Maternal deprivation causes CaMKII downregulation and modulates glutamate, norepinephrine and serotonin in limbic brain areas in a rat model of single prolonged stress

J Affect Disord. 2024 Mar 15:349:286-296. doi: 10.1016/j.jad.2024.01.087. Epub 2024 Jan 9.

Abstract

Background: Early life stress is a major risk factor for later development of psychiatric disorders, including post-traumatic stress disorder (PTSD). An intricate relationship exists between various neurotransmitters (such as glutamate, norepinephrine or serotonin), calcium/calmodulin-dependent protein kinase II (CaMKII), as an important regulator of glutamatergic synaptic function, and PTSD. Here, we developed a double-hit model to investigate the interaction of maternal deprivation (MD) as an early life stress model and single prolonged stress (SPS) as a PTSD model at the behavioral and molecular levels.

Methods: Male Wistar rats exposed to these stress paradigms were subjected to a comprehensive behavioral analysis. In hippocampal synaptosomes we investigated neurotransmitter release and glutamate concentration. The expression of CaMKII and the content of monoamines were determined in selected brain regions. Brain-derived neurotrophic factor (BDNF) mRNA was quantified by radioactive in situ hybridization.

Results: We report a distinct behavioral phenotype in the double-hit group. Double-hit and SPS groups had decreased hippocampal presynaptic glutamatergic function. In hippocampus, double-hit stress caused a decrease in autophosphorylation of CaMKII. In prefrontal cortex, both SPS and double-hit stress had a similar effect on CaMKII autophosphorylation. Double-hit stress, rather than SPS, affected the norepinephrine and serotonin levels in prefrontal cortex, and suppressed BDNF gene expression in prefrontal cortex and hippocampus.

Limitations: The study was conducted in male rats only. The affected brain regions cannot be restricted to hippocampus, prefrontal cortex and amygdala.

Conclusion: Double-hit stress caused more pronounced and distinct behavioral, molecular and functional changes, compared to MD or SPS alone.

Keywords: CaMKII; Double-hit stress; Glutamate release; Maternal deprivation; Post-traumatic stress disorder; Single prolonged stress.

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain-Derived Neurotrophic Factor / genetics
  • Brain-Derived Neurotrophic Factor / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / genetics
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / pharmacology
  • Disease Models, Animal
  • Down-Regulation
  • Glutamic Acid / metabolism
  • Hippocampus / metabolism
  • Humans
  • Male
  • Maternal Deprivation
  • Norepinephrine
  • Rats
  • Rats, Wistar
  • Serotonin* / metabolism
  • Stress Disorders, Post-Traumatic* / genetics

Substances

  • Serotonin
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Brain-Derived Neurotrophic Factor
  • Glutamic Acid
  • Norepinephrine