Cited by 410Effects and risks of endocrine disrupting chemicalsEstrogen and related hormone effectsComputational Drug Discovery Methods

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Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes

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Delfosse, Vanessa, Grimaldi, Marina, Pons, Jean-Luc, Boulahtouf, Abdelhay, le Maire, Albane, Cavailles, Vincent, Labesse, Gilles, Bourguet, William, Balaguer, Patrick·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1203574109PMC PMC3443136

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Abstract

Bisphenol A (BPA) is an industrial compound and a well known endocrine-disrupting chemical with estrogenic activity. The widespread exposure of individuals to BPA is suspected to affect a variety of physiological functions, including reproduction, development, and metabolism. Here we report that the mechanisms by which BPA and two congeners, bisphenol AF and bisphenol C (BPC), bind to and activate estrogen receptors (ER) α and β differ from that used by 17β-estradiol. We show that bisphenols act as partial agonists of ERs by activating the N-terminal activation function 1 regardless of their effect on the C-terminal activation function 2, which ranges from weak agonism (with BPA) to antagonism (with BPC). Crystallographic analysis of the interaction between bisphenols and ERs reveals two discrete binding modes, reflecting the different activities of compounds on ERs. BPA and 17β-estradiol bind to ERs in a similar fashion, whereas, with a phenol ring pointing toward the activation helix H12, the orientation of BPC accounts for the marked antagonist character of this compound. Based on structural data, we developed a protocol for in silico evaluation of the interaction between bisphenols and ERs or other members of the nuclear hormone receptor family, such as estrogen-related receptor γ and androgen receptor, which are two known main targets of bisphenols. Overall, this study provides a wealth of tools and information that could be used for the development of BPA substitutes devoid of nuclear hormone receptor-mediated activity and more generally for environmental risk assessment.

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Result
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Background
Mechanisms of endocrine disruption through nuclear receptors and related pathways
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Background
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“Among them, BPA has been shown to bind the estrogen receptors (ERα and ERβ) (Delfosse et al., 2012), GPR30 (or GPER) (Pupo et al., 2012) and ERRγ with a high affinity (Liu et al., 2012).”
Background
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“Estrogen Binding Affinity Testing The agonistic and antagonistic potentials of bisphenols were analyzed following a literature method (Delfosse et al., 2012) in which ERα, PXR, and AR transcriptional activities were monitored by using corresponding reporter cells HELN ERα, U2OS AR, and HG5LN PXR cells, respectively.”
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Background
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BackgroundMethodInfluential
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Background
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“Delfosse et al. (2012) showed that the production of BPA exceeded 3 million tons per year.”
Background
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BackgroundMethod
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“5 μM) whereas other bisphenols such as BPC or HPTE display much better estrogenic potencies with EC50 values of ≈ 30 nM and 50 nM, respectively [47, 48].”
Background
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BackgroundMethodResultInfluential
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BackgroundInfluential
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Background
DABCO-catalyzed one-pot three component synthesis of dihydropyrano[3,2-c]chromene substituted quinazolines and their evaluation towards anticancer activity
Vodnala, S., Bhavani, A. K. D., Kamutam, R., Naidu, V. G. M., Promila, P., & Chetti, P. (2016) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2016.07.003 · Cited by 29
The Effect of Structural Diversity on Ligand Specificity and Resulting Signaling Differences of Estrogen Receptor α
Xue, Q., Liu, X., Liu, X., Pan, W., Fu, J., & Zhang, A. (2019) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.8b00338 · Cited by 29
The effects of bisphenol A and bisphenol S on adipokine expression and glucose metabolism in human adipose tissue
Ahmed, F., Sarsenbayeva, A., Katsogiannos, P., Aguer, C., & Pereira, M. J. (2020) · Toxicology · doi:10.1016/j.tox.2020.152600 · Cited by 29
“BPA is structurally similar to 17 β -estradiol (E2) and has been shown to have hormone-mimicking properties (Delfosse et al. 2012).”
Background
Activation of steroid hormone receptors: Shed light on the in silico evaluation of endocrine disrupting chemicals
Chen, Q., Tan, H., Yu, H., & Shi, W. F. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.03.003 · Cited by 28
Implication of environmental estrogens on breast cancer treatment and progression
Gonzalez, T. L., Rae, J. M., & Colacino, J. A. (2019) · Toxicology · doi:10.1016/j.tox.2019.03.014 · Cited by 28
“Several studies have provided evidence that BPA behaves as a weak estrogen and is able to bind to ERα (Delfosse et al., 2014; Delfosse et al., 2012).”
