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Immunity. 2016 Mar 15;44(3):634-646. doi: 10.1016/j.immuni.2016.02.019.

Lymphoid-Tissue-Resident Commensal Bacteria Promote Members of the IL-10 Cytokine Family to Establish Mutualism.

Author information

1
Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology, Weill Cornell Medicine, New York, NY 10021 USA; Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY 10021 USA; Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, New York, NY 10021, USA.
2
Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology, Weill Cornell Medicine, New York, NY 10021 USA; Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY 10021 USA; Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, New York, NY 10021, USA.
3
Host Microbiota Interactions Laboratory, Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK.
4
Department of Microbiology and Immunology, The Institute of Medical Science, The University of Toyko, Toyko 108-8639, Japan; Japan Science and Technology Agency, Core Research for Evolutional Science and Technology, Tokyo 102-0076, Japan.
5
Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
6
Department of Computational Biology and Immunology, Memorial Sloan Kettering Cancer Center, New York, NY 10021, USA.
7
Yakult Central Institute, Tokyo 186-8650, Japan.
8
Department of Microbiology and Immunology, Center for Gastrointestinal Biology and Disease, University of North Carolina, Chapel Hill, NC 27599-7032, USA.
9
The Children's Hospital of Philadelphia, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
10
Laboratory of Vaccine Materials, National Institutes of Biomedical Innovation, Health and Nutrition, Osaka 567-0085, Japan.
11
Joan and Sanford I. Weill Department of Medicine, Division of Gastroenterology, Weill Cornell Medicine, New York, NY 10021 USA; Department of Microbiology and Immunology, Weill Cornell Medicine, New York, NY 10021 USA; Jill Roberts Institute for Research in Inflammatory Bowel Disease, Weill Cornell Medicine, New York, NY 10021, USA. Electronic address: gfsonnenberg@med.cornell.edu.

Abstract

Physical separation between the mammalian immune system and commensal bacteria is necessary to limit chronic inflammation. However, selective species of commensal bacteria can reside within intestinal lymphoid tissues of healthy mammals. Here, we demonstrate that lymphoid-tissue-resident commensal bacteria (LRC) colonized murine dendritic cells and modulated their cytokine production. In germ-free and antibiotic-treated mice, LRCs colonized intestinal lymphoid tissues and induced multiple members of the IL-10 cytokine family, including dendritic-cell-derived IL-10 and group 3 innate lymphoid cell (ILC3)-derived IL-22. Notably, IL-10 limited the development of pro-inflammatory Th17 cell responses, and IL-22 production enhanced LRC colonization in the steady state. Furthermore, LRC colonization protected mice from lethal intestinal damage in an IL-10-IL-10R-dependent manner. Collectively, our data reveal a unique host-commensal-bacteria dialog whereby selective subsets of commensal bacteria interact with dendritic cells to facilitate tissue-specific responses that are mutually beneficial for both the host and the microbe.

PMID:
26982365
PMCID:
PMC4845739
DOI:
10.1016/j.immuni.2016.02.019
[Indexed for MEDLINE]
Free PMC Article

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