Icariin restrains NLRP3 inflammasome-mediated Th2 immune responses and ameliorates atopic dermatitis through modulating a novel lncRNA MALAT1/miR-124-3p axis

Pharm Biol. 2023 Dec;61(1):1249-1259. doi: 10.1080/13880209.2023.2244004.

Abstract

Context: Atopic dermatitis (AD) is a common inflammatory skin disease characterized with hyperactivation of type 2 T helper (Th2) immune responses. Icariin is a flavonoid glucoside with anti-inflammatory activities, which has been used to treat multiple diseases.

Objective: The present study investigates the underlying mechanisms by which icariin regulates Th2 responses and AD development.

Materials and methods: BALB/c mice were induced by DNFB to establish AD models, and injected with or without 10 mg/kg icariin for 2 weeks (i.p., daily). CD4+T cells were induced by Th2 condition to simulate AD in vitro, and also treated with or without 100 µM icariin.

Results: Icariin ameliorated AD-like skin lesion, manifested as a significant decrease in dermatitis scores (from 8.00 ± 1.00 to 3.67 ± 0.58), serum IgE levels (from 3119.15 ± 241.81 to 948.55 ± 182.51 ng/mL), epidermal thickness (from 93.86 ± 4.61 to 42.67 ± 2.48 µm) and infiltration of mast cells (from 60.67 ± 3.21 cells to 36.00 ± 2.65 cells). Also, icariin inactivated NLRP3 inflammasome, inhibited Th2 skewing, reduced lncRNA MALAT1 expression, but elevated miR-124-3p expression in vivo and in vitro. MALAT1 increased NLRP3 expression through targeting miR-124-3p. Knockdown of MALAT1 repressed NLRP3 inflammasome activation and mitigated Th1/Th2 imbalance in Th2-conditioned CD4+T cells, whereas both MALAT1 overexpression and miR-124-3p inhibition ablated the inhibitory effects of icariin on Th2 immune responses.

Discussion and conclusions: The findings further improve our understanding of the mechanism by which icariin affects AD progression, and highlights the potential of icariin in the treatment of AD.

Keywords: CD4+T cells; MALAT1; NLRP3; Th2 responses; miR-124-3p.

MeSH terms

  • Animals
  • Dermatitis, Atopic* / drug therapy
  • Flavonoids / pharmacology
  • Inflammasomes
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs* / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • RNA, Long Noncoding* / genetics

Substances

  • RNA, Long Noncoding
  • icariin
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Flavonoids
  • MicroRNAs
  • Mirn124 microRNA, mouse

Grants and funding

This work was supported by the Key R&D and Promotion Project of Henan Province (Tackling Key Problems in Science and Technology) (No. 212102311121).