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Bifidobacteria stabilize claudins at tight junctions and prevent intestinal barrier dysfunction in mouse necrotizing enterocolitis

Am J Pathol. 2013 May;182(5):1595-606. doi: 10.1016/j.ajpath.2013.01.013. Epub 2013 Mar 5.

Abstract

Whether intestinal barrier disruption precedes or is the consequence of intestinal injury in necrotizing enterocolitis (NEC) remains unknown. Using a neonatal mouse NEC model, we examined the changes in intestinal permeability and specific tight-junction (TJ) proteins preceding NEC and asked whether these changes are prevented by administration of Bifidobacterium infantis, a probiotic known to decrease NEC incidence in humans. Compared with dam-fed controls, pups submitted to the NEC protocol developed i) significantly increased intestinal permeability at 12 and 24 hours (as assessed by 70-kDa fluorescein isothiocyanate-dextran transmucosal flux); ii) occludin and claudin 4 internalization at 12 hours (as assessed by immunofluorescence and low-density membrane fraction immunoblotting); iii) increased claudin 2 expression at 6 hours and decreased claudin 4 and 7 expression at 24 hours; and iv) increased claudin 2 protein at 48 hours. Similar results were seen in human NEC, with claudin 2 protein increased. In mice, administration of B. infantis micro-organisms attenuated increases in intestinal permeability, preserved claudin 4 and occludin localization at TJs, and decreased NEC incidence. Thus, an increase in intestinal permeability precedes NEC and is associated with internalization of claudin 4 and occludin. Administration of B. infantis prevents these changes and reduces NEC incidence. The beneficial effect of B. infantis is, at least in part, due to its TJ and barrier-preserving properties.

Publication types

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

MeSH terms

  • Animals
  • Animals, Newborn
  • Bifidobacterium / physiology*
  • Caveolin 1 / metabolism
  • Claudins / genetics
  • Claudins / metabolism*
  • Disease Models, Animal
  • Down-Regulation / genetics
  • Endocytosis
  • Enterocolitis, Necrotizing / metabolism
  • Enterocolitis, Necrotizing / microbiology
  • Enterocolitis, Necrotizing / pathology*
  • Enterocolitis, Necrotizing / physiopathology*
  • Enterocytes / metabolism
  • Enterocytes / pathology
  • Humans
  • Infant
  • Intestines / microbiology*
  • Intestines / pathology*
  • Intestines / physiopathology
  • Intestines / ultrastructure
  • Mice
  • Mice, Inbred C57BL
  • Occludin / metabolism
  • Permeability
  • Protein Transport
  • Stress, Physiological
  • Tight Junctions / metabolism*
  • Tight Junctions / ultrastructure
  • Up-Regulation / genetics

Substances

  • Caveolin 1
  • Claudins
  • Occludin