A multicomponent toxin from Bacillus cereus incites inflammation and shapes host outcome via the NLRP3 inflammasome

Nat Microbiol. 2019 Feb;4(2):362-374. doi: 10.1038/s41564-018-0318-0. Epub 2018 Dec 10.

Abstract

Host recognition of microbial components is essential in mediating an effective immune response. Cytosolic bacteria must secure entry into the host cytoplasm to facilitate replication and, in doing so, liberate microbial ligands that activate cytosolic innate immune sensors and the inflammasome. Here, we identified a multicomponent enterotoxin, haemolysin BL (HBL), that engages activation of the inflammasome. This toxin is highly conserved among the human pathogen Bacillus cereus. The three subunits of HBL bind to the cell membrane in a linear order, forming a lytic pore and inducing activation of the NLRP3 inflammasome, secretion of interleukin-1β and interleukin-18, and pyroptosis. Mechanistically, the HBL-induced pore results in the efflux of potassium and triggers the activation of the NLRP3 inflammasome. Furthermore, HBL-producing B. cereus induces rapid inflammasome-mediated mortality. Pharmacological inhibition of the NLRP3 inflammasome using MCC950 prevents B. cereus-induced lethality. Overall, our results reveal that cytosolic sensing of a toxin is central to the innate immune recognition of infection. Therapeutic modulation of this pathway enhances host protection against deadly bacterial infections.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacillus cereus / immunology*
  • Bacterial Proteins / immunology*
  • Bacterial Proteins / metabolism
  • Cell Membrane / metabolism
  • Cell Membrane / pathology
  • Cells, Cultured
  • Culture Media, Conditioned
  • Enterotoxins / chemistry
  • Enterotoxins / immunology*
  • Enterotoxins / metabolism
  • Female
  • Hemolysin Proteins / immunology*
  • Hemolysin Proteins / metabolism
  • Immunity, Innate
  • Inflammasomes / metabolism*
  • Inflammation*
  • Macrophages / immunology
  • Macrophages / pathology
  • Macrophages / ultrastructure
  • Male
  • Mice
  • Mice, Mutant Strains
  • NLR Family, Pyrin Domain-Containing 3 Protein / antagonists & inhibitors
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Potassium / metabolism
  • Protein Multimerization
  • Pyroptosis
  • Survival Analysis

Substances

  • Bacterial Proteins
  • Culture Media, Conditioned
  • Enterotoxins
  • Hemolysin Proteins
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • hemolysin BL protein, Bacillus
  • Potassium