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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 inflammatory bowel disease (IBD) when maintained in conventional animal facilities. However, they display a minimal and delayed intestinal inflammatory response 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 bacterial agent, Helicobacter hepaticus, induces chronic colitis in SPF-reared IL-10-/- mice and that the disease is accompanied by a type 1 cytokine response (gamma interferon [IFN-gamma ], tumor necrosis factor alpha, and nitric oxide) detected by restimulation of spleen and mesenteric lymph node cells with a soluble H. hepaticus antigen (Ag) preparation. In contrast, wild-type (WT) animals infected with the same bacteria did not develop disease and produced IL-10 as the dominant cytokine in response to Helicobacter Ag. Strong H. hepaticus-reactive antibody responses as measured by Ag-specific total immunoglobulin G (IgG), IgG1, IgG2a, IgG2b, IgG3, and IgA were observed in both WT and IL-10-/- mice. In vivo neutralization of IFN-gamma or IL-12 resulted in a significant reduction of intestinal inflammation in H. hepaticus-infected IL-10-/- mice, suggesting an important role for these cytokines in the development of colitis in the model. Taken together, these microbial reconstitution experiments formally establish that a defined bacterial agent can serve as the immunological target in the development of large bowel inflammation in IL-10-/- mice and argue that in nonimmunocompromised hosts IL-10 stimulated in response to intestinal flora is important in preventing IBD.


* Corresponding author. Mailing address: Immunobiology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Building 4, 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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  • Ge, Z., White, D. A., Whary, M. T., Fox, J. G. (2001). Fluorogenic PCR-Based Quantitative Detection of a Murine Pathogen, Helicobacter hepaticus. J. Clin. Microbiol. 39: 2598-2602 [Abstract] [Full Text]  
  • Lindsay, J. O., Ciesielski, C. J., Scheinin, T., Hodgson, H. J., Brennan, F. M. (2001). The Prevention and Treatment of Murine Colitis Using Gene Therapy with Adenoviral Vectors Encoding IL-10. J. Immunol. 166: 7625-7633 [Abstract] [Full Text]  
  • Shomer, N. H., Dangler, C. A., Schrenzel, M. D., Whary, M. T., Xu, S., Feng, Y., Paster, B. J., Dewhirst, F. E., Fox, J. G. (2001). Cholangiohepatitis and Inflammatory Bowel Disease Induced by a Novel Urease-Negative Helicobacter Species in A/J and Tac:ICR:Hascidf RF Mice. Exp. Biol. Med. 226: 420-428 [Abstract] [Full Text]  
  • FOX, J. G., HANDT, L., XU, S., SHEN, Z., DEWHIRST, F. E., PASTER, B. J., DANGLER, C. A., LODGE, K., MOTZEL, S., KLEIN, H. (2001). Novel Helicobacter species isolated from rhesus monkeys with chronic idiopathic colitis. J Med Microbiol 50: 421-429 [Abstract] [Full Text]  
  • Erdman, S. E., Fox, J. G., Dangler, C. A., Feldman, D., Horwitz, B. H. (2001). Cutting Edge: Typhlocolitis in NF-{{kappa}}B-Deficient Mice. J. Immunol. 166: 1443-1447 [Abstract] [Full Text]  
  • Solnick, J. V., Schauer, D. B. (2001). Emergence of Diverse Helicobacter Species in the Pathogenesis of Gastric and Enterohepatic Diseases. Clin. Microbiol. Rev. 14: 59-97 [Abstract] [Full Text]  
  • Kishi, D., Takahashi, I., Kai, Y., Tamagawa, H., Iijima, H., Obunai, S., Nezu, R., Ito, T., Matsuda, H., Kiyono, H. (2000). Alteration of V{beta} Usage and Cytokine Production of CD4+ TCR {beta}{beta} Homodimer T Cells by Elimination of Bacteroides vulgatus Prevents Colitis in TCR {alpha}-Chain-Deficient Mice. J. Immunol. 165: 5891-5899 [Abstract] [Full Text]  
  • Patterson, M. M., Schrenzel, M. D., Feng, Y., Xu, S., Dewhirst, F. E., Paster, B. J., Thibodeau, S. A., Versalovic, J., Fox, J. G. (2000). Helicobacter aurati sp. nov., a Urease-Positive Helicobacter Species Cultured from Gastrointestinal Tissues of Syrian Hamsters. J. Clin. Microbiol. 38: 3722-3728 [Abstract] [Full Text]  
  • ASSEMAN, C., FOWLER, S., POWRIE, F. (2000). Control of Experimental Inflammatory Bowel Disease by Regulatory T cells. Am. J. Respir. Crit. Care Med. 162: S185-189 [Abstract] [Full Text]  
  • Dieleman, L. A., Arends, A., Tonkonogy, S. L., Goerres, M. S., Craft, D. W., Grenther, W., Sellon, R. K., Balish, E., Sartor, R. B. (2000). Helicobacter hepaticus Does Not Induce or Potentiate Colitis in Interleukin-10-Deficient Mice. Infect. Immun. 68: 5107-5113 [Abstract] [Full Text]  
  • Sutton, P., Kolesnikow, T., Danon, S., Wilson, J., Lee, A. (2000). Dominant Nonresponsiveness to Helicobacter pylori Infection Is Associated with Production of Interleukin 10 but Not Gamma Interferon. Infect. Immun. 68: 4802-4804 [Abstract] [Full Text]  
  • Caradonna, L., Amati, L., Magrone, T., Pellegrino, N.M., Jirillo, E., Caccavo, D. (2000). Invited review: Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. Innate Immunity 6: 205-214 [Abstract]  
  • Rennick, D. M., Fort, M. M. (2000). Lessons From Genetically Engineered Animal Models: XII. IL-10-deficient (IL-10-/-) mice and intestinal inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 278: G829-G833 [Abstract] [Full Text]  
  • CHIEN, C.-C., TAYLOR, N. S., GE, Z., SCHAUER, D. B., YOUNG, V. B., FOX, J. G. (2000). Identification of cdtB homologues and cytolethal distending toxin activity in enterohepatic Helicobacter spp.. J Med Microbiol 49: 525-534 [Abstract] [Full Text]  
  • Young, V. B., Knox, K. A., Schauer, D. B. (2000). Cytolethal Distending Toxin Sequence and Activity in the Enterohepatic Pathogen Helicobacter hepaticus. Infect. Immun. 68: 184-191 [Abstract] [Full Text]  
  • Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L., Powrie, F. (1999). An Essential Role for Interleukin 10 in the Function of Regulatory T Cells That Inhibit Intestinal Inflammation. JEM 190: 995-1004 [Abstract] [Full Text]  
  • Li, C., Corraliza, I., Langhorne, J. (1999). A Defect in Interleukin-10 Leads to Enhanced Malarial Disease in Plasmodium chabaudi chabaudi Infection in Mice. Infect. Immun. 67: 4435-4442 [Abstract] [Full Text]  
  • Jankovic, D., Kullberg, M. C., Noben-Trauth, N., Caspar, P., Ward, J. M., Cheever, A. W., Paul, W. E., Sher, A. (1999). Schistosome-Infected IL-4 Receptor Knockout (KO) Mice, in Contrast to IL-4 KO Mice, Fail to Develop Granulomatous Pathology While Maintaining the Same Lymphokine Expression Profile. J. Immunol. 163: 337-342 [Abstract] [Full Text]  
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