Redox Dysregulation in the Pathophysiology of Schizophrenia and Bipolar Disorder: Insights from Animal Models

Kulak, Anita; Steullet, Pascal; Cabungcal, Jan-Harry; Werge, Thomas; Ingason, Andrés; Cuenod, Michel; Do, Kim Quang

doi:10.1089/ars.2012.4858

Cited by 130Schizophrenia research and treatmentRedox biology and oxidative stressTryptophan and brain disorders

Redox Dysregulation in the Pathophysiology of Schizophrenia and Bipolar Disorder: Insights from Animal Models

Kulak, Anita, Steullet, Pascal, Cabungcal, Jan-Harry, Werge, Thomas, Ingason, Andrés, Cuenod, Michel, Do, Kim Quang·2013·Antioxidants & Redox Signaling

DOI 10.1089/ars.2012.4858

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Abstract

SIGNIFICANCE: Schizophrenia (SZ) and bipolar disorder (BD) are classified as two distinct diseases. However, accumulating evidence shows that both disorders share genetic, pathological, and epidemiological characteristics. Based on genetic and functional findings, redox dysregulation due to an imbalance between pro-oxidants and antioxidant defense mechanisms has been proposed as a risk factor contributing to their pathophysiology. RECENT ADVANCES: Altered antioxidant systems and signs of increased oxidative stress are observed in peripheral tissues and brains of SZ and BD patients, including abnormal prefrontal levels of glutathione (GSH), the major cellular redox regulator and antioxidant. Here we review experimental data from rodent models demonstrating that permanent as well as transient GSH deficit results in behavioral, morphological, electrophysiological, and neurochemical alterations analogous to pathologies observed in patients. Mice with GSH deficit display increased stress reactivity, altered social behavior, impaired prepulse inhibition, and exaggerated locomotor responses to psychostimulant injection. These behavioral changes are accompanied by N-methyl-D-aspartate receptor hypofunction, elevated glutamate levels, impairment of parvalbumin GABA interneurons, abnormal neuronal synchronization, altered dopamine neurotransmission, and deficient myelination. CRITICAL ISSUES: Treatment with the GSH precursor and antioxidant N-acetylcysteine normalizes some of those deficits in mice, but also improves SZ and BD symptoms when given as adjunct to antipsychotic medication. FUTURE DIRECTIONS: These data demonstrate the usefulness of GSH-deficient rodent models to identify the mechanisms by which a redox imbalance could contribute to the development of SZ and BD pathophysiologies, and to develop novel therapeutic approaches based on antioxidant and redox regulator compounds.

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PNNs consist of highly charged chondroitin sulfate proteoglycans, hyaluronan, tenascin, and link proteins.
“These PNNs consist of highly charged chondroitin sulfate proteoglycans (e.g., aggrecan, neurocan, brevican), hyaluronan, tenascin, and link proteins (31).”
From Perineuronal nets protect fast-spiking interneurons against oxidative stress (2013) · cites this paper as [31]
Multiple genetic and external factors collectively lead to redox dysregulation.
“several divergent genetic (e.g. Gclc, Gclm, Disc1, PRODH, G72, NRG1) (9–17) or external factors (e.g. stress, social isolation, ketamine, neonatal ventral hippocampal lesion) (18–24) collectively lead to redox dysregulation.”
From Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons (2015) · cites this paper as [17]
A pharmacologically induced transient postnatal glutathione deficit causes both immediate and long-term decreased density of parvalbumin-immunoreactive cells in the anterior cingulate cortex.
“A pharmacologically induced transient postnatal deficit in GSH causes both immediate and long-term decreased density of parvalbumin-immunoreactive cells in the anterior cingulate cortex (ACC) (Cabungcal et al., 2006; Kulak et al., 2013; Steullet et al., 2011).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Kulak et al., 2013
This oligodendrocyte deficit recovers in adulthood and is accompanied by an increase in prefrontal N-acetylaspartate, suggesting impaired myelin lipid synthesis during prefrontal cortical maturation.
“This deficit, which recovers in adulthood, is accompanied by an increase in prefrontal N-acetylaspartate (das Neves Duarte et al., 2012), suggesting an impaired myelin lipid synthesis during prefrontal cortical maturation (Kulak et al., 2013).”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Kulak et al., 2013
Other systems, such as the dopamine system, and their reciprocal interactions with the proposed hub certainly participate in schizophrenia pathology.
“Moreover, we have to emphasize that other systems such as the dopamine system known to be implicated in schizophrenia and their reciprocal interactions with the proposed “hub” (see: Avshalumov et al., 2007; Baker et al., 2002; Kulak et al., 2013; Lodge and Grace, 2011; Meiser et al., 2013; Meyer and Feldon, 2009; Moller et al., 2013; Steullet et al., 2008) certainly participate to the pathology.”
From Redox dysregulation, neuroinflammation, and NMDA receptor hypofunction: A “central hub” in schizophrenia pathophysiology? (2016) · cites this paper as Kulak et al., 2013

