Differential Regulation of Gonadotropin-Releasing Hormone Neuron Activity and Membrane Properties by Acutely Applied Estradiol: Dependence on Dose and Estrogen Receptor Subtype

Chu, Zhiguo; Andrade, Josefa; Shupnik, Margaret A.; Moenter, Suzanne M.

doi:10.1523/jneurosci.0352-09.2009

Cited by 133Hypothalamic control of reproductive hormonesEstrogen and related hormone effectsNeuroscience and Neuropharmacology Research

Differential Regulation of Gonadotropin-Releasing Hormone Neuron Activity and Membrane Properties by Acutely Applied Estradiol: Dependence on Dose and Estrogen Receptor Subtype

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Chu, Zhiguo, Andrade, Josefa, Shupnik, Margaret A., Moenter, Suzanne M.·2009·The Journal of Neuroscience

DOI 10.1523/jneurosci.0352-09.2009PMC PMC2744362

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Abstract

Gonadotropin-releasing hormone (GnRH) neurons are critical to controlling fertility.In vivo, estradiol can inhibit or stimulate GnRH release depending on concentration and physiological state. We examined rapid, nongenomic effects of estradiol. Whole-cell recordings were made of GnRH neurons in brain slices from ovariectomized mice with ionotropic GABA and glutamate receptors blocked. Estradiol was bath applied and measurements completed within 15 min. Estradiol from high physiological (preovulatory) concentrations (100 p m) to 100 n m enhanced action potential firing, reduced afterhyperpolarizing potential (AHP) and increased slow afterdepolarization amplitudes (ADP), and reduced IAHP and enhanced IADP. The reduction of IAHP was occluded by previous blockade of calcium-activated potassium channels. These effects were mimicked by an estrogen receptor (ER) β-specific agonist and were blocked by the classical receptor antagonist ICI182780. ERα or GPR30 agonists had no effect. The acute stimulatory effect of high physiological estradiol on firing rate was dependent on signaling via protein kinase A. In contrast, low physiological levels of estradiol (10 p m) did not affect intrinsic properties. Without blockade of ionotropic GABA and glutamate receptors, however, 10 p m estradiol reduced firing of GnRH neurons; this was mimicked by an ERα agonist. ERα agonists reduced the frequency of GABA transmission to GnRH neurons; GABA can excite to these cells. In contrast, ERβ agonists increased GABA transmission and postsynaptic response. These data suggest rapid intrinsic and network modulation of GnRH neurons by estradiol is dependent on both dose and receptor subtype. In cooperation with genomic actions, nongenomic effects may play a role in feedback regulation of GnRH secretion.

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High physiological E2 increases GnRH firing frequency in mice via a membrane ERβ-PKA pathway affecting after-hyperpolarization.
“E2 at high physiological concentrations enhance GnRH firing frequency through modulation of the after-hyperpolarization potential via a membrane-mediated ERβ-PKA pathway in mice41.”
From Emerging insights into hypothalamic‐pituitary‐gonadal axis regulation and interaction with stress signalling (2018) · cites this paper as [41]
The Abstract (page unavailable) reports that high-physiological estradiol increased firing and reduced the afterhyperpolarization in GnRH neurons from mice; an ERβ agonist mimicked these effects. The Results (page unavailable) report that PKA inhibition eliminated estradiol’s excitatory effect. The paper suggests PKA involvement but does not establish a specifically membrane-mediated ERβ–PKA pathway or exclude other signaling pathways. (LLM, conf=0.84)
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Herbison AE Skynner MJ Sim JA 2001 Erratum: Lack of detection of estrogen receptor-alpha transcripts in mouse gonadotropin releasing-hormone neurons Endocrinology 142 493 10537149
Moenter SM DeFazio RA 2005 Endogenous gamma-aminobutyric acid can excite GnRH neurons Endocrinology 146 5374 5379 16123153
Yen S Chaney C Judd H 1976 Functional abberations of the hypothalamic-pituitary system in PCOS-a consideration for pathogenesis New York Academic press

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Rapid Direct Action of Estradiol in GnRH Neurons: Findings and Implications
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The Minuses and Pluses of Estradiol Feedback to GnRH Neurons.
Moenter, S. M., Chu, Z., & Sun, J. (2010) · Biology of Reproduction · doi:10.1093/biolreprod/83.s1.48
Self-citation
Steroid Regulation of GnRH Neurons
Moenter, S. M., DeFazio, R. A., Straume, M., & Nunemaker, C. S. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.014 · Cited by 24 · see citing works
Self-citation
Rapid action of estradiol in primate GnRH neurons: The role of estrogen receptor alpha and estrogen receptor beta
Kenealy, B. P., Keen, K. L., & Terasawa, E. (2011) · Steroids · doi:10.1016/j.steroids.2011.02.019 · Cited by 20 · see citing works
Estradiol Increases Glutamate and GABA Neurotransmission into GnRH Neurons via Retrograde NO-Signaling in Proestrous Mice during the Positive Estradiol Feedback Period
Farkas, I., Bálint, F., Farkas, E., Vastagh, C., Fekete, C., & Liposits, Z. (2018) · eNeuro · doi:10.1523/eneuro.0057-18.2018 · Cited by 33 · see citing works

Authors: Chu, Z., Andrade, J., Shupnik, M. A., & Moenter, S. M.
Affiliations: University of Virginia (US)
ORCID: Moenter, Suzanne M.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2009-04-29
Volume: 29
Issue: 17
Pages: 5616-5627
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.0352-09.2009
PMC: PMC2744362
OpenAlex: W2009302214
Cited by: 133
References: 87
Citations by year: 2026: 1 · 2025: 3 · 2024: 1 · 2023: 3 · 2022: 2 · 2021: 7 · 2020: 6 · 2019: 4 · 2018: 11 · 2017: 6 · 2016: 10 · 2015: 11 · 2014: 9 · 2013: 11 · 2012: 12
FWCI: 18.84
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 183 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-34860, HD41469, R29HD034860, R01HD034860, R37HD034860, R01HD041469)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: GnRH neurons, estradiol, non-genomic estrogen signaling, estrogen receptor beta, estrogen receptor alpha, GPR30, action potential firing, afterhyperpolarization, calcium-activated potassium channels, protein kinase A, GABA transmission, glutamatergic neurotransmission, ovariectomized mice
MeSH terms: Animals, Dose-Response Relationship, Drug, Drug Administration Schedule, Estradiol, Female, Gonadotropin-Releasing Hormone, Membrane Potentials, Neurons, Receptors, Estrogen, Time Factors, Protein Subunits, Estrogen Receptor alpha, Estrogen Receptor beta, Mice

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Differential Regulation of Gonadotropin-Releasing Hormone Neuron Activity and Membrane Properties by Acutely Applied Estradiol: Dependence on Dose and Estrogen Receptor Subtype

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