Pre-treatment with amitriptyline causes epigenetic up-regulation of neuroprotection-associated genes and has anti-apoptotic effects in mouse neuronal cells

Neurotoxicol Teratol. 2017 Jul:62:1-12. doi: 10.1016/j.ntt.2017.05.002. Epub 2017 May 13.

Abstract

Antidepressants, such as imipramine and fluoxetine, are known to alter gene expression patterns by inducing changes in the epigenetic status of neuronal cells. There is also some evidence for the anti-apoptotic effect of various groups of antidepressants; however, this effect is complicated and cell-type dependent. Antidepressants of the tricyclic group, in particular amitriptyline, have been suggested to be beneficial in the treatment of neurodegenerative disorders. We examined whether amitriptyline exerts an anti-apoptotic effect via epigenetic mechanisms. Using DNA microarray, we analyzed global gene expression in mouse primary cultured neocortical neurons after treatment with amitriptyline and imipramine. The neuroprotection-associated genes, activating transcription factor 3 (Atf3) and heme oxygenase 1 (Hmox1), were up-regulated at both mRNA and protein levels by treatment with amitriptyline. Quantitative chromatin immunoprecipitation assay revealed that amitriptyline increased enrichments of trimethylation of histone H3 lysine 4 in the promoter regions of Atf3 and Hmox1 and acetylation of histone H3 lysine 9 in the promoter regions of Atf3, which indicate an active epigenetic status. Amitriptyline pre-treatment attenuated 1-methyl-4-phenylpyridinium ion (MPP+)- or amyloid β peptide 1-42 (Aβ1-42)-induced neuronal cell death and inhibited the activation of extracellular signal-regulated kinase 1 and 2 (ERK1/2). We found that Atf3 and Hmox1 were also up-regulated after Aβ1-42 treatment, and were further increased when pre-treated with amitriptyline. Interestingly, the highest up-regulation of Atf3 and Hmox1, at least at mRNA level, was observed after co-treatment with Aβ1-42 and amitriptyline, together with the loss of the neuroprotective effect. These findings suggest preconditioning and neuroprotective effects of amitriptyline; however, further investigations are needed for clarifying the contribution of epigenetic up-regulation of Atf3 and Hmox1 genes.

Keywords: Amitriptyline; Antidepressant; Epigenetic modification; Neurodegenerative disorder; Neuroprotection.

MeSH terms

  • Activating Transcription Factor 3 / metabolism
  • Amitriptyline / administration & dosage*
  • Animals
  • Antidepressive Agents, Tricyclic / administration & dosage*
  • Apoptosis / drug effects*
  • Cell Survival / drug effects
  • Epigenesis, Genetic / drug effects*
  • Heme Oxygenase-1 / metabolism
  • Histones / metabolism
  • Membrane Proteins / metabolism
  • Mice
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Neocortex / drug effects
  • Neocortex / metabolism
  • Neurons / drug effects*
  • Neurons / metabolism
  • Neuroprotective Agents / administration & dosage*
  • Primary Cell Culture
  • RNA, Messenger / metabolism
  • Up-Regulation*

Substances

  • Activating Transcription Factor 3
  • Antidepressive Agents, Tricyclic
  • Atf3 protein, mouse
  • Histones
  • Membrane Proteins
  • Neuroprotective Agents
  • RNA, Messenger
  • Amitriptyline
  • Heme Oxygenase-1
  • Hmox1 protein, mouse
  • Mapk1 protein, mouse
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3