Targeting histone deacetylation for recovery of maternal deprivation-induced changes in BDNF and AKAP150 expression in the VTA

Exp Neurol. 2018 Nov:309:160-168. doi: 10.1016/j.expneurol.2018.08.002. Epub 2018 Aug 10.

Abstract

Severe early life stressors increase the probability of developing psychiatric disorders later in life through modifications in neuronal circuits controlling brain monoaminergic signaling. Our previous work demonstrated that 24 h maternal deprivation (MD) in male Sprague Dawley rats modifies dopamine (DA) signaling from the ventral tegmental area (VTA) through changes at GABAergic synapses that were reversible by in vitro histone deacetylase (HDAC) inhibition which led to restoration of the scaffold A-kinase anchoring protein (AKAP150) signaling and subsequently recovered GABAergic plasticity (Authement et al., 2015). Using a combination of in situ hybridization, Western blots and immunohistochemistry, we confirmed that MD-induced epigenetic modifications at the level of histone acetylation were associated with an upregulation of HDAC2. MD also increased Akap5 mRNA levels in the VTA. Western blot analysis of AKAP150 protein expression showed an increase in synaptic levels of AKAP150 protein in the VTA with an accompanying decrease in synaptic levels of protein kinase A (PKA). Moreover, the abundance of mature brain-derived neurotrophic factor (BDNF) protein of VTA tissues from MD rats was significantly lower than in control groups. In vivo systemic injection with a selective class I HDAC inhibitor (CI-994) was sufficient to reverse MD-induced histone hypoacetylation in the VTA for 24 h after the injection. Furthermore, HDAC inhibition normalized the levels of mBDNF and AKAP150 proteins at 24 h. Our data suggest that HDAC-mediated targeting of BDNF and AKAP-dependent local signaling within VTA could provide novel therapeutics for prevention of later-life psychopathology.

Keywords: A-kinase anchoring protein (AKAP); Brain derived neurotrophic factor (BDNF); Dopamine; Early life stress; Epigenetics; Histone acetylation; Histone deacetylase (HDAC); Histone deacetylase inhibitor (HDAC inhibitor); Maternal deprivation (MD); Ventral tegmental area (VTA).

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • A Kinase Anchor Proteins / metabolism*
  • Acetylation / drug effects
  • Animals
  • Brain-Derived Neurotrophic Factor / metabolism*
  • Dopamine / metabolism
  • Enzyme Inhibitors / pharmacology
  • Gene Expression Regulation / physiology*
  • Histone Deacetylase 2 / genetics
  • Histone Deacetylase 2 / metabolism
  • Histones / metabolism*
  • In Vitro Techniques
  • Male
  • Maternal Deprivation*
  • RNA, Messenger / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Subcellular Fractions / drug effects
  • Subcellular Fractions / metabolism
  • Tyrosine 3-Monooxygenase / metabolism
  • Ventral Tegmental Area / drug effects
  • Ventral Tegmental Area / metabolism*

Substances

  • A Kinase Anchor Proteins
  • Akap5 protein, rat
  • Brain-Derived Neurotrophic Factor
  • Enzyme Inhibitors
  • Histones
  • RNA, Messenger
  • Tyrosine 3-Monooxygenase
  • Hdac2 protein, rat
  • Histone Deacetylase 2
  • Dopamine