High-sensitive sensory neurons exacerbate rosacea-like dermatitis in mice by activating γδ T cells directly

Nat Commun. 2024 Aug 23;15(1):7265. doi: 10.1038/s41467-024-50970-1.

Abstract

Rosacea patients show facial hypersensitivity to stimulus factors (such as heat and capsaicin); however, the underlying mechanism of this hyperresponsiveness remains poorly defined. Here, we show capsaicin stimulation in mice induces exacerbated rosacea-like dermatitis but has no apparent effect on normal skin. Nociceptor ablation substantially reduces the hyperresponsiveness of rosacea-like dermatitis. Subsequently, we find that γδ T cells express Ramp1, the receptor of the neuropeptide CGRP, and are in close contact with these nociceptors in the skin. γδ T cells are significantly increased in rosacea skin lesions and can be further recruited and activated by neuron-secreted CGRP. Rosacea-like dermatitis is reduced in T cell receptor δ-deficient (Tcrd-/-) mice, and the nociceptor-mediated aggravation of rosacea-like dermatitis is also reduced in these mice. In vitro experiments show that CGRP induces IL17A secretion from γδ T cells by regulating inflammation-related and metabolism-related pathways. Finally, rimegepant, a CGRP receptor antagonist, shows efficacy in the treatment of rosacea-like dermatitis. In conclusion, our findings demonstrate a neuron-CGRP-γδT cell axis that contributes to the hyperresponsiveness of rosacea, thereby showing that targeting CGRP is a potentially effective therapeutic strategy for rosacea.

MeSH terms

  • Animals
  • Calcitonin Gene-Related Peptide* / metabolism
  • Capsaicin* / pharmacology
  • Dermatitis / immunology
  • Dermatitis / metabolism
  • Dermatitis / pathology
  • Disease Models, Animal
  • Humans
  • Interleukin-17 / immunology
  • Interleukin-17 / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nociceptors / metabolism
  • Receptors, Antigen, T-Cell, gamma-delta* / genetics
  • Receptors, Antigen, T-Cell, gamma-delta* / metabolism
  • Receptors, Calcitonin Gene-Related Peptide / metabolism
  • Rosacea* / immunology
  • Sensory Receptor Cells* / metabolism
  • Skin / immunology
  • Skin / metabolism
  • Skin / pathology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Calcitonin Gene-Related Peptide
  • Capsaicin
  • Receptors, Antigen, T-Cell, gamma-delta
  • Interleukin-17
  • Receptors, Calcitonin Gene-Related Peptide