Gastric stem cells promote inflammation and gland remodeling in response to Helicobacter pylori via Rspo3-Lgr4 axis

EMBO J. 2022 Jul 4;41(13):e109996. doi: 10.15252/embj.2021109996. Epub 2022 Jun 29.

Abstract

Helicobacter pylori is a pathogen that colonizes the stomach and causes chronic gastritis. Helicobacter pylori can colonize deep inside gastric glands, triggering increased R-spondin 3 (Rspo3) signaling. This causes an expansion of the "gland base module," which consists of self-renewing stem cells and antimicrobial secretory cells and results in gland hyperplasia. The contribution of Rspo3 receptors Lgr4 and Lgr5 is not well explored. Here, we identified that Lgr4 regulates Lgr5 expression and is required for H. pylori-induced hyperplasia and inflammation, while Lgr5 alone is not. Using conditional knockout mice, we reveal that R-spondin signaling via Lgr4 drives proliferation of stem cells and also induces NF-κB activity in the proliferative stem cells. Upon exposure to H. pylori, the Lgr4-driven NF-κB activation is responsible for the expansion of the gland base module and simultaneously enables chemokine expression in stem cells, resulting in gland hyperplasia and neutrophil recruitment. This demonstrates a connection between R-spondin-Lgr and NF-κB signaling that links epithelial stem cell behavior and inflammatory responses to gland-invading H. pylori.

Keywords: Helicobacter pylori; Lgr4; Lgr5; NF-κB; R-spondin 3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Helicobacter pylori*
  • Hyperplasia / metabolism
  • Hyperplasia / pathology
  • Inflammation / pathology
  • Mice
  • NF-kappa B / metabolism
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism
  • Stem Cells / metabolism
  • Stomach

Substances

  • LGR4 protein, mouse
  • NF-kappa B
  • Receptors, G-Protein-Coupled

Associated data

  • GEO/GSE165028