Nitric oxide donor-induced hyperpermeability of cultured intestinal epithelial monolayers: role of superoxide radical, hydroxyl radical, and peroxynitrite

Biochim Biophys Acta. 1998 Sep 16;1425(1):189-203. doi: 10.1016/s0304-4165(98)00072-5.

Abstract

Many of the cytopathic effects of nitric oxide (NO*) are mediated by peroxynitrite (PN), a product of the reaction between NO* and superoxide radical (O2*-). In the present study, we investigated the role of PN, O2*- and hydroxyl radical (OH*) as mediators of epithelial hyperpermeability induced by the NO* donor, S-nitroso-N-acetylpenicillamine (SNAP), and the PN generator, 3-morpholinosydnonimine (SIN-1). Caco-2BBe enterocytic monolayers were grown on permeable supports in bicameral chambers. Epithelial permeability, measured as the apical-to-basolateral flux of fluorescein disulfonic acid, increased after 24 h of incubation with 5.0 mM SNAP or SIN-1. Addition of 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide, an NO* scavenger, or Tiron, an O2*- scavenger, reduced the increase in permeability induced by both donor compounds. The SNAP-induced increase in permeability was prevented by allopurinol, an inhibitor of xanthine oxidase (a source of endogenous O2*-). Diethyldithiocarbamate, a superoxide dismutase inhibitor, and pyrogallol, an O2* generator, potentiated the increase in permeability induced by SNAP. Addition of the PN scavengers deferoxamine, urate, or glutathione, or the OH* scavenger mannitol, attenuated the increase in permeability induced by both SNAP and SIN-1. Both donor compounds decreased intracellular levels of glutathione and protein-bound sulfhydryl groups, suggesting the generation of a potent oxidant. These results support a role for PN, and possibly OH*, in the pathogenesis of NO* donor-induced intestinal epithelial hyperpermeability.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antioxidants / pharmacology
  • Caco-2 Cells
  • Epithelial Cells / drug effects
  • Epithelial Cells / physiology
  • Free Radical Scavengers / pharmacology
  • Glutathione / metabolism
  • Humans
  • Hydroxyl Radical / pharmacology
  • Intestinal Absorption / drug effects*
  • Intestinal Absorption / physiology
  • Intestines / drug effects
  • Intestines / physiology
  • Kinetics
  • Molsidomine / analogs & derivatives
  • Molsidomine / pharmacology
  • Nitrates / pharmacology
  • Nitric Oxide / physiology
  • Nitric Oxide Donors / pharmacology*
  • Penicillamine / analogs & derivatives
  • Penicillamine / pharmacology
  • Permeability / drug effects
  • Superoxide Dismutase / pharmacology
  • Superoxides / pharmacology

Substances

  • Antioxidants
  • Free Radical Scavengers
  • Nitrates
  • Nitric Oxide Donors
  • S-nitro-N-acetylpenicillamine
  • Superoxides
  • peroxynitric acid
  • Nitric Oxide
  • Hydroxyl Radical
  • linsidomine
  • Molsidomine
  • Superoxide Dismutase
  • Glutathione
  • Penicillamine