Preconception paternal bisphenol A exposure induces sex-specific anxiety and depression behaviors in adult rats.

Ying Fan,Hui Zhang,Xianyue Zhen,Beibei Zhang,Jian Liu,Chong Tian,Shibin Ding,Nannan Wu,Qilin Liu,Maoshu Zhu,Liangneng Zhou,Xin Jin,Dongliang He,Yun Zhang,Taibiao Li,Anne Manyande,Judith Homberg

doi:10.1371/journal.pone.0192434

Abstract

Bisphenol A (BPA), an environmental endocrine-disrupting compound, has drawn a great attention for its adverse effect on behavioral development. Maternal exposure to this compound has been reported to induce anxiety and depression in offspring, but the effect of its paternal exposure is rarely discussed. This study investigated whether preconception paternal BPA exposure can affect the emotions of male rats and their offspring. Eighteen adult male rats (F0) received either a vehicle or 50 μg/kg/day BPA diet for 21 weeks and were then mated with non-exposed females to produce offspring (F1). The affective behaviors of F0 and F1 rats were evaluated in the open-field test, the elevated-plus maze and the forced swimming test, and their serum corticosterone were then examined. BPA exposure induced increased anxiety behaviors along with increased serum corticosterone in F0 rats. This paternal exposure also led to increased anxiety behaviors in F1 females and aggravated depression behaviors in both sexes of F1 rats. Furthermore, only F1 females exhibited increased serum corticosterone. Overall, these data indicate that preconception paternal exposure to a low dose of BPA may induce transgenerational sex-specific impairments in the affection of adult rats.

Highlights

To investigate the effect of Bisphenol A (BPA) on anxiety behaviors of F0 rats, we evaluated their performances in an open-field test (OFT) after 23 weeks of BPA exposure (n = 9, each)
To determine if BPA might change the serum corticosterone, we examined the tail blood sample from F0 rats one day before and about 30 min after OFT (n = 9, each)
As far as we know, this is the first study to investigate the effect of paternal BPA on affective behaviors in rats

Summary

Introduction

Bisphenol A (BPA), member of a class of endocrine disrupting chemicals (EDCs), has been widely used in food containers and packages for many years, and human beings are widely. Prenatal and early-life stage exposure to BPA have both been reported to induce adverse behavioral problems including hyperactivity, inattention, conduct problems and increased levels of anxiety and depression in children[8]. BPA exposure at low levels (below 50 μg/kg/day) has been reported to induce behavioral changes[9,10,11,12], cognitive deficits[13,14,15]and increased anxiety behavior[15]. Whether paternal exposure to a low dose of BPA can affect behavior remains unclear. We investigated the affective levels in F1 offspring to assess the consequences of paternal BPA exposure at a dose of 50 μg/kg/day. We analyzed the serum corticosterone, a key marker of hypothalamic–pituitary–adrenal (HPA) axis [19, 20], before and after the final behavioral test in order to gain further insight into the underlying mechanisms

Materials & methods

Results

Discussion