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CD4⁺CD25⁺ T_R Cells Suppress Innate Immune Pathology Through Cytokine-dependent Mechanisms

Kevin J. Maloy¹, Laurence Salaun¹, Rachel Cahill², Gordon Dougan², Nigel J. Saunders¹ and Fiona Powrie¹

¹ Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford, OX1 3RE, United Kingdom
² Department of Biological Sciences, Centre for Molecular Microbiology and Infection, Imperial College, South Kensington London, SW7 2AZ United Kingdom

Address correspondence to K. Maloy, Sir William Dunn School of Pathology, University of Oxford, South Parks Rd., Oxford, OX1 3RE, UK. Phone: 44-1865-285489; Fax: 44-1865-275591; E-mail: kevin.maloy{at}path.ox.ac.uk

CD4⁺CD25⁺ regulatory T (T_R) cells can inhibit a variety of autoimmune and inflammatory diseases, but the precise mechanisms by which they suppress immune responses in vivo remain unresolved. Here, we have used Helicobacter hepaticus infection of T cell–reconstituted recombination-activating gene (RAG)^-/- mice as a model to study the ability of CD4⁺CD25⁺ T_R cells to inhibit bacterially triggered intestinal inflammation. H. hepaticus infection elicited both T cell-mediated and T cell–independent intestinal inflammation, both of which were inhibited by adoptively transferred CD4⁺CD25⁺ T_R cells. T cell–independent pathology was accompanied by activation of the innate immune system that was also inhibited by CD4⁺CD25⁺ T_R cells. Suppression of innate immune pathology was dependent on T cell–derived interleukin 10 and also on the production of transforming growth factor ß. Thus, CD4⁺CD25⁺ T_R cells do not only suppress adaptive T cell responses, but are also able to control pathology mediated by innate immune mechanisms.

Key Words: regulatory T cells • Helicobacter • immune tolerance • mucosal immunity • IL-10

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• Suffia*, I., Reckling*, S. K., Salay*, G., Belkaid*, Y. (2005). A Role for CD103 in the Retention of CD4+CD25+ Treg and Control of Leishmania major Infection. J. Immunol. 174: 5444-5455 [Abstract] [Full Text]  
• Taylor, M. D., LeGoff, L., Harris, A., Malone, E., Allen, J. E., Maizels, R. M. (2005). Removal of Regulatory T Cell Activity Reverses Hyporesponsiveness and Leads to Filarial Parasite Clearance In Vivo. J. Immunol. 174: 4924-4933 [Abstract] [Full Text]  
• Smith, D. W., Nagler-Anderson, C. (2005). Preventing Intolerance: The Induction of Nonresponsiveness to Dietary and Microbial Antigens in the Intestinal Mucosa. J. Immunol. 174: 3851-3857 [Abstract] [Full Text]  
• Kleinewietfeld, M., Puentes, F., Borsellino, G., Battistini, L., Rotzschke, O., Falk, K. (2005). CCR6 expression defines regulatory effector/memory-like cells within the CD25+CD4+ T-cell subset. Blood 105: 2877-2886 [Abstract] [Full Text]  
• Walker, M. R., Carson, B. D., Nepom, G. T., Ziegler, S. F., Buckner, J. H. (2005). De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+CD25- cells. Proc. Natl. Acad. Sci. USA 102: 4103-4108 [Abstract] [Full Text]  
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• Murphy, T. J., Choileain, N. N., Zang, Y., Mannick, J. A., Lederer, J. A. (2005). CD4+CD25+ Regulatory T Cells Control Innate Immune Reactivity after Injury. J. Immunol. 174: 2957-2963 [Abstract] [Full Text]  
• Loughry, A., Fairchild, S., Athanasou, N., Edwards, J., Hall, F. C. (2005). Inflammatory arthritis and dermatitis in thymectomized, CD25+ cell-depleted adult mice. Rheumatology (Oxford) 44: 299-308 [Abstract] [Full Text]  
• Freeman, C. M., Chiu, B.-C., Stolberg, V. R., Hu, J., Zeibecoglou, K., Lukacs, N. W., Lira, S. A., Kunkel, S. L., Chensue, S. W. (2005). CCR8 Is Expressed by Antigen-Elicited, IL-10-Producing CD4+CD25+ T Cells, Which Regulate Th2-Mediated Granuloma Formation in Mice. J. Immunol. 174: 1962-1970 [Abstract] [Full Text]  
• Hanash, A. M., Levy, R. B. (2005). Donor CD4+CD25+ T cells promote engraftment and tolerance following MHC-mismatched hematopoietic cell transplantation. Blood 105: 1828-1836 [Abstract] [Full Text]  
• Wei, B., Velazquez, P., Turovskaya, O., Spricher, K., Aranda, R., Kronenberg, M., Birnbaumer, L., Braun, J. (2005). Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proc. Natl. Acad. Sci. USA 102: 2010-2015 [Abstract] [Full Text]  
• Eksteen, B, Walker, L S K, Adams, D H (2005). Immune regulation and colitis: suppression of acute inflammation allows the development of chronic inflammatory bowel disease. Gut 54: 4-6 [Full Text]  
• Gregg, R. K., Jain, R., Schoenleber, S. J., Divekar, R., Bell, J. J., Lee, H.-H., Yu, P., Zaghouani, H. (2004). A Sudden Decline in Active Membrane-Bound TGF-{beta} Impairs Both T Regulatory Cell Function and Protection against Autoimmune Diabetes. J. Immunol. 173: 7308-7316 [Abstract] [Full Text]  
• Chen, G., Zeng, W., Miyazato, A., Billings, E., Maciejewski, J. P., Kajigaya, S., Sloand, E. M., Young, N. S. (2004). Distinctive gene expression profiles of CD34 cells from patients with myelodysplastic syndrome characterized by specific chromosomal abnormalities. Blood 104: 4210-4218 [Abstract] [Full Text]  
• Henriksson, G., Helgeland, L., Midtvedt, T., Stierna, P., Brandtzaeg, P. (2004). Immune Response to Mycoplasma pulmonis in Nasal Mucosa Is Modulated by the Normal Microbiota. Am. J. Respir. Cell Mol. Bio. 31: 657-662 [Abstract] [Full Text]  
• Huber, S., Schramm, C., Lehr, H. A., Mann, A., Schmitt, S., Becker, C., Protschka, M., Galle, P. R., Neurath, M. F., Blessing, M. (2004). Cutting Edge: TGF-{beta} Signaling Is Required for the In Vivo Expansion and Immunosuppressive Capacity of Regulatory CD4+CD25+ T Cells. J. Immunol. 173: 6526-6531 [Abstract] [Full Text]  
• Roers, A., Siewe, L., Strittmatter, E., Deckert, M., Schluter, D., Stenzel, W., Gruber, A. D., Krieg, T., Rajewsky, K., Muller, W. (2004). T Cell-specific Inactivation of the Interleukin 10 Gene in Mice Results in Enhanced T Cell Responses but Normal Innate Responses to Lipopolysaccharide or Skin Irritation. JEM 200: 1289-1297 [Abstract] [Full Text]  

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