Modeling Epithelial Homeostasis and Perturbation in Three-Dimensional Human Esophageal Organoids

Biomolecules. 2024 Sep 5;14(9):1126. doi: 10.3390/biom14091126.

Abstract

Background: Esophageal organoids from a variety of pathologies including cancer are grown in Advanced Dulbecco's Modified Eagle Medium-Nutrient Mixture F12 (hereafter ADF). However, the currently available ADF-based formulations are suboptimal for normal human esophageal organoids, limiting the ability to compare normal esophageal organoids with those representing a given disease state. Methods: We have utilized immortalized normal human esophageal epithelial cell (keratinocyte) lines EPC1 and EPC2 and endoscopic normal esophageal biopsies to generate three-dimensional (3D) organoids. To optimize the ADF-based medium, we evaluated the requirement of exogenous epidermal growth factor (EGF) and inhibition of transforming growth factor-(TGF)-β receptor-mediated signaling, both key regulators of the proliferation of human esophageal keratinocytes. We have modeled human esophageal epithelial pathology by stimulating esophageal 3D organoids with interleukin (IL)-13, an inflammatory cytokine, or UAB30, a novel pharmacological activator of retinoic acid signaling. Results: The formation of normal human esophageal 3D organoids was limited by excessive EGF and intrinsic TGFβ-receptor-mediated signaling. Optimized HOME0 improved normal human esophageal organoid formation. In the HOME0-grown organoids, IL-13 and UAB30 induced epithelial changes reminiscent of basal cell hyperplasia, a common histopathologic feature in broad esophageal disease conditions including eosinophilic esophagitis. Conclusions: HOME0 allows modeling of the homeostatic differentiation gradient and perturbation of the human esophageal epithelium while permitting a comparison of organoids from mice and other organs grown in ADF-based media.

Keywords: basal cell hyperplasia; eosinophilic esophagitis; epidermal growth factor; esophagus; organoids; retinoic acid; transforming growth factor-β.

MeSH terms

  • Cell Line
  • Cell Proliferation / drug effects
  • Epidermal Growth Factor / metabolism
  • Epidermal Growth Factor / pharmacology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Esophagus* / drug effects
  • Esophagus* / metabolism
  • Esophagus* / pathology
  • Homeostasis*
  • Humans
  • Keratinocytes / cytology
  • Keratinocytes / drug effects
  • Keratinocytes / metabolism
  • Models, Biological
  • Organoids* / drug effects
  • Organoids* / metabolism
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction / drug effects

Substances

  • Epidermal Growth Factor
  • Receptors, Transforming Growth Factor beta