Gut Microbiome

Microbiota-derived 4-HPAA alleviates Crohn's disease by stabilizing SIRT1 and reprogramming macrophage immunometabolism.

TL;DR

A diet-associated microbial metabolite pathway involving Flavonifractor plautii, 4-hydroxyphenylacetic acid (4-HPAA), and SIRT1 signaling links polyphenol-rich dietary intervention to macrophage immunometabolic regulation and intestinal barrier protection in Crohn's disease models.

Key Findings

An Aronia berry polyphenol-rich diet alleviated colitis, reduced mucosal injury, and improved epithelial barrier integrity in mouse models of Crohn's disease.

  • IL-10-/- and TNBS-induced colitis mouse models were used to evaluate the effects of dietary intervention.
  • The diet reduced mucosal injury and improved epithelial barrier integrity in both models.
  • The study used integrated metagenomic, metabolomic, and transcriptomic analyses combined with in vivo and in vitro mechanistic experiments.

Multi-omics analyses identified Flavonifractor plautii enrichment and increased microbiota-derived 4-hydroxyphenylacetic acid (4-HPAA) levels as major diet-associated changes.

  • Metagenomic analysis was used to identify diet-responsive microbial taxa.
  • Metabolomic analysis identified 4-HPAA as a key diet-associated metabolite.
  • F. plautii was identified as the primary bacterial taxon enriched in response to the polyphenol-rich diet.
  • The enrichment of F. plautii and elevated 4-HPAA were the two major diet-associated changes detected by multi-omics.

F. plautii supplementation was associated with increased 4-HPAA production, and 4-HPAA administration partially reproduced the intestinal protective phenotype in vivo.

  • Bacterial strain supplementation experiments were conducted to assess F. plautii's role in 4-HPAA production.
  • 4-HPAA administration as a candidate metabolite was evaluated in vivo.
  • 4-HPAA only partially reproduced the intestinal protective phenotype, suggesting additional mechanisms may be involved.
  • The findings establish a functional link between F. plautii colonization and 4-HPAA-mediated intestinal protection.

4-HPAA suppressed pro-inflammatory macrophage activation and promoted oxidative metabolic remodeling in macrophages.

  • In vitro mechanistic experiments were used to assess 4-HPAA effects on macrophages.
  • 4-HPAA promoted oxidative metabolic remodeling, suggesting a shift in macrophage immunometabolism.
  • Pro-inflammatory activation was suppressed by 4-HPAA treatment in macrophage models.
  • The metabolic remodeling is described as a 'reprogramming' of macrophage immunometabolism.

4-HPAA stabilized SIRT1 by limiting ubiquitination-mediated proteasomal degradation, thereby activating SIRT1-PGC-1α signaling.

  • The mechanism involves 4-HPAA reducing ubiquitination-mediated proteasomal degradation of SIRT1 protein.
  • SIRT1 stabilization led to activation of the SIRT1-PGC-1α signaling pathway.
  • This mechanistic link connects a gut microbiota-derived metabolite to an epigenetic/metabolic regulatory axis in macrophages.

Myeloid SIRT1 deficiency attenuated the effects of 4-HPAA on macrophage polarization, inflammatory cytokine expression, and epithelial barrier-associated proteins.

  • Myeloid-specific SIRT1-deficient models were used to confirm the SIRT1-dependent mechanism.
  • Loss of SIRT1 in myeloid cells reduced 4-HPAA's ability to modulate macrophage polarization.
  • 4-HPAA's effects on inflammatory cytokine expression were attenuated in myeloid SIRT1-deficient conditions.
  • Epithelial barrier-associated protein expression was also affected by myeloid SIRT1 deficiency, indicating a macrophage-to-epithelium signaling axis.

What This Means

This research suggests that eating a diet rich in polyphenols — compounds found in foods like Aronia berries — can help reduce intestinal inflammation associated with Crohn's disease by changing the composition of gut bacteria and the molecules they produce. In mouse models of Crohn's disease, animals fed a polyphenol-rich diet showed less colon damage, better gut lining integrity, and reduced inflammation. Using advanced molecular analysis tools, the researchers traced these benefits to a specific gut bacterium called Flavonifractor plautii, which increased in abundance on the polyphenol diet and produced higher levels of a molecule called 4-hydroxyphenylacetic acid (4-HPAA). This research suggests that 4-HPAA acts as a key messenger between gut bacteria and the immune system. Specifically, 4-HPAA was found to calm overactive immune cells called macrophages — which play a central role in the chronic inflammation seen in Crohn's disease — by stabilizing a protein called SIRT1. Normally, SIRT1 gets broken down in inflamed macrophages, but 4-HPAA blocks this breakdown, allowing SIRT1 to activate a protective signaling pathway (SIRT1-PGC-1α) that shifts macrophages away from an inflammatory state and toward a more restorative, energy-efficient mode. When the researchers removed SIRT1 specifically from immune cells, the protective effects of 4-HPAA were largely lost, confirming that SIRT1 is essential to this process. This research suggests that the chain of events — polyphenol-rich diet → F. plautii enrichment → 4-HPAA production → SIRT1 stabilization → reduced macrophage inflammation → improved gut barrier — represents a new biological pathway connecting diet, gut bacteria, and immune regulation in Crohn's disease. These findings may have practical implications for developing dietary or microbiome-based strategies to complement existing treatments for Crohn's disease and related inflammatory bowel conditions, though further research in humans would be needed to confirm these effects.

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Citation

Cheng C, Cheng S, Jiang W, Fu S, Shang Y, Tang X, et al.. (2026). Microbiota-derived 4-HPAA alleviates Crohn's disease by stabilizing SIRT1 and reprogramming macrophage immunometabolism.. Apoptosis : an international journal on programmed cell death. https://doi.org/10.1007/s10495-026-02417-9