Increased endothelial cell-leukocyte interaction in murine schistosomiasis: possible priming of endothelial cells by the disease

PLoS One. 2011;6(8):e23547. doi: 10.1371/journal.pone.0023547. Epub 2011 Aug 10.

Abstract

Background and aims: Schistosomiasis is an intravascular parasitic disease associated with inflammation. Endothelial cells control leukocyte transmigration and vascular permeability being modulated by pro-inflammatory mediators. Recent data have shown that endothelial cells primed in vivo in the course of a disease keep the information in culture. Herein, we evaluated the impact of schistosomiasis on endothelial cell-regulated events in vivo and in vitro.

Methodology and principal findings: The experimental groups consisted of Schistosoma mansoni-infected and age-matched control mice. In vivo infection caused a marked influx of leukocytes and an increased protein leakage in the peritoneal cavity, characterizing an inflamed vascular and cellular profile. In vitro leukocyte-mesenteric endothelial cell adhesion was higher in cultured cells from infected mice as compared to controls, either in the basal condition or after treatment with the pro-inflammatory cytokine tumor necrosis factor (TNF). Nitric oxide (NO) donation reduced leukocyte adhesion to endothelial cells from control and infected groups; however, in the later group the effect was more pronounced, probably due to a reduced NO production. Inhibition of control endothelial NO synthase (eNOS) increased leukocyte adhesion to a level similar to the one observed in the infected group. Besides, the adhesion of control leukocytes to endothelial cells from infected animals is similar to the result of infected animals, confirming that schistosomiasis alters endothelial cells function. Furthermore, NO production as well as the expression of eNOS were reduced in cultured endothelial cells from infected animals. On the other hand, the expression of its repressor protein, namely caveolin-1, was similar in both control and infected groups.

Conclusion/significance: Schistosomiasis increases vascular permeability and endothelial cell-leukocyte interaction in vivo and in vitro. These effects are partially explained by a reduced eNOS expression. In addition, our data show that the disease primes endothelial cells in vivo, which keep the acquired phenotype in culture.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caveolin 1 / metabolism
  • Cell Adhesion
  • Cell Communication*
  • Cell Movement
  • Cells, Cultured
  • Endothelial Cells / enzymology
  • Endothelial Cells / pathology*
  • Leukocytes / pathology*
  • Male
  • Mesentery / pathology
  • Mice
  • Nitric Oxide / biosynthesis
  • Nitric Oxide Synthase Type III / metabolism
  • Peritoneal Cavity / pathology
  • Schistosoma mansoni / physiology
  • Schistosomiasis / enzymology
  • Schistosomiasis / pathology*

Substances

  • Caveolin 1
  • Nitric Oxide
  • Nitric Oxide Synthase Type III