The chemically stable analogue of resolvin D1 ameliorates experimental autoimmune encephalomyelitis by mediating the resolution of inflammation

Int Immunopharmacol. 2024 Oct 25:140:112740. doi: 10.1016/j.intimp.2024.112740. Epub 2024 Aug 7.

Abstract

While Resolvin D1 (RvD1) shows promise in resolving inflammation in experimental autoimmune encephalomyelitis (EAE), its pro-resolving roles on dendritic cells (DCs) remain unknown, and the chemical instability of RvD1 poses significant challenges to its drug development. This study aims to investigate whether 4-(2'-methoxyphenyl)-1-[2'-[N-(2″-pyridinyl)-p-fluorobenzamido]ethyl]piperazine (p-MPPF), a novel chemically stable analogue of RvD1, can play a pro-resolving role in EAE, particularly on DCs, and if p-MPPF could serve as a potential substitute for RvD1. We showed that both RvD1 and p-MPPF mediated the resolution of inflammation in EAE, as evidenced by ameliorated EAE progression, attenuated pathological changes in the spinal cord, altered cytokine expression profile in serum, and reduced proportion of pro-inflammatory immune cells in the spleen. Utilizing DCs derived from both the spleen and bone marrow of EAE, our investigation showed that RvD1 and p-MPPF prevented DC maturation, decreased pro-inflammatory cytokine secretion, shifted DCs away from a pro-inflammatory phenotype, increased the phagocytosis capacity of DCs, and suppressed their ability to induce differentiation of CD4+ T cells into Th1 and Th17 subsets. For underlying intracellular mechanisms, we found that RvD1 and p-MPPF down-regulated the lactate dehydrogenase A signaling pathways. Comparisons between RvD1 and p-MPPF showed that they exerted overlapped pro-resolving effects to a large extent. This study demonstrates that both RvD1 and p-MPPF exert therapeutic effects on EAE by mediating inflammation resolution, which is closely associated with modulating DC immune function towards a tolerogenic phenotype. SPM mimetics may serve as a more promising therapeutic drug.

Keywords: Dendritic cell; Experimental autoimmune encephalomyelitis; Resolvin D1; The resolution of inflammation; p-MPPF.

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Anti-Inflammatory Agents / therapeutic use
  • Cells, Cultured
  • Cytokines* / metabolism
  • Dendritic Cells* / drug effects
  • Dendritic Cells* / immunology
  • Docosahexaenoic Acids* / chemistry
  • Docosahexaenoic Acids* / pharmacology
  • Docosahexaenoic Acids* / therapeutic use
  • Encephalomyelitis, Autoimmune, Experimental* / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental* / immunology
  • Female
  • Inflammation / drug therapy
  • Inflammation / immunology
  • Mice
  • Mice, Inbred C57BL
  • Piperazines / chemistry
  • Piperazines / pharmacology
  • Piperazines / therapeutic use
  • Spinal Cord / drug effects
  • Spinal Cord / immunology
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Spleen / drug effects
  • Spleen / immunology
  • Th17 Cells / drug effects
  • Th17 Cells / immunology

Substances

  • Anti-Inflammatory Agents
  • Cytokines
  • Docosahexaenoic Acids
  • Piperazines
  • resolvin D1