Synaptic plasticity impairment and hypofunction of NMDA receptors induced by glutathione deficit: Relevance to schizophrenia

Steullet, P.; Neijt, H.C.; Cuénod, M.; Do, K.Q.

doi:10.1016/j.neuroscience.2005.10.014

Cited by 173Neuroscience and Neuropharmacology ResearchSchizophrenia research and treatmentAmino Acid Enzymes and Metabolism

Synaptic plasticity impairment and hypofunction of NMDA receptors induced by glutathione deficit: Relevance to schizophrenia

Steullet, P., Neijt, H.C., Cuénod, M., Do, K.Q.·2006·Neuroscience

DOI 10.1016/j.neuroscience.2005.10.014

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Abstract

Increasing evidence suggests that the metabolism of glutathione, an endogenous redox regulator, is abnormal in schizophrenia. Patients show a deficit in glutathione levels in the cerebrospinal fluid and prefrontal cortex and a reduction in gene expression of the glutathione synthesizing enzymes. We investigated whether such glutathione deficit altered synaptic transmission and plasticity in slices of rat hippocampus, with particular emphasis on NMDA receptor function. An approximately 40% decrease in brain glutathione levels was induced by s.c. administration of L-buthionine-(S,R)-sulfoximine, an inhibitor of glutathione synthesis. Such glutathione deficit did not affect the basal synaptic transmission, but produced several NMDA receptor-dependent and -independent effects. Glutathione deficit caused an increase in excitability of CA1 pyramidal cells. The paired-pulse facilitation was diminished in glutathione-depleted slices, in a manner that was independent of NMDA receptor activity. This suggests that lowering glutathione levels altered presynaptic mechanisms involved in neurotransmitter release. NMDA receptor-dependent long-term potentiation induced by high-frequency stimulation was impaired in glutathione-depleted slices. Pharmacologically isolated NMDA receptor-mediated field excitatory postsynaptic potentials were significantly smaller in L-buthionine-(S,R)-sulfoximine-treated than in control slices. Hypofunction of NMDA receptors under glutathione deficit was explained at least in part by an excessive oxidation of the extracellular redox-sensitive sites of the NMDA receptors. These results indicate that a glutathione deficit, like that observed in schizophrenics, alters short- and long-term synaptic plasticity and affects NMDA receptor function. Thus, glutathione deficit could be one causal factor for the hypofunction of NMDA receptors in schizophrenia.

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Age-associated shifts in intracellular redox state to a pro-oxidizing environment are linked to reduced NMDAR activity via the redox regulation of CaMKII, and can be rescued by intracellular GSH.
“Ageassociated shifts in intracellular redox state to a pro-oxidizing environment have been linked to reduced NMDAR activity via the redox regulation of calcium/ calmodulin-dependent protein kinase type II (CaMKII), and can be rescued by intracellular GSH 72 .”
From Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis (2016) · cites this paper as [72]

