Microglial NLRP3-gasdermin D activation impairs blood-brain barrier integrity through interleukin-1β-independent neutrophil chemotaxis upon peripheral inflammation in mice

Nat Commun. 2025 Jan 15;16(1):699. doi: 10.1038/s41467-025-56097-1.

Abstract

Blood-brain barrier (BBB) disintegration is a key contributor to neuroinflammation; however, the biological processes governing BBB permeability under physiological conditions remain unclear. Here, we investigate the role of NLRP3 inflammasome in BBB disruption following peripheral inflammatory challenges. Repeated intraperitoneal lipopolysaccharide administration causes NLRP3-dependent BBB permeabilization and myeloid cell infiltration into the brain. Using a mouse model with cell-specific hyperactivation of NLRP3, we identify microglial NLRP3 activation as essential for peripheral inflammation-induced BBB disruption. Conversely, NLRP3 and microglial gasdermin D (GSDMD) deficiency markedly attenuates lipopolysaccharide-induced BBB breakdown. Notably, IL-1β is not required for NLRP3-GSDMD-mediated BBB disruption. Instead, microglial NLRP3-GSDMD axis upregulates CXCL chemokines and matrix metalloproteinases around BBB via producing GDF-15, promoting the recruitment of CXCR2-containing neutrophils. Inhibition of neutrophil infiltration and matrix metalloproteinase activity significantly reduces NLRP3-mediated BBB impairment. Collectively, these findings reveal the important role of NLRP3-driven chemokine production in BBB disintegration, suggesting potential therapeutic targets to mitigate neuroinflammation.

MeSH terms

  • Animals
  • Blood-Brain Barrier* / drug effects
  • Blood-Brain Barrier* / metabolism
  • Gasdermins
  • Inflammasomes / metabolism
  • Inflammation* / metabolism
  • Inflammation* / pathology
  • Interleukin-1beta* / metabolism
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Lipopolysaccharides*
  • Male
  • Matrix Metalloproteinases / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia* / drug effects
  • Microglia* / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism
  • Neuroinflammatory Diseases / immunology
  • Neuroinflammatory Diseases / metabolism
  • Neutrophil Infiltration / drug effects
  • Neutrophils* / immunology
  • Neutrophils* / metabolism
  • Phosphate-Binding Proteins* / metabolism
  • Receptors, Interleukin-8B / metabolism

Substances

  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Interleukin-1beta
  • Nlrp3 protein, mouse
  • Gsdmd protein, mouse
  • Phosphate-Binding Proteins
  • Lipopolysaccharides
  • Intracellular Signaling Peptides and Proteins
  • Inflammasomes
  • Matrix Metalloproteinases
  • IL1B protein, mouse
  • Receptors, Interleukin-8B
  • Gasdermins