Expression of Acid-Sensing Ion Channel 3 in Afferents Averts Long-Term Sensitization and the Development of Visceral Pain

Int J Mol Sci. 2024 Nov 21;25(23):12503. doi: 10.3390/ijms252312503.

Abstract

Sensitization of primary afferents is essential for the development of pain, but the molecular events involved in this process and its reversal are poorly defined. Recent studies revealed that acid-sensing ion channels (ASICs) control the excitability of nociceptors in the urinary bladder. Using genetic and pharmacological tools we show that ASICs are functionally coupled with voltage-gated Ca2+ channels to mediate Ca2+ transients evoked by acidification in sensory neurons. Genetic deletion of Asic3 of these sensory neurons does not alter the mechanical response of bladder afferents to distension in naïve mice. Both control and sensory neuron conditional Asic3 knockout (Asic3-KO) mice with chemical cystitis induced by cyclophosphamide (CYP) administration exhibit frequent low volume voiding events. However, these changes are transient and revert over time. Of major significance, in Asic3-KO mice, CYP treatment results in the sensitization of a subset of bladder afferents and pelvic allodynia that persist beyond the resolution of the inflammatory process. Thus, ASICs function is necessary to prevent long-term sensitization of visceral nociceptors.

Keywords: acid-sensing ion channels; chemical cystitis; sensory neurons; urinary bladder; visceral pain.

MeSH terms

  • Acid Sensing Ion Channels* / genetics
  • Acid Sensing Ion Channels* / metabolism
  • Animals
  • Cyclophosphamide / adverse effects
  • Cystitis / chemically induced
  • Cystitis / genetics
  • Cystitis / metabolism
  • Hyperalgesia / genetics
  • Hyperalgesia / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Nociceptors / metabolism
  • Sensory Receptor Cells / metabolism
  • Urinary Bladder* / innervation
  • Urinary Bladder* / metabolism
  • Urinary Bladder* / pathology
  • Visceral Pain* / genetics
  • Visceral Pain* / metabolism

Substances

  • Acid Sensing Ion Channels
  • ASIC3 protein, mouse
  • Cyclophosphamide