Background
Angiogenic Activity and Mechanism for Bisphenols on Endothelial Cell and Mouse: Evidence of a Structural-Selective Effect
Lu, L., Shen, L., Cui, S., Huang, Y., Gao, Y., Zhu, X., Lu, S., Zhang, C., & Zhuang, S. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c03883 · Cited by 27
Determination of bisphenol analogues in food-contact plastics using diode array detector, charged aerosol detector and evaporative light-scattering detector
Wang, H., Song, S., Shao, M., Gao, Y., Yang, C., Li, Y., Wang, W., He, Y., & Li, P. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.109778 · Cited by 27
Disparate toxicity mechanisms of parabens with different alkyl chain length in freshwater biofilms: Ecological hazards associated with antibiotic resistome
Liu, S., Wang, P., Wang, C., Chen, J., Wang, X., Hu, B., & Shan, X. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.163168 · Cited by 26
Neutrophils life under estrogenic and xenoestrogenic control
Nowak, K., Jabłońska, E., & Ratajczak–Wrona, W. (2018) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2018.10.015 · Cited by 26
Reporter cell lines to evaluate the selectivity of chemicals for human and zebrafish estrogen and peroxysome proliferator activated γ receptors
Grimaldi, M., Boulahtouf, A., Delfosse, V., Thouënnon, E., Bourguet, W., & Balaguer, P. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00212 · Cited by 25
“To gain structural insights into the zfERα selectivity of 16αLE2 in human and zebrafish ERs, we used the web-based server EDMon (Endocrine Disruptor Monitoring; http://atome2. cbs.cnrs.fr/AT2B/SERVER/EDMon.html) (Delfosse et al., 2012) to model zfERs in complex with this ligand.”
Method
Combined Effects of Nonylphenol and Bisphenol A on the Human Prostate Epithelial Cell Line RWPE-1
Gan, W., Zhou, M., Xiang, Z., Han, X., & Li, D. (2015) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph120404141 · Cited by 26
In silico discovery and validation of potent small-molecule inhibitors targeting the activation function 2 site of human oestrogen receptor α
Singh, K., Munuganti, R. S. N., Leblanc, E., Lin, Y. L., Leung, E. Y., Lallous, N., Butler, M. S., Cherkasov, A. R., & Rennie, P. S. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0529-8 · Cited by 26
“60 Å resolution) [41].”
Spatial and temporal distributions of bisphenol analogues in water and sediment from the Lanzhou section of the Yellow River, China
Zhao, X., Zhang, H., Chen, Z., Wang, X., & Shen, J. (2020) · Arabian Journal of Geosciences · doi:10.1007/s12517-020-06122-y · Cited by 25
Identification of Potential Bisphenol A (BPA) Exposure Biomarkers in Ovarian Cancer
Zahra, A., Dong, Q., Hall, M., Jeyaneethi, J., Silva, E. A., Karteris, E., & Sisu, C. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10091979 · Cited by 24
A PROSS-designed extensively mutated estrogen receptor α variant displays enhanced thermal stability while retaining native allosteric regulation and structure
Kriegel, M., Wiederanders, H. J., Alkhashrom, S., Eichler, J., & Muller, Y. A. (2021) · Scientific Reports · doi:10.1038/s41598-021-89785-1 · Cited by 25
Therapeutic effects of astragaloside IV and Astragalus spinosus saponins against bisphenol A-induced neurotoxicity and DNA damage in rats
Essawy, A. E., Elkader, H. A. E. A., Khamiss, O., Eweda, S. M., & Abdou, H. M. (2021) · PeerJ · doi:10.7717/peerj.11930 · Cited by 26
“This perturbation leading to massive proliferation and differentiation of neurons, producing endogenous estrogen, disruption in nuclear translocation of estrogen receptors (ER) and modifying the genetic and epigenetic programming (Chung et al., 2011; Delfosse et al., 2012; Kundakovic et al., 2013; Xu et al., 2014).”
Background
Estrogenicity of halogenated bisphenol A: in vitro and in silico investigations
Zhang, J., Li, T., Wang, T., Yuan, C., Zhong, S., Guan, T., Li, Z., Wang, Y., Yu, H., Luo, Q., et al. (2017) · Archives of Toxicology · doi:10.1007/s00204-017-2127-2 · Cited by 24
Bisphenol AF promotes estrogen receptor-positive breast cancer cell proliferation through amphiregulin-mediated crosstalk with receptor tyrosine kinase signaling
Zhao, Q., Howard, E. W., Parris, A. B., Ma, Z., Xing, Y., & Yang, X. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216469 · Cited by 24
Is There a Link between Bisphenol A (BPA), a Key Endocrine Disruptor, and the Risk for SARS-CoV-2 Infection and Severe COVID-19?
