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Xenoestrogen action in breast cancer: impact on ER-dependent transcription and mitogenesis

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Summary

Several estrogen mimics (xenoestrogens) inappropriately activate the estrogen receptor (ER) in the absence of endogenous ligand. Given the importance of the ER in breast cancer growth and regulation, delineating the impact of these agents under conditions related to tumor treatment is of significant importance. We examined the effect of two prevalent xenoestrogens (bisphenol A and coumestrol) on ER activation and ER-dependent mitogenesis in breast cancer cells. We show that the ability of these agents to induce mitogenesis was restricted to conditions of estrogen depletion, and that these agents failed to cooperate with estradiol to induce MCF-7 breast cancer cell growth. These observations are consistent with the impact of each agent specifically on exogenous ER activation as monitored in HeLa cells, wherein the xenoestrogens activated the receptor in the absence of estradiol but failed to cooperate with estrogen. Tamoxifen blocked bisphenol A and coumestrol-mediated ER activation, indicating that exposure to these agents is unlikely to disrupt such therapeutic intervention. The response of tumor-derived ER alleles to these xenoestrogens was also examined. Although the xenoestrogens failed to alter ER-Y537S function, the ER-D351Y mutant demonstrated an enhanced response to bisphenol A. Moreover, tamoxifen enhanced the agonistic effects of xenoestrogens on ER-D351Y. Lastly, we examined the impact of ER co-activator overexpression on xenoestrogen response. Bisphenol A and coumestrol exhibited differential responses to co-activators with regard to ER activation. However, when using mitogenesis as an endpoint, these co-activators were insufficient to provide a significant growth advantage. Combined, these data demonstrate that bisphenol A and coumestrol can impact ER activity and ER-dependent proliferation in breast cancer cells, but the influence of these agents is restricted to conditions of estrogen depletion, selective mutation of the ER, and expression of specific co-activators.

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Acknowledgements

We would like to thank Drs. Erik Knudsen, Lisa Morey, Christin Petre, and Yelena Wetherill, in addition to Kevin Link, William Zagorski, Craig Burd, and Jon Lenihan for the technical assistance and critical reading of the manuscript. The authors gratefully acknowledge Drs. James Fagin and Sohaib Khan for discussions and constructive comments.

Funding This work was funded without conflict of interest by NIEHS Training Grant ES-07250–13 Environmental Mutagenesis and Cancer (to J.K.H), NIH Grant R01 CA93404 and RO1 CA 099996 (to K.E.K.), and NIEHS Core Grant E30-ES-06096 Center for Environmental Genetics.

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  1. Department of Cell Biology, University of Cincinnati College of Medicine, Cincinnati, Ohio, 45267-0521, USA

    J.K. Hess-Wilson, J. Boldison, K.E. Weaver & K.E. Knudsen

  2. Center for Environmental Genetics, University of Cincinnati College of Medicine, Cincinnati, Ohio, 45267-0521, USA

    K.E. Knudsen

  3. Department of Cell Biology, University of Cincinnati College of Medicine, 3125 Eden Ave., 670521, Cincinnati, Ohio, 45267-0521, USA

    K.E. Knudsen

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  1. J.K. Hess-Wilson
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Hess-Wilson, J., Boldison, J., Weaver, K. et al. Xenoestrogen action in breast cancer: impact on ER-dependent transcription and mitogenesis. Breast Cancer Res Treat 96, 279–292 (2006). https://doi.org/10.1007/s10549-005-9082-y

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