Distinctive colonic mucosal cytokine signature in new-onset, untreated pediatric Crohn disease

J Pediatr Gastroenterol Nutr. 2014 Nov;59(5):553-61. doi: 10.1097/MPG.0000000000000480.

Abstract

Objective: The aim of the study was to compare the colonic mucosal immune response in children with new, untreated Crohn disease (CD-New), CD in remission (CD-Remission), and unaffected children (CTRL [controls]).

Methods: We performed flow cytometry of mitogen-stimulated colonic lamina propria mononuclear cells isolated from colonic biopsies and 72-hour biopsy explant cultures, and analyzed the supernatant by an unbiased multiplex cytokine array of 45 analytes.

Results: Thirty-six children were studied (mean age 14 ± 3 years, 14 girls): 12 CD-New, 11 CD-Remission, and 13 CTRL. We found that stimulation of lamina propria mononuclear cells isolated from colonic biopsies induced comparable intracellular cytokine levels of interferon (IFN-γ), interleukin (IL)-17, and tumor necrosis factor (TNF)-α in T cells from CD-New, CD-Remission, and CTRL, suggesting that mucosal innate inflammation plays a larger role than activated T cells in CD-New. To measure factors released during the ongoing inflammatory response in CD-New, we cultured colonic biopsy explants and uncovered 13/45 factors that were significantly higher in CD-New versus CD-Remission, whereas 10 were increased in CD-New over CTRL. Ingenuity Pathway Analysis software revealed the anticipated interconnectivity of TNF-α, IL-6, and CSF-2 in CD-New of the colon. A novel subnetwork of chemokines was, however, evident, whereas IL-17a appeared as a peripheral factor. Principal component analysis and hierarchal clustering showed that CD-New and CD-Remission separated into distinct subgroups based on the 13 factors.

Conclusions: At diagnosis of inflammatory bowel disease, the colonic cytokine response contains a predominance of innate immune factors, with chemoattractants and vascular adhesion molecules playing a central role.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Cell Adhesion Molecules / metabolism
  • Chemokines / metabolism
  • Child
  • Colon / metabolism*
  • Crohn Disease / immunology*
  • Crohn Disease / metabolism
  • Cytokines / metabolism*
  • Disease Progression
  • Female
  • Humans
  • Immunity, Innate*
  • Inflammation / metabolism*
  • Interferon-gamma / metabolism
  • Interleukin-17 / metabolism
  • Interleukin-6 / metabolism
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / metabolism
  • Male
  • Principal Component Analysis
  • T-Lymphocytes / metabolism
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Cell Adhesion Molecules
  • Chemokines
  • Cytokines
  • Interleukin-17
  • Interleukin-6
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma

Supplementary concepts

  • Pediatric Crohn's disease