NMDA Receptor Modulates Spinal Iron Accumulation Via Activating DMT1(-)IRE in Remifentanil-Induced Hyperalgesia

J Pain. 2021 Jan;22(1):32-47. doi: 10.1016/j.jpain.2020.03.007. Epub 2020 Jun 20.

Abstract

N-methyl-D-aspartate (NMDA) receptor activation is known to be critical in remifentanil-induced hyperalgesia. Evidence indicates that iron accumulation participates in NMDA neurotoxicity. This study aims to investigate the role of iron accumulation in remifentanil-induced hyperalgesia. Remifentanil was delivered intravenously in rats to induce hyperalgesia. The NMDA receptor antagonist MK-801 was intrathecally administrated. The levels of divalent metal transporter 1 without iron-responsive element [DMT1(-)IRE] and iron were detected. Behavior testing was performed in DMT1(-)IRE knockdown rats and rats treated with iron chelator DFO. Meanwhile, the spinal dorsal horn neurons were cultured and transfected with DMT1(-)IRE siRNA, and then respectively incubated with remifentanil and MK-801. The levels of intracellular Ca2+ and iron were assessed by fluorescence imaging. Our data revealed that spinal DMT1(-)IRE and iron content significantly increased in remifentanil-treated rats, and MK-801 inhibited the enhancements. DMT1(-)IRE knockdown and DFO prevented against remifentanil-induced hyperalgesia. Notably, the levels of Ca2+ and iron increased in remifentanil-incubated neurons, and these growths can be blocked by MK-801. DMT1(-)IRE knockdown attenuated iron accumulation but did not influence Ca2+ influx. This study suggests that DMT1(-)IRE-mediated iron accumulation is likely to be the downstream event following NMDA receptor activation and Ca2+ influx, contributing to remifentanil-induced hyperalgesia. PERSPECTIVE: Remifentanil-induced hyperalgesia is common even when used within clinical accepted doses. This study presents that aberrant iron accumulation is involved in the development of remifentanil-induced hyperalgesia in vivo and in vitro. Iron chelation may be a potential therapeutic strategy for the prevention of hyperalgesia in populations at high risk.

Keywords: DMT1(-)IRE; NMDA receptor; Remifentanil; hyperalgesia; iron accumulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics, Opioid / administration & dosage
  • Analgesics, Opioid / pharmacology*
  • Animals
  • Cation Transport Proteins / metabolism*
  • Cells, Cultured
  • Dizocilpine Maleate / pharmacology
  • Excitatory Amino Acid Antagonists / administration & dosage
  • Excitatory Amino Acid Antagonists / pharmacology*
  • Hyperalgesia / chemically induced*
  • Hyperalgesia / prevention & control*
  • Iron / metabolism*
  • Iron Chelating Agents / pharmacology*
  • Male
  • Posterior Horn Cells / drug effects*
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Transgenic
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism*
  • Receptors, Opioid, mu / agonists
  • Remifentanil / administration & dosage
  • Remifentanil / pharmacology*
  • Signal Transduction / physiology
  • Spine / metabolism*

Substances

  • Analgesics, Opioid
  • Cation Transport Proteins
  • Excitatory Amino Acid Antagonists
  • Iron Chelating Agents
  • Receptors, N-Methyl-D-Aspartate
  • Receptors, Opioid, mu
  • solute carrier family 11- (proton-coupled divalent metal ion transporters), member 2
  • Dizocilpine Maleate
  • Iron
  • Remifentanil