Inhibition of acid-sensing ion channels by diminazene and APETx2 evoke partial and highly variable antihyperalgesia in a rat model of inflammatory pain

Br J Pharmacol. 2018 Jun;175(12):2204-2218. doi: 10.1111/bph.14089. Epub 2018 Jan 3.

Abstract

Background and purpose: Acid-sensing ion channels (ASICs) are primary acid sensors in mammals, with the ASIC1b and ASIC3 subtypes being involved in peripheral nociception. The antiprotozoal drug diminazene is a moderately potent ASIC inhibitor, but its analgesic activity has not been assessed.

Experimental approach: We determined the ASIC subtype selectivity of diminazene and the mechanism by which it inhibits ASICs using voltage-clamp electrophysiology of Xenopus oocytes expressing ASICs 1-3. Its peripheral analgesic activity was then assessed relative to APETx2, an ASIC3 inhibitor, and morphine, in a Freund's complete adjuvant (FCA)-induced rat model of inflammatory pain.

Key results: Diminazene inhibited homomeric rat ASICs with IC50 values of ~200-800 nM, via an open channel and subtype-dependent mechanism. In rats with FCA-induced inflammatory pain in one hindpaw, diminazene and APETx2 evoked more potent peripheral antihyperalgesia than morphine, but the effect was partial for APETx2. APETx2 potentiated rat ASIC1b at concentrations 30-fold to 100-fold higher than the concentration inhibiting ASIC3, which may have implications for its use in in vivo experiments.

Conclusions and implications: Diminazene and APETx2 are moderately potent ASIC inhibitors, both inducing peripheral antihyperalgesia in a rat model of chronic inflammatory pain. APETx2 has a more complex ASIC pharmacology, which must be considered when it is used as a supposedly selective ASIC3 inhibitor in vivo. Our use of outbred rats revealed responders and non-responders when ASIC inhibition was used to alleviate inflammatory pain, which is aligned with the concept of number-needed-to-treat in human clinical studies.

Linked articles: This article is part of a themed section on Recent Advances in Targeting Ion Channels to Treat Chronic Pain. To view the other articles in this section visit http://onlinelibrary.wiley.com/doi/10.1111/bph.v175.12/issuetoc.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acid Sensing Ion Channel Blockers / chemistry
  • Acid Sensing Ion Channel Blockers / pharmacology
  • Acid Sensing Ion Channels / metabolism*
  • Animals
  • Chronic Pain / drug therapy*
  • Chronic Pain / metabolism
  • Cnidarian Venoms / metabolism*
  • Diminazene / chemistry
  • Diminazene / pharmacology*
  • Disease Models, Animal
  • Hyperalgesia / drug therapy*
  • Hyperalgesia / metabolism
  • Hypoglycemic Agents / chemistry
  • Hypoglycemic Agents / pharmacology*
  • Inflammation / drug therapy*
  • Inflammation / metabolism
  • Male
  • Pain Measurement
  • Rats
  • Rats, Sprague-Dawley
  • Xenopus laevis

Substances

  • APETx2 protein, Anthopleura elegantissima
  • Acid Sensing Ion Channel Blockers
  • Acid Sensing Ion Channels
  • Cnidarian Venoms
  • Hypoglycemic Agents
  • Diminazene