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J. Biol. Chem., Vol. 276, Issue 29, 27071-27076, July 20, 2001

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Plasma Membrane Estrogen Receptors Are Coupled to Endothelial Nitric-oxide Synthase through G_i^*

Myra H. Wyckoff, Ken L. Chambliss, Chieko Mineo, Ivan S. Yuhanna, Michael E. Mendelsohn^§, Susanne M. Mumby^¶, and Philip W. Shaul

From the Departments of  Pediatrics and ^¶ Pharmacology, University of Texas Southwestern Medical Center, Dallas, Texas 75390 and the ^§ Molecular Cardiology Research Institute, New England Medical Center and Tufts University School of Medicine, Boston, Massachusetts 02111

Estrogen causes rapid endothelial nitric oxide (NO) production because of the activation of plasma membrane-associated estrogen receptors (ER) coupled to endothelial NO synthase (eNOS). In the present study, we determined the role of G proteins in eNOS activation by estrogen. Estradiol-17 (E₂, 10⁸ M) and acetylcholine (10⁵ M) caused comparable increases in NOS activity (15 min) in intact endothelial cells that were fully blocked by pertussis toxin (Ptox). In addition, exogenous guanosine 5'-O-(2- thiodiphosphate) inhibited E₂-mediated eNOS stimulation in isolated endothelial plasma membranes, and Ptox prevented enzyme activation by E₂ in COS-7 cells expressing ER and eNOS. Coimmunoprecipitation studies of plasma membranes from COS-7 cells transfected with ER and specific G proteins demonstrated E₂-stimulated interaction between ER and G_i but not between ER and either G_q or G_s; the observed ER-G_i interaction was blocked by the ER antagonist ICI 182,780 and by Ptox. E₂-stimulated ER-G_i interaction was also demonstrable in endothelial cell plasma membranes. Cotransfection of G_i into COS-7 cells expressing ER and eNOS yielded a 3-fold increase in E₂-mediated eNOS stimulation, whereas cotransfection with a protein regulator of G protein signaling, RGS4, inhibited the E₂ response. These findings indicate that eNOS stimulation by E₂ requires plasma membrane ER coupling to G_i and that activated G_i mediates the requisite downstream signaling events. Thus, novel G protein coupling enables a subpopulation of ER to initiate signal transduction at the cell surface. Similar mechanisms may underly the nongenomic actions of other steroid hormones.

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