Extracellular acidosis is a novel danger signal alerting innate immunity via the NLRP3 inflammasome

J Biol Chem. 2013 May 10;288(19):13410-9. doi: 10.1074/jbc.M112.426254. Epub 2013 Mar 25.

Abstract

Background: Local acidosis has been demonstrated in ischemic tissues and at inflammatory sites.

Results: Acidic extracellular pH triggers NLRP3 inflammasome activation and interleukin-1β secretion in human macrophages.

Conclusion: Acidic pH represents a novel danger signal alerting the innate immunity.

Significance: Local acidosis may promote inflammation at ischemic and inflammatory sites. Local extracellular acidification has been demonstrated at sites of ischemia and inflammation. IL-1β is one of the key proinflammatory cytokines, and thus, its synthesis and secretion are tightly regulated. The NLRP3 (nucleotide-binding domain leucine-rich repeat containing family, pyrin domain containing 3) inflammasome complex, assembled in response to microbial components or endogenous danger signals, triggers caspase-1-mediated maturation and secretion of IL-1β. In this study, we explored whether acidic environment is sensed by immune cells as an inflammasome-activating danger signal. Human macrophages were exposed to custom cell culture media at pH 7.5-6.0. Acidic medium triggered pH-dependent secretion of IL-1β and activation of caspase-1 via a mechanism involving potassium efflux from the cells. Acidic extracellular pH caused rapid intracellular acidification, and the IL-1β-inducing effect of acidic medium could be mimicked by acidifying the cytosol with bafilomycin A1, a proton pump inhibitor. Knocking down the mRNA expression of NLRP3 receptor abolished IL-1β secretion at acidic pH. Remarkably, alkaline extracellular pH strongly inhibited the IL-1β response to several known NLRP3 activators, demonstrating bipartite regulatory potential of pH on the activity of this inflammasome. The data suggest that acidic environment represents a novel endogenous danger signal alerting the innate immunity. Low pH may thus contribute to inflammation in acidosis-associated pathologies such as atherosclerosis and post-ischemic inflammatory responses.

Keywords: Acidosis; Inflammasome; Inflammation; Innate Immunity; Interleukin; Macrophages; Nod-like Receptors (NLR).

MeSH terms

  • Acidosis / immunology
  • Acidosis / metabolism*
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Caspase 1 / metabolism
  • Cell Hypoxia
  • Cells, Cultured
  • Culture Media
  • Cytokines / genetics
  • Cytokines / metabolism
  • Enzyme Activation
  • Extracellular Fluid / metabolism
  • Humans
  • Hydrogen-Ion Concentration
  • Immunity, Innate*
  • Inflammasomes / metabolism*
  • Inflammation Mediators / metabolism
  • Lipopolysaccharides / pharmacology
  • Macrolides / pharmacology
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Mice
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Potassium / metabolism
  • Proton Pump Inhibitors / pharmacology
  • Transcriptional Activation

Substances

  • Carrier Proteins
  • Culture Media
  • Cytokines
  • Inflammasomes
  • Inflammation Mediators
  • Lipopolysaccharides
  • Macrolides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Proton Pump Inhibitors
  • bafilomycin A1
  • Caspase 1
  • Potassium