题名

Membrane-Initiated Estrogen Actions on Ion Channels and the Induction of Lordosis, the Rodent Female Sexual Behavior

DOI

10.4077/CJP.2009.AMH044

作者

Lee-Ming Kow；Donald W. Pfaff

关键词

estrogens ； estrogen receptors ； ion cannels ； modulation ； single-unit activity ； current clamp ； whole-cell recording ； hypothalamic ventromedial nucleus

期刊名称

The Chinese Journal of Physiology

卷期/出版年月

52卷4期（2009 / 08 / 01）

页次

175 - 195

内容语文

英文
英文摘要

The explosive increase of research in ”membrane-initiated” (also called ”non-genomic” or ”rapid” or ”acute”) estrogen actions in the past ten years not only established them as legitimate but also showed that they can activate many signaling pathways that can lead indirectly or even directly to the modulation of genomic functions. The latter raised the possibility that estrogens' membrane-initiated actions can synergize with their genomic actions. We have turned this possibility into a reality by first using cultured cells and then whole animals. With cultured neuroblastoma and MCF-7 breast cancer cells, we demonstrated that membrane-initiated estrogen actions could facilitate subthreshold doses of estradiol to accomplish a transcriptional facilitation, and found that the facilitation was mediated, at least in part, by pathways involving PKA and PKC. Using the estrogen-dependent rodent female sexual behavior, lordosis, as a study model, we found that implantation of a membrane-impermeable estrogen, which by itself could not induce the behavior, in the hypothalamic ventromedial nucleus (VMN) of female rats facilitated subthreshold estradiol similarly implanted later to induce lordosis. These findings, to our knowledge, comprise the first demonstration of the synergism between estrogen's membraneinitiated and genomic actions. Consistent with our cell culture studies, the facilitation of lordosis induction also required functioning PKA and PKC. Several lines of evidence indicated that an increase in neuronal activity during the initial stage of estrogen administration is required for the induction of lordosis. Therefore, whether the activity of VMN neurons is modulated by the membrane-initiated actions of the estrogen applied to the hypothalamus was investigated. With extracellular single-neuron recording of VMN cells in hypothalamic slices of female rats, it was found that acutely applied estradiol (acute E2) could i) potentiate the excitation mediated by two distinct types of receptors, G protein-coupled excitatory histamine (HA) receptors and NMDA ion channel/receptors, and ii) attenuate inhibition caused by G protein-coupled inhibitory HA receptors. These findings raised the possibility that acute E2 can potentially working through three independent mechanisms to modulate these responses. This possibility was evaluated using whole cell patch clamp studies. Corresponding to extracellular recording findings, HA could evoke de- and/or hyper-polarization, and NMDA could evoke only depolarization. Acute application of E2 could, again, potentiate HA and NMDA depolarization and attenuate HA hyperpolarization. To search for mechanisms, pharmacological analyses of HA responses were performed to define receptors responsible for excitation and inhibition, and effects of acute E2 on individual types of HA receptors were studied. Results from these studies, together with current knowledge about HA receptors, point to a likely mechanism underlying non-genomic estrogen modulations of HA responses: acute E2 inhibits K(superscript +) channels through the facilitation of G(subscript q/11) coupled to histaminergic H1 receptors, to potentiate HA depolarization/ excitation as well as to attenuate hyperpolarization/inhibition. We also searched for mechanism(s) underlying acute E2 potentiation of NMDA depolarization/excitation by characterizing NMDA actions. We found that both NMDA and acute E2 could reduce afterhyperpolarizations, which are mediated by Ca(superscript ++)-activated K(superscript +) channels. Therefore, attenuation of these channels appears to be one way acute E2 can potentiate NMDA depolarization/excitation. Thus, in the induction of lordosis at least, membraneinitiated non-genomic estrogen actions appear to facilitate genomic actions by both activating signaling pathways involving PKA and PKC and by inhibiting certain K(superscript +) channels.
主题分类 醫藥衛生 > 基礎醫學
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