Inflammasome activation and IL-1β/IL-18 processing are influenced by distinct pathways in microglia

J Neurochem. 2011 Nov;119(4):736-48. doi: 10.1111/j.1471-4159.2011.07481.x. Epub 2011 Oct 11.

Abstract

Microglia are important innate immune effectors against invading CNS pathogens, such as Staphylococcus aureus (S. aureus), a common etiological agent of brain abscesses typified by widespread inflammation and necrosis. The NLRP3 inflammasome is a protein complex involved in IL-1β and IL-18 processing following exposure to both pathogen- and danger-associated molecular patterns. Although previous studies from our laboratory have established that IL-1β is a major cytokine product of S. aureus-activated microglia and is pivotal for eliciting protective anti-bacterial immunity during brain abscess development, the molecular machinery responsible for cytokine release remains to be determined. Therefore, the functional role of the NLRP3 inflammasome and its adaptor protein apoptosis-associated speck-like protein (ASC) in eliciting IL-1β and IL-18 release was examined in primary microglia. Interestingly, we found that IL-1β, but not IL-18 production, was significantly attenuated in both NLRP3 and ASC knockout microglia following exposure to live S. aureus. NLRP3 inflammasome activation was partially dependent on autocrine/paracrine ATP release and α- and γ-hemolysins produced by live bacteria. A cathepsin B inhibitor attenuated IL-β release from NLRP3 and ASC knockout microglia, demonstrating the existence of alternative inflammasome-independent mechanisms for IL-1β processing. In contrast, microglial IL-18 secretion occurred independently of cathepsin B and inflammasome action. Collectively, these results demonstrate that microglial IL-1β processing is regulated by multiple pathways and diverges from mechanisms utilized for IL-18 cleavage. Understanding the molecular events that regulate IL-1β production is important for modulating this potent proinflammatory cytokine during CNS disease.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Animals, Newborn
  • Apoptosis Regulatory Proteins
  • Bacterial Proteins / pharmacology
  • Bacterial Toxins / pharmacology
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Cytoskeletal Proteins / deficiency
  • Cytoskeletal Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Drug Interactions
  • Enzyme Inhibitors / pharmacology
  • Enzyme-Linked Immunosorbent Assay / methods
  • Hemolysin Proteins / pharmacology
  • Interleukin-18 / metabolism*
  • Interleukin-1beta / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / drug effects
  • Microglia / immunology
  • Microglia / metabolism*
  • Microglia / microbiology
  • Models, Biological
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Purinergic P2 Receptor Antagonists / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Staphylococcus aureus / pathogenicity
  • Staphylococcus aureus / physiology
  • Thiazoles / pharmacology
  • Time Factors

Substances

  • AZ 11645373
  • Apoptosis Regulatory Proteins
  • Bacterial Proteins
  • Bacterial Toxins
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins
  • Cytoskeletal Proteins
  • Enzyme Inhibitors
  • Hemolysin Proteins
  • Interleukin-18
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Purinergic P2 Receptor Antagonists
  • Pycard protein, mouse
  • Thiazoles
  • gamma-hemolysin, Staphylococcus aureus
  • staphylococcal alpha-toxin
  • Adenosine Triphosphate