Somatostatin, neuronal vulnerability and behavioral emotionality

Mol Psychiatry. 2015 Mar;20(3):377-87. doi: 10.1038/mp.2014.184. Epub 2015 Jan 20.

Abstract

Somatostatin (SST) deficits are common pathological features in depression and other neurological disorders with mood disturbances, but little is known about the contribution of SST deficits to mood symptoms or causes of these deficits. Here we show that mice lacking SST (Sst(KO)) exhibit elevated behavioral emotionality, high basal plasma corticosterone and reduced gene expression of Bdnf, Cortistatin and Gad67, together recapitulating behavioral, neuroendocrine and molecular features of human depression. Studies in Sst(KO) and heterozygous (Sst(HZ)) mice show that elevated corticosterone is not sufficient to reproduce the behavioral phenotype, suggesting a putative role for Sst cell-specific molecular changes. Using laser capture microdissection, we show that cortical SST-positive interneurons display significantly greater transcriptome deregulations after chronic stress compared with pyramidal neurons. Protein translation through eukaryotic initiation factor 2 (EIF2) signaling, a pathway previously implicated in neurodegenerative diseases, was most affected and suppressed in stress-exposed SST neurons. We then show that activating EIF2 signaling through EIF2 kinase inhibition mitigated stress-induced behavioral emotionality in mice. Taken together, our data suggest that (1) low SST has a causal role in mood-related phenotypes, (2) deregulated EIF2-mediated protein translation may represent a mechanism for vulnerability of SST neurons and (3) that global EIF2 signaling has antidepressant/anxiolytic potential.

Publication types

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

MeSH terms

  • Adenine / analogs & derivatives
  • Adenine / pharmacology
  • Adenine / therapeutic use
  • Animals
  • Antidepressive Agents / pharmacology
  • Antidepressive Agents / therapeutic use
  • Brain-Derived Neurotrophic Factor / metabolism
  • Corticosterone / blood
  • Disease Models, Animal
  • Eukaryotic Initiation Factor-2 / metabolism
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / genetics
  • Glutamate Decarboxylase / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Gyrus Cinguli / pathology*
  • Indoles / pharmacology
  • Indoles / therapeutic use
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Mood Disorders / blood
  • Mood Disorders / etiology
  • Mood Disorders / genetics*
  • Mood Disorders / pathology*
  • Neurons / metabolism
  • Signal Transduction / genetics
  • Somatostatin / genetics
  • Somatostatin / metabolism*
  • Stress, Psychological / blood
  • Stress, Psychological / complications
  • Stress, Psychological / genetics
  • Transcriptome / genetics

Substances

  • 7-methyl-5-(1-((3-(trifluoromethyl)phenyl)acetyl)-2,3-dihydro-1H-indol-5-yl)-7H-pyrrolo(2,3-d)pyrimidin-4-amine
  • Antidepressive Agents
  • Brain-Derived Neurotrophic Factor
  • Eukaryotic Initiation Factor-2
  • Indoles
  • Green Fluorescent Proteins
  • Somatostatin
  • Glutamate Decarboxylase
  • glutamate decarboxylase 1
  • Adenine
  • Corticosterone