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

Thomas C. Fung, Nicholas J. Bessman, Matthew R. Hepworth, Nitin Kumar, Naoko Shibata, Dmytro Kobuley, Kelvin Wang, Carly G.K. Ziegler, Jeremy Goc, Tatsuichiro Shima, Yoshinori Umesaki, R. Balfour Sartor, Kaede V. Sullivan, Trevor D. Lawley, Jun Kunisawa, Hiroshi Kiyono, Gregory F. Sonnenberg

Research output: Contribution to journalArticlepeer-review

64 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)634-646
Number of pages13
JournalImmunity
Volume44
Issue number3
DOIs
Publication statusPublished - 2016 Mar 15
Externally publishedYes

ASJC Scopus subject areas

  • Immunology and Allergy
  • Immunology
  • Infectious Diseases

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