Resident Enteric Bacteria Are Necessary for Development of Spontaneous Colitis and Immune System Activation in Interleukin-10-Deficient Mice

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Infection and Immunity, November 1998, p. 5224-5231, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Resident Enteric Bacteria Are Necessary for Development of Spontaneous Colitis and Immune System Activation in Interleukin-10-Deficient Mice

Rance K. Sellon,¹ Susan Tonkonogy,² Michael Schultz,³ Levinus A. Dieleman,³ Wetonia Grenther,¹ Ed Balish,⁴ Donna M. Rennick,⁵ and R. Balfour Sartor³^,^*

Department of Companion Animal and Special Species¹ and Department of Microbiology, Pathology and Parasitology, Center for Gastrointestinal Biology and Disease,² College of Veterinary Medicine, North Carolina State University, Raleigh, North Carolina 27606; Division of Digestive Diseases and Nutrition, Department of Medicine and Center for Gastrointestinal Biology and Disease, School of Medicine, University of North Carolina- Chapel Hill, Chapel Hill, North Carolina 27599-7080³; and Departments of Surgery and Microbiology, University of Wisconsin, Madison, Wisconsin,⁴ and Department of Immunology, DNAX Corporation, Palo Alto, California⁵

Received 25 March 1998/Returned for modification 15 July 1998/Accepted 20 August 1998

Mice with targeted deletion of the gene for interleukin-10 (IL-10) spontaneously develop enterocolitis when maintained inconventional conditions but develop only colitis when kept inspecific-pathogen-free (SPF) environments. This study tested thehypothesis that enteric bacteria are necessary for the developmentof spontaneous colitis and immune system activation in IL-10-deficientmice. IL-10-deficient mice were maintained in either SPF conditionsor germfree conditions or were populated with bacteria known tocause colitis in other rodent models. IL-10-deficient mice keptin SPF conditions developed colitis in all segments of the colon(cecum and proximal and distal colon). These mice exhibited immunesystem activation as evidenced by increased expression of CD44on CD4⁺ T cells; increased mesenteric lymph node cell numbers; and increasedproduction of immunoglobulin A (IgA), IgG1, and IL-12 p40 fromcolon fragment cultures. Mice populated with bacterial strains,including Bacteroides vulgatus, known to induce colitis in otherrodent models had minimal colitis. Germfree IL-10-deficient micehad no evidence of colitis or immune system activation. We concludetherefore that resident enteric bacteria are necessary for thedevelopment of spontaneous colitis and immune system activationin IL-10-deficient mice.

^* Corresponding author. Mailing address: Division of Digestive Diseases and Nutrition, CB # 7080, University of North Carolina,Chapel Hill, NC 27599-7080. Phone: (919) 966-0149. Fax: (919)966-7468. E-mail: rbs{at}med.unc.edu.

Infection and Immunity, November 1998, p. 5224-5231, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

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