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. 2024 Dec;154(6):1450-1461.
doi: 10.1016/j.jaci.2024.06.024. Epub 2024 Aug 12.

Skin microdialysis detects distinct immunologic patterns in chronic inflammatory skin diseases

Moritz Maximilian Hollstein  1 , Stephan Traidl  2 , Anne Heetfeld  3 , Susann Forkel  3 , Andreas Leha  4 , Natalia Alkon  5 , Jannik Ruwisch  6 , Christof Lenz  7 , Michael Peter Schön  3 , Martin Schmelz  8 , Patrick Brunner  9 , Martin Steinhoff  10 , Timo Buhl  3
Affiliations
Free article

Skin microdialysis detects distinct immunologic patterns in chronic inflammatory skin diseases

Moritz Maximilian Hollstein et al. J Allergy Clin Immunol. 2024 Dec.
Free article

Abstract

Background: Insight into the pathophysiology of inflammatory skin diseases, especially at the proteomic level, is severely hampered by the lack of adequate in situ data.

Objective: We characterized lesional and nonlesional skin of inflammatory skin diseases using skin microdialysis.

Methods: Skin microdialysis samples from patients with atopic dermatitis (AD, n = 6), psoriasis vulgaris (PSO, n = 7), or prurigo nodularis (PN, n = 6), as well as healthy controls (n = 7), were subjected to proteomic and multiplex cytokine analysis. Single-cell RNA sequencing of skin biopsy specimens was used to identify the cellular origin of cytokines.

Results: Among the top 20 enriched Gene Ontology (GO; geneontology.org) annotations, nicotinamide adenine dinucleotide metabolic process, regulation of secretion by cell, and pyruvate metabolic process were elevated in microdialysates from lesional AD skin compared with both nonlesional skin and controls. The top 20 enriched Kyoto Encyclopedia of Genes and Genomes (KEGG; genome.jp/kegg) pathways in these 3 groups overlapped almost completely. In contrast, nonlesional skin from patients with PSO or PN and control skin showed no overlap with lesional skin in this KEGG pathway analysis. Lesional skin from patients with PSO, but not AD or PN, showed significantly elevated protein levels of MCP-1 compared with nonlesional skin. IL-8 was elevated in lesional versus nonlesional AD and PSO skin, whereas IL-12p40 and IL-22 were higher only in lesional PSO skin. Integrated single-cell RNA sequencing data revealed identical cellular sources of these cytokines in AD, PSO, and PN.

Conclusion: On the basis of microdialysates, the proteomic data of lesional PSO and PN skin, but not lesional AD skin, differed significantly from those of nonlesional skin. IL-8, IL-22, MCP-1, and IL-12p40 might be suitable markers for minimally invasive molecular profiling.

Keywords: Microdialysis; atopic dermatitis; pruritus; psoriasis vulgaris.

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Conflict of interest statement

Disclosure statement Supported in part by Kiniksa (San Diego, Calif) and a scholarship from the Deutsche Forschungsgemeinschaft (DFG 413501650 to M.M.H.). Disclosure of potential conflict of interest: The authors declare that they have no relevant conflicts of interest.