finally, it would be of great importance to apply these results to the development of new therapeutic approaches for the treatment of ulcerative colitis.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 2 , June 2014 , pp. 210 - 218
Copyright
Copyright © Cambridge University Press 2013 

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References

Abraham, C. & Cho, J.H. (2009) IL-23 and autoimmunity: new insights into the pathogenesis of inflammatory bowel disease. Annual Review of Medicine 60, 97–110.Google Scholar
Agrawal, A., Singh, P.P., Bottazzi, B., Garlanda, C. & Mantovani, A. (2009) Pattern recognition by pentraxins. pp. 98–116in Kishore, U. (Ed.) Target pattern recognition in innate immunity. Texas, USA, Landes Bioscience, Springer Science+Business Media.Google Scholar
Al-Chaer, E., Kawasaki, M. & Pasricha, P. (2000) A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 119, 1276–1285.CrossRefGoogle ScholarPubMed
Belkaid, Y. & Tarbell, K. (2009) Regulatory T cells in the control of host–microorganism interactions. Annual Review of Immunology 27, 551–589.Google Scholar
Boismenu, R. & Chen, Y. (2000) Insights from mouse models of colitis. Journal of Leukocyte Biology 67, 267–278.Google Scholar
Boitelle, A., Di Lorenzo, C., Scales, H.E., Devaney, E., Kennedy, M.W., Garside, P. & Lawrence, C.E. (2005) Contrasting effects of acute and chronic gastro-intestinal helminth infections on a heterologous immune response in a transgenic adoptive transfer model. International Journal of Parasitology 35, 765–775.Google Scholar
Bottazzi, B., Bastone, A., Doni, A., Garlanda, C., Valentino, S., Deban, L., Maina, V., Cotena, A., Moalli, F., Vago, L., Salustri, A., Romani, L. & Mantovani, A. (2006) The long pentraxin PTX3 as a link among innate immunity, inflammation, and female fertility. Journal of Leukocyte Biology 79, 909–912.CrossRefGoogle Scholar
Castagliulo, I., Karalis, K., Valenick, L., Pasha, A., Nikulasson, S., Wlk, M. & Pothoulakis, C. (2001) Endogenous corticosteroids modulate Clostridium difficile toxin A-induced enteritis in rats. American Journal of Physiology. Gastrointestinal and Liver Physiology 280, G539–G545.Google Scholar
Chao, K., Zhong, B.H., Zhang, S.H., Gong, X.R., Yao, J.Y. & Chen, M.H. (2011) Imbalance of CD4(+) T cell subgroups in ulcerative colitis. Zhonghua Yi Xue Za Zhi 91, 1605–1608.Google Scholar
Dunn, I.J. & Wright, K.A. (1985) Cell injury caused by Trichinella spiralis in the mucosal epithelium of B10A mice. Journal of Parasitology 71, 757–766.Google Scholar
Ekbom, A., Helmick, C., Zack, M. & Adami, H.O. (1990) Ulcerative colitis and colorectal cancer: a population-based study. New England Journal of Medicine 323, 1228–1233.CrossRefGoogle ScholarPubMed
Elliott, D.E., Metwali, A., Leung, J., Setiawan, T., Blum, A.M., Ince, M.N., Bazzone, L.E., Stadecker, M.J., Urban, J.F. Jr & Weinstock, J.V. (2008) Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. Journal of Immunology 181, 2414–2419.Google Scholar
Everts, B., Perona-Wright, G., Smits, H.H., Hokke, C.H., van der Ham, A.J., Fitzsimmons, C.M., Doenhoff, M.J., van der Bosch, J., Mohrs, K., Haas, H., Mohrs, M., Yazdanbakhsh, M. & Schramm, G. (2009) Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. Journal of Experimental Medicine 206, 1673–1680.Google Scholar
Everts, B., Smits, H.H., Hokke, C.H. & Yazdanbakhsh, M. (2010) Helminths and dendritic cells: sensing and regulating via pattern recognition receptors, Th2 and Treg responses. European Journal of Immunology 40, 1525–1537.CrossRefGoogle ScholarPubMed