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Selective neuronal vulnerability to oxidative stress in the brain
Wang, X. (2010) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2010.00012 · Cited by 1,008 · see citing works
Long-Chain ω-3 Fatty Acids for Indicated Prevention of Psychotic Disorders: A Randomized, Placebo-Controlled Trial
Amminger, G. P., Schäfer, M. R., Papageorgiou, K., Klier, C. M., Cotton, S. M., Harrigan, S. M., Mackinnon, A., McGorry, P. D., & Berger, G. E. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2009.192 · Cited by 896 · see citing works
Glutamate and Schizophrenia: Phencyclidine, N‐Methyl‐d‐Aspartate Receptors, and Dopamine–Glutamate Interactions
Javitt, D. C. (2007) · International review of neurobiology · doi:10.1016/s0074-7742(06)78003-5 · Cited by 563 · see citing works
N-Acetyl Cysteine as a Glutathione Precursor for Schizophrenia—A Double-Blind, Randomized, Placebo-Controlled Trial
Berk, M., Copolov, D., Dean, O., Lu, K., Jeavons, S., Schapkaitz, I., Anderson-Hunt, M., Judd, F., Katz, F., Katz, P., et al. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.03.004 · Cited by 552 · see citing works
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N-Acetyl Cysteine for Depressive Symptoms in Bipolar Disorder—A Double-Blind Randomized Placebo-Controlled Trial
Berk, M., Copolov, D. L., Dean, O., Lu, K., Jeavons, S., Schapkaitz, I., Anderson-Hunt, M., & Bush, A. I. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.04.022 · Cited by 500 · see citing works
NMDA Receptor Hypofunction, Parvalbumin-Positive Neurons, and Cortical Gamma Oscillations in Schizophrenia
Gonzalez-Burgos, G., & Lewis, D. A. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs010 · Cited by 478 · see citing works
Oxidative stress in schizophrenia: An integrated approach
Bitanihirwe, B. K. Y., & Woo, T.-U. W. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.008 · Cited by 474 · see citing works
The promise of N-acetylcysteine in neuropsychiatry
Berk, M., Malhi, G. S., Gray, L. J., & Dean, O. M. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.01.001 · Cited by 434 · see citing works
N-methyl-d-aspartate (NMDA) receptor dysfunction or dysregulation: The final common pathway on the road to schizophrenia?
Kantrowitz, J. T., & Javitt, D. C. (2010) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2010.04.006 · Cited by 397 · see citing works
Redox dysregulation, neurodevelopment, and schizophrenia
Do, K. Q., Cabungcal, J. H., Frank, A., Steullet, P., & Cuenod, M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.05.001 · Cited by 384 · see citing works
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Glutathione Precursor, N-Acetyl-Cysteine, Improves Mismatch Negativity in Schizophrenia Patients
Lavoie, S., Murray, M. M., Deppen, P., Knyazeva, M. G., Berk, M., Boulat, O., Bovet, P., Bush, A. I., Conus, P., Copolov, D., et al. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301624 · Cited by 371 · see citing works
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Neurophysiological biomarkers for drug development in schizophrenia
Javitt, D. C., Spencer, K., Thaker, G. K., Winterer, G., & Hajós, M. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2463 · Cited by 340 · see citing works
Impaired glutathione synthesis in schizophrenia: Convergent genetic and functional evidence
Gysin, R., Kraftsik, R., Sandell, J., Bovet, P., Chappuis, C., Conus, P., Deppen, P., Preisig, M., Ruiz, V., Steullet, P., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706778104 · Cited by 309 · see citing works
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Linking early-life NMDAR hypofunction and oxidative stress in schizophrenia pathogenesis
Hardingham, G. E., & Do, K. Q. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.19 · Cited by 304 · see citing works
Overview on the Effects of N-Acetylcysteine in Neurodegenerative Diseases
Tardiolo, G., Bramanti, P., & Mazzon, E. (2018) · Molecules · doi:10.3390/molecules23123305 · Cited by 287 · see citing works
The origin of NMDA receptor hypofunction in schizophrenia
Nakazawa, K., & Sapkota, K. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107426 · Cited by 277 · see citing works
Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology?
Steullet, P., Cabungcal, J. H., Monin, A., Dwir, D., O'Donnell, P., Cuenod, M., & Do, K. Q. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2014.06.021 · Cited by 262 · see citing works
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Glutamatergic theories of schizophrenia.
Javitt, D. C. (2010) · PubMed · Cited by 248 · see citing works
Schizophrenia and Oxidative Stress: Glutamate Cysteine Ligase Modifier as a Susceptibility Gene
