Interactions between Trichinella spiralis infection and induced colitis in mice.

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.

[1]  K. Soga,et al.  Literature review in cases with exacerbation of ulcerative colitis induced by treatment with interferon and/or ribavirin , 2011, Journal of gastroenterology and hepatology.

[2]  J. Mendoza,et al.  Mucosal healing for predicting clinical outcome in patients with ulcerative colitis using thiopurines in monotherapy. , 2011, European journal of internal medicine.

[3]  D. Higgins,et al.  Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega , 2011, Molecular systems biology.

[4]  R. Grencis,et al.  Trichinella spiralis antigens prime mixed Th1/Th2 response but do not induce de novo generation of Foxp3+ T cells in vitro , 2011, Parasite immunology.

[5]  M. Coles,et al.  CD4+CD25+ Regulatory Cells Contribute to the Regulation of Colonic Th2 Granulomatous Pathology Caused by Schistosome Infection , 2011, PLoS neglected tropical diseases.

[6]  B. Zhong,et al.  [Imbalance of CD4(+) T cell subgroups in ulcerative colitis]. , 2011, Zhonghua yi xue za zhi.

[7]  T. Ushiki,et al.  Long pentraxin 3 (PTX3) expression and release by neutrophils in vitro and in ulcerative colitis , 2011, Pathology international.

[8]  W. Strober,et al.  Proinflammatory cytokines in the pathogenesis of inflammatory bowel diseases. , 2011, Gastroenterology.

[9]  Y. Zhong,et al.  Efficacy of oral colon-specific delivery capsule of low-molecular-weight heparin on ulcerative colitis. , 2011, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[10]  J. Sung,et al.  Systematic review of animal models of post-infectious/post-inflammatory irritable bowel syndrome , 2011, Journal of Gastroenterology.

[11]  A. Rudensky,et al.  Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway , 2010, The Journal of experimental medicine.

[12]  Toshiaki Shimizu,et al.  Increased mucosal expression of GATA‐3 and STAT‐4 in pediatric ulcerative colitis , 2010, Pediatrics international : official journal of the Japan Pediatric Society.

[13]  B. Everts,et al.  Helminths and dendritic cells: Sensing and regulating via pattern recognition receptors, Th2 and Treg responses , 2010, European journal of immunology.

[14]  S. Durum,et al.  Synergy of IL-23 and Th17 Cytokines: New Light on Inflammatory Bowel Disease , 2010, Neurochemical Research.

[15]  Rodrigo Lopez,et al.  A new bioinformatics analysis tools framework at EMBL–EBI , 2010, Nucleic Acids Res..

[16]  R. Maizels,et al.  Regulation of pathogenesis and immunity in helminth infections , 2009, The Journal of experimental medicine.

[17]  F. Guarner.  Prebiotics, Probiotics and Helminths: The ‘Natural’ Solution? , 2009, Digestive Diseases.

[18]  B. Everts,et al.  Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses , 2009, The Journal of experimental medicine.

[19]  K. Garsed,et al.  Postinfectious irritable bowel syndrome. , 2009, Gastroenterology.

[20]  Judy H. Cho,et al.  IL-23 and autoimmunity: new insights into the pathogenesis of inflammatory bowel disease. , 2009, Annual review of medicine.

[21]  Y. Belkaid,et al.  Regulatory T cells in the control of host-microorganism interactions (*). , 2009, Annual review of immunology.

[22]  D. McKay.  The therapeutic helminth? , 2009, Trends in parasitology.

[23]  W. Khan,et al.  Helminth antigen‐based strategy to ameliorate inflammation in an experimental model of colitis , 2009, Clinical and experimental immunology.

[24]  D. Elliott,et al.  Colonization with Heligmosomoides polygyrus Suppresses Mucosal IL-17 Production1 , 2008, The Journal of Immunology.

[25]  Yuelei Shen,et al.  TGF-β-induced Foxp3 inhibits TH17 cell differentiation by antagonizing RORγt function , 2008, Nature.

[26]  D. Littman,et al.  Transcriptional regulation of Th17 cell differentiation. , 2007, Seminars in immunology.

[27]  D. Elliott,et al.  Heligmosomoides polygyrus Promotes Regulatory T-Cell Cytokine Production in the Murine Normal Distal Intestine , 2007, Infection and Immunity.

[28]  D. McKay,et al.  Helminth infection enhances disease in a murine TH2 model of colitis. , 2007, Gastroenterology.

[29]  M. Harnett,et al.  Molecular basis of worm‐induced immunomodulation , 2006, Parasite immunology.

[30]  Kazuhiko Nakamura,et al.  Novel strategies for the treatment of inflammatory bowel disease: Selective inhibition of cytokines and adhesion molecules. , 2006, World journal of gastroenterology.

[31]  M. Riddle,et al.  Postinfectious Irritable Bowel Syndrome—A Meta-Analysis , 2006, The American Journal of Gastroenterology.

