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Infection and Immunity, October 2008, p. 4772-4782, Vol. 76, No. 10
0019-9567/08/$08.00+0     doi:10.1128/IAI.00744-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Anti-Inflammatory Mechanisms of Enteric Heligmosomoides polygyrus Infection against Trinitrobenzene Sulfonic Acid-Induced Colitis in a Murine Model {triangledown}

Thomas L. Sutton,1 Aiping Zhao,2 Kathleen B. Madden,3 Justin E. Elfrey,2,{dagger} Blaine A. Tuft,1,{ddagger} Carolyn A. Sullivan,1 Joseph F. Urban Jr.,4 and Terez Shea-Donohue2*

Department of Pediatrics, Walter Reed Army Medical Center, Washington, DC 20307,1 Department of Medicine and the Mucosal Biology Research Center, University of Maryland School of Medicine, Baltimore, Maryland 21201,2 Department of Pediatrics, Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814,3 Diet, Genomics, & Immunology Laboratory, Beltsville Human Nutrition Research Center, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, Maryland 207054

Received 1 June 2007/ Returned for modification 17 July 2007/ Accepted 12 July 2008

Recent studies showed that enteric helminth infection improved symptoms in patients with inflammatory bowel disease as well as in experimental models of colitis. The aim of this study was to determine the mechanism of the protective effect of helminth infection on colitis-induced changes in immune and epithelial cell function. BALB/c mice received an oral infection of Heligmosomoides polygyrus third-stage larvae, were given intrarectal saline or trinitrobenzene sulfonic acid (TNBS) on day 10 postinfection, and were studied 4 days later. Separate groups of mice received intrarectal saline or TNBS on day 10 and were studied on day 14. Muscle-free colonic mucosae were mounted in Ussing chambers to measure mucosal permeability and secretion. Expression of cytokines was assessed by quantitative real-time PCR, and mast cells were visualized by immunohistochemistry. TNBS-induced colitis induced mucosal damage, upregulated Th1 cytokines, and depressed secretory responses. Heligmosomoides polygyrus elevated Th2 cytokine expression, increased mast cell infiltration and mucosal resistance, and also reduced some secretory responses. Prior H. polygyrus infection prevented TNBS-induced upregulation of Th1 cytokines and normalized secretory responses to specific agonists. TNBS-induced colitis did not alter H. polygyrus-induced mast cell infiltration or upregulation of Th2 cytokine expression. The results indicate that the protective mechanism of enteric nematode infection against TNBS-induced colitis involves prevention of Th1 cytokine expression and improved colonic function by a mechanism that may involve mast cell-mediated protection of neural control of secretory function. Similar response patterns could account for the clinical improvement seen in inflammatory bowel disease with helminthic therapy.

* Corresponding author. Mailing address: Mucosal Biology Research Center, University of Maryland School of Medicine, 20 Penn Street, Baltimore, MD 21201. Phone: (410) 706-5503. Fax: (410) 706-5508. E-mail: tdonohue{at}mbrc.umaryland.edu

{triangledown} Published ahead of print on 21 July 2008.

Editor: W. A. Petri, Jr.

{dagger} Present address: New York College of Osteopathic Medicine, Old Westbury, NY 11568.

{ddagger} Present address: Department of Pediatrics, Naval Medical Center, Portsmouth, VA 23708.

Infection and Immunity, October 2008, p. 4772-4782, Vol. 76, No. 10
0019-9567/08/$08.00+0     doi:10.1128/IAI.00744-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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