Endothelial Cell-Derived Extracellular Vesicles Promote Aberrant Neutrophil Trafficking and Subsequent Remote Lung Injury

Adv Sci (Weinh). 2024 Oct;11(38):e2400647. doi: 10.1002/advs.202400647. Epub 2024 Aug 9.

Abstract

The development of acute respiratory distress syndrome (ARDS) in sepsis is associated with substantial morbidity and mortality. However, the molecular pathogenesis underlying sepsis-induced ARDS remains elusive. Neutrophil heterogeneity and dysfunction contribute to uncontrolled inflammation in patients with ARDS. A specific subset of neutrophils undergoing reverse transendothelial migration (rTEM), which is characterized by an activated phenotype, is implicated in the systemic dissemination of inflammation. Using single-cell RNA sequencing (scRNA-seq), it identified functionally activated neutrophils exhibiting the rTEM phenotype in the lung of a sepsis mouse model using cecal ligation and puncture. The prevalence of neutrophils with the rTEM phenotype is elevated in the blood of patients with sepsis-associated ARDS and is positively correlated with disease severity. Mechanically, scRNA-seq and proteomic analys revealed that inflamed endothelial cell (EC) released extracellular vesicles (EVs) enriched in karyopherin subunit beta-1 (KPNB1), promoting abluminal-to-luminal neutrophil rTEM. Additionally, EC-derived EVs are elevated and positively correlated with the proportion of rTEM neutrophils in clinical sepsis. Collectively, EC-derived EV is identified as a critical regulator of neutrophil rTEM, providing insights into the contribution of rTEM neutrophils to sepsis-associated lung injury.

Keywords: ALI/ARDS; endothelial cells; extracellular vesicles; neutrophils; sepsis.

MeSH terms

  • Animals
  • Disease Models, Animal*
  • Endothelial Cells* / metabolism
  • Extracellular Vesicles* / metabolism
  • Humans
  • Lung Injury / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neutrophils* / metabolism
  • Respiratory Distress Syndrome / metabolism
  • Sepsis* / complications
  • Sepsis* / immunology
  • Sepsis* / metabolism
  • Transendothelial and Transepithelial Migration