Zahra, A., Sisu, C., Silva, E. A., Greca, S.-C. D. A., Randeva, H. S., Chatha, K. K., Kyrou, I., & Karteris, E. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9103296 · Cited by 23
Knowledge Gap in Understanding the Steroidogenic Acute Regulatory Protein Regulation in Steroidogenesis Following Exposure to Bisphenol A and Its Analogues
Jefferi, N. E. S., Shamhari, A. ‘., Hamid, Z. A., Budin, S. B., Zulkifly, A. M. Z., Roslan, F. N., & Taib, I. S. (2022) · Biomedicines · doi:10.3390/biomedicines10061281 · Cited by 23
“BPs are frequently used in the production of polycarbonates and epoxy resins [1].”
Background
Chemicals of environmental concern as inhibitors of human placental 3β-hydroxysteroid dehydrogenase 1 and aromatase: Screening and docking analysis
Tang, L., Shi, L., Tang, Y., Ying, Y., Dong, Y., Li, H., & Ge, R. (2022) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2022.110243 · Cited by 23
Beyond Estrogenicity: A Comparative Assessment of Bisphenol A and Its Alternatives in In Vitro Assays Questions Safety of Replacements
Srebny, V., Henneberger, L., König, M., Huchthausen, J., Braasch, J., & Escher, B. I. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c07018 · Cited by 23
Discovery of novel oestrogen receptor α agonists and antagonists by screening a revisited privileged structure moiety for nuclear receptors
Masuya, T., Iwamoto, M., Liu, X., & Matsushima, A. (2019) · Scientific Reports · doi:10.1038/s41598-019-46272-y · Cited by 22
Impact of perinatal bisphenol A and 17β estradiol exposure: Comparing hormone receptor response
Leonel, E. C. R., Campos, S. G. P., Guerra, L. H. A., Bedolo, C. M., Vilamaior, P. S. L., Calmon, M. F., Rahal, P., Amorim, C. A., & Taboga, S. R. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.109918 · Cited by 22
Design, synthesis, characterization, crystal structure, Hirshfeld surface analysis, DFT calculations, anticancer, angiogenic properties of new pyrazole carboxamide derivatives
Kumar, A. D., Kameshwar, V. H., Srinivasan, B., S, N. S., Kumara, K., Lokanath, N. K., Byrappa, K., & Kumar, K. A. (2021) · Journal of Molecular Structure · doi:10.1016/j.molstruc.2021.130271 · Cited by 22
New bisphenol A and bisphenol S analogs: Evaluation of their hERα agonistic and antagonistic activities using the OECD 455 in-vitro assay and molecular modeling
Durcik, M., Hiti, L., Tomašič, T., & Mašič, L. P. (2022) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2022.109820 · Cited by 22
Hepatic consequences of a mixture of endocrine-disrupting chemicals in male mice.
Rahman, M. S., Pang, W.-K., Amjad, S., Ryu, D.-Y., Adegoke, E. O., Park, Y.-J., & Pang, M. (2022) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2022.129236 · Cited by 20
Loss of Hippocampal Oligodendrocytes Contributes to the Deficit of Contextual Fear Learning in Adult Rats Experiencing Early Bisphenol A Exposure
Xu, X., Fan, S., He, Y., Ke, X., Song, C., Xiao, Y., Zhang, W.-H., Zhang, J.-Y., Yin, X., Kato, N., et al. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0003-3 · Cited by 25
“Since many EBE adversities on neurons also require ER [15], this receptor may be a common mediator of EBE adversity in the brain.”
Background
Advancements in Microfluidic Systems for the Study of Female Reproductive Biology
Bodke, V. V., & Burdette, J. E. (2021) · Endocrinology · doi:10.1210/endocr/bqab078 · Cited by 22
Molecular modelling methods in food safety: Bisphenols as case study
Cavaliere, F., Lorenzetti, S., & Cozzini, P. (2020) · Food and Chemical Toxicology · doi:10.1016/j.fct.2020.111116 · Cited by 21
Endocrine disruptor chemicals, adipokines and reproductive functions
Kurowska, P., Mlyczyńska, E., Dawid, M., Respekta, N., Pich, K., Serra, L., Dupont, J., & Rak, A. (2022) · Endocrine · doi:10.1007/s12020-022-03061-4 · Cited by 25
“First of all, plasticizers, like BPA, bind to the hormone-binding site of the E2 receptor (ERs) [22].”