Tosic, M., Ott, J., Barral, S., Bovet, P., Deppen, P., Gheorghita, F., Matthey, M.-L., Parnas, J., Preisig, M., Saraga, M., et al. (2006) · The American Journal of Human Genetics · doi:10.1086/507566 · Cited by 234 · see citing works
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Antipsychotic Drugs: Comparison in Animal Models of Efficacy, Neurotransmitter Regulation, and Neuroprotection
Lieberman, J. A., Bymaster, F. P., Meltzer, H. Y., Deutch, A. Y., Duncan, G. E., Marx, C. E., Aprille, J. R., Dwyer, D. S., Li, X., Mahadik, S. P., et al. (2008) · Pharmacological Reviews · doi:10.1124/pr.107.00107 · Cited by 223 · see citing works
Oxidative Stress in Traumatic Brain Injury
Fesharaki‐Zadeh, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232113000 · Cited by 220 · see citing works
Thinking Outside the Cleft to Understand Synaptic Activity: Contribution of the Cystine-Glutamate Antiporter (System xc−) to Normal and Pathological Glutamatergic Signaling
Bridges, R., Lutgen, V., Lobner, D., & Baker, D. A. (2012) · Pharmacological Reviews · doi:10.1124/pr.110.003889 · Cited by 205 · see citing works
Imaging glutamate in schizophrenia: review of findings and implications for drug discovery
Poels, E. M. P., Kegeles, L. S., Kantrowitz, J. T., Slifstein, M., Javitt, D. C., Lieberman, J. A., Abi-Dargham, A., & Girgis, R. R. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.136 · Cited by 205 · see citing works
Juvenile Antioxidant Treatment Prevents Adult Deficits in a Developmental Model of Schizophrenia
Cabungcal, J.-H., Counotte, D. S., Lewis, E. M., Tejeda, H. A., Piantadosi, P., Pollock, C., Calhoon, G. G., Sullivan, E. M., Presgraves, E., Kil, J., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.028 · Cited by 204 · see citing works
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Redox Dysregulation Affects the Ventral But Not Dorsal Hippocampus: Impairment of Parvalbumin Neurons, Gamma Oscillations, and Related Behaviors
Steullet, P., Cabungcal, J.-H., Kulak, A., Kraftsik, R., Chen, Y., Dalton, T. P., Cuenod, M., & Do, K. Q. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3857-09.2010 · Cited by 202 · see citing works
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Mitochondria, Metabolism, and Redox Mechanisms in Psychiatric Disorders
Kim, Y., Vadodaria, K. C., Lenkei, Z., Kato, T., Gage, F. H., Marchetto, M. C., & Santos, R. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2018.7606 · Cited by 189 · see citing works
The Glutathione System: A New Drug Target in Neuroimmune Disorders
Morris, G., Anderson, G., Dean, O. M., Berk, M., Gałecki, P., Martín-Subero, M., & Maes, M. H. J. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8705-x · Cited by 187 · see citing works
The Glutathione System in Parkinson’s Disease and Its Progression
Bjørklund, G., Peana, M., Maes, M., Dadar, M., & Severin, B. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.004 · Cited by 186 · see citing works
Inflammation in schizophrenia: A question of balance
Leza, J. C., García‐Bueno, B., Bioque, M., Arango, C., Parellada, M., Kim, Q., O’Donnell, P., & Bernardo, M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.014 · Cited by 183 · see citing works
Neuroinflammation and Oxidative Stress in Psychosis and Psychosis Risk
Barron, H., Hafizi, S., Andreazza, A. C., & Mizrahi, R. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030651 · Cited by 176 · see citing works
Does schizophrenia arise from oxidative dysregulation of parvalbumin-interneurons in the developing cortex?
Behrens, M. M., & B, T. J. S. A. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.06.002 · Cited by 160 · see citing works
Implications for reactive oxygen species in schizophrenia pathogenesis
Koga, M., Serritella, A. V., Sawa, A., & Sedlak, T. W. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.06.022 · Cited by 158 · see citing works
N-Acetylcysteine as an Adjunct to Risperidone for Treatment of Negative Symptoms in Patients With Chronic Schizophrenia: A Randomized, Double-Blind, Placebo-Controlled Study
Farokhnia, M., Azarkolah, A., Adinehfar, F., Khodaie-Ardakani, M.-R., Hosseini, S.-M.-R., Yekehtaz, H., Tabrizi, M., Rezaei, F., Salehi, B., Sadeghi, S.-M.-H., et al. (2013) · Clinical Neuropharmacology · doi:10.1097/wnf.0000000000000001 · Cited by 155 · see citing works
Glutathione and glutamate in schizophrenia: a 7T MRS study
Kumar, J., Liddle, E. B., Fernandes, C. C., Palaniyappan, L. K., Hall, E. L., Robson, S. E., Simmonite, M., Jan, F., Katshu, M. Z. U. H., Qureshi, A., et al. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0104-7 · Cited by 154 · see citing works
The role of glutathione redox imbalance in autism spectrum disorder: A review
