Chronic Administration of Benzo(a)pyrene Induces Memory Impairment and Anxiety-Like Behavior and Increases of NR2B DNA Methylation

PLoS One. 2016 Feb 22;11(2):e0149574. doi: 10.1371/journal.pone.0149574. eCollection 2016.

Abstract

Background: Recently, an increasing number of human and animal studies have reported that exposure to benzo(a)pyrene (BaP) induces neurological abnormalities and is also associated with adverse effects, such as tumor formation, immunosuppression, teratogenicity, and hormonal disorders. However, the exact mechanisms underlying BaP-induced impairment of neurological function remain unclear. The aim of this study was to examine the regulating mechanisms underlying the impact of chronic BaP exposure on neurobehavioral performance.

Methods: C57BL mice received either BaP in different doses (1.0, 2.5, 6.25 mg/kg) or olive oil twice a week for 90 days. Memory and emotional behaviors were evaluated using Y-maze and open-field tests, respectively. Furthermore, levels of mRNA expression were measured by using qPCR, and DNA methylation of NMDA receptor 2B subunit (NR2B) was examined using bisulfate pyrosequencing in the prefrontal cortex and hippocampus.

Results: Compared to controls, mice that received BaP (2.5, 6.25 mg/kg) showed deficits in short-term memory and an anxiety-like behavior. These behavioral alterations were associated with a down-regulation of the NR2B gene and a concomitant increase in the level of DNA methylation in the NR2B promoter in the two brain regions.

Conclusions: Chronic BaP exposure induces an increase in DNA methylation in the NR2B gene promoter and down-regulates NR2B expression, which may contribute to its neurotoxic effects on behavioral performance. The results suggest that NR2B vulnerability represents a target for environmental toxicants in the brain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anxiety* / chemically induced
  • Anxiety* / metabolism
  • Anxiety* / pathology
  • Anxiety* / physiopathology
  • Behavior, Animal / drug effects*
  • Benzo(a)pyrene / toxicity*
  • DNA Methylation / drug effects*
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Hippocampus / physiopathology
  • Humans
  • Male
  • Memory Disorders* / chemically induced
  • Memory Disorders* / metabolism
  • Memory Disorders* / pathology
  • Memory Disorders* / physiopathology
  • Mice
  • Prefrontal Cortex / metabolism
  • Prefrontal Cortex / pathology
  • Prefrontal Cortex / physiopathology
  • Receptors, N-Methyl-D-Aspartate / metabolism*

Substances

  • NR2B NMDA receptor
  • Receptors, N-Methyl-D-Aspartate
  • Benzo(a)pyrene

Grants and funding

This work was supported by the Science and Technology Innovation Fund of Shanxi Medical University (Grant #2010-01201006 for Wenping Zhang) and the Shanxi Scholar Exchange Fund (Grant #2010-40 for Wenping Zhang) and Shanxi Scholarship Council of China (Grant #2015-051 For Mei Qiang). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.