Lysophosphatidic acid enhances pulmonary epithelial barrier integrity and protects endotoxin-induced epithelial barrier disruption and lung injury

J Biol Chem. 2009 Sep 4;284(36):24123-32. doi: 10.1074/jbc.M109.007393. Epub 2009 Jul 8.

Abstract

Lysophosphatidic acid (LPA), a bioactive phospholipid, induces a wide range of cellular effects, including gene expression, cytoskeletal rearrangement, and cell survival. We have previously shown that LPA stimulates secretion of pro- and anti-inflammatory cytokines in bronchial epithelial cells. This study provides evidence that LPA enhances pulmonary epithelial barrier integrity through protein kinase C (PKC) delta- and zeta-mediated E-cadherin accumulation at cell-cell junctions. Treatment of human bronchial epithelial cells (HBEpCs) with LPA increased transepithelial electrical resistance (TER) by approximately 2.0-fold and enhanced accumulation of E-cadherin to the cell-cell junctions through Galpha(i)-coupled LPA receptors. Knockdown of E-cadherin with E-cadherin small interfering RNA or pretreatment with EGTA (0.1 mm) prior to LPA (1 microm) treatment attenuated LPA-induced increases in TER in HBEpCs. Furthermore, LPA induced tyrosine phosphorylation of focal adhesion kinase (FAK) and overexpression of the FAK inhibitor, and FAK-related non-kinase-attenuated LPA induced increases in TER and E-cadherin accumulation at cell-cell junctions. Overexpression of dominant negative protein kinase delta and zeta attenuated LPA-induced phosphorylation of FAK, accumulation of E-cadherin at cell-cell junctions, and an increase in TER. Additionally, lipopolysaccharide decreased TER and induced E-cadherin relocalization from cell-cell junctions to cytoplasm in a dose-dependent fashion, which was restored by LPA post-treatment in HBEpCs. Intratracheal post-treatment with LPA (5 microm) reduced LPS-induced neutrophil influx, protein leak, and E-cadherin shedding in bronchoalveolar lavage fluids in a murine model of acute lung injury. These data suggest a protective role of LPA in airway inflammation and remodeling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cadherins / genetics
  • Cadherins / metabolism
  • Cytokines / genetics
  • Cytokines / metabolism
  • Dose-Response Relationship, Drug
  • Epithelial Cells / metabolism*
  • Epithelial Cells / pathology
  • Focal Adhesion Kinase 1 / genetics
  • Focal Adhesion Kinase 1 / metabolism
  • Humans
  • Lipopolysaccharides / toxicity*
  • Lung Injury / chemically induced
  • Lung Injury / genetics
  • Lung Injury / metabolism*
  • Lung Injury / pathology
  • Lung Injury / prevention & control*
  • Lysophospholipids / pharmacology*
  • Mice
  • Phosphorylation / drug effects
  • Phosphorylation / genetics
  • Protein Kinase C-delta / genetics
  • Protein Kinase C-delta / metabolism
  • Protein Kinase C-epsilon / genetics
  • Protein Kinase C-epsilon / metabolism
  • Receptors, Lysophosphatidic Acid / genetics
  • Receptors, Lysophosphatidic Acid / metabolism
  • Respiratory Mucosa / metabolism*
  • Respiratory Mucosa / pathology

Substances

  • Cadherins
  • Cytokines
  • Lipopolysaccharides
  • Lysophospholipids
  • Receptors, Lysophosphatidic Acid
  • Focal Adhesion Kinase 1
  • PTK2 protein, human
  • Ptk2 protein, mouse
  • Protein Kinase C-delta
  • Protein Kinase C-epsilon
  • lysophosphatidic acid