Melatonin treatment increases skin microbiota-derived propionic acid to alleviate atopic dermatitis

J Allergy Clin Immunol. 2024 Nov 21:S0091-6749(24)01236-3. doi: 10.1016/j.jaci.2024.11.019. Online ahead of print.

Abstract

Background: Melatonin has been reported to relieve the inflammatory symptoms and improve sleep disturbance in AD patients. Recent studies showed that melatonin exerted beneficial actions by remodeling intestinal microbiota composition; however, whether the beneficial effects of melatonin in AD were mediated by the modulation of skin microbiota remains unclear.

Objective: We sought to investigate the mechanism by which melatonin treatment-induced changes in the skin microbiota composition further alleviated AD.

Methods: The changes in skin bacterial composition after melatonin treatment were detected by 16S-rRNA sequencing. The further mechanism was explored in calcipotriol (MC903)-induced AD mice and HaCaT cells through skin microbiota transplantation experiment, quantification detection of short chain fatty acids (SCFAs), transcriptome and single cell sequencing analysis, reverse transcription quantitative PCR (RT-qPCR), western blotting, and CCK8 assay.

Results: We demonstrated that melatonin reshaped the skin microbiota in AD mice. The transplantation of skin microbiota from melatonin-treated mice alleviated AD symptoms in mice. Skin microbiota-derived SCFAs especially propionic acid were increased in the skin of melatonin-treated AD mice, which further inhibited fatty acid-binding protein 5 (FABP5) expression to alleviate AD. Propionic acid also inhibited FABP5 expression in HaCaT cells, which was reversed by the treatment of G-protein-coupled receptor 43 (GPR43) inhibitor GLPG0974. Moreover, GLPG0974 also blocked melatonin's therapeutic effects on AD mice.

Conclusion: Our study demonstrates that melatonin alleviates AD through skin microbiota/propionic acid/GPR43/FABP5 axis, highlighting a novel role of melatonin as a modulator of skin microbiota to alleviate AD.

Keywords: FABP5; atopic dermatitis; melatonin; propionic acid; skin microbiota.