Neurosteroid withdrawal regulates GABA-A receptor α4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway

Gangisetty, O.; Reddy, D.S.

doi:10.1016/j.neuroscience.2010.07.037

Cited by 84Epilepsy research and treatmentNeuroscience and Neuropharmacology ResearchPharmacological Effects and Toxicity Studies

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Neurosteroid withdrawal regulates GABA-A receptor α4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway

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Gangisetty, O., Reddy, D.S.·2010·Neuroscience

DOI 10.1016/j.neuroscience.2010.07.037PMC PMC2939139

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Abstract

Neurosteroids regulate GABA-A receptor plasticity. Neurosteroid withdrawal occurs during menstruation and is associated with a marked increase in expression of GABA-A receptor α4-subunit, a key subunit linked to enhanced neuronal excitability, seizure susceptibility and benzodiazepine resistance. However, the molecular mechanisms underlying the upregulation of α4-subunit expression remain unclear. Here we utilized the progesterone receptor (PR) knockout mouse to investigate molecular pathways of PR and the transcription factor early growth response factor-3 (Egr3) in regulation of the GABA-A receptor α4-subunit expression in the hippocampus in a mouse neurosteroid withdrawal paradigm. Neurosteroid withdrawal induced a threefold increase in α4-subunit expression in wild-type mice, but this upregulation was unchanged in PR knockout mice. The expression of Egr3, which controls α4-subunit transcription, was increased significantly following neurosteroid withdrawal in wild-type and PR knockout mice. Neurosteroid withdrawal-induced α4-subunit upregulation was completely suppressed by antisense Egr3 inhibition. In the hippocampus kindling model of epilepsy, there was heightened seizure activity, significant reduction in the antiseizure sensitivity of diazepam (a benzodiazepine insensitive at α4βγ-receptors) and conferral of increased seizure protection of flumazenil (a low-affinity agonist at α4βγ-receptors) in neurosteroid-withdrawn wild-type and PR knockout mice. These observations are consistent with enhanced α4-containing receptor abundance in vivo. Neurosteroid withdrawal-induced seizure exacerbation, diazepam insensitivity, and flumazenil efficacy in the kindling model were reversed by inhibition of Egr3. These results indicate that neurosteroid withdrawal-induced upregulation of GABA-A receptor α4-subunit expression is mediated by the Egr3 via a PR-independent signaling pathway. These findings help advance our understanding of the molecular basis of catamenial epilepsy, a neuroendocrine condition that occurs around the perimenstrual period and is characterized by neurosteroid withdrawal-linked seizure exacerbations in women with epilepsy.

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This prediction is consistent with reported correlations between neurosteroids and a series of neurological disorders, including migraine, postpartum-depression, epilepsy, anxiety, cognitive and psychiatric disorders.
“Such a prediction is consistent with reported correlations between neurosteroids and a series of neurological disorders, including migraine, postpartum-depression, epilepsy, anxiety, cognitive and psychiatric disorders [56,144,145].”
From Fibromyalgia pathogenesis explained by a neuroendocrine multistable model (2024) · cites this paper as [56]
The Introduction (page unavailable) states that neurosteroids have a significant role in epilepsy, anxiety, and postpartum depression; the Discussion also reports increased seizure activity after neurosteroid withdrawal. The passages found do not address migraine or cognitive and psychiatric disorders as a broader category, so they support only part of the cited list. (LLM, conf=0.88)
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Authors: Gangisetty, O., & Reddy, D. S.
Affiliations: Texas A&M Health Science Center (US)
Corresponding author: Reddy, D.S.
ORCID: Gangisetty, O.
Reddy, D.S.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2010-10
Volume: 170
Issue: 3
Pages: 865-880
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2010.07.037
PMC: PMC2939139
OpenAlex: W15119525
Cited by: 84
References: 93
Citations by year: 2026: 3 · 2025: 1 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 6 · 2020: 4 · 2019: 4 · 2018: 3 · 2017: 6 · 2016: 7 · 2015: 4 · 2014: 7 · 2013: 8 · 2012: 13
FWCI: 6.12
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Health, NINDS (R01 NS051398)
Topics: Health Sciences › Medicine › Clinical Neurology › Epilepsy research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Pharmacological Effects and Toxicity Studies
Keywords: progesterone receptor, EGR3, catamenial epilepsy, seizure susceptibility, flumazenil, hippocampus, kindling model, menstrual cycle
MeSH terms: Animals, Diazepam, Drug Administration Schedule, Female, Flumazenil, Gene Expression Regulation, Hippocampus, Kindling, Neurologic, Mice, Inbred C57BL, Pregnanolone, Progesterone, Receptors, GABA-A, Receptors, Progesterone, Signal Transduction, Up-Regulation, Mice, Knockout, Neurotransmitter Agents, Oligodeoxyribonucleotides, Antisense, Mice, Early Growth Response Protein 3

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Neurosteroid withdrawal regulates GABA-A receptor α4-subunit expression and seizure susceptibility by activation of progesterone receptor-independent early growth response factor-3 pathway

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