Targeted endothelial gene deletion of triggering receptor expressed on myeloid cells-1 protects mice during septic shock

Cardiovasc Res. 2018 May 1;114(6):907-918. doi: 10.1093/cvr/cvy018.

Abstract

Aims: TREM-1 (Triggering Receptor Expressed on Myeloid cells-1) is an immunoreceptor expressed on neutrophils and monocytes/macrophages whose role is to amplify the inflammatory response driven by Toll-Like Receptors engagement. The pharmacological inhibition of TREM-1 confers protection in several pre-clinical models of acute inflammation. In this study, we aimed to decipher the role of TREM-1 on the endothelium.

Methods and results: We first showed by qRT-PCR, flow cytometry and confocal microscopy that TREM-1 was expressed in human pulmonary microvascular endothelial cells as well as in mouse vasculature (aorta, mesenteric artery, and pulmonary vessels). TREM-1 expression was upregulated following septic insult. We next observed that TREM-1 engagement impaired mouse vascular reactivity and promoted vascular inflammation. The pharmacological inhibition of TREM-1 (using the synthetic inhibitory peptide LR12) prevented these disorders both in vitro and in vivo. We generated endothelium-conditional Trem-1 ko mice (EndoTREM-1-/-) and submitted them to a caecal ligation and puncture-induced septic shock. As compared with wild-type littermates, targeted endothelial Trem-1 deletion conferred protection during septic shock in modulating inflammatory cells mobilization and activation, in restoring vasoreactivity, and in improving the survival.

Conclusion: We reported that TREM-1 is expressed and inducible in endothelial cells and plays a direct role in vascular inflammation and dysfunction. The targeted deletion of endothelial Trem-1 conferred protection during septic shock in modulating inflammatory cells mobilization and activation, restoring vasoreactivity, and improving survival. The effect of TREM-1 on vascular tone, while impressive, deserves further investigations including the design of endothelium-specific TREM-1 inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Endothelial Cells / microbiology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Endothelium, Vascular / microbiology
  • Endothelium, Vascular / physiopathology
  • Endotoxins / pharmacology
  • Humans
  • Inflammation Mediators / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Monocytes / metabolism
  • Neutrophil Infiltration
  • Neutrophils / metabolism
  • Oligopeptides / pharmacology
  • Sepsis / metabolism
  • Sepsis / microbiology
  • Sepsis / physiopathology
  • Sepsis / prevention & control*
  • Signal Transduction
  • Triggering Receptor Expressed on Myeloid Cells-1 / antagonists & inhibitors
  • Triggering Receptor Expressed on Myeloid Cells-1 / deficiency*
  • Triggering Receptor Expressed on Myeloid Cells-1 / genetics
  • Triggering Receptor Expressed on Myeloid Cells-1 / metabolism
  • Vasoconstriction
  • Vasodilation

Substances

  • Endotoxins
  • Inflammation Mediators
  • Oligopeptides
  • TREM1 protein, human
  • TREM1 protein, mouse
  • Triggering Receptor Expressed on Myeloid Cells-1
  • endotoxin, Escherichia coli