Endothelial-to-mesenchymal transition in lipopolysaccharide-induced acute lung injury drives a progenitor cell-like phenotype

Am J Physiol Lung Cell Mol Physiol. 2016 Jun 1;310(11):L1185-98. doi: 10.1152/ajplung.00074.2016. Epub 2016 Apr 22.

Abstract

Pulmonary vascular endothelial function may be impaired by oxidative stress in endotoxemia-derived acute lung injury. Growing evidence suggests that endothelial-to-mesenchymal transition (EndMT) could play a pivotal role in various respiratory diseases; however, it remains unclear whether EndMT participates in the injury/repair process of septic acute lung injury. Here, we analyzed lipopolysaccharide (LPS)-treated mice whose total number of pulmonary vascular endothelial cells (PVECs) transiently decreased after production of reactive oxygen species (ROS), while the population of EndMT-PVECs significantly increased. NAD(P)H oxidase inhibition suppressed EndMT of PVECs. Most EndMT-PVECs derived from tissue-resident cells, not from bone marrow, as assessed by mice with chimeric bone marrow. Bromodeoxyuridine-incorporation assays revealed higher proliferation of capillary EndMT-PVECs. In addition, EndMT-PVECs strongly expressed c-kit and CD133. LPS loading to human lung microvascular endothelial cells (HMVEC-Ls) induced reversible EndMT, as evidenced by phenotypic recovery observed after removal of LPS. LPS-induced EndMT-HMVEC-Ls had increased vasculogenic ability, aldehyde dehydrogenase activity, and expression of drug resistance genes, which are also fundamental properties of progenitor cells. Taken together, our results demonstrate that LPS induces EndMT of tissue-resident PVECs during the early phase of acute lung injury, partly mediated by ROS, contributing to increased proliferation of PVECs.

Keywords: acute lung injury; cell transformation; endothelial-to-mesenchymal transition; progenitor cells; reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Lung Injury / immunology*
  • Acute Lung Injury / pathology
  • Animals
  • Apoptosis
  • Cell Proliferation
  • Cell Transdifferentiation
  • Cells, Cultured
  • Endothelial Progenitor Cells / immunology
  • Endothelial Progenitor Cells / physiology*
  • Endothelium, Vascular / immunology
  • Endothelium, Vascular / pathology
  • Female
  • Gene Expression
  • Lipopolysaccharides / pharmacology*
  • Mice, Inbred C57BL
  • NADPH Oxidases / metabolism
  • Phenotype
  • Reactive Oxygen Species / metabolism
  • Transforming Growth Factor beta1 / biosynthesis
  • Transforming Growth Factor beta1 / genetics
  • Transforming Growth Factor beta2 / biosynthesis
  • Transforming Growth Factor beta2 / genetics

Substances

  • Lipopolysaccharides
  • Reactive Oxygen Species
  • Transforming Growth Factor beta1
  • Transforming Growth Factor beta2
  • NADPH Oxidases