Alpha-tocopherylquinone differentially modulates claudins to enhance intestinal epithelial tight junction barrier via AhR and Nrf2 pathways

Cell Rep. 2023 Jul 25;42(7):112705. doi: 10.1016/j.celrep.2023.112705. Epub 2023 Jun 30.

Abstract

Defects in intestinal epithelial tight junctions (TJs) allow paracellular permeation of noxious luminal antigens and are important pathogenic factors in inflammatory bowel disease (IBD). We show that alpha-tocopherylquinone (TQ), a quinone-structured oxidation product of vitamin E, consistently enhances the intestinal TJ barrier by increasing barrier-forming claudin-3 (CLDN3) and reducing channel-forming CLDN2 in Caco-2 cell monolayers (in vitro), mouse models (in vivo), and surgically resected human colons (ex vivo). TQ reduces colonic permeability and ameliorates colitis symptoms in multiple colitis models. TQ, bifunctionally, activates both aryl hydrocarbon receptor (AhR) and nuclear factor erythroid 2-related factor 2 (Nrf2) pathways. Genetic deletion studies reveal that TQ-induced AhR activation transcriptionally increases CLDN3 via xenobiotic response element (XRE) in the CLDN3 promoter. Conversely, TQ suppresses CLDN2 expression via Nrf2-mediated STAT3 inhibition. TQ offers a naturally occurring, non-toxic intervention for enhancement of the intestinal TJ barrier and adjunct therapeutics to treat intestinal inflammation.

Keywords: CP: Cell biology; alpha-tocopherylquinone; aryl hydrocarbon receptor; claudin-2; claudin-3; inflammatory bowel disease; intestinal permeability; tight junction.

Publication types

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

MeSH terms

  • Animals
  • Caco-2 Cells
  • Claudins* / metabolism
  • Colitis* / metabolism
  • Humans
  • Intestinal Mucosa / metabolism
  • Mice
  • NF-E2-Related Factor 2 / metabolism
  • Permeability
  • Receptors, Aryl Hydrocarbon / genetics
  • Tight Junctions / metabolism
  • Vitamin E / metabolism

Substances

  • Claudins
  • NF-E2-Related Factor 2
  • Receptors, Aryl Hydrocarbon
  • tocopherylquinone
  • Vitamin E