Critical role for the AIM2 inflammasome during acute CNS bacterial infection

J Neurochem. 2014 May;129(4):704-11. doi: 10.1111/jnc.12669. Epub 2014 Feb 19.

Abstract

Interleukin-1β (IL-1β) is essential for eliciting protective immunity during the acute phase of Staphylococcus aureus (S. aureus) infection in the central nervous system (CNS). We previously demonstrated that microglial IL-1β production in response to live S. aureus is mediated through the Nod-like receptor protein 3 (NLRP3) inflammasome, including the adapter protein ASC (apoptosis-associated speck-like protein containing a caspase-1 recruitment domain), and pro-caspase 1. Here, we utilized NLRP3, ASC, and caspase 1/11 knockout (KO) mice to demonstrate the functional significance of inflammasome activity during CNS S. aureus infection. ASC and caspase 1/11 KO animals were exquisitely sensitive, with approximately 50% of mice succumbing to infection within 24 h. Unexpectedly, the survival of NLRP3 KO mice was similar to wild-type animals, suggesting the involvement of an alternative upstream sensor, which was later identified as absent in melanoma 2 (AIM2) based on the similar disease patterns between AIM2 and ASC KO mice. Besides IL-1β, other key inflammatory mediators, including IL-6, CXCL1, CXCL10, and CCL2 were significantly reduced in the CNS of AIM2 and ASC KO mice, implicating autocrine/paracrine actions of IL-1β, as these mediators do not require inflammasome processing for secretion. These studies demonstrate a novel role for the AIM2 inflammasome as a critical molecular platform for regulating IL-1β release and survival during acute CNS S. aureus infection.

Keywords: AIM2; ASC; Staphylococcus aureus; caspase 1; inflammasome; interleukin-1.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins
  • Brain Abscess / immunology*
  • Brain Abscess / metabolism
  • Brain Abscess / microbiology
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins / genetics
  • Carrier Proteins / physiology
  • Caspase 1 / deficiency
  • Caspase 1 / physiology
  • Caspases / deficiency
  • Caspases / physiology
  • Caspases, Initiator
  • Cytokines / metabolism
  • Cytoskeletal Proteins / deficiency
  • Cytoskeletal Proteins / physiology
  • DNA, Bacterial / immunology
  • DNA-Binding Proteins
  • Disease Susceptibility
  • Female
  • Immunity, Innate
  • Inflammasomes / physiology*
  • Inflammation Mediators / physiology
  • Interleukin-1beta / metabolism
  • Male
  • Methicillin-Resistant Staphylococcus aureus / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microglia / metabolism
  • Models, Immunological
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nuclear Proteins / deficiency
  • Nuclear Proteins / physiology*
  • Phenotype
  • Staphylococcal Infections / immunology*
  • Staphylococcal Infections / metabolism

Substances

  • Aim2 protein, mouse
  • Apoptosis Regulatory Proteins
  • CARD Signaling Adaptor Proteins
  • Carrier Proteins
  • Cytokines
  • Cytoskeletal Proteins
  • DNA, Bacterial
  • DNA-Binding Proteins
  • Inflammasomes
  • Inflammation Mediators
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Nuclear Proteins
  • Pycard protein, mouse
  • Casp4 protein, mouse
  • Caspases
  • Caspases, Initiator
  • Caspase 1