Deficiency of claudin-18 causes paracellular H+ leakage, up-regulation of interleukin-1β, and atrophic gastritis in mice

Gastroenterology. 2012 Feb;142(2):292-304. doi: 10.1053/j.gastro.2011.10.040. Epub 2011 Nov 10.

Abstract

Background & aims: Although defects in tight junction (TJ) epithelial paracellular barrier function are believed to be a primary cause of inflammation, the mechanisms responsible remain largely unknown.

Methods: We generated knockout mice of stomach-type claudin-18, a major component of TJs in the stomach.

Results: Cldn18(-/-) mice were afflicted with atrophic gastritis that started on postnatal day 3. This coincided with a decrease in intragastric pH due to H(+) secretion from parietal cells and concomitant up-regulation of the cytokines, interleukin-1β, cyclooxygenase-2, and KC, resulting in spasmolytic polypeptide-expressing metaplasia (SPEM). Oral administration of hydrochloric acid on postnatal day 1 induced the expression of these cytokines in Cldn18(-/-) infant stomach, but not in Cldn18(+/+) mice. A paracellular H(+) leak in Cldn18(-/-) stomach was detected by electrophysiology and H(+) titration, and freeze-fracture electron microscopy showed structural defects in the TJs, in which the tightly packed claudin-18 (stomach-type)-based TJ strands were lost, leaving a loose meshwork of strands consisting of other claudin species.

Conclusions: These findings provide evidence that claudin-18 normally forms a paracellular barrier against H(+) in the stomach and that its deficiency causes paracellular H(+) leak, a persistent up-regulation of proinflammatory cytokines, chronic recruitment of neutrophils, and the subsequent development of SPEM in atrophic gastritis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chemokine CXCL1 / metabolism
  • Claudins / deficiency*
  • Claudins / genetics
  • Claudins / metabolism
  • Cyclooxygenase 2 / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Freeze Fracturing
  • Gastric Mucosa / immunology
  • Gastric Mucosa / metabolism*
  • Gastric Mucosa / pathology
  • Gastritis, Atrophic / etiology*
  • Gastritis, Atrophic / metabolism
  • Gastritis, Atrophic / pathology
  • Humans
  • Hydrogen-Ion Concentration
  • Interleukin-1beta / metabolism*
  • Metaplasia
  • Mice
  • Mice, Knockout
  • Microscopy, Electron
  • Neutrophil Infiltration
  • Parietal Cells, Gastric / metabolism
  • Tight Junctions / metabolism*
  • Tight Junctions / ultrastructure
  • Up-Regulation

Substances

  • Chemokine CXCL1
  • Claudins
  • Cldn18 protein, mouse
  • Cxcl1 protein, mouse
  • Interleukin-1beta
  • Ptgs2 protein, mouse
  • Cyclooxygenase 2