Outer membrane vesicles derived from Escherichia coli up-regulate expression of endothelial cell adhesion molecules in vitro and in vivo

PLoS One. 2013;8(3):e59276. doi: 10.1371/journal.pone.0059276. Epub 2013 Mar 14.

Abstract

Escherichia coli, as one of the gut microbiota, can evoke severe inflammatory diseases including peritonitis and sepsis. Gram-negative bacteria including E. coli constitutively release nano-sized outer membrane vesicles (OMVs). Although E. coli OMVs can induce the inflammatory responses without live bacteria, the effect of E. coli OMVs in vivo on endothelial cell function has not been previously elucidated. In this study, we show that bacteria-free OMVs increased the expression of endothelial intercellular adhesion molecule-1 (ICAM-1), E-selectin and vascular cell adhesion molecule-1, and enhanced the leukocyte binding on human microvascular endothelial cells in vitro. Inhibition of NF-κB and TLR4 reduced the expression of cell adhesion molecules in vitro. OMVs given intraperitoneally to the mice induced ICAM-1 expression and neutrophil sequestration in the lung endothelium, and the effects were reduced in ICAM-1(-/-) and TLR4(-/-) mice. When compared to free lipopolysaccharide, OMVs were more potent in inducing both ICAM-1 expression as well as leukocyte adhesion in vitro, and ICAM-1 expression and neutrophil sequestration in the lungs in vivo. This study shows that OMVs potently up-regulate functional cell adhesion molecules via NF-κB- and TLR4-dependent pathways, and that OMVs are more potent than free lipopolysaccharide.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • E-Selectin / genetics
  • E-Selectin / metabolism
  • Escherichia coli / drug effects
  • Escherichia coli / metabolism*
  • Intercellular Adhesion Molecule-1 / genetics
  • Intercellular Adhesion Molecule-1 / metabolism*
  • Lipopolysaccharides / pharmacology
  • Mice
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Neutrophils / drug effects
  • Neutrophils / metabolism
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / metabolism
  • Vascular Cell Adhesion Molecule-1 / genetics
  • Vascular Cell Adhesion Molecule-1 / metabolism

Substances

  • E-Selectin
  • Lipopolysaccharides
  • NF-kappa B
  • Toll-Like Receptor 4
  • Vascular Cell Adhesion Molecule-1
  • Intercellular Adhesion Molecule-1

Grants and funding

This work was supported by a grant from the Korean Ministry of Education, Science and Technology, FPR08B1-240 of the 21C Frontier Functional Proteomics Program, and by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MEST) (No.20120005634). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.