AUTHOR=Ma Emily Z. , Deng Junwen , Parthasarathy Varsha , Lee Kevin K. , Pritchard Thomas , Guo Shenghao , Zhang Cissy , Kwatra Madan M. , Le Anne , Kwatra Shawn G. TITLE=Integrated plasma metabolomic and cytokine analysis reveals a distinct immunometabolic signature in atopic dermatitis JOURNAL=Frontiers in Immunology VOLUME=15 YEAR=2024 URL=https://www.frontiersin.org/journals/immunology/articles/10.3389/fimmu.2024.1354128 DOI=10.3389/fimmu.2024.1354128 ISSN=1664-3224 ABSTRACT=Importance

Disease models for atopic dermatitis (AD) have primarily focused on understanding underlying environmental, immunologic, and genetic etiologies. However, the role of metabolic mechanisms in AD remains understudied.

Objective

To investigate the circulating blood metabolomic and cytokine profile of AD as compared to healthy control patients.

Design

This study collected plasma from 20 atopic dermatitis with moderate-to-severe itch (score of ≥5 on the itch Numeric Rating Scale and IGA score ≥3) and 24 healthy control patients. Mass-spectrometry based metabolite data were compared between AD and healthy controls. Unsupervised and supervised machine learning algorithms and univariate analysis analyzed metabolic concentrations. Metabolite enrichment and pathway analyses were performed on metabolites with significant fold change between AD and healthy control patients. To investigate the correlation between metabolites levels and cytokines, Spearman’s rank correlation coefficients were calculated between metabolites and cytokines.

Setting

Patients were recruited from the Johns Hopkins Itch Center and dermatology outpatient clinics in the Johns Hopkins Outpatient Center.

Participants

The study included 20 atopic dermatitis patients and 24 healthy control patients.

Main outcomes and measures

Fold changes of metabolites in AD vs healthy control plasma.

Results

In patients with AD, amino acids isoleucine, tyrosine, threonine, tryptophan, valine, methionine, and phenylalanine, the amino acid derivatives creatinine, indole-3-acrylic acid, acetyl-L-carnitine, L-carnitine, 2-hydroxycinnamic acid, N-acetylaspartic acid, and the fatty amide oleamide had greater than 2-fold decrease (all P-values<0.0001) compared to healthy controls. Enriched metabolites were involved in branched-chain amino acid (valine, leucine, and isoleucine) degradation, catecholamine biosynthesis, thyroid hormone synthesis, threonine metabolism, and branched and long-chain fatty acid metabolism. Dysregulated metabolites in AD were positively correlated cytokines TARC and MCP-4 and negatively correlated with IL-1a and CCL20.

Conclusions and relevance

Our study characterized novel dysregulated circulating plasma metabolites and metabolic pathways that may be involved in the pathogenesis of AD. These metabolic pathways serve as potential future biomarkers and therapeutic targets in the treatment of AD.