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de Gelder, B., Vroomen, J., de Jong, S. J., Masthoff, E., Trompenaars, F. J., & Hodiamont, P. P. G. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.02.013 · Cited by 128 · see citing works
N-acetylcysteine normalizes neurochemical changes in the glutathione-deficient schizophrenia mouse model during development
das Neves Duarte, J. M., Kulak, A., Gholam-Razaee, M. M., Cuenod, M., Gruetter, R., & Do, K. Q. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.07.035 · Cited by 124 · see citing works
Self-citation
Bipolar Disorder, Schizoaffective Disorder, and Schizophrenia Overlap
Laursen, T. M., Agerbo, E., & Pedersen, C. B. (2009) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.08m04807 · Cited by 121 · see citing works
Neuropsychological performance and family history in children at age 7 who develop adult schizophrenia or bipolar psychosis in the New England Family Studies
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Amphetamine psychosis and schizophrenia: A dual model
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Neural synchronization deficits to auditory stimulation in bipolar disorder
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Cross-sectional similarities and differences between schizophrenia, schizoaffective disorder and mania or mixed mania with mood-incongruent psychotic features
Pini, S., de Queiroz, V., Dell’Osso, L., Abelli, M., Mastrocinque, C., Saettoni, M., Catena, M., & Cassano, G. B. (2004) · European Psychiatry · doi:10.1016/j.eurpsy.2003.07.007 · Cited by 105 · see citing works
Platelet serotonin and plasma prolactin and cortisol in healthy, depressed and schizophrenic women
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N-acetyl cysteine add-on treatment for bipolar II disorder: a subgroup analysis of a randomized placebo-controlled trial
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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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Reactive Dopamine Metabolites and Neurotoxicity
Hastings, T. G., Lewis, D. A., & Zigmond, M. J. (1996) · Advances in experimental medicine and biology · doi:10.1007/978-1-4757-9480-9_13 · Cited by 94 · see citing works
The NADPH Oxidase NOX2 Controls Glutamate Release: A Novel Mechanism Involved in Psychosis-Like Ketamine Responses
Sorce, S., Schiavone, S., Tucci, P., Colaianna, M., Jaquet, V., Cuomo, V., Dubois‐Dauphin, M., Trabace, L., & Krause, K. H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1491-10.2010 · Cited by 92 · see citing works
Behavioral phenotyping of glutathione-deficient mice: Relevance to schizophrenia and bipolar disorder
Kulak, A., Cuenod, M., & Do, K. Q. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.10.020 · Cited by 90 · see citing works
Self-citation
Association of common copy number variants at the glutathione S-transferase genes and rare novel genomic changes with schizophrenia
Rodríguez-Santiago, B., Brunet, A., Sobrino, B., Serra-Juhé, C., Flores, R., Armengol, L., Vilella, E., Gabau, E., Guitart, M., Guillamat, R., et al. (2010) · Molecular Psychiatry · doi:10.1038/mp.2009.53 · Cited by 88 · see citing works
Modulation of neuronal and recombinant GABAA receptors by redox reagents
Amato, A., Connolly, C. N., Moss, S. J., & Smart, T. G. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.0035z.x · Cited by 85 · see citing works
Platelet serotonin, plasma cortisol, and dexamethasone suppression test in schizophrenic patients
Mück‐Šeler, D., Pivac, N., Jakovljević, M., & Brzović, Z. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00174-7 · Cited by 84 · 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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Life Events and High-Trait Reactivity Together Predict Psychotic Symptom Increases in Schizophrenia
Docherty, N. M., St-Hilaire, A., Aakre, J. M., & Seghers, J. P. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn002 · Cited by 83 · see citing works
Parvalbumin Neurons in the Entorhinal Cortex of Subjects Diagnosed With Bipolar Disorder or Schizophrenia
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Glutathione depletion in the brain disrupts short-term spatial memory in the Y-maze in rats and mice
Dean, O. M., Bush, A. I., Berk, M., Copolov, D., & van den Buuse, M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.11.017 · Cited by 81 · see citing works
Magnetic Resonance Spectroscopy Study of the Antioxidant Defense System in Schizophrenia
Matsuzawa, D., & Hashimoto, K. (2011) · Antioxidants & Redox Signaling · doi:10.1089/ars.2010.3453 · Cited by 79 · see citing works
Neurobiological trait abnormalities in bipolar disorder
