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Molecular Endocrinology 16 (1): 116-127
Copyright © 2002 by The Endocrine Society

Linkage of Rapid Estrogen Action to MAPK Activation by ER{alpha}-Shc Association and Shc Pathway Activation

Robert X.-D. Song, Robert A. McPherson, Liana Adam, Yongde Bao, Margaret Shupnik, Rakesh Kumar and Richard J. Santen

Departments of Internal Medicine (R.X.-D.S., R.A.M., M.S., R.J.S.) and Biomolecular Research Facility (Y.B.), University of Virginia School of Medicine, Charlottesville, Virginia 22908; and Department of Molecular & Cellular Oncology (L.A., R.K.), University of Texas M.D. Anderson Cancer Center, Houston, Texas 77030

Address all correspondence and requests for reprints to: Dr. Robert X. Song, Division of Hematology and Oncology, University of Virginia Health Science Center, Charlottesville, Virginia 22901. E-mail: rs5wf{at}virginia.edu

E2 rapidly activates MAPK in breast cancer cells, and the mechanism for this effect has not been fully identified. Since growth factor-induced MAPK activation involves signaling via the adapter protein Shc (Src-homology and collagen homology) and its association with membrane receptors, we hypothesized that breast cancer cells utilize similar signaling mechanisms in response to E2. In the present study, we demonstrated that E2 rapidly induced Shc phosphorylation and Shc-Grb2 (growth factor receptor binding protein 2)-Sos (son of sevenless) complex formation in MCF-7 cells. Overexpression of dominant negative Shc blocked the effect of E2 on MAPK, indicating a critical role of Shc in E2 action. Using selective inhibitors, we also demonstrated that ER{alpha} and Src are upstream regulators of Shc. A rapid physical association between ER{alpha} and Shc upon E2 stimulation further evidenced the role of ER{alpha} on Shc activation. Mutagenesis studies showed that the phosphotyrosine binding and SH2 domains of Shc are required to interact with the activation function 1, but not activation function 2, domain of ER{alpha}. Using a glutathione-S-transferanse-Shc pull-down assay, we demonstrated that this ER{alpha}-Shc association was direct. Biological consequences of this pathway were further investigated at the genomic and nongenomic levels. E2 stimulated MAPK-mediated Elk-1 transcriptional activity. Confocal microscopy studies showed that E2 rapidly induced formation of membrane ruffles, pseudopodia, and ER{alpha} membrane translocation. The E2-induced morphological changes were prevented by antiestrogen. Together our results demonstrate that ER{alpha} can mediate the rapid effects of E2 on Shc, MAPK, Elk-1, and morphological changes in breast cancer cells




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