Impaired cAMP and Rac 1 signaling contribute to TNF-alpha-induced endothelial barrier breakdown in microvascular endothelium

Microcirculation. 2009 Aug;16(6):521-33. doi: 10.1080/10739680902967427. Epub 2009 Jun 4.

Abstract

Objective: In sepsis, tumor necrosis factor-alpha (TNF-alpha) contributes to endothelial barrier breakdown. The involvement of Rho A/rho kinase signaling has recently been challenged. Here, we tested the role of cAMP and Rac 1 signaling.

Materials and methods: For this study, we took in vivo measurements of hydraulic conductivity in postcapillary mesenteric venules of adult rats. Measurements of transendothelial electrical resistence (TER), fluorescein isothiocyanate-dextran flux, Western blotting, immunostaining, and enzyme-linked immunosorbent assay-based measurements of cAMP levels and Rho-GTPase activity in human microvascular endothelial cells.

Results: TNF-alpha disrupted endothelial barrier functions in vivo and in vitro. Under these conditions, Rho A activity was significantly increased, whereas Rac 1 activity was decreased and Cdc42 was unaltered. Moreover, cAMP levels were reduced. Rho kinase inhibition, using Y27632, did not prevent TNF-alpha-induced barrier breakdown. In contrast, preincubation with forskolin and rolipram (F/R) to increase cAMP and cytotoxic necrotizing factor 1 to activate Rac 1 and Rho A abolished TNF-alpha-induced barrier breakdown in vivo and in vitro. Moreover, inactivation of Rac 1 was blocked by F/R-mediated increase of cAMP, whereas Rho A activation was only partially inhibited.

Conclusion: Our data indicate that decrease of cAMP and Rac 1 inactivation, rather than Rho A activation, contribute to TNF-alpha-induced endothelial barrier breakdown in vivo and in vitro.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amides / pharmacology
  • Animals
  • Cells, Cultured
  • Cyclic AMP / metabolism*
  • Endothelium / drug effects
  • Endothelium / metabolism
  • Female
  • Humans
  • In Vitro Techniques
  • Intercellular Junctions / drug effects
  • Intercellular Junctions / metabolism
  • Lymphotoxin-alpha
  • Male
  • Microcirculation / drug effects*
  • Microcirculation / physiology*
  • Neuropeptides / antagonists & inhibitors
  • Neuropeptides / metabolism*
  • Protein Kinase Inhibitors / pharmacology
  • Pyridines / pharmacology
  • Rats
  • Rats, Wistar
  • Recombinant Proteins / pharmacology
  • Signal Transduction / drug effects
  • Venules / drug effects
  • Venules / metabolism
  • rac GTP-Binding Proteins / antagonists & inhibitors
  • rac GTP-Binding Proteins / metabolism*
  • rac1 GTP-Binding Protein
  • rho GTP-Binding Proteins / metabolism
  • rho-Associated Kinases / antagonists & inhibitors
  • rho-Associated Kinases / metabolism
  • rhoA GTP-Binding Protein

Substances

  • Amides
  • Lymphotoxin-alpha
  • Neuropeptides
  • Protein Kinase Inhibitors
  • Pyridines
  • Rac1 protein, mouse
  • Recombinant Proteins
  • Y 27632
  • Cyclic AMP
  • rho-Associated Kinases
  • RhoA protein, mouse
  • rac GTP-Binding Proteins
  • rac1 GTP-Binding Protein
  • rho GTP-Binding Proteins
  • rhoA GTP-Binding Protein