Aspergillus fumigatus-derived gliotoxin impacts innate immune cell activation through modulating lipid mediator production in macrophages

Immunology. 2024 Dec;173(4):748-767. doi: 10.1111/imm.13857. Epub 2024 Sep 13.

Abstract

Gliotoxin (GT), a secondary metabolite and virulence factor of the fungal pathogen Aspergillus fumigatus, suppresses innate immunity and supports the suppression of host immune responses. Recently, we revealed that GT blocks the formation of the chemotactic lipid mediator leukotriene (LT)B4 in activated human neutrophils and monocytes, and in rodents in vivo, by directly inhibiting LTA4 hydrolase. Here, we elucidated the impact of GT on LTB4 biosynthesis and the entire lipid mediator networks in human M1- and M2-like monocyte-derived macrophages (MDMs) and in human tissue-resident alveolar macrophages. In activated M1-MDMs with high capacities to generate LTs, the formation of LTB4 was effectively suppressed by GT, connected to attenuated macrophage phagocytic activity as well as human neutrophil movement and migration. In resting macrophages, especially in M1-MDMs, GT elicited strong formation of prostaglandins, while bacterial exotoxins from Staphylococcus aureus evoked a broad spectrum of lipid mediator biosynthesis in both MDM phenotypes. We conclude that GT impairs functions of activated innate immune cells through selective suppression of LTB4 biosynthesis, while GT may also prime the immune system by provoking prostaglandin formation in macrophages.

Keywords: Aspergillus fumigatus; gliotoxin; leukotriene; lipid mediators; macrophages; prostaglandin.

MeSH terms

  • Aspergillus fumigatus* / immunology
  • Cells, Cultured
  • Gliotoxin* / immunology
  • Gliotoxin* / pharmacology
  • Humans
  • Immunity, Innate*
  • Leukotriene B4 / metabolism
  • Macrophage Activation
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Macrophages, Alveolar / immunology
  • Macrophages, Alveolar / metabolism
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Phagocytosis
  • Prostaglandins / immunology
  • Prostaglandins / metabolism
  • Staphylococcus aureus / immunology

Substances

  • Gliotoxin
  • Leukotriene B4
  • Prostaglandins