Nrf2 Activation Attenuates Chronic Constriction Injury-Induced Neuropathic Pain via Induction of PGC-1 α-Mediated Mitochondrial Biogenesis in the Spinal Cord

Oxid Med Cell Longev. 2021 Oct 21:2021:9577874. doi: 10.1155/2021/9577874. eCollection 2021.

Abstract

Background: Neuropathic pain is a debilitating disease with few effective treatments. Emerging evidence indicates the involvement of mitochondrial dysfunction and oxidative stress in neuropathic pain. Nuclear factor erythroid 2-related factor 2 (Nrf2) is a potent regulator of the antioxidant response system. In this study, we investigated whether RTA-408 (RTA, a novel synthetic triterpenoid under clinical investigation) could activate Nrf2 and promote mitochondrial biogenesis (MB) to reverse neuropathic pain and the underlying mechanisms.

Methods: Neuropathic pain was induced by chronic constriction injury (CCI) of the sciatic nerve. Pain behaviors were measured via the von Frey test and Hargreaves plantar test. The L4-6 spinal cord was collected to examine the activation of Nrf2 and MB.

Results: RTA-408 treatment significantly reversed mechanical allodynia and thermal hyperalgesia in CCI mice in a dose-dependent manner. Furthermore, RTA-408 increased the activity of Nrf2 and significantly restored MB that was impaired in CCI mice in an Nrf2-dependent manner. Peroxisome proliferator-activated receptor-gamma coactivator-1alpha (PGC-1α) is the key regulator of MB. We found that the PGC-1α activator also induced a potent analgesic effect in CCI mice. Moreover, the antinociceptive effect of RTA-408 was reversed by the preinjection of the PGC-1α inhibitor.

Conclusions: Nrf2 activation attenuates chronic constriction injury-induced neuropathic pain via induction of PGC-1α-mediated mitochondrial biogenesis in the spinal cord. Our results indicate that Nrf2 may be a potential therapeutic strategy to ameliorate neuropathic pain and many other disorders with oxidative stress and mitochondrial dysfunction.

MeSH terms

  • Analgesics / pharmacology*
  • Animals
  • Chronic Disease
  • Constriction, Pathologic
  • Disease Models, Animal
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • NF-E2-Related Factor 2 / agonists*
  • NF-E2-Related Factor 2 / metabolism
  • Neuralgia / metabolism
  • Neuralgia / pathology
  • Neuralgia / physiopathology
  • Neuralgia / prevention & control*
  • Organelle Biogenesis*
  • Pain Threshold / drug effects
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / metabolism*
  • Sciatic Neuropathy / drug therapy*
  • Sciatic Neuropathy / metabolism
  • Sciatic Neuropathy / pathology
  • Sciatic Neuropathy / physiopathology
  • Signal Transduction
  • Spinal Cord / drug effects*
  • Spinal Cord / metabolism
  • Spinal Cord / pathology
  • Spinal Cord / physiopathology
  • Triterpenes / pharmacology*

Substances

  • Analgesics
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, rat
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, rat
  • Triterpenes
  • omaveloxolone