How Nox2-Containing NADPH Oxidase Affects Cortical Circuits in the NMDA Receptor Antagonist Model of Schizophrenia

Wang, Xin; Pinto-Duarte, António; Sejnowski, Terrence J.; Behrens, M. Margarita

doi:10.1089/ars.2012.4907

Cited by 46Schizophrenia research and treatmentNeuroscience and Neuropharmacology ResearchNeurotransmitter Receptor Influence on Behavior

How Nox2-Containing NADPH Oxidase Affects Cortical Circuits in the NMDA Receptor Antagonist Model of Schizophrenia

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Wang, Xin, Pinto-Duarte, António, Sejnowski, Terrence J., Behrens, M. Margarita·2013·Antioxidants & Redox Signaling

DOI 10.1089/ars.2012.4907PMC PMC3603498

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Abstract

SIGNIFICANCE: Schizophrenia is a complex neuropsychiatric disorder affecting around 1% of the population worldwide. Its mode of inheritance suggests a multigenic neurodevelopmental disorder with symptoms appearing during late adolescence/early adulthood, with its onset strongly influenced by environmental stimuli. Many neurotransmitter systems, including dopamine, glutamate, and gamma-aminobutyric acid, show alterations in affected individuals, and the behavioral and physiological characteristics of the disease can be mimicked by drugs that produce blockade of N-methyl-d-aspartate glutamate receptors (NMDARs). RECENT ADVANCES: Mounting evidence suggests that drugs that block NMDARs specifically impair the inhibitory capacity of parvalbumin-expressing (PV+) fast-spiking neurons in adult and developing rodents, and alterations in these inhibitory neurons is one of the most consistent findings in the schizophrenic postmortem brain. Disruption of the inhibitory capacity of PV+ inhibitory neurons will alter the functional balance between excitation and inhibition in prefrontal cortical circuits producing impairment of working memory processes such as those observed in schizophrenia. CRITICAL ISSUES: Mechanistically, the effect of NMDAR antagonists can be attributed to the activation of the Nox2-dependent reduced form of nicotinamide adenine dinucleotide phosphate oxidase pathway in cortical neurons, which is consistent with the emerging role of oxidative stress in the pathogenesis of mental disorders, specifically schizophrenia. Here we review the mechanisms by which NMDAR antagonists produce lasting impairment of the cortical PV+ neuronal system and the roles played by Nox2-dependent oxidative stress mechanisms. FUTURE DIRECTIONS: The discovery of the pathways by which oxidative stress leads to unbalanced excitation and inhibition in cortical neural circuits opens a new perspective toward understanding the biological underpinnings of schizophrenia.

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Early postnatal, but not adolescent, deletion of Grin1 in mouse forebrain interneurons reduced parvalbumin and GAD1 expression and caused cortical disinhibition and asynchrony.
“Early post-natal, but not adolescent, deletion of Grin1 in mouse forebrain interneurons reduced their expression of parvalbumin and glutamate decarboxylase 1 (GAD1, also known as GAD67), and caused cortical disinhibition and asynchrony 30,31 .”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [31]

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Dysbindin-1 mutant mice implicate reduced fast-phasic inhibition as a final common disease mechanism in schizophrenia
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Association of NR3A with theN-Methyl-d-aspartate Receptor NR1 and NR2 Subunits
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ROS and Brain Diseases: The Good, the Bad, and the Ugly
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FORUM REVIEW ARTICLE How Nox2-Containing NADPH Oxidase Affects Cortical Circuits in the NMDA Receptor Antagonist Model of Schizophrenia
Wang, X., Pinto‐Duarte, A., B, T. J. S. A., & Behrens, M. M. (2013)
Self-citation
Behavioral and neurochemical consequences of cortical oxidative stress on parvalbumin-interneuron maturation in rodent models of schizophrenia
Powell, S. B., Sejnowski, T. J., & Behrens, M. M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.01.049 · Cited by 164 · see citing works
Self-citation
Antioxidant Treatment in Male Mice Prevents Mitochondrial and Synaptic Changes in an NMDA Receptor Dysfunction Model of Schizophrenia
Phensy, A. J., Driskill, C. M., Lindquist, K. A., Guo, L., Jeevakumar, V., Fowler, B., Du, H., & Kroener, S. (2017) · eNeuro · doi:10.1523/eneuro.0081-17.2017 · Cited by 41 · see citing works
Redox Regulation of NMDA Receptors in a Ketamine Model of Schizophrenia
Schulman, A. D. (2013) · eScholarship (California Digital Library)
Can N-Methyl-D-Aspartate Receptor Hypofunction in Schizophrenia Be Localized to an Individual Cell Type?
Bygrave, A. M., Kilonzo, K., Kullmann, D. M., Bannerman, D. M., & Kätzel, D. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00835 · Cited by 32 · see citing works

Authors: Wang, X., Pinto-Duarte, A., Sejnowski, T. J., & Behrens, M. M.
Affiliations: Salk Institute for Biological Studies (US)
The Salk Institute for Biological Studies, La Jolla, California.
Corresponding author: Wang, Xin
ORCID: Behrens, M. Margarita
Venue: Antioxidants & Redox Signaling
Publisher: SAGE Publications
Published: 2013-04-20
Volume: 18
Issue: 12
Pages: 1444-1462
ISSN: 1523-0864 (ISSN-L)
1557-7716
DOI: 10.1089/ars.2012.4907
PMC: PMC3603498
OpenAlex: W2059143392
Cited by: 46
References: 255
Citations by year: 2026: 2 · 2025: 7 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 9 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 7 · 2016: 3 · 2015: 1 · 2014: 3 · 2013: 3
FWCI: 0.30
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Antioxidants and Redox Signaling (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Howard Hughes Medical Institute
Pfizer
Life Sciences Research Foundation
Calouste Gulbenkian Foundation
National Institute of Mental Health (R01MH091407, MH091407)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: schizophrenia, NMDA receptor antagonists, NOX2, NADPH oxidase, oxidative stress, fast-spiking interneurons, cortical circuits, excitation-inhibition balance, prefrontal cortex, working memory, glutamate receptor blockade
MeSH terms: NADPH Oxidase 2, Animals, Brain, Humans, Membrane Glycoproteins, Neurons, Oxidation-Reduction, Schizophrenia, Ion Channel Gating, Receptors, N-Methyl-D-Aspartate, Excitatory Amino Acid Antagonists, NADPH Oxidases

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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How Nox2-Containing NADPH Oxidase Affects Cortical Circuits in the NMDA Receptor Antagonist Model of Schizophrenia

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