Increased cocaine-induced conditioned place preference during periadolescence in maternally separated male BALB/c mice: the role of cortical BDNF, microRNA-212, and MeCP2

Psychopharmacology (Berl). 2016 Sep;233(17):3279-88. doi: 10.1007/s00213-016-4373-z. Epub 2016 Jul 9.

Abstract

Rationale: Early life stress is a major risk factor for cocaine addiction; however, the underlying molecular mechanisms remain relatively unexplored. MicroRNA-212 (miR-212) and methyl CpG binding protein 2 (MeCP2) have recently emerged as key regulators of brain-derived neurotrophic factor (BDNF) signaling during the acquisition and maintenance of cocaine-seeking behaviors.

Objectives: We therefore investigated the effect of maternal separation (MS) on cocaine-induced conditioned place preference (CPP) during periadolescence and how this influences miR-212, Mecp2, and Bdnf expressions in the prefrontal cortex.

Methods: Male BALB/c mice subjected to MS (3 h/day) from postnatal day 2 to 15 or normal animal facility rearing (AFR) were tested for CPP at postnatal day 45, or not exposed to experimental manipulations (drug-naïve animals). Cultured primary cortical neurons were used to determine miR-212 expression changes following depolarization by KCL treatment.

Results: MS increased cocaine-induced CPP and decreased Bdnf exon IV expression, which correlated with higher CPP scores in such animals. An experience-dependent decrease in miR-212 expression was observed following CPP test. This effect was mimicked in primary cortical neurons in vitro, under activity-dependent conditions. In contrast, increased Mecp2 expression was found after CPP test, suggesting an opposing relationship between miR-212 and Mecp2 expression following cocaine place preference acquisition. However, these effects were not present in mice exposed to MS.

Conclusions: Together, our results suggest that early life stress can enhance the motivational salience for cocaine-paired cues during periadolescence, and that altered expression of miR-212, Mecp2, and Bdnf in the prefrontal cortex is involved in this process.

Keywords: Adolescence; Brain-derived neurotrophic factor; Cocaine; Conditioned place preference; Maternal separation; microRNAs.

MeSH terms

  • Animals
  • Brain-Derived Neurotrophic Factor / drug effects
  • Brain-Derived Neurotrophic Factor / genetics*
  • Cocaine / pharmacology*
  • Cocaine-Related Disorders
  • Conditioning, Classical / drug effects*
  • Dopamine Uptake Inhibitors / pharmacology*
  • Male
  • Maternal Deprivation*
  • Methyl-CpG-Binding Protein 2 / drug effects
  • Methyl-CpG-Binding Protein 2 / genetics*
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs / drug effects
  • MicroRNAs / metabolism*
  • Prefrontal Cortex / drug effects
  • Prefrontal Cortex / metabolism*

Substances

  • Brain-Derived Neurotrophic Factor
  • Dopamine Uptake Inhibitors
  • MIRN212 microRNA, mouse
  • Mecp2 protein, mouse
  • Methyl-CpG-Binding Protein 2
  • MicroRNAs
  • Cocaine