Prenatal cocaine exposure impairs cognitive function of progeny via insulin growth factor II epigenetic regulation

Neurobiol Dis. 2015 Oct:82:54-65. doi: 10.1016/j.nbd.2015.05.014. Epub 2015 Jun 6.

Abstract

Studies have showed that prenatal cocaine exposure (PCOC) can impair cognitive function and social behavior of the offspring; however, the mechanism underlying such effect is poorly understood. Insulin-like growth factor II (Igf-II), an imprinted gene, has a critical role in memory consolidation and enhancement. We hypothesized that epigenetic regulation of hippocampal Igf-II may attribute to the cognitive deficits of PCOC offspring. We used Morris water maze and open-field task to test the cognitive function in PCOC offspring. The epigenetic alteration involved in hippocampal Igf-II expression deficit in PCOC offspring was studied by determining Igf-II methylation status, DNA methyltransferases (DNMT) expressions and L-methionine level. Moreover, IGF-II rescue experiments were performed and the downstream signalings were investigated in PCOC offspring. In behavioral tests, we observed impaired spatial learning and memory and increased anxiety in PCOC offspring; moreover, hippocampal IGF-II mRNA and protein expressions were significantly decreased. Hippocampal methylation of cytosine-phospho-guanine (CpG) dinucleotides in differentially methylated region (DMR) 2 of Igf-II was elevated in PCOC offspring, which may be driven by the upregulation of L-methionine and DNA methyltransferase (DNMT) 1. Importantly, intra-hippocampal injection of recombinant IGF-II reactivated the repressed calcium calmodulin kinase II α (CaMKIIα) and reversed cognitive deficits in PCOC offspring. Collectively, our findings suggest that cocaine exposure during pregnancy impairs cognitive function of offspring through epigenetic modification of Igf-II gene. Enhancing IGF-II signaling may represent a novel therapeutical strategy for cocaine-induced cognitive impairment.

Keywords: CaMKIIα; Cognitive function; DNA methylation; DNMTs; IGF-II; Prenatal cocaine exposure; l-Methionine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2 / metabolism
  • Cocaine / pharmacology*
  • Cognition / drug effects*
  • Cognition / physiology
  • DNA Methylation / drug effects
  • Epigenesis, Genetic*
  • Female
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Insulin-Like Growth Factor II / genetics*
  • Insulin-Like Growth Factor II / metabolism
  • Insulin-Like Growth Factor II / pharmacology
  • Maze Learning / drug effects
  • Maze Learning / physiology
  • Mice
  • Phosphorylation
  • Pregnancy
  • Prenatal Exposure Delayed Effects / genetics*
  • Prenatal Exposure Delayed Effects / metabolism
  • Prenatal Exposure Delayed Effects / psychology

Substances

  • Insulin-Like Growth Factor II
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Cocaine