Prenatal nutritional deficiency reprogrammed postnatal gene expression in mammal brains: implications for schizophrenia

Int J Neuropsychopharmacol. 2014 Oct 31;18(4):pyu054. doi: 10.1093/ijnp/pyu054.

Abstract

Background: Epidemiological studies have identified prenatal exposure to famine as a risk factor for schizophrenia, and animal models of prenatal malnutrition display structural and functional brain abnormalities implicated in schizophrenia.

Methods: The offspring of the RLP50 rat, a recently developed animal model of prenatal famine malnutrition exposure, was used to investigate the changes of gene expression and epigenetic modifications in the brain regions. Microarray gene expression analysis was carried out in the prefrontal cortex and the hippocampus from 8 RLP50 offspring rats and 8 controls. MBD-seq was used to test the changes in DNA methylation in hippocampus depending on prenatal malnutrition exposure.

Results: In the prefrontal cortex, offspring of RLP50 exhibit differences in neurotransmitters and olfactory-associated gene expression. In the hippocampus, the differentially-expressed genes are related to synaptic function and transcription regulation. DNA methylome profiling of the hippocampus also shows widespread but systematic epigenetic changes; in most cases (87%) this involves hypermethylation. Remarkably, genes encoded for the plasma membrane are significantly enriched for changes in both gene expression and DNA methylome profiling screens (p = 2.37×10(-9) and 5.36×10(-9), respectively). Interestingly, Mecp2 and Slc2a1, two genes associated with cognitive impairment, show significant down-regulation, and Slc2a1 is hypermethylated in the hippocampus of the RLP50 offspring.

Conclusions: Collectively, our results indicate that prenatal exposure to malnutrition leads to the reprogramming of postnatal brain gene expression and that the epigenetic modifications contribute to the reprogramming. The process may impair learning and memory ability and result in higher susceptibility to schizophrenia.

Keywords: DNA methylation; hippocampus; prefrontal cortex; schizophrenia; transcriptome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • DNA Methylation
  • Disease Models, Animal
  • Disease Susceptibility
  • Epigenesis, Genetic
  • Female
  • Gene Expression / physiology*
  • Glucose Transporter Type 1 / genetics
  • Glucose Transporter Type 1 / metabolism
  • Hippocampus / metabolism*
  • Methyl-CpG-Binding Protein 2 / genetics
  • Methyl-CpG-Binding Protein 2 / metabolism
  • Microarray Analysis
  • Phenotype
  • Prefrontal Cortex / metabolism*
  • Pregnancy
  • Prenatal Exposure Delayed Effects*
  • Prenatal Nutritional Physiological Phenomena*
  • Rats, Sprague-Dawley
  • Schizophrenia
  • Starvation / physiopathology*

Substances

  • Glucose Transporter Type 1
  • Mecp2 protein, rat
  • Methyl-CpG-Binding Protein 2
  • Slc2a1 protein, rat