Fabia, R., Willen, R., Ar'Rajab, A., Andersson, R., Ahren, B. & Beng-mark, S. (1992) Acetic acid-induced colitis in the rat: a reproducible experimental model for acute ulcerative colitis. European Surgical Research 24, 211–225.Google Scholar
Finkelman, F.D., Shea-Donohue, T., Morris, S.C., Gildea, L., Strait, R., Madden, K.B., Schopf, L. & Urban, J.F. (2004) Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139–155.Google Scholar
Fox, J.G., Beck, P., Dangler, C.A., Whary, M.T., Wang, T.C., Shi, H.N. & Nagler-Anderson, C. (2000) Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nature Medicine 6, 536–542.Google Scholar
Friend, D.R. (2005) New oral delivery systems of treatment of inflammatory bowel disease. Advanced Drug Delivery Reviews 57, 247–265.Google Scholar
Fuss, I.J., Heller, F., Boirivant, M., Leon, F., Yoshida, M., Fichtner-Feigl, S., Yang, Z., Exley, M., Kitani, A., Blumberg, R.S., Mannon, P. & Strober, W. (2004) Non classical CD1d-restricted NKT cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. Journal of Clinical Investigation 113, 1490–1497.Google Scholar
Garlanda, C., Bottazzi, B., Bastone, A. & Mantovani, A. (2005) Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annual Review of Immunology 23, 337–366.CrossRefGoogle ScholarPubMed
Gionchetti, P., Amadini, C., Rizzello, F., Venturi, A. & Campieri, M. (2002) Treatment of mild to moderate ulcerative colitis and pouchitis. Alimentary Pharmacology and Therapeutics 16, 13–19.Google Scholar
Goujon, M., McWilliam, H., Li, W., Valentin, F., Squizzato, S., Paern, J. & Lopez, R. (2010) A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Research 38, W695–W699.Google Scholar
Grainger, J.R., Smith, K.A., Hewitson, J.P., McSorley, H.J., Harcus, Y., Filbey, K.J., Finney, C.A., Greenwood, E.J., Knox, D.P., Wilson, M.S., Belkaid, Y., Rudensky, A.Y. & Maizels, R.M. (2010) Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. Journal of Experimental Medicine 207, 2331–2341.CrossRefGoogle ScholarPubMed
Grencis, R.K., Hultner, L. & Else, K.J. (1991) Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology 74, 329–332.Google Scholar
Guarner, F. (2009) Prebiotics, probiotics and helminths: the ‘natural’ solution? Digestive Diseases 27, 412–417.Google Scholar
Halvorson, H., Schlett, C. & Riddle, M. (2006) Postinfectious irritable bowel syndrome – a meta-analysis. American Journal of Gastroenterology 101, 1894–1899.Google Scholar
Harnett, W. & Harnett, M.M. (2006) Molecular basis of worm-induced immunomodulation. Parasite Immunology 28, 535–543.CrossRefGoogle ScholarPubMed
Hunter, M.M., Wang, A. & McKay, D.M. (2007) Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology 132, 1320–1330.CrossRefGoogle Scholar
Ilic, N., Worthington, J.J., Gruden-Movsesijan, A., Travis, M.A., Sofronic-Milosavljevic, L. & Grencis, R.K. (2011) Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro. Parasite Immunology 33, 572–582.CrossRefGoogle Scholar
Ishikawa, N., Goyal, P.K., Mahida, Y.R., Li, F.P. & Wakelin, D. (1998) Early cytokine responses during intestinal parasitic infections. Immunology 93, 257–263.Google Scholar
Ivanov, I.I., Zhou, L. & Littman, D.R. (2007) Transcriptional regulation of Th17 cell differentiation. Seminars in Immunology 19, 409–417.Google Scholar
Jeannin, P., Bottazzi, B., Sironi, M., Doni, A., Rusnati, M., Presta, M., Maina, V., Magistrelli, G., Haeuw, J.F., Hoeffel, G., Thieblemont, N., Corvaia, N., Garlanda, C., Delneste, Y. & Mantovani, A. (2005) Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 22, 551–560.Google Scholar
