Endogenous interleukin-10 constrains Th17 cells in patients with inflammatory bowel disease

J Transl Med. 2011 Dec 16:9:217. doi: 10.1186/1479-5876-9-217.

Abstract

Background: Th17 cells play a role in inflammation. Interleukin (IL)-10 is a potent anti-inflammatory cytokine. However, it is poorly understood whether and how endogenous IL-10 impacts the development of Th17 cells in human pathologies.

Materials and methods: We examined the relationship between IL-10 and Th17 cells in patients with Crohn's disease and in IL-10-deficient (IL-10-/-) mice. Th17 cells and dendritic cells (DCs) were defined by flow cytometry and evaluated by functional studies.

Results: We detected elevated levels of IL-17 and Th17 cells in the intestinal mucosa of patients with Crohn's disease. Intestinal DCs from Crohn's patients produced more IL-1β than controls and were superior to blood DCs in Th17 induction through an IL-1-dependent mechanism. Furthermore, IL-17 levels were negatively associated with those of IL-10 and were positively associated those of IL-1β in intestinal mucosa. These data point toward an in vivo cellular and molecular link among endogenous IL-10, IL-1, and Th17 cells in patients with Crohn's disease. We further investigated this relationship in IL-10(-/-) mice. We observed a systemic increase in Th17 cells in IL-10(-/-) mice when compared to wild-type mice. Similar to the intestinal DCs in patients with Crohn's disease, murine IL-10-/- DCs produced more IL-1β than their wild-type counterparts and promoted Th17 cell development in an IL-1-dependent manner. Finally, in vivo blockade of IL-1 receptor signaling reduced Th17 cell accumulation and inflammation in a mouse model of chemically-induced colitis.

Conclusions: Endogenous IL-10 constrains Th17 cell development through the control of IL-1 production by DCs, and reaffirms the crucial anti-inflammatory role of IL-10 in patients with chronic inflammation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Crohn Disease / complications
  • Crohn Disease / immunology*
  • Crohn Disease / pathology*
  • Dendritic Cells / immunology
  • Female
  • Humans
  • Inflammation / complications
  • Inflammation / pathology
  • Inflammation Mediators / metabolism
  • Interleukin-1 / metabolism
  • Interleukin-10 / metabolism*
  • Interleukin-17 / metabolism
  • Intestines / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Receptors, Interleukin-1 / antagonists & inhibitors
  • Receptors, Interleukin-1 / metabolism
  • Signal Transduction / immunology
  • Th17 Cells / immunology*

Substances

  • Inflammation Mediators
  • Interleukin-1
  • Interleukin-17
  • Receptors, Interleukin-1
  • Interleukin-10