[32]  Shimon Sakaguchi,et al.  Foxp3+CD25+CD4+ natural regulatory T cells in dominant self‐tolerance and autoimmune disease , 2006, Immunological reviews.

[33]  Yunjin Jung,et al.  Evaluation of 5-aminosalicyltaurine as a colon-specific prodrug of 5-aminosalicylic acid for treatment of experimental colitis. , 2006, European journal of pharmaceutical sciences : official journal of the European Federation for Pharmaceutical Sciences.

[34]  C. Garlanda,et al.  The long pentraxin PTX3 as a link among innate immunity, inflammation, and female fertility , 2006, Journal of leukocyte biology.

[35]  R. Maizels,et al.  Suppression of allergic airway inflammation by helminth-induced regulatory T cells , 2005, The Journal of experimental medicine.

[36]  C. Lawrence,et al.  Contrasting effects of acute and chronic gastro-intestinal helminth infections on a heterologous immune response in a transgenic adoptive transfer model. , 2005, International journal for parasitology.

[37]  Pascale Jeannin,et al.  Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. , 2005, Immunity.

[38]  D. Friend.  New oral delivery systems for treatment of inflammatory bowel disease. , 2005, Advanced drug delivery reviews.

[39]  U. Klotz,et al.  Topical delivery of therapeutic agents in the treatment of inflammatory bowel disease. , 2005, Advanced drug delivery reviews.

[40]  Robert W. Summers,et al.  Vomiting in the recently anticoagulated patient , 2004, Gut.

[41]  F. Finkelman,et al.  Interleukin‐4‐ and interleukin‐13‐mediated host protection against intestinal nematode parasites , 2004, Immunological reviews.

[42]  R. Maizels,et al.  Helminth parasites – masters of regulation , 2004, Immunological reviews.

[43]  P. Mannon,et al.  Nonclassical CD1d-restricted NK T cells that produce IL-13 characterize an atypical Th2 response in ulcerative colitis. , 2004, The Journal of clinical investigation.

[44]  E. van Marck,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 , 2003, Gut.

[45]  A. Mustafa,et al.  Evaluating the prophylactic potential of zafirlukast against the toxic effects of acetic acid on the rat colon. , 2003, Toxicology letters.

[46]  Rick M. Maizels,et al.  Immune Regulation by helminth parasites: cellular and molecular mechanisms , 2003, Nature Reviews Immunology.

[47]  Nigel J. Saunders,et al.  CD4+CD25+ TR Cells Suppress Innate Immune Pathology Through Cytokine-dependent Mechanisms , 2003, The Journal of experimental medicine.

[48]  A. Hoerauf,et al.  Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). , 2002, Microbes and infection.

[49]  W. Khan,et al.  Intestinal Nematode Infection Ameliorates Experimental Colitis in Mice , 2002, Infection and Immunity.

[50]  P. Gionchetti,et al.  Treatment of mild to moderate ulcerative colitis and pouchitis , 2002, Alimentary pharmacology & therapeutics.

[51]  Maria Yazdanbakhsh,et al.  Allergy, parasites, and the hygiene hypothesis. , 2002, Science.

[52]  K. Else,et al.  Leucocyte recruitment during enteric nematode infection , 2001, Immunology.

[53]  C. Hogaboam,et al.  Tapeworm Infection Reduces Epithelial Ion Transport Abnormalities in Murine Dextran Sulfate Sodium-Induced Colitis , 2001, Infection and Immunity.

[54]  C. Pothoulakis,et al.  Endogenous corticosteroids modulate Clostridium difficile toxin A-induced enteritis in rats. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[55]  P. Pasricha,et al.  A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. , 2000, Gastroenterology.

[56]  Mark T. Whary,et al.  Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy , 2000, Nature Medicine.

[57]  Yaping Chen,et al.  Insights from mouse models of colitis , 2000, Journal of leukocyte biology.

[58]  Anita B. Roberts,et al.  REGULATION OF IMMUNE RESPONSES BY TGF-β* , 1998 .

[59]  Y. Mahida,et al.  Early cytokine responses during intestinal parasitic infections , 1998, Immunology.

[60]  C. Parkos,et al.  Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. , 1997, Gastroenterology.

[61]  K. Else,et al.  Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. , 1991, Immunology.

[62]  H. Adami,et al.  Ulcerative colitis and colorectal cancer. A population-based study. , 1990, The New England journal of medicine.

[63]  Dunn Ij,et al.  Cell injury caused by Trichinella spiralis in the mucosal epithelium of B10A mice. , 1985 .

[64]  C. Garlanda,et al.  Pattern recognition by pentraxins. , 2009, Advances in experimental medicine and biology.

[65]  C. Garlanda,et al.  Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. , 2005, Annual review of immunology.

[66]  R. Willén,et al.  Acetic acid-induced colitis in the rat: a reproducible experimental model for acute ulcerative colitis. , 1992, European surgical research. Europaische chirurgische Forschung. Recherches chirurgicales europeennes.