Interferon-gamma induces epithelial reprogramming driving CXCL11-mediated T-cell migration

J Leukoc Biol. 2025 Feb 13;117(2):qiae205. doi: 10.1093/jleuko/qiae205.

Abstract

The cytokine interferon-gamma plays a multifaceted role in intestinal immune responses ranging from anti- to proinflammatory depending on the setting. Here, using a 3D co-culture system based on human intestinal epithelial organoids, we explore the capacity of interferon-gamma exposure to reprogram intestinal epithelia and thereby directly modulate lymphocyte responses. Interferon-gamma treatment of organoids led to transcriptional reprogramming, marked by a switch to a proinflammatory gene expression profile, including transcriptional upregulation of the chemokines CXCL9, CXCL10, and CXCL11. Proteomic analysis of organoid-conditioned medium posttreatment confirmed chemokine secretion. Interferon-gamma treatment of organoids led to enhanced T-cell migration in a CXCL11-dependent manner without affecting T-cell activation status. Taken together, our results suggest a specific role for CXCL11 in T-cell recruitment that could be targeted to prevent T-cell trafficking to the inflamed intestine.

Keywords: T lymphocytes; chemotaxis; interferon-gamma; intestinal epithelium.

MeSH terms

  • Cell Movement* / drug effects
  • Cellular Reprogramming* / drug effects
  • Chemokine CXCL11* / genetics
  • Chemokine CXCL11* / immunology
  • Chemokine CXCL11* / metabolism
  • Coculture Techniques
  • Epithelial Cells* / drug effects
  • Humans
  • Interferon-gamma* / pharmacology
  • Intestinal Mucosa* / cytology
  • Intestinal Mucosa* / drug effects
  • Intestinal Mucosa* / immunology
  • Intestinal Mucosa* / metabolism
  • Lymphocyte Activation
  • Organoids / cytology
  • Organoids / drug effects
  • Organoids / immunology
  • Organoids / metabolism
  • T-Lymphocytes* / cytology
  • T-Lymphocytes* / drug effects
  • T-Lymphocytes* / immunology

Substances

  • Interferon-gamma
  • Chemokine CXCL11
  • CXCL11 protein, human