Estrogen Modulation of Endothelial Nitric Oxide Synthase
Ken L. Chambliss and
Philip W. Shaul
Department of Pediatrics, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas 75390
Correspondence: Address all correspondence and requests for reprints to: Philip W. Shaul, M.D., Department of Pediatrics, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas Texas 75390. E-mail: pshaul{at}mednet.swmed.edu
Over the past decade, clinical and basic research has demonstratedthat estrogen has a dramatic impact on the response to vascularinjury and the development of atherosclerosis. Further workhas indicated that this is at least partially mediated by anenhancement in nitric oxide (NO) production by the endothelialisoform of NO synthase (eNOS) due to increases in both eNOSexpression and level of activation. The effects on eNOS abundanceare primarily mediated at the level of gene transcription, andthey are dependent on estrogen receptors (ERs), which classicallyserve as transcription factors, but they are independent ofestrogen response element action. Estrogen also has potent nongenomiceffects on eNOS activity mediated by a subpopulation of ER localizedto caveolae in endothelial cells, where they are coupled toeNOS in a functional signaling module. These observations, whichemphasize dependence on cell surface-associated receptors, provideevidence for the existence of a steroid receptor fast-actioncomplex, or SRFC, in caveolae. Estrogen binding to ER on theSRFC in caveolae leads to Gi activation, which mediates downstreamevents. The downstream signaling includes activation of tyrosinekinase-MAPK and Akt/protein kinase B signaling, stimulationof heat shock protein 90 binding to eNOS, and perturbation ofthe local calcium environment, leading to eNOS phosphorylationand calmodulin-mediated eNOS stimulation. These unique genomicand nongenomic processes are critical to the vasoprotectiveand atheroprotective characteristics of estrogen. In addition,they serve as excellent paradigms for further elucidation ofnovel mechanisms of steroid hormone action.
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localized to caveolae in endothelial cells, where they are coupled to eNOS in a functional signaling module. These observations, which emphasize dependence on cell surface-associated receptors, provide evidence for the existence of a steroid receptor fast-action complex, or SRFC, in caveolae. Estrogen binding to ER