Jung, Y., Kim, H.H., Kim, H., Kong, H., Choi, B., Yang, Y. & Kim, Y. (2006) Evaluation of 5-aminosalicytaurine as a colon specific prodrug of 5-aminosalicylic acid for treatment of experimental colitis. European Journal of Pharmaceutical Sciences 28, 26–33.Google Scholar
Khan, W.I., Blennerhasset, P.A., Varghese, A.K., Chowdhury, S.K., Omsted, P., Deng, Y. & Collins, S.M. (2002) Intestinal nematode infection ameliorates experimental colitis in mice. Infection and Immunity 70, 5931–5937.Google Scholar
Klotz, U. & Schwab, M. (2005) Topical delivery of therapeutic agents in the treatment of inflammatory bowel disease. Advanced Drug Delivery Reviews 57, 267–279.Google Scholar
Letterio, J.J. & Roberts, A.B. (1998) Regulation of immune responses by TGF-beta. Annual Review of Immunology 16, 137–161.Google Scholar
López-Palacios, N., Mendoza, J.L., Taxonera, C., Lana, R., López-Jamar, J.M. & Díaz-Rubio, M. (2011) Mucosal healing for predicting clinical outcome in patients with ulcerative colitis using thiopurines in monotherapy. European Journal of Internal Medicine 22, 621–625.Google Scholar
Luo, J.Y., Zhong, Y., Cao, J.C. & Cui, H.F. (2011) Efficacy of oral colon-specific delivery capsule of low-molecular-weight heparin on ulcerative colitis. Biomedicine and Pharmacotherapy 65, 111–117.CrossRefGoogle ScholarPubMed
Mahgoub, A.A., El-Medany, A.A., Hager, H.H., Mustafa, A.A. & El-Sabah, D.M. (2003) Evaluating the prophylactic potential of zafirlukast against the toxic effects of acetic acid on the rat colon. Toxicology Letters 145, 79–87.Google Scholar
Maizels, R.M. & Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews. Immunology 3, 733–744.CrossRefGoogle ScholarPubMed
Maizels, R.M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M.D. & Allen, J.E. (2004) Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle ScholarPubMed
Maizels, R.M., Pearce, E.J., Artis, D., Yazdanbakhsh, M. & Wynn, T.A. (2009) Regulation of pathogenesis and immunity in helminth infections. Journal of Experimental Medicine 206, 2059–2066.Google Scholar
Maloy, K.J., Salaun, L., Cahill, R., Dougan, G., Saunders, N.J. & Powrie, F. (2003) CD4+ CD25+ TR cells suppress innate immune pathology through cytokine-dependent mechanisms. Journal of Experimental Medicine 197, 111–119.Google Scholar
McDermott, J.R., Grencis, R.K. & Else, K.J. (2001) Leukocyte recruitment during enteric nematode infection. Immunology 103, 505–510.Google Scholar
McKay, D.M. (2009) The therapeutic helminth? Trends in Parasitology 25, 109–114.Google Scholar
Moreels, T.G., Nieuwendijk, R.J., De Man, J.G., De Winter, B.Y., Herman, A.G., Van Marck, E.A. & Pelckmans, P.A. (2004) 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 53, 99–107.CrossRefGoogle ScholarPubMed
Motomura, Y., Wang, H., Deng, Y., El-Sharkawy, R.T., Verdu, E.F. & Khan, W.I. (2009) Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clinical and Experimental Immunology 155, 88–95.Google Scholar
Nakamura, K., Honda, K., Mizutani, T., Akiho, H. & Harada, N. (2006) Novel strategies for the treatment of inflammatory bowel disease: selective inhibition of cytokines and adhesion molecules. World Journal of Gastroenterology 12, 4628–4635.Google Scholar
Nusrat, A., Parkos, C.A., Liang, T.W., Carnes, D.K. & Madara, J.L. (1997) Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 113, 1489–1500.CrossRefGoogle ScholarPubMed
