Sensory ASIC3 channel exacerbates psoriatic inflammation via a neurogenic pathway in female mice

Nat Commun. 2024 Jun 20;15(1):5288. doi: 10.1038/s41467-024-49577-3.

Abstract

Psoriasis is an immune-mediated skin disease associated with neurogenic inflammation, but the underlying molecular mechanism remains unclear. We demonstrate here that acid-sensing ion channel 3 (ASIC3) exacerbates psoriatic inflammation through a sensory neurogenic pathway. Global or nociceptor-specific Asic3 knockout (KO) in female mice alleviates imiquimod-induced psoriatic acanthosis and type 17 inflammation to the same extent as nociceptor ablation. However, ASIC3 is dispensable for IL-23-induced psoriatic inflammation that bypasses the need for nociceptors. Mechanistically, ASIC3 activation induces the activity-dependent release of calcitonin gene-related peptide (CGRP) from sensory neurons to promote neurogenic inflammation. Botulinum neurotoxin A and CGRP antagonists prevent sensory neuron-mediated exacerbation of psoriatic inflammation to similar extents as Asic3 KO. In contrast, replenishing CGRP in the skin of Asic3 KO mice restores the inflammatory response. These findings establish sensory ASIC3 as a critical constituent in psoriatic inflammation, and a promising target for neurogenic inflammation management.

MeSH terms

  • Acid Sensing Ion Channels* / genetics
  • Acid Sensing Ion Channels* / metabolism
  • Animals
  • Calcitonin Gene-Related Peptide* / genetics
  • Calcitonin Gene-Related Peptide* / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Imiquimod
  • Inflammation / metabolism
  • Interleukin-23 / genetics
  • Interleukin-23 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Neurogenic Inflammation / metabolism
  • Nociceptors / metabolism
  • Psoriasis* / chemically induced
  • Psoriasis* / genetics
  • Psoriasis* / metabolism
  • Psoriasis* / pathology
  • Sensory Receptor Cells* / metabolism
  • Skin / metabolism
  • Skin / pathology

Substances

  • Acid Sensing Ion Channels
  • ASIC3 protein, mouse
  • Calcitonin Gene-Related Peptide
  • Imiquimod
  • Interleukin-23