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Functional Importance of Regional Differences in Localized Gene Expression of Receptors for IL-13 in Murine Gut¹

Motoko Morimoto^2,*,, Masahiro Morimoto^2,,, Aiping Zhao^*,, Kathleen B. Madden, Harry Dawson, Fred D. Finkelman^¶,||, Margaret Mentink-Kane^#, Joseph F. Urban, Jr, Thomas A. Wynn^# and Terez Shea-Donohue^3,*,

^* Department of Medicine and Mucosal Biology Research Center, University of Maryland School of Medicine, Baltimore, MD 21201; Nutritional Requirements and Function Laboratory, Beltsville Human Nutrition Research Center, Agricultural Research Service, U.S. Department of Agriculture, Beltsville, MD 20705; Laboratory of Veterinary Pathology, Faculty of Agriculture, Yamaguchi University, Yamaguchi, Japan; Department of Pediatrics, Uniformed Services University of the Health Sciences, Bethesda, MD 20814; ^¶ Department of Medicine and Department of Pediatrics, University of Cincinnati, Cincinnati, OH 45267; ^|| Cincinnati Veterans Administration Medical Center, Cincinnati, OH 45220; and ^# Division of Parasitology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892

IL-13 induces a STAT6-dependent hypercontractility of intestinal smooth muscle that is mediated by binding to the IL-13R1 component of the type 2 IL-4R that is linked to STAT6. IL-13 also binds to the IL-13R2 that is not linked to STAT6 and functions to limit the effects of IL-13 in vivo. In this study we assessed the contributions of regional and cellular differences in the distribution of the IL-13R components to the physiological regulation of smooth muscle function in wild-type mice and mice deficient in STAT6 or IL-13R2. The expression of IL-13 and IL-13R2 was higher in colon than in small intestine. Laser capture microdissection of specific cell types revealed that the expression of IL-13R2 was higher in the smooth muscle layer compared with levels in the epithelial cells of the mucosa. In contrast, there was a uniform distribution of IL-131 in smooth muscle, epithelia, and myenteric neurons. The significant hypercontractility of smooth muscle in mice deficient in IL-13R2, but not in STAT6, shows the physiological importance of IL-13 binding to IL-13R2. The pronounced differences in the expression of IL-13R2 suggest that the gut has developed sophisticated mechanisms for controlling the physiological and pathophysiological activities of IL-13.

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