Fibrostenotic eosinophilic esophagitis might reflect epithelial lysyl oxidase induction by fibroblast-derived TNF-α

J Allergy Clin Immunol. 2019 Jul;144(1):171-182. doi: 10.1016/j.jaci.2018.10.067. Epub 2018 Dec 20.

Abstract

Background: Fibrosis and stricture are major comorbidities in patients with eosinophilic esophagitis (EoE). Lysyl oxidase (LOX), a collagen cross-linking enzyme, has not been investigated in the context of EoE.

Objective: We investigated regulation of epithelial LOX expression as a novel biomarker and functional effector of fibrostenotic disease conditions associated with EoE.

Methods: LOX expression was analyzed by using RNA-sequencing, PCR assays, and immunostaining in patients with EoE; cytokine-stimulated esophageal 3-dimensional organoids; and fibroblast-epithelial cell coculture, the latter coupled with fluorescence-activated cell sorting.

Results: Gene ontology and pathway analyses linked TNF-α and LOX expression in patients with EoE, which was validated in independent sets of patients with fibrostenotic conditions. TNF-α-mediated epithelial LOX upregulation was recapitulated in 3-dimensional organoids and coculture experiments. We find that fibroblast-derived TNF-α stimulates epithelial LOX expression through activation of nuclear factor κB and TGF-β-mediated signaling. In patients receiver operating characteristic analyses suggested that LOX upregulation indicates disease complications and fibrostenotic conditions in patients with EoE.

Conclusions: There is a novel positive feedback mechanism in epithelial LOX induction through fibroblast-derived TNF-α secretion. Esophageal epithelial LOX might have a role in the development of fibrosis with substantial translational implications.

Keywords: Eosinophilic esophagitis; TGF-β; TNF-α; coculture; fibrosis; lysyl oxidase.

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Biomarkers / metabolism*
  • Cells, Cultured
  • Child
  • Child, Preschool
  • Coculture Techniques
  • Constriction, Pathologic
  • Eosinophilic Esophagitis / diagnosis
  • Eosinophilic Esophagitis / genetics*
  • Epithelial Cells / physiology*
  • Esophagus / pathology*
  • Female
  • Fibroblasts / physiology*
  • Fibrosis
  • Gene Ontology
  • Humans
  • Infant
  • Male
  • Middle Aged
  • Protein-Lysine 6-Oxidase / genetics*
  • Protein-Lysine 6-Oxidase / metabolism
  • Tumor Necrosis Factor-alpha / metabolism*
  • Up-Regulation
  • Young Adult

Substances

  • Biomarkers
  • Tumor Necrosis Factor-alpha
  • LOX protein, human
  • Protein-Lysine 6-Oxidase