Pharmacological blocking of neutrophil extracellular traps attenuates immunothrombosis and neuroinflammation in cerebral cavernous malformation

Nat Cardiovasc Res. 2024 Dec;3(12):1549-1567. doi: 10.1038/s44161-024-00577-y. Epub 2024 Dec 4.

Abstract

Cerebral cavernous malformation (CCM) is a neurovascular disease with symptoms such as strokes, hemorrhages and neurological deficits. With surgery being the only treatment strategy, understanding the molecular mechanisms of CCM is crucial in finding alternative therapeutic options for CCM. Neutrophil extracellular traps (NETs) were recently reported in CCM, and NETs were shown to have positive or negative effects in different disease contexts. In this study, we investigated the roles of NETs in CCM by pharmacologically inhibiting NET formation using Cl-amidine (a peptidyl arginine deiminase inhibitor). We show here that Cl-amidine treatment reduced lesion burden, coagulation and endothelial-to-mesenchymal transition. Furthermore, NETs promoted the activation of microglia and fibroblasts, leading to increased neuroinflammation and a chronic wound microenvironment in CCM. The inhibition of NET formation caused endothelial quiescence and promoted a healthier microenvironment. Our study suggests the inhibition of NETs as a potential therapeutic strategy in CCM.

MeSH terms

  • Animals
  • Cells, Cultured
  • Disease Models, Animal
  • Enzyme Inhibitors / pharmacology
  • Enzyme Inhibitors / therapeutic use
  • Epithelial-Mesenchymal Transition / drug effects
  • Extracellular Traps* / drug effects
  • Extracellular Traps* / immunology
  • Extracellular Traps* / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Fibroblasts / pathology
  • Hemangioma, Cavernous, Central Nervous System* / drug therapy
  • Hemangioma, Cavernous, Central Nervous System* / immunology
  • Hemangioma, Cavernous, Central Nervous System* / pathology
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia / drug effects
  • Microglia / immunology
  • Microglia / metabolism
  • Microglia / pathology
  • Neuroinflammatory Diseases / drug therapy
  • Neuroinflammatory Diseases / immunology
  • Neuroinflammatory Diseases / pathology
  • Neutrophils / drug effects
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Ornithine / analogs & derivatives
  • Ornithine / pharmacology
  • Ornithine / therapeutic use
  • Signal Transduction / drug effects

Substances

  • N-alpha-benzoyl-N5-(2-chloro-1-iminoethyl)-L-ornithine amide
  • Ornithine
  • Enzyme Inhibitors