Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala

Cao, Jinyan; Rebuli, Meghan E.; Rogers, James; Todd, Karina L.; Leyrer, Stephanie M.; Ferguson, Sherry A.; Patisaul, Heather B.

doi:10.1093/toxsci/kft035

Cited by 141Effects and risks of endocrine disrupting chemicalsSexual Differentiation and DisordersEstrogen and related hormone effects

Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala

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Cao, Jinyan, Rebuli, Meghan E., Rogers, James, Todd, Karina L., Leyrer, Stephanie M., Ferguson, Sherry A., Patisaul, Heather B.·2013·Toxicological Sciences

DOI 10.1093/toxsci/kft035PMC PMC3627558

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Abstract

Bisphenol A (BPA) exposure is ubiquitous, and in laboratory animals, early-life BPA exposure has been shown to alter sex-specific neural organization, neuroendocrine physiology, and behavior. The specific mechanisms underlying these brain-related outcomes, however, remain largely unknown, constraining the capacity to ascertain the potential human relevance of neural effects observed in animal models. In the perinatal rat brain, estrogen is masculinizing, suggesting that BPA-induced perturbation of estrogen receptor (ESR) expression may underpin later in-life neuroendocrine effects. We hypothesized that prenatal BPA exposure alters sex-specific ESR1 (ERα) and ESR2 (ERβ) expression in postnatal limbic nuclei. Sprague Dawley rats were mated and gavaged on gestational days (GDs) 6-21 with vehicle, 2.5 or 25 μg/kg bw/day BPA, or 5 or 10 μg/kg bw/day ethinyl estradiol. An additional group was restrained but not gavaged (naïve control). Offspring were sacrificed the day after birth to quantify ESR gene expression throughout the hypothalamus and amygdala by in situ hybridization. Relative to the vehicle group, significant effects of BPA were observed on ESR1 and ESR2 expression throughout the mediobasal hypothalamus and amygdala in both sexes. Significant differences in ESR expression were also observed in the mediobasal hypothalamus and amygdala of the naïve control group compared with the vehicle group, highlighting the potential for gavage to influence gene expression in the developing brain. These results indicate that ESR expression in the neonatal brain of both sexes can be altered by low-dose prenatal BPA exposure.

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Developmental exposure to doses as low as 2.5 μg/kg bw sex specifically alters the mRNA expression of ERα and ERβ in sexually dimorphic hypothalamic and limbic subnuclei in the neonatal and older rat brain.
“For example, we have repeatedly shown that developmental exposure to doses as low as 2.5 µg/kg bw sex specifically alters the mRNA expression of ERα and ERβ in sexually dimorphic hypothalamic and limbic subnuclei in the neonatal and older rat brain (86–90).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [86]
The ESR1 results report changes at the BPA 2.5 dose in neonatal hypothalamic and amygdaloid regions, with some effects differing by sex; the paper also reports ESR2 changes. But the Discussion says that whether the limbic expression changes persist beyond the neonatal period remained under study, so this source does not establish the claim for older rat brains. It also cautions that prenatal exposure generally did not significantly alter sex differences in receptor expression. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Developmental BPA exposure can perturb ERα and ERβ gene expression throughout the rat hypothalamus and components of the mesolimbic dopamine system, including the PVN and BnST, across the lifespan.
“We have repeatedly shown that developmental BPA exposure can perturb ERα and ERβ gene expression throughout the rat hypothalamus and components of the mesolimbic dopamine system, including the PVN and BnST (86–90), across the lifespan.”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [86]
The Abstract and Results report that prenatal BPA exposure altered ESR1 (ERα) and ESR2 (ERβ) expression in specific hypothalamic and amygdaloid regions of neonatal rats. The Image analysis and film quantification section lists the regions studied, which do not include the PVN or BnST. The paper measured offspring shortly after birth; its Discussion says the potential long-term effects remain unclear, so it does not establish altered expression across the lifespan. (LLM, conf=0.88)
Experimental — accuracy not yet measured
An earlier study of siblings of the subjects of the current study described differences in the naïve and vehicle control groups.
“This became potentially relevant because an earlier study of siblings of the subjects of the current study described differences in the naïve and vehicle control groups (Cao et al., 2013).”
From Developmental Treatment with Ethinyl Estradiol, but Not Bisphenol A, Causes Alterations in Sexually Dimorphic Behaviors in Male and Female Sprague Dawley Rats (2014) · cites this paper as Cao et al., 2013

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Prenatal Bisphenol A (BPA) Exposure Alters Sex Specific Estrogen Receptor Expression in the Neonatal Rat Hypothalamus and Amygdala
Words, K., Toxicology, D., Sciences, T., & Patisaul, H. B. (2013)
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Investigation of the effects of subchronic low dose oral exposure to bisphenol A (BPA) and ethinyl estradiol (EE) on estrogen receptor expression in the juvenile and adult female rat hypothalamus
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Sex-specific Esr2 mRNA expression in the rat hypothalamus and amygdala is altered by neonatal bisphenol A exposure
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Neonatal bisphenol A exposure alters sexually dimorphic gene expression in the postnatal rat hypothalamus
Cao, J., Mickens, J. A., McCaffrey, K. A., Leyrer, S. M., & Patisaul, H. B. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2011.11.002 · Cited by 102 · see citing works
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Authors: Cao, J., Rebuli, M. E., Rogers, J., Todd, K. L., Leyrer, S. M., Ferguson, S. A., & Patisaul, H. B.
Affiliations: North Carolina State University (US)
National Center for Toxicological Research (US)
ORCID: Cao, Jinyan
Rebuli, Meghan E.
Ferguson, Sherry A.
Patisaul, Heather B.
Venue: Toxicological Sciences
Publisher: Oxford University Press (OUP)
Published: 2013-03-01
Volume: 133
Issue: 1
Pages: 157-173
ISSN: 1096-0929 (ISSN-L)
1096-6080
DOI: 10.1093/toxsci/kft035
PMC: PMC3627558
OpenAlex: W2124972415
Cited by: 141
References: 104
Citations by year: 2026: 4 · 2025: 1 · 2023: 7 · 2022: 5 · 2021: 9 · 2020: 12 · 2019: 13 · 2018: 15 · 2017: 11 · 2016: 12 · 2015: 28 · 2014: 15 · 2013: 9
FWCI: 15.68
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Toxicological Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HighWire Press Open Archive (submittedVersion)
Funders: North Carolina State University
U.S. Public Health Service (R01-16001-04S1)
National Institute of Environmental Health Sciences (R01ES016001)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords: bisphenol A, estrogen receptor alpha, estrogen receptor beta, sex differences, hypothalamus, amygdala, neonatal brain development, masculinization, ethinyl estradiol, endocrine disruptors, limbic system
MeSH terms: Bisphenol A Compounds, Amygdala, Animals, Animals, Newborn, Benzhydryl Compounds, Dose-Response Relationship, Drug, Female, Hypothalamus, Male, Phenols, Pregnancy, Prenatal Exposure Delayed Effects, Receptors, Estrogen, Sex Factors, Rats, Sprague-Dawley, Gene Expression Regulation, Developmental, Estrogen Receptor alpha, Estrogen Receptor beta, Rats, Endocrine Disruptors

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Prenatal bisphenol A exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala

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