Helicobacter hepaticus Triggers Colitis in Specific-Pathogen-Free Interleukin-10 (IL-10)-Deficient Mice through an IL-12- and Gamma Interferon-Dependent Mechanism

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Infection and Immunity, November 1998, p. 5157-5166, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Helicobacter hepaticus Triggers Colitis in Specific-Pathogen-Free Interleukin-10 (IL-10)-Deficient Mice through an IL-12- and Gamma Interferon-Dependent Mechanism

Marika C. Kullberg,¹^,^* Jerrold M. Ward,² Peter L. Gorelick,³ Patricia Caspar,¹ Sara Hieny,¹ Allen Cheever,¹^,⁴ Dragana Jankovic,¹ and Alan Sher¹

Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892-0425¹; Veterinary and Tumor Pathology Section, Animal Sciences Branch, Office of Laboratory Animal Resources, Division of Basic Sciences, National Cancer Institute,² and Animal Health Diagnostic Laboratory, Laboratory Animal Sciences Program, NCI-FCRDC, Science Applications International Corporation,³ Frederick, Maryland 21702-1201; and The Biomedical Research Institute, Rockville, Maryland 20852⁴

Received 23 June 1998/Accepted 11 August 1998

Mice rendered deficient in interleukin-10 (IL-10) by gene targeting (IL-10^/ mice) develop chronic enterocolitis resembling human inflammatorybowel disease (IBD) when maintained in conventional animal facilities.However, they display a minimal and delayed intestinal inflammatoryresponse when reared under specific-pathogen-free (SPF) conditions,suggesting the involvement of a microbial component in pathogenesis.We show here that experimental infection with a single bacterialagent, Helicobacter hepaticus, induces chronic colitis in SPF-rearedIL-10^/ mice and that the disease is accompanied by a type 1 cytokineresponse (gamma interferon [IFN- $gamma$ ], tumor necrosis factor alpha,and nitric oxide) detected by restimulation of spleen and mesentericlymph node cells with a soluble H. hepaticus antigen (Ag) preparation.In contrast, wild-type (WT) animals infected with the same bacteriadid not develop disease and produced IL-10 as the dominant cytokinein response to Helicobacter Ag. Strong H. hepaticus-reactive antibodyresponses as measured by Ag-specific total immunoglobulin G (IgG),IgG1, IgG2a, IgG2b, IgG3, and IgA were observed in both WT andIL-10^/ mice. In vivo neutralization of IFN- $gamma$ or IL-12 resulted in asignificant reduction of intestinal inflammation in H. hepaticus-infectedIL-10^/ mice, suggesting an important role for these cytokines in thedevelopment of colitis in the model. Taken together, these microbialreconstitution experiments formally establish that a defined bacterialagent can serve as the immunological target in the developmentof large bowel inflammation in IL-10^/ mice and argue that in nonimmunocompromised hosts IL-10 stimulatedin response to intestinal flora is important in preventing IBD.

^* Corresponding author. Mailing address: Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergyand Infectious Diseases, National Institutes of Health, Building4, Room 126, 4 Center Dr. MSC 0425, Bethesda, MD 20892-0425. Phone:(301) 496-8218. Fax: (301) 402-0890. E-mail: MKULLBERG{at}atlas.niaid.nih.gov.

Infection and Immunity, November 1998, p. 5157-5166, Vol. 66, No. 11
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

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