Mechanical induction of group V phospholipase A(2) causes lung inflammation and acute lung injury

Am J Physiol Lung Cell Mol Physiol. 2013 May 15;304(10):L689-700. doi: 10.1152/ajplung.00047.2013. Epub 2013 Mar 22.

Abstract

Ventilation at high tidal volume may cause lung inflammation and barrier dysfunction that culminates in ventilator-induced lung injury (VILI). However, the mechanisms by which mechanical stimulation triggers the inflammatory response have not been fully elucidated. This study tested the hypothesis that onset of VILI is triggered by activation of secretory group V phospholipase A(2) (gVPLA2) in pulmonary vascular endothelium exposed to excessive mechanical stretch. High-magnitude cyclic stretch (18% CS) increased expression and surface exposure of gVPLA2 in human pulmonary endothelial cells (EC). CS-induced gVPLA2 activation was required for activation of ICAM-1 expression and polymorphonuclear neutrophil (PMN) adhesion to CS-preconditioned EC. By contrast, physiological CS (5% CS) had no effect on gVPLA2 activation or EC-PMN adhesion. CS-induced ICAM-1 expression and EC-PMN adhesion were attenuated by the gVPLA2-blocking antibody (MCL-3G1), general inhibitor of soluble PLA2, LY311727, or siRNA-induced EC gVPLA2 knockdown. In vivo, ventilator-induced lung leukocyte recruitment, cell and protein accumulation in the alveolar space, and total lung myeloperoxidase activity were strongly suppressed in gVPLA2 mouse knockout model or upon administration of MCL-3G1. These results demonstrate a novel role for gVPLA2 as the downstream effector of pathological mechanical stretch leading to an inflammatory response associated with VILI.

Keywords: acute lung injury; cyclic stretch; endothelial cells; group V soluble phospholipase A2 inflammation; neutrophil adhesion.

Publication types

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

MeSH terms

  • Acute Lung Injury / enzymology*
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Animals
  • Cells, Cultured
  • Endothelial Cells / enzymology
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Endothelium, Vascular / enzymology
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / pathology
  • Enzyme Induction
  • Humans
  • Intercellular Adhesion Molecule-1 / metabolism
  • Leukocytes / enzymology
  • Leukocytes / metabolism
  • Leukocytes / pathology
  • Lung / enzymology
  • Lung / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neutrophils / enzymology
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Phospholipases A2 / biosynthesis*
  • Pneumonia / enzymology*
  • Pneumonia / metabolism
  • Pneumonia / pathology
  • Stress, Mechanical
  • Tidal Volume / physiology
  • Ventilator-Induced Lung Injury / enzymology
  • Ventilator-Induced Lung Injury / metabolism
  • Ventilator-Induced Lung Injury / pathology

Substances

  • Intercellular Adhesion Molecule-1
  • Phospholipases A2