Inhibition of SIRT1 in hippocampal CA1 ameliorates PTSD-like behaviors in mice by protections of neuronal plasticity and serotonin homeostasis via NHLH2/MAO-A pathway

Biochem Biophys Res Commun. 2019 Oct 15;518(2):344-350. doi: 10.1016/j.bbrc.2019.08.060. Epub 2019 Aug 14.

Abstract

Hippocampal SIRT1 dysfunction and gene variation have previously been found potentially involved in depressive and anxiety disorders. However, the exact role of SIRT1 in post-traumatic stress disorder (PTSD) is not well understood. Here, we employed multiple genetic and pharmacological approaches targeting SIRT1 to verify the effects of SIRT1 on SPS-induced PTSD-like behaviors and its potential cellular and molecular mechanisms. We first demonstrated that Sirt1 knockout mice showed milder PTSD-like behavior after single prolonged stress (SPS) induction than wild type mice. Moreover, the expression of SIRT1 in the ventral CA1 (vCA1) region of hippocampus showed no significant changes following SPS induction, but the activity of SIRT1 enzyme was significantly increased post-SPS. Osmotic administration of EX527 in vCA1, a SIRT1 inhibitor, was shown to normalize the SIRT1 activity in SPS mice. Mechanically, EX527 rescued the acetylation of helix-loop-helix transcription factor 2 (NHLH2) and transcriptionally inhibited the increase of MAO-A expression in the vCA1, which thus suppressed the decomposition of the neurotransmitter serotonin into 5-hydroxydoleacetic acid (5-HIAA). Morphologically, Golgi staining showed that EX527 treatment improved the abnormal neuronal structure plasticity in the vCA1 region after SPS, including reversing the atrophic dendrites and the decreased dendritic spines. Finally, SIRT1 inhibitor effectively alleviated fear conditioning responses and anxiety-like behaviors. Our study first demonstrated that the development of PTSD-like behaviors was causatively related to the abnormal increase of SIRT1 activity in the ventral hippocampal CA1 region. And we also provided evidence that SIRT1 inhibition might exert therapeutic effects on PTSD by maintaining serotonin homeostasis through transcriptional inhibition of MAO-A, and thereby remodeled synaptic plasticity in the vCA1 region.

Keywords: MAO-A; NHLH2; PTSD; SIRT1; Ventral CA1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • CA1 Region, Hippocampal / drug effects
  • Carbazoles / therapeutic use*
  • Gene Deletion
  • Homeostasis / drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Monoamine Oxidase / metabolism
  • Neuronal Plasticity / drug effects*
  • Neuroprotective Agents / therapeutic use*
  • Serotonin / metabolism
  • Signal Transduction / drug effects
  • Sirtuin 1 / antagonists & inhibitors
  • Sirtuin 1 / genetics*
  • Sirtuin 1 / metabolism
  • Stress Disorders, Post-Traumatic / drug therapy*
  • Stress Disorders, Post-Traumatic / genetics*
  • Stress Disorders, Post-Traumatic / metabolism

Substances

  • 6-chloro-2,3,4,9-tetrahydro-1H-carbazole-1-carboxamide
  • Basic Helix-Loop-Helix Transcription Factors
  • Carbazoles
  • Neuroprotective Agents
  • Nhlh2 protein, mouse
  • Serotonin
  • Monoamine Oxidase
  • Sirtuin 1