Ohtani, K., Ohtsuka, Y., Ikuse, T., Baba, Y., Yamakawa, Y., Aoyagi, Y., Fujii, T., Kudo, T., Nagata, S. & Shimizu, T. (2010) Increased mucosal expression of GATA-3 and STAT-4 in pediatric ulcerative colitis. Pediatrics International 52, 584–589.Google Scholar
Qin, H.Y., Wu, J.C., Tong, X.D., Sung, J.J., Xu, H.X. & Bian, Z.X. (2011) Systematic review of animal models of post-infectious/post-inflammatory irritable bowel syndrome. Journal of Gastroenterology 46, 164–174.CrossRefGoogle ScholarPubMed
Reardon, C., Sanchez, A., Hogaboam, C.M. & McKay, D.M. (2001) Tape-worm infection reduces the epithelial ion transport abnormalities in murine dextran-sulfate sodium-induced colitis. Infection and Immunity 69, 4417–4423.Google Scholar
Sakaguchi, S., Ono, M., Setoguchi, R., Yagi, H., Hori, S., Fehervari, Z., Shimizu, J., Takahashi, T. & Nomura, T. (2006) Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunological Reviews 212, 8–27.Google Scholar
Satoguina, J., Mempel, M., Larbi, J., Badusche, M., Loliger, C., Adjei, O., Gachelin, G., Fleischer, B. & Hoerauf, A. (2002) Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes and Infection 4, 1291–1300.Google Scholar
Savchenko, A.S., Inoue, A., Ohashi, R., Jiang, S., Hasegawa, G., Tanaka, T., Hamakubo, T., Kodama, T., Aoyagi, Y., Ushiki, T. & Naito, M. (2011) Long pentraxin 3 (PTX3) expression and release by neutrophils in vitro and in ulcerative colitis. Pathology International 61, 290–297.Google Scholar
Setiawan, T., Metwali, A., Blum, A.M., Ince, M.N., Urban, J.F. Jr, Elliott, D.E. & Weinstock, J.V. (2007) Heligmosomoides polygyrus promotes regulatory T cell cytokine production in normal distal murine intestine. Infection and Immunity 75, 4655–4663.Google Scholar
Shen, W. & Durum, S.K. (2010) Synergy of IL-23 and Th17 cytokines: new light on inflammatory bowel disease. Neurochemical Research 35, 940–946.Google Scholar
Sievers, F., Wilm, A., Dineen, D.G., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J.D. & Higgins, D. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular Systems Biology 7, 539.Google Scholar
Strober, W. & Fuss, I.J. (2011) Pro-inflammatory cytokines in the pathogenesis of inflammatory bowel diseases. Gastroenterology 140, 1756–1767.CrossRefGoogle Scholar
Summers, R.W., Elliott, D.E., Urban, J.F. Jr, Thompson, R. & Weinstock, J.V. (2005) Trichuris suis therapy in Crohn's disease. Gut 54, 87–90.Google Scholar
Turner, J.D., Jenkins, G.R., Hogg, K.G., Aynsley, S.A., Paveley, R.A., Cook, P.C., Coles, M.C. & Mountford, A.P. (2011) CD4+ CD25+ regulatory cells contribute to the regulation of colonic Th2 granulomatous pathology caused by schistosome infection. PLoS Neglected Tropical Diseases 5, e1269.Google Scholar
Watanabe, T., Hirono, H., Hasegawa, K., Soga, K. & Shibasaki, K. (2011) Literature review in cases with exacerbation of ulcerative colitis induced by treatment with interferon and/or ribavirin. Journal of Gastroenterology and Hepatology 26, 1709–1716.Google Scholar
Wilson, M.S., Taylor, M.D., Balic, A., Finney, C.A.M., Lamb, J.R. & Maizels, R.M. (2005) Suppression of allergic airway inflammation by helminth-induced regulatory T cells. Journal of Experimental Medicine 7, 1199–1212.Google Scholar
Yazdanbakhsh, M., Kremsner, P.G. & van Ree, R. (2002) Allergy, parasites and the hygiene hypothesis. Science 296, 490–494.Google Scholar
Zhou, L., Lopes, J.E., Chong, M.M., Ivanov, I.I., Min, R., Victora, G.D., Shen, Y., Du, J., Rubtsov, Y.P., Rudensky, A.Y., Ziegler, S.F. & Littman, D.R. (2008) TGF-β-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORγt function. Nature 453, 236–240.Google Scholar