Differential role of Rho GTPases in intestinal epithelial barrier regulation in vitro

J Cell Physiol. 2011 May;226(5):1196-203. doi: 10.1002/jcp.22446.

Abstract

Maintenance of intestinal epithelial barrier functions is crucial to prevent systemic contamination by microbes that penetrate from the gut lumen. GTPases of the Rho-family such as RhoA, Rac1, and Cdc42 are known to be critically involved in the regulation of intestinal epithelial barrier functions. However, it is still unclear whether inactivation or activation of these GTPases exerts barrier protection or not. We tested the effects of Rho GTPase activities on intestinal epithelial barrier functions by using the bacterial toxins cytotoxic necrotizing factor 1 (CNF-1), toxin B, C3 transferase (C3 TF), and lethal toxin (LT) in an in vitro model of the intestinal epithelial barrier. Incubation of cell monolayers with CNF-1 for 3 h induced exclusive activation of RhoA whereas Rac1 and Cdc42 activities were unchanged. As revealed by FITC-dextran flux and measurements of transepithelial electrical resistance (TER) intestinal epithelial permeability was significantly increased under these conditions. Inhibition of Rho kinase via Y27632 blocked barrier destabilization of CNF-1 after 3 h. In contrast, after 24 h of incubation with CNF-1 only Rac1 and Cdc42 but not RhoA were activated which resulted in intestinal epithelial barrier stabilization. Toxin B to inactivate RhoA, Rac1, and Cdc42 as well as Rac1 inhibitor LT increased intestinal epithelial permeability. Similar effects were observed after inhibition of RhoA/Rho kinase signaling by C3 TF or Y27632. Taken together, these data demonstrate that both activation and inactivation of RhoA signaling increased paracellular permeability whereas activation of Rac1 and Cdc42 correlated with stabilized barrier functions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP Ribose Transferases / pharmacology
  • Amides / pharmacology
  • Bacterial Proteins / pharmacology
  • Bacterial Toxins / pharmacology
  • Botulinum Toxins / pharmacology
  • Caco-2 Cells
  • Dextrans / metabolism
  • Dose-Response Relationship, Drug
  • Electric Impedance
  • Enzyme Activation
  • Escherichia coli Proteins / pharmacology
  • Fluorescein-5-isothiocyanate / analogs & derivatives
  • Fluorescein-5-isothiocyanate / metabolism
  • Humans
  • Intercellular Junctions / drug effects
  • Intercellular Junctions / enzymology
  • Intestinal Mucosa / drug effects
  • Intestinal Mucosa / enzymology*
  • Permeability
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines / pharmacology
  • Time Factors
  • cdc42 GTP-Binding Protein / metabolism
  • rac1 GTP-Binding Protein / metabolism
  • rho GTP-Binding Proteins / metabolism*
  • rho-Associated Kinases / antagonists & inhibitors
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein / metabolism

Substances

  • Amides
  • Bacterial Proteins
  • Bacterial Toxins
  • Dextrans
  • Escherichia coli Proteins
  • Protein Kinase Inhibitors
  • Pyridines
  • RAC1 protein, human
  • fluorescein isothiocyanate dextran
  • lethal toxin LT, Clostridium sordellii
  • toxB protein, Clostridium difficile
  • cytotoxic necrotizing factor type 1
  • RHOA protein, human
  • Y 27632
  • ADP Ribose Transferases
  • exoenzyme C3, Clostridium botulinum
  • rho-Associated Kinases
  • Botulinum Toxins
  • cdc42 GTP-Binding Protein
  • rac1 GTP-Binding Protein
  • rho GTP-Binding Proteins
  • rhoA GTP-Binding Protein
  • Fluorescein-5-isothiocyanate