Developmental Exposure to Estradiol and Bisphenol A Increases Susceptibility to Prostate Carcinogenesis and Epigenetically Regulates Phosphodiesterase Type 4 Variant 4
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Abstract
Early developmental perturbations have been linked to adult-onset prostate pathology, including excessive exposure to estrogenic compounds; however, the molecular basis for this imprinting event is not known. An important and controversial health concern is whether low-dose exposures to hormonally active environmental estrogens, such as bisphenol A, can promote human diseases, including prostate cancer. Here, we show that transient developmental exposure of rats to low, environmentally relevant doses of bisphenol A or estradiol increases prostate gland susceptibility to adult-onset precancerous lesions and hormonal carcinogenesis. We found permanent alterations in the DNA methylation patterns of multiple cell signaling genes, suggesting an epigenetic basis for estrogen imprinting. For phosphodiesterase type 4 variant 4 (PDE4D4), an enzyme responsible for cyclic AMP breakdown, a specific methylation cluster was identified in the 5′-flanking CpG island that was gradually hypermethylated with aging in normal prostates, resulting in loss of gene expression. Early and prolonged hypomethylation at this site following neonatal estradiol or bisphenol A exposure resulted in continued, elevated PDE4D4 expression. Cell line studies confirmed that site-specific methylation is involved in transcriptional silencing of the PDE4D4 gene and showed hypomethylation of this gene in prostate cancer cells. Importantly, the PDE4D4 alterations in the estrogen-exposed prostates were distinguishable before histopathologic changes of the gland, making PDE4D4 a candidate molecular marker for prostate cancer risk assessment as a result of endocrine disruptors. In total, these findings indicate that low-dose exposures to ubiquitous environmental estrogens affect the prostate epigenome during development and, in so doing, promote prostate disease with aging. (Cancer Res 2006; 66(11): 5624-32)
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Epigenetic alterations have been implicated in BPA-associated changes in pathology and function in several hormone-responsive tissues including the brain.
“Epigenetic alterations have been implicated in BPA-associated changes in pathology and function in several hormone-responsive tissues including the brain [ 49 , 130 , 138–141 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [138]
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- Authors
- Ho, S.-M., Tang, W.-Y., Belmonte de Frausto, J., & Prins, G. S.
- Affiliations
- University of Cincinnati (US)
- 2Department of Urology, University of Illinois at Chicago, Chicago, Illinois
- University of Illinois Chicago (US)
- Venue
- Cancer Research
- Published
- 2006-06-01
- Volume
- 66
- Issue
- 11
- Pages
- 5624-5632
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- PMC
- PMC2276876
- OpenAlex
- W1994048261
- Cited by
- 796
- References
- 53
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 21 · 2023: 22 · 2022: 21 · 2021: 36 · 2020: 24 · 2019: 34 · 2018: 30 · 2017: 44 · 2016: 47 · 2015: 65 · 2014: 38 · 2013: 67 · 2012: 63
- FWCI
- 20.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- University of Illinois at Chicago
- National Institute of Diabetes and Digestive and Kidney Diseases (DK 40890, R01DK040890)
- National Institute of Environmental Health Sciences (ES12281, P30ES006096, R21ES012281, R01ES015584)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Prostate Cancer Treatment and Research
- Keywords
- bisphenol A, estradiol, early life exposure, prostate cancer, epigenetic regulation, DNA methylation, endocrine disruptors, precancerous lesions, transcriptional silencing, CpG island hypomethylation, aging
- MeSH terms
- Bisphenol A Compounds, Animals, Animals, Newborn, Benzhydryl Compounds, Dose-Response Relationship, Drug, Estradiol, Female, Isoenzymes, Male, Phenols, Precancerous Conditions, Pregnancy, Prostate, Prostatic Neoplasms, 3',5'-Cyclic-AMP Phosphodiesterases, Rats, Sprague-Dawley, Genomic Imprinting, DNA Methylation, Genetic Predisposition to Disease, Epigenesis, Genetic, Rats, Cyclic Nucleotide Phosphodiesterases, Type 4
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