Skin treatment with non-thermal plasma modulates the immune system through miR-223-3p and its target genes

RNA Biol. 2024 Jan;21(1):31-44. doi: 10.1080/15476286.2024.2361571. Epub 2024 Jun 3.

Abstract

Non-thermal plasma, a partially ionized gas, holds significant potential for clinical applications, including wound-healing support, oral therapies, and anti-tumour treatments. While its applications showed promising outcomes, the underlying molecular mechanisms remain incompletely understood. We thus apply non-thermal plasma to mouse auricular skin and conducted non-coding RNA sequencing, as well as single-cell blood sequencing. In a time-series analysis (five timepoints spanning 2 hours), we compare the expression of microRNAs in the plasma-treated left ears to the unexposed right ears of the same mice as well as to the ears of unexposed control mice. Our findings indicate specific effects in the treated ears for a set of five miRNAs: mmu-miR-144-5p, mmu-miR-144-3p, mmu-miR-142a-5p, mmu-miR-223-3p, and mmu-miR-451a. Interestingly, mmu-miR-223-3p also exhibits an increase over time in the right non-treated ear of the exposed mice, suggesting systemic effects. Notably, this miRNA, along with mmu-miR-142a-5p and mmu-miR-144-3p, regulates genes and pathways associated with wound healing and tissue regeneration (namely ErbB, FoxO, Hippo, and PI3K-Akt signalling). This co-regulation is particularly remarkable considering the significant seed dissimilarities among the miRNAs. Finally, single-cell sequencing of PBMCs reveals the downregulation of 12 from 15 target genes in B-cells, Cd4+ and Cd8+ T-cells. Collectively, our data provide evidence for a systemic effect of non-thermal plasma.

Keywords: Non-thermal plasma; cell adhesion; miR-223-3p; miRNA; single blood cell sequencing; wound healing.

MeSH terms

  • Animals
  • Gene Expression Profiling
  • Gene Expression Regulation* / drug effects
  • Immune System / metabolism
  • Mice
  • MicroRNAs* / genetics
  • Plasma Gases* / pharmacology
  • Signal Transduction
  • Skin* / metabolism
  • Wound Healing / drug effects

Substances

  • MicroRNAs
  • MIRN223 microRNA, mouse
  • Plasma Gases

Grants and funding

We acknowledge funding by Deutsche Forschungsgemeinschaft (DFG-project: Compute- und Storage Cluster with project number 469073465). For the Development of the software pipeline used to process the single-cell data, we are supported by funds of the European Health and Digital Executive Agency (HaDEA) (Project number 101057548-EPIVINF).