Background
Fate of contaminants of emerging concern in two wastewater treatment plants after retrofitting tertiary treatment for reduction of nitrogen discharge
Chen, T., Zeng, Q., Cao, M., Zhang, L., Adyari, B., Ma, C., Wang, K., Gao, D., Hu, A., Sun, Q., et al. (2024) · Environmental Research · doi:10.1016/j.envres.2024.118344 · Cited by 22
Metabolites of n-Butylparaben and iso-Butylparaben Exhibit Estrogenic Properties in MCF-7 and T47D Human Breast Cancer Cell Lines
Gonzalez, T. L., Moos, R. K., Gersch, C. L., Johnson, M. D., Richardson, R. J., Koch, H. M., & Rae, J. M. (2018) · Toxicological Sciences · doi:10.1093/toxsci/kfy063 · Cited by 21
PLHC-1 topminnow liver cells: An alternative model to investigate the toxicity of plastic additives in the aquatic environment
Pérez‐Albaladejo, E., Solís, A., Bani, I., & Porte, C. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2020.111746 · Cited by 20
“BPA has been detected in surface waters (up to 95 µ g/L) and in wild fish ( µ g/kg range), where it exerts its biological activity predominantly through interaction with steroid hormone receptors (Delfosse et al., 2012; Lee et al., 2015).”
The Mixture of Bisphenol-A and Its Substitutes Bisphenol-S and Bisphenol-F Exerts Obesogenic Activity on Human Adipose-Derived Stem Cells
Reina-Pérez, I., Olivas-Martínez, A., Mustieles, V., Salamanca‐Fernández, E., Molina-Molina, J.-M., Olea, N., & Fernández, M. F. (2022) · Toxics · doi:10.3390/toxics10060287 · Cited by 23
Emission of Bisphenol A and Four New Analogs from Industrial Wastewater Treatment Plants in the Production Processes of Polypropylene and Polyethylene Terephthalate in South America
Fernández, J. A. H., Cano, H., & Puello-Polo, E. (2022) · Sustainability · doi:10.3390/su141710919 · Cited by 20
Determination of biochemical and histopathological changes on testicular and epididymis tissues induced by exposure to insecticide Imidacloprid during postnatal development in rats
Sardar, A., David, M., Jahan, S., Afsar, T., Ahmad, A., Ullah, A., Almajwal, A. M., Shafique, H., & Razak, S. (2023) · BMC Pharmacology and Toxicology · doi:10.1186/s40360-023-00709-3 · Cited by 20
“In addition, studies indicated that IMD and acetamiprid exposure during in-vitro conditions adversely change the early embryonic development and sperm functions, morphological alterations and DNA damage in rodents [23, 24].”
BackgroundResultInfluential
Known and emerging factors modulating estrogenic effects of endocrine-disrupting chemicals
Zhang, W., Luo, Y., Zhang, L., Cai, Q., & Pan, X. (2013) · Environmental Reviews · doi:10.1139/er-2013-0047 · Cited by 20
“2), whereas differences in the van der Waals’ interaction (51 in E2 complex, 42 in BPA complex) may explain the weaker affinity of BPA binding to ER (Delfosse et al. 2012).”
BackgroundMethodInfluential
Implications of plastic-derived endocrine disruptors on human health
Ojo, A., Agbeye, O. D., Ogwa, T. O., Adedoyin, D., Rotimi, D., & Ojo, O. (2025) · Toxicology Mechanisms and Methods · doi:10.1080/15376516.2025.2510525 · Cited by 24
“…the natural hormone 17β-estradiol, bisphenols act as partial agonists, stabilizing the n-terminal activation function (AF-1) but failing to fully stabilize the C-terminal activation function (AF-2), which is critical for coactivator recruitment and robust gene transcription (Delfosse et al. 2012).”
