Spinal caspase-6 contributes to remifentanil-induced hyperalgesia via regulating CCL21/CXCR3 pathway in rats

Neurosci Lett. 2020 Mar 16:721:134802. doi: 10.1016/j.neulet.2020.134802. Epub 2020 Jan 31.

Abstract

Background: Neuroinflammation in the spinal cord is a pathological event in remifentanil-induced hyperalgesia (RIH), but its underlying molecular mechanisms remain unclear. Recent studies recapitulate the significance of the intracellular protease caspase-6 in the release of inflammatory mediators and synaptic plasticity in pathologic pain. Also, chemokine CCL21 is involved in microglia activation and nociceptive transduction. This study examined whether spinal caspase-6 is associated with RIH via CCL21 and its receptor CXCR3.

Methods: The acute exposure to remifentanil (1 μg kg-1 min-1for 60 min) was used to establish RIH, verified by assessment of mechanical paw withdrawal threshold and thermal paw withdrawal latency. The caspase-6 inhibitor, a neutralizing antibody against CCL21 (anti-CCL21), a selective CXCR3 antagonist NBI-74330, recombinant caspase-6 and CCL21 were used for the investigation of pathogenesis as well as the prevention of hyperalgesia. The expression of caspase-6, CCL21 and CXCR3 was also evaluated by RT-qPCR and Western blot.

Results: This study discovered mechanical allodynia and thermal hyperalgesia along with the increase in the expression of spinal caspase-6 and CCL21/CXCR3 after remifentanil exposure. Central caspase-6 inhibition prevented behavioral RIH and spinal up-regulation of CCL21/CXCR3 level. Intrathecal anti-CCL21 injection reduced RIH and spinal expression of CXCR3. The delivery of recombinant caspase-6 facilitated acute nociceptive hypersensitivity and increased spinal CXCR3 release in naïve rats, reversing by co-application of anti-CCL21. Also, NBI-74330 attenuated RIH and exogenous CCL21-caused acute pain behaviors.

Conclusion: This study highlighted that spinal caspase-6-mediated up-regulation of CCL21/CXCR3 is vital in the pathogenesis of RIH in rats.

Keywords: CCL21; CXCR3; Caspase-6; Remifentanil-induced hyperalgesia; Spinal cord.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics, Opioid / toxicity
  • Animals
  • Caspase 6 / metabolism*
  • Chemokine CCL21 / metabolism*
  • Hot Temperature / adverse effects
  • Hyperalgesia / chemically induced
  • Hyperalgesia / metabolism*
  • Male
  • Physical Stimulation / adverse effects
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, CXCR3 / metabolism*
  • Remifentanil / toxicity*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism*

Substances

  • Analgesics, Opioid
  • Chemokine CCL21
  • Cxcr3 protein, rat
  • Receptors, CXCR3
  • Caspase 6
  • Remifentanil