Bjørklund, G., Tinkov, A. A., Hosnedlová, B., Kizek, R., Ajsuvakova, O. P., Chirumbolo, S., Геннадиевна, С. М., Peana, M., Dadar, M., El-Ansary, A. K., et al. (2020) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.07.017 · Cited by 150 · see citing works
Schizophrenia: Linking prenatal infection to cytokines, the tryptophan catabolite (TRYCAT) pathway, NMDA receptor hypofunction, neurodevelopment and neuroprogression
Anderson, G., & Maes, M. H. J. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.06.014 · Cited by 144 · see citing works
Neurodevelopmental damage after prenatal infection: role of oxidative stress in the fetal brain
Lanté, F., Meunier, J., Guiramand, J., Maurice, T., Cavalier, M., de Jesus Ferreira, M.-C., Aimar, R., Cohen-Solal, C., Vignes, M., & Barbanel, G. (2007) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.01.027 · Cited by 140 · see citing works
Synaptic NMDA receptor activity is coupled to the transcriptional control of the glutathione system
Baxter, P. S., Bell, K. F. S., Hasel, P., Kaindl, A. M., Fricker, M., Thomson, D., Cregan, S. P., Gillingwater, T. H., & Hardingham, G. E. (2015) · Nature Communications · doi:10.1038/ncomms7761 · Cited by 139 · see citing works
Animal models of bipolar mania: The past, present and future
Logan, R. W., & McClung, C. A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2015.08.041 · Cited by 136 · see citing works
Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia
Cuénod, M., Steullet, P., Cabungcal, J.-H., Dwir, D., Khadimallah, I., Klauser, P., Conus, P., & Kim, Q. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01374-w · Cited by 129 · see citing works
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Late <i>N</i>‐acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation
Lanté, F., Meunier, J., Guiramand, J., De Jesus Ferreira, M., Cambonie, G., Aimar, R., Cohen‐Solal, C., Maurice, T., Vignes, M., & Barbanel, G. (2008) · Hippocampus · doi:10.1002/hipo.20421 · Cited by 124 · see citing works
Redox Dysregulation in the Pathophysiology of Schizophrenia and Bipolar Disorder: Insights from Animal Models
Kulak, A., Steullet, P., Cabungcal, J.-H., Werge, T., Ingason, A., Cuenod, M., & Do, K. Q. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4858 · Cited by 124 · see citing works
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Thinking Glutamatergically: Changing Concepts of Schizophrenia Based Upon Changing Neurochemical Models
Kantrowitz, J. T., & Javitt, D. C. (2010) · Clinical Schizophrenia & Related Psychoses · doi:10.3371/csrp.4.3.6 · Cited by 118 · see citing works
Glutamate in schizophrenia: Neurodevelopmental perspectives and drug development
Egerton, A., Grace, A. A., Stone, J. M., Bossong, M. G., Sand, M. S., & McGuire, P. K. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.09.013 · Cited by 113 · see citing works
Contribution of Cystine–Glutamate Antiporters to the Psychotomimetic Effects of Phencyclidine
Baker, D. L., Madayag, A., Kristiansen, L. V., Meador‐Woodruff, J. H., Haroutunian, V. H., & Raju, I. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301532 · Cited by 112 · see citing works
Spatial and temporal boundaries of NMDA receptor hypofunction leading to schizophrenia
Nakazawa, K., Jeevakumar, V., & Nakao, K. (2017) · npj Schizophrenia · doi:10.1038/s41537-016-0003-3 · Cited by 110 · see citing works
Theranostic Biomarkers for Schizophrenia
Perković, M. N., Erjavec, G. N., Štrac, D. Š., Uzun, S., Kozumplik, O., & Pivac, N. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040733 · Cited by 97 · see citing works
Potential Roles of Redox Dysregulation in the Development of Schizophrenia
Perkins, D. O., Jeffries, C. D., & Do, K. Q. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.03.016 · Cited by 103 · see citing works
Antioxidant Therapies in Traumatic Brain Injury
Pietro, V. D., Yakoub, K. M., Caruso, G., Lazzarino, G., Signoretti, S., Barbey, A. K., Tavazzi, B., Lazzarino, G., Belli, A., & Amorini, A. M. (2020) · Antioxidants · doi:10.3390/antiox9030260 · Cited by 101 · see citing works
Effects of Bisphenol-A and Other Endocrine Disruptors Compared With Abnormalities of Schizophrenia: An Endocrine-Disruption Theory of Schizophrenia
Brown, J. S. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm147 · Cited by 100 · see citing works
Glutathione levels and activities of glutathione metabolism enzymes in patients with schizophrenia: A systematic review and meta-analysis
Tsugawa, S., Noda, Y., Tarumi, R., Mimura, Y., Yoshida, K., Iwata, Y., ElSalhy, M., Kuromiya, M., Kurose, S., Masuda, F., et al. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881119845820 · Cited by 99 · see citing works
