Butyrate-induced IL-22 expression in fish macrophages contributes to bacterial clearance

Fish Shellfish Immunol. 2023 Feb:133:108545. doi: 10.1016/j.fsi.2023.108545. Epub 2023 Jan 13.

Abstract

IL-22 has been characterized as a critical cytokine in maintaining barrier integrity and host immunity. So far, it has been known that IL-22 is mainly produced by lymphoid lineage cells. In the present study, we have thoroughly investigated butyrate-induced production and function of IL-22 in fish macrophages. Our results demonstrated that short-chain fatty acids (SCFAs), major microbiota-derived metabolites, promoted the expression of IL-22 in head kidney macrophages (HKMs) of turbot (Scophthalmus maximus L.). Interestingly, butyrate-mediated intracellular bacterial killing in HKMs diminished when IL-22 expression was interfered. Furthermore, the turbot fed the diet containing sodium butyrate (NaB) exhibited significantly lower mortality after bacterial infection, compared to the fish fed a basal diet. At the meantime, a higher level of IL-22 expression and bactericidal activity was detected in HKMs from the turbot fed NaB-supplemented diet. In addition, NaB treatment promoted the expression of antimicrobial peptides (AMPs) β-defensins in zebrafish (Danio rerio). However, butyrate-induced expression of AMPs was reduced in IL-22 mutant zebrafish compared to wild-type (WT) fish. Meanwhile, NaB treatment was incapable to protect IL-22 mutant fish from bacterial infection as it did in WT zebrafish. Importantly, our results demonstrated that IL-22 expression was remarkably suppressed in macrophage-depleted zebrafish, indicating that macrophage might be a cell source of IL-22 production in vivo. In conclusion, all these findings collectively revealed that SCFAs regulated the production and function of IL-22 in fish macrophages, which facilitated host resistance to bacterial invasion.

Keywords: Antimicrobial peptides; IL-22; Infection; Macrophage; Short-chain fatty acids (SCFAs).

MeSH terms

  • Animals
  • Bacteria
  • Butyric Acid / metabolism
  • Butyric Acid / pharmacology
  • Fatty Acids, Volatile / metabolism
  • Interleukin-22
  • Interleukins* / genetics
  • Interleukins* / metabolism
  • Macrophages
  • Zebrafish*

Substances

  • Interleukins
  • Butyric Acid
  • Fatty Acids, Volatile