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Am J Physiol Gastrointest Liver Physiol 285: G1028-G1036, 2003. First published July 24, 2003; doi:10.1152/ajpgi.00066.2003
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NEUROREGULATION AND MOTILITY

Human ENS regulates the intestinal epithelial barrier permeability and a tight junction-associated protein ZO-1 via VIPergic pathways

Michel Neunlist,1,* Férial Toumi,1,* Tsvetelina Oreschkova,1 Marc Denis,1 Joel Leborgne,2 Christian L. Laboisse,1,3 Jean-Paul Galmiche,1,2 and Anne Jarry1

1Institut National de la Santé et de la Recherche Médicale U539, Faculté de Médecine, 2Pôle Digestif, and 3Service d'Anatomie Pathologique, Centre Hospitalier Universitaire. Hôtel Dieu, 44035 Nantes, France

Submitted 7 February 2003 ; accepted in final form 14 July 2003

Although the enteric nervous system (ENS) has been shown to regulate various mucosal functions, its role in the physiological control of the human intestinal epithelial barrier is unknown. The aim of this study was to investigate whether the ENS is able to modulate epithelial barrier permeability and a key tight junction-associated protein, zonula occludens-1 (ZO-1). Therefore, we developed a co-culture model, consisting of human submucosa containing the submucosal neuronal network and human polarized colonic epithelial monolayers (HT29-Cl.16E or Caco-2). Submucosal neurons were activated by electrical field stimulation (EFS). Permeability was assessed by measuring the flux of paracellular permeability markers (FITC-dextran or FITC-inulin) across epithelial monolayers. Expression of ZO-1 was determined by immunofluorescence, quantitative immunoblot analysis, and real time RT-PCR. Using the coculture model, we showed that EFS of submucosal neurons resulted in a reduction in FITC-dextran or FITC-inulin fluxes, which was blocked by TTX. In HT29-Cl.16E, the effect of submucosal neuron activation was blocked by a VIP receptor antagonist (VIPra) and reproduced by VIP. Furthermore, ZO-1 expression (mRNA, protein) assessed in HT29-Cl.16E, was significantly increased after submucosal neuron activation by EFS. These effects on ZO-1 expression were blocked by TTX and VIPra and reproduced by VIP. In conclusion, our results strongly suggest a modulatory role of VIPergic submucosal neuronal pathways on intestinal epithelial barrier permeability and ZO-1 expression.

submucosal neurons; human colon; permeability; vasoactive intestinal peptide; enteric nervous system


Address for reprint requests and other correspondence: A. Jarry, Institut National de la Santé et de la Recherche Médicale U 539, Faculté de Médecine, 1, rue Gaston Veil, 44035 Nantes Cedex, France (E-mail: ajarry{at}sante.univ-nantes.fr).




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