Angiopoietin-like 4 protects against endothelial dysfunction during bacterial sepsis

Nat Microbiol. 2024 Sep;9(9):2434-2447. doi: 10.1038/s41564-024-01760-4. Epub 2024 Aug 5.

Abstract

Loss of endothelial integrity and vascular leakage are central features of sepsis pathogenesis; however, no effective therapeutic mechanisms for preserving endothelial integrity are available. Here we show that, compared to dermal microvessels, brain microvessels resist infection by Neisseria meningitidis, a bacterial pathogen that causes sepsis and meningitis. By comparing the transcriptional responses to infection in dermal and brain endothelial cells, we identified angiopoietin-like 4 as a key factor produced by the brain endothelium that preserves blood-brain barrier integrity during bacterial sepsis. Conversely, angiopoietin-like 4 is produced at lower levels in the peripheral endothelium. Treatment with recombinant angiopoietin-like 4 reduced vascular leakage, organ failure and death in mouse models of lethal sepsis and N. meningitidis infection. Protection was conferred by a previously uncharacterized domain of angiopoietin-like 4, through binding to the heparan proteoglycan, syndecan-4. These findings reveal a potential strategy to prevent endothelial dysfunction and improve outcomes in patients with sepsis.

MeSH terms

  • Angiopoietin-Like Protein 4 / genetics
  • Angiopoietin-Like Protein 4 / metabolism
  • Animals
  • Blood-Brain Barrier / metabolism
  • Brain / metabolism
  • Brain / microbiology
  • Brain / pathology
  • Disease Models, Animal*
  • Endothelial Cells* / metabolism
  • Endothelial Cells* / microbiology
  • Endothelium, Vascular / metabolism
  • Endothelium, Vascular / microbiology
  • Humans
  • Meningococcal Infections / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Neisseria meningitidis / genetics
  • Neisseria meningitidis / metabolism
  • Sepsis* / microbiology

Substances

  • Angiopoietin-Like Protein 4