Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model

IndroductionImpaired depolarizing-to-hyperpolarizing (D/H) switch of gamma-aminobutyric acid (GABA) is reported during brain development in rodent valproate-model of autism spectrum disorder (VPA-ASD). We hypothesize that this impairment triggers NADPH oxidases (NOXs)-induced reactive oxygen species...

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Main Authors: Basma A. Yasseen, Hadeer Abdelkhalek, Sara Gohar, Yasmin Hatem, Hajar El-Sayed, Aya A. Elkhodiry, Aya Galal, Aya Samir, Nouran Al-Shehaby, Malak W. Elbenhawi, Rehab Hamdy, Christine S. Prince, Azza G. Kamel, Mohamed A. Badawy, Ghada F. Soliman, Soha Aly ElMorsy, Tamer M. Gamal El-Din, Ebtehal El-Demerdash, Sameh S. Ali, Engy A. Abdel-Rahman
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Language:English
Published: Frontiers Media S.A. 2025-05-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2025.1571008/full
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author Basma A. Yasseen
Hadeer Abdelkhalek
Sara Gohar
Sara Gohar
Yasmin Hatem
Hajar El-Sayed
Aya A. Elkhodiry
Aya Galal
Aya Samir
Aya Samir
Nouran Al-Shehaby
Malak W. Elbenhawi
Rehab Hamdy
Christine S. Prince
Azza G. Kamel
Mohamed A. Badawy
Ghada F. Soliman
Soha Aly ElMorsy
Tamer M. Gamal El-Din
Ebtehal El-Demerdash
Ebtehal El-Demerdash
Sameh S. Ali
Engy A. Abdel-Rahman
Engy A. Abdel-Rahman
author_facet Basma A. Yasseen
Hadeer Abdelkhalek
Sara Gohar
Sara Gohar
Yasmin Hatem
Hajar El-Sayed
Aya A. Elkhodiry
Aya Galal
Aya Samir
Aya Samir
Nouran Al-Shehaby
Malak W. Elbenhawi
Rehab Hamdy
Christine S. Prince
Azza G. Kamel
Mohamed A. Badawy
Ghada F. Soliman
Soha Aly ElMorsy
Tamer M. Gamal El-Din
Ebtehal El-Demerdash
Ebtehal El-Demerdash
Sameh S. Ali
Engy A. Abdel-Rahman
Engy A. Abdel-Rahman
author_sort Basma A. Yasseen
collection DOAJ
description IndroductionImpaired depolarizing-to-hyperpolarizing (D/H) switch of gamma-aminobutyric acid (GABA) is reported during brain development in rodent valproate-model of autism spectrum disorder (VPA-ASD). We hypothesize that this impairment triggers NADPH oxidases (NOXs)-induced reactive oxygen species (ROS) overproduction.MethodsHere, we followed the impact of prenatal exposure to VPA on the synaptic protein expression of potassium chloride cotransporter 2 (KCC2), sodium potassium chloride cotransporter 1 (NKCC1) and, in brains of male and female Wistar rats during infantile (P15), juvenile (P30) and adult (P60) stages. We also assessed alterations in synaptic NOX isoforms 2 and 4 (NOX2 and NOX4) activities and expressions in developing rat brains.ResultsOur findings revealed a significant reduction in KCC2 expression and a concomitant increase in NOX activity and NOX4 expression in synaptosomes of VPA-exposed rats, particularly at P15 and P30. Prenatal exposure to shikonin, (10 mg/kg/day, intraperitoneal (i.p.) into pregnant dam, daily from G12.5 until birth), ameliorated these effects by reducing synaptic protein expression of NOX4, generally quenched synaptic NOX activity and enhanced synaptic protein expression of KCC2. Indeed, shikonin reversed VPA-induced sociability deficits in ASD rats.DiscussionThese results suggest that targeting the NOX-ROS pathway may be a potential therapeutic strategy for ASD.
