A microbially produced AhR ligand promotes a Tph1-driven tolerogenic program in multiple sclerosis

Sci Rep. 2024 Mar 20;14(1):6651. doi: 10.1038/s41598-024-57400-8.

Abstract

Multiple sclerosis is a debilitating autoimmune disease, characterized by chronic inflammation of the central nervous system. While the significance of the gut microbiome on multiple sclerosis pathogenesis is established, the underlining mechanisms are unknown. We found that serum levels of the microbial postbiotic tryptophan metabolite indole-3-carboxaldehyde (3-IAld) inversely correlated with disease duration in multiple sclerosis patients. Much like the host-derived tryptophan derivative L-Kynurenine, 3-IAld would bind and activate the Aryl hydrocarbon Receptor (AhR), which, in turn, controls endogenous tryptophan catabolic pathways. As a result, in peripheral lymph nodes, microbial 3-IAld, affected mast-cell tryptophan metabolism, forcing mast cells to produce serotonin via Tph1. We thus propose a protective role for AhR-mast-cell activation driven by the microbiome, whereby natural metabolites or postbiotics will have a physiological role in immune homeostasis and may act as therapeutic targets in autoimmune diseases.

Keywords: 3-IAld; Aryl hydrocarbon receptor; Mast cells; Multiple sclerosis; Serotonin.

MeSH terms

  • Humans
  • Kynurenine / metabolism
  • Ligands
  • Multiple Sclerosis*
  • Receptors, Aryl Hydrocarbon / metabolism
  • Tryptophan Hydroxylase / metabolism
  • Tryptophan* / metabolism

Substances

  • Kynurenine
  • Ligands
  • Receptors, Aryl Hydrocarbon
  • Tryptophan
  • TPH1 protein, human
  • Tryptophan Hydroxylase
  • AHR protein, human