Insights into CNS ageing from animal models of senescence
Yeoman, M. S., Scutt, G., & Faragher, R. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3230 · Cited by 98 · see citing works
A randomized placebo-controlled trial of an omega-3 fatty acid and vitamins E+C in schizophrenia
Bentsen, H., Osnes, K., Refsum, H., Solberg, D. K., & Bøhmer, T. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.110 · Cited by 97 · see citing works
Therapeutic effect of adjunctive N-acetyl cysteine (NAC) on symptoms of chronic schizophrenia: A double-blind, randomized clinical trial
Sepehrmanesh, Z., Heidary, M., Akasheh, N., Akbari, H., & Heidary, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.11.001 · Cited by 97 · see citing works
Glutathione deficit during development induces anomalies in the rat anterior cingulate GABAergic neurons: Relevance to schizophrenia
Cabungcal, J.-H., Nicolas, D., Kraftsik, R., Cuénod, M., Do, K. Q., & Hornung, J.-P. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.01.003 · Cited by 96 · see citing works
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Glutathione Restores the Mechanism of Synaptic Plasticity in Aged Mice to That of the Adult
Robillard, J. M., Gordon, G. R., Choi, H. B., Christie, B. R., & MacVicar, B. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020676 · Cited by 89 · see citing works
One-carbon metabolism and schizophrenia: current challenges and future directions
Krebs, M., Bellon, A., Mainguy, G., Jay, T. M., & Frieling, H. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2009.10.001 · Cited by 87 · see citing works
Schizophrenia is primed for an increased expression of depression through activation of immuno-inflammatory, oxidative and nitrosative stress, and tryptophan catabolite pathways
Anderson, G., Maes, M. H. J., & Berk, M. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.07.016 · Cited by 83 · see citing works
Could Alzheimer’s Disease Originate in the Periphery and If So How So?
Morris, G., Berk, M., Maes, M. H. J., & Puri, B. K. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1092-y · Cited by 83 · see citing works
Transitory glutathione deficit during brain development induces cognitive impairment in juvenile and adult rats: Relevance to schizophrenia
Cabungcal, J.-H., Preissmann, D., Delseth, C., Cuénod, M., Kim, Q., & Schenk, F. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.03.001 · Cited by 83 · see citing works
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Glutathione precursor N-acetyl-cysteine modulates EEG synchronization in schizophrenia patients: a double-blind, randomized, placebo-controlled trial
Carmeli, C., Knyazeva, M. G., Cuénod, M., & Do, K. Q. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029341 · Cited by 81 · see citing works
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Effects of pre-natal alcohol exposure on hippocampal synaptic plasticity: Sex, age and methodological considerations
Fontaine, C. J., Patten, A. R., Sickmann, H. M., Helfer, J. L., & Christie, B. R. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.02.014 · Cited by 79 · see citing works
The impact of glutathione metabolism in autism spectrum disorder
Bjørklund, G., Doşa, M. D., Maes, M. H. J., Dadar, M., Frye, R. E., Peana, M., & Chirumbolo, S. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105437 · Cited by 77 · see citing works
Stimulated Efflux of Amino Acids and Glutathione from Cultured Hippocampal Slices by Omission of Extracellular Calcium
Stridh, M. H., Tranberg, M., Weber, S. G., Blomstrand, F., & Sandberg, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m704153200 · Cited by 72 · see citing works
Molecular Profiles of Parvalbumin-Immunoreactive Neurons in the Superior Temporal Cortex in Schizophrenia
Pietersen, C. Y., Mauney, S. A., Kim, S. S., Passeri, E., Lim, M. P., Rooney, R. J., Goldstein, J. M., Petryshen, T. L., Seidman, L. J., Shenton, M. E., et al. (2014) · Journal of Neurogenetics · doi:10.3109/01677063.2013.878339 · Cited by 67 · see citing works
Deletion of selenoprotein P results in impaired function of parvalbumin interneurons and alterations in fear learning and sensorimotor gating
Pitts, M. W., Raman, A. V., Hashimoto, A. C., Todorovic, C., Nichols, R. A., & Berry, M. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.02.017 · Cited by 67 · see citing works
Impaired Attention and Synaptic Senescence of the Prefrontal Cortex Involves Redox Regulation of NMDA Receptors
Guidi, M., Kumar, A., & Foster, T. C. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3523-14.2015 · Cited by 63 · see citing works
Glutathione Modulates Ca2+ Influx and Oxidative Toxicity Through TRPM2 Channel in Rat Dorsal Root Ganglion Neurons
