IL-17A-producing NKp44(-) group 3 innate lymphoid cells accumulate in Familial Adenomatous Polyposis duodenal tissue

Nat Commun. 2025 Apr 25;16(1):3873. doi: 10.1038/s41467-025-58907-y.

Abstract

Familial adenomatous polyposis (FAP) is an inherited gastrointestinal syndrome associated with duodenal adenoma formation. Even among carriers of the same genetic variant, duodenal phenotypes vary, indicating that additional factors, such as the local immune system, play a role. We observe an increase in duodenal IL-17A(+)NKp44(-) innate lymphoid type 3 cell (ILC3) in FAP, localized near the epithelium and enriched in adenomas and carcinomas. Elevated IL1B, IL23A, and DLL4 transcript levels correlate with IL-17A(+)NKp44(-)ILC3 accumulation, and in vitro studies with duodenal organoids confirmed this relationship. Bulk RNA sequencing reveals upregulated Reactive oxygen species (ROS)-inducing enzymes DUOX2 and DUOXA2 in FAP adenomas. IL-17A-stimulated FAP organoids show increased DUOX2/DUOXA2 expression, Duox2 protein, and ROS production, leading to DNA damage, suggesting a mechanism by which these immune cells promote tumorigenesis. These findings suggest IL-17A(+)NKp44(-)ILC3s may contribute to a local environment that makes the epithelium more submissive for oncogenic transformation in FAP.

MeSH terms

  • Adenomatous Polyposis Coli* / genetics
  • Adenomatous Polyposis Coli* / immunology
  • Adenomatous Polyposis Coli* / metabolism
  • Adenomatous Polyposis Coli* / pathology
  • DNA Damage
  • Dual Oxidases
  • Duodenal Neoplasms* / genetics
  • Duodenal Neoplasms* / immunology
  • Duodenal Neoplasms* / metabolism
  • Duodenal Neoplasms* / pathology
  • Duodenum* / immunology
  • Duodenum* / metabolism
  • Duodenum* / pathology
  • Female
  • Humans
  • Immunity, Innate
  • Interleukin-17* / genetics
  • Interleukin-17* / immunology
  • Interleukin-17* / metabolism
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • Interleukin-23 Subunit p19 / genetics
  • Interleukin-23 Subunit p19 / metabolism
  • Lymphocytes* / immunology
  • Lymphocytes* / metabolism
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • Organoids / metabolism
  • Reactive Oxygen Species / metabolism

Substances

  • Interleukin-17
  • Dual Oxidases
  • DUOX2 protein, human
  • Reactive Oxygen Species
  • IL17A protein, human
  • Interleukin-23 Subunit p19
  • IL23A protein, human
  • Interleukin-1beta
  • NADPH Oxidases
  • IL1B protein, human
  • Membrane Proteins