Astrocytic c-Jun N-terminal kinase-histone deacetylase-2 cascade contributes to glutamate transporter-1 decrease and mechanical allodynia following peripheral nerve injury in rats

Brain Res Bull. 2021 Oct:175:213-223. doi: 10.1016/j.brainresbull.2021.07.024. Epub 2021 Jul 29.

Abstract

Decrease of glutamate transporter-1 (GLT-1) in the spinal dorsal horn after nerve injury induces enhanced excitatory transmission and causes persistent pain. Histone deacetylases (HDACs)-catalyzed deacetylation might contribute to the decrease of GLT-1, while the detailed mechanisms have yet to be fully elaborated. Spinal nerve ligation (SNL) induced significant increases of HDAC2 and decreases of GLT-1 in spinal astrocytes. Intrathecal infusion of the HDAC2 inhibitors attenuated the decrease of GLT-1 and enhanced phosphorylation of glutamate receptors. GLT-1 and phosphorylated c-Jun N-terminal kinase (JNK) were highly colocalized in the spinal cord, and a large number of pJNK positive cells were HDAC2 positive. Intrathecally infusion of the JNK inhibitor SP600125 significantly inhibited SNL-induced upregulation of HDAC2. SNL-induced HDAC2 up-regulation could be inhibited by the neutralizing anti-tumor necrosis factor-α (TNF-α) binding protein etanercept or the microglial inhibitor minocycline. In cultured astrocytes, TNF-α induced enhanced phosphorylation of JNK and a significant increase of HDAC2, as well as a remarkable decrease of GLT-1, which could be prevented by SP600125 or the HDAC2 specific inhibitor CAY10683. Our data suggest that astrocytic JNK-HDAC2 cascade contributes to GLT-1 decrease and mechanical allodynia following peripheral nerve injury. Neuroimmune activation after peripheral nerve injury could induce epigenetic modification changes in astrocytes and contribute to chronic pain maintenance.

Keywords: Astrocytes; C-Jun N-terminal kinase; Glutamate transporter-1; Histone deacetylase; Neuropathic pain; Spinal cord.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anthracenes / pharmacology
  • Astrocytes / pathology*
  • Carbamates / pharmacology
  • Cells, Cultured
  • Etanercept / metabolism
  • Excitatory Amino Acid Transporter 2 / genetics*
  • Histone Deacetylase 2 / genetics*
  • Hyperalgesia / pathology*
  • JNK Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • JNK Mitogen-Activated Protein Kinases / genetics*
  • Male
  • Microglia / drug effects
  • Minocycline / pharmacology
  • Neuralgia / genetics
  • Neuralgia / pathology
  • Peripheral Nerve Injuries / genetics*
  • Peripheral Nerve Injuries / pathology*
  • Rats
  • Rats, Sprague-Dawley
  • Signal Transduction / genetics*
  • Spinal Nerves / injuries
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Anthracenes
  • Carbamates
  • Excitatory Amino Acid Transporter 2
  • Slc1a2 protein, mouse
  • Tumor Necrosis Factor-alpha
  • santacruzamate A
  • pyrazolanthrone
  • JNK Mitogen-Activated Protein Kinases
  • Hdac2 protein, rat
  • Histone Deacetylase 2
  • Minocycline
  • Etanercept