4-Octyl Itaconate Inhibits Proinflammatory Cytokine Production in Behcet's Uveitis and Experimental Autoimmune Uveitis

Inflammation. 2024 Jun;47(3):909-920. doi: 10.1007/s10753-023-01950-y. Epub 2024 Jan 6.

Abstract

4-octyl itaconate (4-OI) is an anti-inflammatory metabolite that activates the nuclear-factor-E2-related factor 2 (NRF2) signaling. In the current work, we investigated whether 4-OI could affect the production of proinflammatory cytokines in Behcet's uveitis (BU) and experimental autoimmune uveitis (EAU). Peripheral blood mononuclear cells (PBMCs) of active BU patients and healthy individuals with in vitro 4-OI treatment were performed to assess the influence of 4-OI on the proinflammatory cytokine production. EAU was induced and used for investigating the influence of 4-OI on the proinflammatory cytokine production in vivo. The flow cytometry, qPCR, and ELISA were performed to detect proinflammatory cytokine expression. NRF2 signaling activation was evaluated by qPCR and western blotting (WB). Splenic lymphocyte transcriptome was performed by RNA sequencing. The NRF2 expression by BU patients-derived PBMCs was lower than that by healthy individuals. After treatment with 4-OI, the proportion of Th17 cells, along with the expression of proinflammatory cytokines (IL-17, TNF-α, MCP-1, and IL-6) by PBMCs, were downregulated, and anti-inflammatory cytokine (IL-10) expression was upregulated, although IFN-γ expression was unaffected. The EAU severity was ameliorated by 4-OI in association with a lower splenic Th1/Th17 cell proportion and increased nuclear NRF2 expression. Additionally, 4-OI downregulated a set of 248 genes, which were enriched in pathways of positive regulation of immune responses. The present study shows an inhibitory effect of 4-OI on the proinflammatory cytokine production in active BU patients and EAU mice, possibly mediated through activating NRF2 signaling. These findings suggest that 4-OI could act as a potential therapeutic drug for the treatment and prevention of BU in the future study.

Keywords: 4-octyl-itaconate; Behcet’s uveitis; Peripheral blood mononuclear cells; Th17 responses; Uveitis.

MeSH terms

  • Adult
  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Anti-Inflammatory Agents / therapeutic use
  • Autoimmune Diseases* / drug therapy
  • Behcet Syndrome* / drug therapy
  • Behcet Syndrome* / immunology
  • Behcet Syndrome* / metabolism
  • Cytokines* / biosynthesis
  • Cytokines* / metabolism
  • Female
  • Humans
  • Inflammation Mediators / antagonists & inhibitors
  • Inflammation Mediators / metabolism
  • Leukocytes, Mononuclear / drug effects
  • Leukocytes, Mononuclear / immunology
  • Leukocytes, Mononuclear / metabolism
  • Male
  • Mice
  • NF-E2-Related Factor 2* / metabolism
  • Succinates* / pharmacology
  • Succinates* / therapeutic use
  • Th17 Cells / drug effects
  • Th17 Cells / immunology
  • Th17 Cells / metabolism
  • Uveitis* / drug therapy
  • Uveitis* / immunology
  • Uveitis* / metabolism

Substances

  • Cytokines
  • Succinates
  • NF-E2-Related Factor 2
  • 4-octyl itaconate
  • Anti-Inflammatory Agents
  • Inflammation Mediators
  • NFE2L2 protein, human