Angiopoietin-1 protects against endotoxin-induced neonatal lung injury and alveolar simplification in mice

Pediatr Res. 2022 May;91(6):1405-1415. doi: 10.1038/s41390-021-01544-0. Epub 2021 May 12.

Abstract

Background: Sepsis in premature newborns is a risk factor for bronchopulmonary dysplasia (BPD), but underlying mechanisms of lung injury remain unclear. Aberrant expression of endothelial cell (EC) angiopoietin 2 (ANGPT2) disrupts angiopoietin 1 (ANGPT1)/TIE2-mediated endothelial quiescence, and is implicated in sepsis-induced acute respiratory distress syndrome in adults. We hypothesized that recombinant ANGPT1 will mitigate sepsis-induced ANGPT2 expression, inflammation, acute lung injury (ALI), and alveolar remodeling in the saccular lung.

Methods: Effects of recombinant ANGPT1 on lipopolysaccharide (LPS)-induced endothelial inflammation were evaluated in human pulmonary microvascular endothelial cells (HPMEC). ALI and long-term alveolar remodeling were assessed in newborn mice exposed to intraperitoneal LPS and recombinant ANGPT1 pretreatment.

Results: LPS dephosphorylated EC TIE2 in association with increased ANGPT2 in vivo and in vitro. ANGPT1 suppressed LPS and ANGPT2-induced EC inflammation in HPMEC. Neonatal mice treated with LPS had increased lung cytokine expression, neutrophilic influx, and cellular apoptosis. ANGPT1 pre-treatment suppressed LPS-induced lung Toll-like receptor signaling, inflammation, and ALI. LPS-induced acute increases in metalloproteinase 9 expression and elastic fiber breaks, as well as a long-term decrease in radial alveolar counts, were mitigated by ANGPT1.

Conclusions: In an experimental model of sepsis-induced BPD, ANGPT1 preserved endothelial quiescence, inhibited ALI, and suppressed alveolar simplification.

Impact: Key message: Angiopoietin 1 inhibits LPS-induced neonatal lung injury and alveolar remodeling. Additions to existing literature: Demonstrates dysregulation of angiopoietin-TIE2 axis is important for sepsis- induced acute lung injury and alveolar simplification in experimental BPD. Establishes recombinant Angiopoietin 1 as an anti-inflammatory therapy in BPD.

Impact: Angiopoietin 1-based interventions may represent novel therapies for mitigating sepsis-induced lung injury and BPD in premature infants.

Publication types

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

MeSH terms

  • Acute Lung Injury* / metabolism
  • Acute Lung Injury* / prevention & control
  • Angiopoietin-1 / metabolism
  • Angiopoietin-1 / pharmacology
  • Angiopoietin-2 / metabolism
  • Angiopoietin-2 / pharmacology
  • Animals
  • Bronchopulmonary Dysplasia* / metabolism
  • Bronchopulmonary Dysplasia* / prevention & control
  • Endothelial Cells / metabolism
  • Endotoxins / metabolism
  • Endotoxins / pharmacology
  • Humans
  • Infant, Newborn
  • Inflammation / metabolism
  • Lipopolysaccharides / pharmacology
  • Lung
  • Mice
  • Sepsis*

Substances

  • Angiopoietin-1
  • Angiopoietin-2
  • Endotoxins
  • Lipopolysaccharides