Nazıroğlu, M., Özgül, C., Çiğ, B., Doğan, S., & Uğuz, A. C. (2011) · The Journal of Membrane Biology · doi:10.1007/s00232-011-9382-6 · Cited by 63 · see citing works
Markers of fungal translocation are elevated during post-acute sequelae of SARS-CoV-2 and induce NF-κB signaling
Giron, L. B., Peluso, M. J., Ding, J., Kenny, G., Zilberstein, N., Koshy, J., Hong, K. Y., Rasmussen, H. E., Miller, G. E., Bishehsari, F., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.160989 · Cited by 63 · see citing works
Genetic Dysregulation of Glutathione Synthesis Predicts Alteration of Plasma Thiol Redox Status in Schizophrenia
Gysin, R., Kraftsik, R., Boulat, O., Bovet, P., Conus, P., Comte-Krieger, E., Polari, A. R., Steullet, P., Preisig, M., Bellier-Teichmann, T., et al. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3463 · Cited by 62 · see citing works
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Cocaine-Induced Adaptations in Cellular Redox Balance Contributes to Enduring Behavioral Plasticity
Uys, J. D. K., Knackstedt, L. A., Hurt, P., Tew, K. D., Manevich, Y., Hutchens, S., Townsend, D. M., & Kalivas, P. W. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.143 · Cited by 60 · see citing works
Chronic stress, hippocampus and parvalbumin-positive interneurons: what do we know so far?
Zaletel, I. V., Filipović, D., & Puškaš, N. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0042 · Cited by 57 · see citing works
Glutathione-coordinated metal complexes as substrates for cellular transporters
Pearson, S. A., & Cowan, J. A. (2021) · Metallomics · doi:10.1093/mtomcs/mfab015 · Cited by 57 · see citing works
Risperidone reverses phencyclidine induced decrease in glutathione levels and alterations of antioxidant defense in rat brain
Stojković, T., Radonjić, N. V., Velimirović, M., Jevtić, G., POPOVIC, V. M., Doknić, M., & Petronijević, N. (2012) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2012.06.013 · Cited by 53 · see citing works
Accelerating neuronal aging in in vitro model brain disorders: a focus on reactive oxygen species
Campos, P. B., Paulsen, B. S., & Rehen, S. K. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00292 · Cited by 52 · see citing works
Role of GABAergic antagonism in the neuroprotective effects of bilobalide
Kiewert, C., Kumar, V., Hildmann, O., Rueda, M., Hartmann, J., Naik, R. S., & Klein, J. (2006) · Brain Research · doi:10.1016/j.brainres.2006.10.042 · Cited by 52 · see citing works
Melatonin reverts methamphetamine-induced learning and memory impairments and hippocampal alterations in mice
Veschsanit, N., Yang, J., Ngampramuan, S., Viwatpinyo, K., Pinyomahakul, J., Lwin, T., Chancharoen, P., Rungruang, S., Govitrapong, P., & Mukda, S. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.118844 · Cited by 47 · see citing works
Impairments in hippocampal synaptic plasticity following prenatal ethanol exposure are dependent on glutathione levels
Patten, A. R., Brocardo, P. S., Sakiyama, C., Wortman, R. C., Noonan, A., Gil‐Mohapel, J., & Christie, B. R. (2013) · Hippocampus · doi:10.1002/hipo.22199 · Cited by 45 · see citing works
The ameliorative effect ofN‐acetylcysteine against penconazole induced neurodegenerative and neuroinflammatory disorders in rats
Morgan, A. M., Hassanen, E. I., Ogaly, H. A., Dulmani, S. A. A., Al‐Zahrani, F. A. M., Galal, M. K., Kamel, S., Rashad, M. M., Ibrahim, M. A., & Hussien, A. M. (2021) · Journal of Biochemical and Molecular Toxicology · doi:10.1002/jbt.22884 · Cited by 45 · see citing works
Cognitive Impairment in Schizophrenia: a Review of Developmental and Genetic Models, and Pro-cognitive Profile of the Optimised D3 > D2 Antagonist, S33138
Millan, M. J., & Brocco, M. (2008) · Therapies · doi:10.2515/therapie:2008041 · Cited by 44 · see citing works
Fluorescence Probe for Imaging N-Methyl- d -aspartate Receptors and Monitoring GSH Selectively Using Two-Photon Microscopy
Kwon, N., Lim, C. S., Ko, G., Ha, J., Lee, D., Yin, J., Kim, H. M., & Yoon, J. (2021) · Analytical Chemistry · doi:10.1021/acs.analchem.1c02350 · Cited by 43 · see citing works
The impact of alcohol and tobacco use on in vivo glutathione in youth with bipolar disorder: An exploratory study
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Decrease in brain glutathione (GSH) in schizophrenia: effects of a deficiency in GSH on synaptic transmission and plasticity
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Schizophrenia: glutathione deficit as a new vulnerability factor for disconnectivity syndrome
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Self-citation
Schizophrenia: glutathione deficit in cerebrospinal fluid and prefrontal cortex in vivo
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Self-citation

