Neurotrophic tyrosine kinase receptor 1 is a direct transcriptional and epigenetic target of IL-13 involved in allergic inflammation

Mucosal Immunol. 2015 Jul;8(4):785-98. doi: 10.1038/mi.2014.109. Epub 2014 Nov 12.

Abstract

Although interleukin (IL)-13 and neurotrophins are functionally important for the pathogenesis of immune responses, the interaction of these pathways has not been explored. Herein, by interrogating IL-13-induced responses in human epithelial cells we show that neurotrophic tyrosine kinase receptor, type 1 (NTRK1), a cognate, high-affinity receptor for nerve growth factor (NGF), is an early transcriptional IL-13 target. Induction of NTRK1 was accompanied by accumulation of activating epigenetic marks in the promoter; transcriptional and epigenetic changes were signal transducer and activator of transcription 6 dependent. Using eosinophilic esophagitis as a model for human allergic inflammation, we found that NTRK1 was increased in inflamed tissue and dynamically expressed as a function of disease activity and that the downstream mediator of NTRK1 signaling early growth response 1 protein was elevated in allergic inflammatory tissue compared with control tissue. Unlike NTRK1, its ligand NGF was constitutively expressed in control and disease states, indicating that IL-13-stimulated NTRK1 induction is a limiting factor in pathway activation. In epithelial cells, NGF and IL-13 synergistically induced several target genes, including chemokine (C-C motif) ligand 26 (eotaxin-3). In summary, we have demonstrated that IL-13 confers epithelial cell responsiveness to NGF by regulating NTRK1 levels by a transcriptional and epigenetic mechanism and that this process likely contributes to allergic inflammation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cluster Analysis
  • Early Growth Response Protein 1 / metabolism
  • Eosinophilic Esophagitis / genetics
  • Eosinophilic Esophagitis / metabolism
  • Eosinophilic Esophagitis / pathology
  • Epigenesis, Genetic*
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation* / drug effects
  • Gene Silencing
  • Humans
  • Hypersensitivity / genetics*
  • Hypersensitivity / metabolism*
  • Interleukin-13 / metabolism*
  • Interleukin-13 / pharmacology
  • Nerve Growth Factor / pharmacology
  • Receptor, trkA / genetics*
  • STAT6 Transcription Factor / genetics
  • STAT6 Transcription Factor / metabolism
  • Transcription, Genetic*

Substances

  • Early Growth Response Protein 1
  • Interleukin-13
  • STAT6 Transcription Factor
  • Nerve Growth Factor
  • Receptor, trkA