The HDAC1/c-JUN complex is essential in the promotion of nerve injury-induced neuropathic pain through JNK signaling

Eur J Pharmacol. 2018 Apr 15:825:99-106. doi: 10.1016/j.ejphar.2018.02.034.

Abstract

Histone deacetylase inhibitors (HDACIs) interfere with the epigenetic process of histone acetylation and are known to have analgesic properties in models of chronic inflammatory pain. Administration of a selective HDAC1 inhibitor (LG325) in SNI-subjected mice significantly attenuated behavior related to injury-induced pain. Understanding the HDAC1 pathway in epigenetic regulation of pathological pain is of great medical relevance. Spared nerve injury (SNI) mice showed a significant increase in the HDAC1 protein levels within spinal cord in coincidence with the nociceptive phenotype at 1 and 3 weeks after nerve injury. No variation in HDAC3, DNMT3a, AcH3, MBD3 and MeCP2 levels was detected. Increased expression of HDAC1 is accompanied by activation of the JNK-c-Jun signaling pathway. A robust spinal JNK-1 overphosphorylation was observed post nerve-injury along with a selective JNK-dependent increase in p-c-Jun and HDAC1 protein levels. Co-immunoprecipitation experiments showed the presence of a heterodimeric complex between HDAC1 and c-Jun in SNI mice indicating that these transcription factors can act together to regulate transcription through heterodimerization. Stimulation of c-Jun phosphorylation was prevented by the selective HDAC1 inhibitor LG325. We found that HDAC1 was associated with c-Jun in nuclei of spinal dorsal horn astrocytes expressing JNK. On the other hand, the presence of HDAC1 and c-Jun interaction was not detected in control mice. These findings provide new insights into the mechanisms underlying the anti-nociceptive activity of HDAC inhibitors. Taken together, these data support a role for histone deacetylase in the emergence of neuropathic pain.

Keywords: HDAC1; JNK; Nerve injury; Neuropathic pain; cJun.

MeSH terms

  • Analgesics / pharmacology
  • Animals
  • Astrocytes / drug effects
  • Astrocytes / metabolism
  • Chronic Pain / drug therapy
  • Chronic Pain / metabolism
  • Histone Deacetylase 1 / metabolism*
  • MAP Kinase Signaling System / drug effects
  • MAP Kinase Signaling System / physiology*
  • Male
  • Mice
  • Nervous System Diseases / drug therapy
  • Nervous System Diseases / metabolism*
  • Neuralgia / drug therapy
  • Neuralgia / metabolism*
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Proto-Oncogene Proteins c-jun / metabolism*
  • Spinal Cord / drug effects
  • Spinal Cord / metabolism
  • Spinal Cord Dorsal Horn / drug effects
  • Spinal Cord Dorsal Horn / metabolism
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / physiology

Substances

  • Analgesics
  • Proto-Oncogene Proteins c-jun
  • Hdac1 protein, mouse
  • Histone Deacetylase 1