Authors: Steullet, P., Neijt, H. C., Cuénod, M., & Do, K. Q.
Affiliations: Centre Hospitalier Universitaire Vaudois (CH)
Novartis (Switzerland) (CH)
University of Lausanne (CH)
ORCID: Steullet, P.
Cuénod, M.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2006-01
Volume: 137
Issue: 3
Pages: 807-819
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2005.10.014
OpenAlex: W2004830149
Cited by: 173
References: 87
Citations by year: 2025: 4 · 2024: 3 · 2023: 4 · 2022: 5 · 2021: 13 · 2020: 6 · 2019: 6 · 2018: 10 · 2017: 12 · 2016: 11 · 2015: 12 · 2014: 11 · 2013: 9 · 2012: 16
FWCI: 2.65
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
Keywords: NMDA receptor hypofunction, synaptic plasticity, schizophrenia, L-buthionine sulfoximine, glutathione synthesis inhibition, paired-pulse facilitation, long-term potentiation, presynaptic neurotransmitter release, hippocampus, glutathione metabolism
MeSH terms: Animals, Antimetabolites, Electric Stimulation, Electrophysiology, Glutamate-Cysteine Ligase, Glutathione, Membrane Potentials, Synaptic Transmission, Neuronal Plasticity, Schizophrenia, Synapses, Receptors, N-Methyl-D-Aspartate, Rats, Wistar, Long-Term Potentiation, Buthionine Sulfoximine, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques

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Synaptic plasticity impairment and hypofunction of NMDA receptors induced by glutathione deficit: Relevance to schizophrenia

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