IL-33 controls IL-22-dependent antibacterial defense by modulating the microbiota

Proc Natl Acad Sci U S A. 2024 May 28;121(22):e2310864121. doi: 10.1073/pnas.2310864121. Epub 2024 May 23.

Abstract

IL-22 plays a critical role in defending against mucosal infections, but how IL-22 production is regulated is incompletely understood. Here, we show that mice lacking IL-33 or its receptor ST2 (IL-1RL1) were more resistant to Streptococcus pneumoniae lung infection than wild-type animals and that single-nucleotide polymorphisms in IL33 and IL1RL1 were associated with pneumococcal pneumonia in humans. The effect of IL-33 on S. pneumoniae infection was mediated by negative regulation of IL-22 production in innate lymphoid cells (ILCs) but independent of ILC2s as well as IL-4 and IL-13 signaling. Moreover, IL-33's influence on IL-22-dependent antibacterial defense was dependent on housing conditions of the mice and mediated by IL-33's modulatory effect on the gut microbiota. Collectively, we provide insight into the bidirectional crosstalk between the innate immune system and the microbiota. We conclude that both genetic and environmental factors influence the gut microbiota, thereby impacting the efficacy of antibacterial immune defense and susceptibility to pneumonia.

Keywords: IL-22; IL-33; Streptococcus pneumoniae; microbiota; pneumonia.

MeSH terms

  • Animals
  • Gastrointestinal Microbiome / immunology
  • Humans
  • Immunity, Innate*
  • Interleukin-1 Receptor-Like 1 Protein* / genetics
  • Interleukin-1 Receptor-Like 1 Protein* / immunology
  • Interleukin-1 Receptor-Like 1 Protein* / metabolism
  • Interleukin-22*
  • Interleukin-33* / genetics
  • Interleukin-33* / immunology
  • Interleukin-33* / metabolism
  • Interleukins* / genetics
  • Interleukins* / immunology
  • Interleukins* / metabolism
  • Lymphocytes / immunology
  • Lymphocytes / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microbiota / immunology
  • Pneumonia, Pneumococcal / immunology
  • Pneumonia, Pneumococcal / microbiology
  • Polymorphism, Single Nucleotide
  • Streptococcus pneumoniae* / immunology

Substances

  • Interleukin-33
  • Interleukins
  • Interleukin-22
  • Interleukin-1 Receptor-Like 1 Protein
  • Il33 protein, mouse
  • Il1rl1 protein, mouse