ESR1 Mutations Associated With Estrogen Insensitivity Syndrome Change Conformation of Ligand-Receptor Complex and Altered Transcriptome Profile
Li, Y., Hamilton, K. J., Perera, L., Wang, T., Gruzdev, A., Jefferson, T. B., Zhang, A. X., Mathura, E., Gerrish, K., Wharey, L., et al. (2020) · Endocrinology · doi:10.1210/endocr/bqaa050 · Cited by 19
Disruption of androgen receptor signaling by chlorpyrifos (CPF) and its environmental degradation products: a structural insight
Hazarika, J., Ganguly, M., Borgohain, G., Sarma, S., Bhuyan, P., & Mahanta, R. (2021) · Journal of Biomolecular Structure and Dynamics · doi:10.1080/07391102.2021.1875885 · Cited by 19
“The docking simulations of CPF and its degradation products with AR in this study support the in silico findings of earlier molecular modeling study (Delfosse et al., 2012; Kol sek et al., 2015; Rehan et al., 2015; Wang et al., 2010, 2013) of human AR with different environmental contaminants like Bisphenol A (BPA), 4…”
Additive cardiotoxicity of a bisphenol mixture in zebrafish embryos: The involvement of calcium channel and pump
Arrokhman, S., Luo, Y.-H., & Lin, P. (2023) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2023.115225 · Cited by 21
A consolidated method for screening the endocrine activity of drinking water
Chevolleau, S., Debrauwer, L., Stroheker, T., Viglino, L., Mourahib, I., Meireles, M.-H., Grimaldi, M., Balaguer, P., & Gioia, L. D. (2016) · Food Chemistry · doi:10.1016/j.foodchem.2016.06.089 · Cited by 18
“Cell lines used in this study have been described previously (Bellet et al., 2012; Delfosse et al., 2012; Fini et al., 2012).”
Method
Estrogen receptor-based fluorescence polarization assay for bisphenol analogues and molecular modeling study of their complexation mechanism
Zhang, J., Wu, W., Wang, Y., Xing, X., Zhong, S., Guan, T., Zhang, T., Hou, L., & Li, T. (2018) · Analytica Chimica Acta · doi:10.1016/j.aca.2018.05.034 · Cited by 18
Mechanistic in silico modeling of bisphenols to predict estrogen and glucocorticoid disrupting potentials
Chen, Q., Zhou, C., Shi, W. F., Wang, X., Xia, P., Song, M., Liu, J., Zhu, H., Zhang, X., Wei, S., et al. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.138854 · Cited by 18

Authors: Delfosse, V., Grimaldi, M., Pons, J.-L., Boulahtouf, A., le Maire, A., Cavailles, V., Labesse, G., Bourguet, W., & Balaguer, P.
Affiliations: Centre National de la Recherche Scientifique (FR)
Inserm (FR)
Centre de Biochimie Structurale, Institut National de la Santé et de la Recherche Médicale U1054, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5048, Universités Montpellier 1 and 2, 34090 Montpellier, France; and
Institut de Recherche en Cancérologie de Montpellier, Institut National de la Santé et de la Recherche Médicale U896, Centre Régional de Lutte contre le Cancer Val d’Aurelle Paul Lamarque, Université Montpellier 1, 34298 Montpellier, France
ORCID: Delfosse, Vanessa
Boulahtouf, Abdelhay
Labesse, Gilles
Bourguet, William
Balaguer, Patrick
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2012-08-27
Volume: 109
Issue: 37
Pages: 14930-14935
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1203574109
PMC: PMC3443136
OpenAlex: W2140633565
Cited by: 405
References: 45
Citations by year: 2026: 28 · 2025: 33 · 2024: 26 · 2023: 33 · 2022: 34 · 2021: 40 · 2020: 38 · 2019: 35 · 2018: 25 · 2017: 26 · 2016: 19 · 2015: 25 · 2014: 23 · 2013: 20
FWCI: 15.31
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
Topics: Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Drug Discovery › Computational Drug Discovery Methods
Keywords: bisphenol A, bisphenol AF, bisphenol C, estrogen receptor alpha, estrogen receptor beta, endocrine disruptors, partial agonists, estrogen receptor antagonism, crystal structure, estrogen-related receptor gamma, androgen receptor, nuclear receptors, BPA substitutes, risk assessment, virtual screening
MeSH terms: Bisphenol A Compounds, Animals, Benzhydryl Compounds, Cell Line, Chromatography, Gel, Crystallography, Dose-Response Relationship, Drug, Estradiol, Fluorescence Polarization, Humans, Luciferases, Models, Molecular, Phenols, Oncorhynchus mykiss, Receptors, Cytoplasmic and Nuclear, Reverse Transcriptase Polymerase Chain Reaction, Estrogen Receptor alpha, Estrogen Receptor beta, Endocrine Disruptors

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Structural and mechanistic insights into bisphenols action provide guidelines for risk assessment and discovery of bisphenol A substitutes

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