Internalized Cryptococcus neoformans Activates the Canonical Caspase-1 and the Noncanonical Caspase-8 Inflammasomes

J Immunol. 2015 Nov 15;195(10):4962-72. doi: 10.4049/jimmunol.1500865. Epub 2015 Oct 14.

Abstract

Cryptococcus neoformans is an opportunistic fungal pathogen that causes cryptococcosis in immunocompromised patients as well as immunocompetent individuals. Host cell surface receptors that recognize C. neoformans have been widely studied. However, intracellular sensing of this pathogen is still poorly understood. Our previous studies have demonstrated that both biofilm and acapsular mutant of C. neoformans are able to activate the NOD-like receptor family, pyrin domain-containing 3 (NLRP3) inflammasome. In the current study, it was found that opsonization-mediated internalization of encapsulated C. neoformans also activated the canonical NLRP3-apoptosis-associated speck-like protein containing a CARD (ASC)-caspase-1 inflammasome. In addition, the internalized C. neoformans activated the noncanonical NLRP3-ASC-caspase-8 inflammasome as well, which resulted in robust IL-1β secretion and cell death from caspase-1-deficient primary dendritic cells. Interestingly, we found that caspase-1 was inhibitory for the activation of caspase-8 in dendritic cells upon C. neorformans challenge. Further mechanistic studies showed that both phagolysosome membrane permeabilization and potassium efflux were responsible for C. neoformans-induced activation of either the canonical NLRP3-ASC-caspase-1 inflammasome or the noncanonical NLRP3-ASC-caspase-8 inflammasome. Moreover, challenge with zymosan also led to the activation of the noncanonical NLRP3-ASC-caspase-8 inflammasome in cells absent for caspase-1. Collectively, these findings uncover a number of novel signaling pathways for the innate immune response of host cells to C. neoformans infection and suggest that manipulating NLRP3 signaling may help to control fungal challenge.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology
  • Caspase 1 / genetics
  • Caspase 1 / immunology*
  • Caspase 8 / genetics
  • Caspase 8 / immunology*
  • Cell Line, Tumor
  • Cryptococcosis / genetics
  • Cryptococcosis / immunology*
  • Cryptococcosis / pathology
  • Cryptococcus neoformans / immunology*
  • Dendritic Cells / immunology
  • Dendritic Cells / pathology
  • Enzyme Activation / genetics
  • Enzyme Activation / immunology
  • Humans
  • Immunity, Innate / genetics
  • Inflammasomes / genetics
  • Inflammasomes / immunology*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology
  • Mice
  • Mice, Knockout
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Signal Transduction / genetics
  • Signal Transduction / immunology

Substances

  • Carrier Proteins
  • IL1B protein, human
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Nlrp3 protein, mouse
  • CASP8 protein, human
  • Casp8 protein, mouse
  • Caspase 8
  • Caspase 1