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J. Biol. Chem., Vol. 277, Issue 52, 50768-50775, December 27, 2002
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§,§,§¶,¶, and§
**
From the Estrogen binds to receptors that
translocate to the plasma membrane and to the nucleus. The rapid,
non-genomic actions of this sex steroid are attributed to membrane
action, while gene transcription occurs through nuclear receptor
function. However, gene transcription can also result from estrogen
signaling initiated at the membrane, but the relative importance of
this mechanism is not known. In vascular endothelial cells (EC),
estradiol (E2) activates several kinase
cascades, including phosphatidylinositol 3-phosphate (PI3K)/Akt,
a signaling pathway that impacts EC biology. We determined here by DNA
microarray that 40-min exposure to E2 significantly
increased 250 genes in EC, up-regulation that was substantially
prevented by the PI3K inhibitor, LY294002. This coincided with maximum
E2-induced PI3K activity at 15-30 min. An important
vascular gene strongly up-regulated by E2 in our array
produces cyclooxygenase-2 (Cox-2). In cultured EC, E2
induced both Cox-2 gene expression and new Cox-2 protein
synthesis by 40 and 60 min, respectively, and rapidly stimulated the
secretion of prostaglandins PGI2 and PGE2. The
up-regulation of gene expression reflected transcriptional
transactivation, shown using Cox-2 promoter/luciferase reporters in the EC. Soluble inhibitors or dominant negative constructs for PI3K and Akt prevented all these actions of E2.
Functionally, EC migration was induced by the sex steroid, and this was
significantly reversed by NS-398, a Cox-2 inhibitor. Gene transcription
and cell biological effects of estrogen emanate from rapid and specific signaling, integrating cell surface and nuclear actions of this steroid.
Division of Endocrinology, Veterans
Affairs Medical Center, Long Beach, Long Beach, California 90822 and the Departments of § Medicine, Pharmacology,
and ¶ Molecular Biology and Biochemistry, University of
California, Irvine, Irvine, California 92717
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