Loss of interleukin-10 or transforming growth factor β signaling in the human colon initiates a T-helper 1 response via distinct pathways

Gastroenterology. 2011 Nov;141(5):1887-96.e1-2. doi: 10.1053/j.gastro.2011.08.002. Epub 2011 Aug 10.

Abstract

Background & aims: Signaling via interleukin (IL)-10 or transforming growth factor (TGF)-β is disrupted in subpopulations of patients with inflammatory bowel disease, but it is not clear how a T-helper (Th) 1 cell response is induced. We studied conversion of human mucosal innate immune cells into inflammatory cells and the initiation of a Th1 cell response following loss of IL-10 or TGF-β signaling.

Methods: We depleted IL-10 or TGF-β from explant cultures of human normal colonic mucosa using immunoneutralization. Pharmacologic inhibitors and antibodies were used to determine the factors involved in the initiation of an interferon (IFN)-γ response following loss of TGF-β or IL-10 signaling. Cytokines produced by mucosal cells were assessed by enzyme-linked immunosorbent assay and quantitative reverse-transcriptase polymerase chain reaction. The subsets of cells involved in cytokine production were determined by in situ immunofluorescence analysis and flow cytometry after digestion of the explants with collagenase.

Results: Depletion of IL-10 from human normal colonic mucosa resulted in an IFN-γ response, characterized by early-stage secretion of mature IL-18 and production of the active form of caspase-1 by macrophages and some epithelial cells. A caspase-1 inhibitor or the IL-18 antagonist IL-18-binding protein blocked this response. By contrast, depletion of TGF-β resulted in an IFN-γ response that was preceded by and required secretion of IL-12 from macrophages, dendritic cells, and epithelial cells.

Conclusions: Innate immune cells (macrophages and epithelial cells) activate a Th1 cell response in explant cultures of human normal colonic mucosa depleted in IL-10 or TGF-β via distinct, nonredundant pathways. These pathways might contribute to the pathogenesis of inflammatory bowel disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Caspase 1 / metabolism
  • Cells, Cultured
  • Colon / metabolism
  • Colon / pathology*
  • Female
  • Humans
  • Immunity, Innate / physiology
  • Inflammatory Bowel Diseases / etiology
  • Inflammatory Bowel Diseases / metabolism
  • Interferon-gamma / metabolism
  • Interleukin-10 / deficiency*
  • Interleukin-10 / metabolism
  • Interleukin-12 / metabolism
  • Interleukin-18 / metabolism
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / pathology
  • Male
  • Middle Aged
  • Signal Transduction / physiology*
  • Th1 Cells / metabolism
  • Th1 Cells / pathology*
  • Transforming Growth Factor beta / deficiency*
  • Transforming Growth Factor beta / metabolism

Substances

  • Interleukin-18
  • Transforming Growth Factor beta
  • Interleukin-10
  • Interleukin-12
  • Interferon-gamma
  • Caspase 1