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spelling doaj-art-2d416655d6c54048aa87b5eec532df152025-08-20T03:21:34ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122025-05-011610.3389/fphar.2025.15710081571008Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat modelBasma A. Yasseen0Hadeer Abdelkhalek1Sara Gohar2Sara Gohar3Yasmin Hatem4Hajar El-Sayed5Aya A. Elkhodiry6Aya Galal7Aya Samir8Aya Samir9Nouran Al-Shehaby10Malak W. Elbenhawi11Rehab Hamdy12Christine S. Prince13Azza G. Kamel14Mohamed A. Badawy15Ghada F. Soliman16Soha Aly ElMorsy17Tamer M. Gamal El-Din18Ebtehal El-Demerdash19Ebtehal El-Demerdash20Sameh S. Ali21Engy A. Abdel-Rahman22Engy A. Abdel-Rahman23Tumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptCancer Research UK Scotland Institute, Glasgow, United KingdomTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptPreclinical and Translational Research Center, Faculty of Pharmacy, Ain Shams University, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptDepartment of Biotechnology, Faculty of Science, Cairo University, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptDepartment of Medical Pharmacology, Faculty of Medicine, Cairo University, Cairo, EgyptDepartment of Medical Pharmacology, Faculty of Medicine, Cairo University, Cairo, EgyptDepartment of Pharmacology, University of Washington, Seattle, WA, United StatesPreclinical and Translational Research Center, Faculty of Pharmacy, Ain Shams University, Cairo, EgyptDepartment of Pharmacology, Faculty of Pharmacy, Ain-Shams University, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptTumor Biology Research Program, Research Department, Children’s Cancer Hospital Egypt, Cairo, EgyptDepartment of Pharmacology, Faculty of Medicine, Assiut University, Assiut, EgyptIndroductionImpaired depolarizing-to-hyperpolarizing (D/H) switch of gamma-aminobutyric acid (GABA) is reported during brain development in rodent valproate-model of autism spectrum disorder (VPA-ASD). We hypothesize that this impairment triggers NADPH oxidases (NOXs)-induced reactive oxygen species (ROS) overproduction.MethodsHere, we followed the impact of prenatal exposure to VPA on the synaptic protein expression of potassium chloride cotransporter 2 (KCC2), sodium potassium chloride cotransporter 1 (NKCC1) and, in brains of male and female Wistar rats during infantile (P15), juvenile (P30) and adult (P60) stages. We also assessed alterations in synaptic NOX isoforms 2 and 4 (NOX2 and NOX4) activities and expressions in developing rat brains.ResultsOur findings revealed a significant reduction in KCC2 expression and a concomitant increase in NOX activity and NOX4 expression in synaptosomes of VPA-exposed rats, particularly at P15 and P30. Prenatal exposure to shikonin, (10 mg/kg/day, intraperitoneal (i.p.) into pregnant dam, daily from G12.5 until birth), ameliorated these effects by reducing synaptic protein expression of NOX4, generally quenched synaptic NOX activity and enhanced synaptic protein expression of KCC2. Indeed, shikonin reversed VPA-induced sociability deficits in ASD rats.DiscussionThese results suggest that targeting the NOX-ROS pathway may be a potential therapeutic strategy for ASD.https://www.frontiersin.org/articles/10.3389/fphar.2025.1571008/fullASDGABA D/H switchsynaptosomesKCC2NOXshikonin
spellingShingle Basma A. Yasseen
Hadeer Abdelkhalek
Sara Gohar
Sara Gohar
Yasmin Hatem
Hajar El-Sayed
Aya A. Elkhodiry
Aya Galal
Aya Samir
Aya Samir
Nouran Al-Shehaby
Malak W. Elbenhawi
Rehab Hamdy
Christine S. Prince
Azza G. Kamel
Mohamed A. Badawy
Ghada F. Soliman
Soha Aly ElMorsy
Tamer M. Gamal El-Din
Ebtehal El-Demerdash
Ebtehal El-Demerdash
Sameh S. Ali
Engy A. Abdel-Rahman
Engy A. Abdel-Rahman
Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
Frontiers in Pharmacology
ASD
GABA D/H switch
synaptosomes
KCC2
NOX
shikonin
title Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
title_full Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
title_fullStr Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
title_full_unstemmed Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
title_short Prenatal modulation of NADPH-oxidase reverses the deranged GABA switch and rescues behavioral deficits in valproate ASD rat model
title_sort prenatal modulation of nadph oxidase reverses the deranged gaba switch and rescues behavioral deficits in valproate asd rat model
topic ASD
GABA D/H switch
synaptosomes
KCC2
NOX
shikonin
url https://www.frontiersin.org/articles/10.3389/fphar.2025.1571008/full
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