Synergistic role of gut-microbial L-ornithine in enhancing ustekinumab efficacy for Crohn's disease

Cell Metab. 2025 May 6;37(5):1089-1102.e7. doi: 10.1016/j.cmet.2025.01.007. Epub 2025 Feb 19.

Abstract

The role of the intestinal microbiome in Crohn's disease (CD) treatment remains poorly understood. This study investigates microbe-host interactions in CD patients undergoing ustekinumab (UST) therapy. Fecal metagenome, metabolome, and host transcriptome data from 85 CD patients were analyzed using multi-omics integration and mediation analysis. Our findings reveal significant microbiome-metabolite-host interactions. Specifically, Faecalibacterium prausnitzii was linked to altered L-ornithine biosynthesis, resulting in higher L-ornithine levels in patients before UST therapy. In vivo and in vitro studies demonstrated that microbiome-derived L-ornithine enhances UST treatment sensitivity in CD by disrupting the host IL-23 receptor signaling and inhibiting Th17 cell stabilization through the IL-12RB1/TYK2/STAT3 axis. L-ornithine significantly enhances the therapeutic efficacy of UST in CD patients, as demonstrated in a prospective clinical trial. These findings suggest that targeting specific microbe-host metabolic pathways may improve the efficacy of inflammatory bowel disease (IBD) treatments.

Keywords: Crohn’ s disease; EGR1; Faecalibacterium prausnitzii; IL-12/IL-23 signaling pathway; IL-12RB1; L-ornithine; Th17 cell; mediation analysis; multi-omics; ustekinumab.

MeSH terms

  • Adult
  • Animals
  • Crohn Disease* / drug therapy
  • Crohn Disease* / metabolism
  • Crohn Disease* / microbiology
  • Faecalibacterium prausnitzii / metabolism
  • Feces / microbiology
  • Female
  • Gastrointestinal Microbiome* / drug effects
  • Humans
  • Male
  • Mice
  • Middle Aged
  • Ornithine* / metabolism
  • Ornithine* / pharmacology
  • Receptors, Interleukin / metabolism
  • Signal Transduction / drug effects
  • Th17 Cells / drug effects
  • Th17 Cells / immunology
  • Th17 Cells / metabolism
  • Treatment Outcome
  • Ustekinumab* / pharmacology
  • Ustekinumab* / therapeutic use

Substances

  • Ustekinumab
  • Ornithine
  • Receptors, Interleukin