Langan, C., & McDonald, C. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.39 · Cited by 77 · see citing works
Oxidative Stress in Schizophrenia: Pathogenetic and Therapeutic Implications
Yao, J. K., & Reddy, R. D. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3646 · Cited by 76 · see citing works
Face Recognition Memory Deficits and Visual Object Memory Performance in Patients With Schizophrenia and Their Relatives
Calkins, M. E., Gur, R. C., Ragland, J. D., & Gur, R. E. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.10.1963 · Cited by 75 · see citing works
Evidence of Disrupted Prepulse Inhibition in Unaffected Siblings of Bipolar Disorder Patients
Giakoumaki, S. G., Roussos, P., Rogdaki, M., Karli, C., Bitsios, P., & Frangou, S. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.12.002 · Cited by 72 · see citing works
Association of DISC1 and TSNAX genes and affective disorders in the depression case–control (DeCC) and bipolar affective case–control (BACCS) studies
Schosser, A., Gaysina, D., Cohen‐Woods, S., Chow, P. C., Martucci, L., Craddock, N. J., FARMER, A. E., Korszun, A., Gunasinghe, C., Gray, J., et al. (2009) · Molecular Psychiatry · doi:10.1038/mp.2009.21 · Cited by 72 · see citing works
Low brain glutathione and ascorbic acid associated with dopamine uptake inhibition during rat's development induce long-term cognitive deficit: relevance to schizophrenia
Castagné, V., Rougemont, M., Cuénod, M., & Kim, Q. (2003) · Neurobiology of Disease · doi:10.1016/j.nbd.2003.09.005 · Cited by 71 · see citing works
Genetic polymorphisms of glutathione S-transferases GSTM1, GSTT1, GSTP1 and GSTA1 as risk factors for schizophrenia
Gravina, P., Spoletini, I., Masini, S., Valentini, A., Vanni, D., Paladini, E., Bossù, P., Caltagirone, C., Federici, G., Spalletta, G., et al. (2010) · Psychiatry Research · doi:10.1016/j.psychres.2010.10.008 · Cited by 71 · see citing works
Levodopa: Alterations in behavior
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The Cortisol Awakening Response in Bipolar Illness: A Pilot Study
Deshauer, D., Duffy, A. C., Alda, M., Grof, E., Albuquerque, J., & Grof, P. (2003) · The Canadian Journal of Psychiatry · doi:10.1177/070674370304800706 · Cited by 65 · see citing works
Effects of N-acetyl-cysteine treatment on glutathione depletion and a short-term spatial memory deficit in 2-cyclohexene-1-one-treated rats
Choy, K. H. C., Dean, O. M., Berk, M., Bush, A. I., & van den Buuse, M. (2010) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2010.09.035 · Cited by 62 · see citing works
Ferulic acid attenuated cognitive deficits and increase in carbonyl proteins induced by buthionine-sulfoximine in mice
Mamiya, T., Kise, M., & Morikawa, K. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.10.029 · Cited by 61 · see citing works
Lack of Maternal Glutamate Cysteine Ligase Modifier Subunit (Gclm) Decreases Oocyte Glutathione Concentrations and Disrupts Preimplantation Development in Mice
Nakamura, B. N., Fielder, T. J., Hoang, Y. D., Lim, J., McConnachie, L. A., Kavanagh, T. J., & Luderer, U. (2011) · Endocrinology · doi:10.1210/en.2011-0207 · Cited by 60 · see citing works
Gender differences in prepulse inhibition (PPI) in bipolar disorder: men have reduced PPI, women have increased PPI
Gogos, A., van den Buuse, M., & Rossell, S. L. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709000480 · Cited by 56 · see citing works
Behavioral and biochemical effects of glutathione depletion in the rat brain
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An animal model with relevance to schizophrenia: sex-dependent cognitive deficits in osteogenic disorder-Shionogi rats induced by glutathione synthesis and dopamine uptake inhibition during development
Castagné, V., Cuénod, M., & Do, K. Q. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.11.012 · Cited by 50 · see citing works
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A single photon emission computerized tomography (SPECT) study of regional cerebral blood flow in bipolar disorder
Bhardwaj, R., Chakrabarti, S., Mittal, B. R., & Sharan, P. (2010) · The World Journal of Biological Psychiatry · doi:10.3109/15622970802575977 · Cited by 50 · see citing works
Visual object processing in schizophrenia: evidence for an associative agnosic deficit
Gabrovska, V. S., Laws, K. R., Sinclair, J., et al. (2002) · Schizophrenia Research · doi:10.1016/s0920-9964(02)00168-8 · Cited by 49 · see citing works
Spatial Learning and Memory Deficits Induced by Dopamine Administration with Decreased Glutathione
Shukitt‐Hale, B., Erat, S., & Joseph, J. A. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(97)00399-7 · Cited by 46 · see citing works
Treatment of agitation in bipolar disorder across the life cycle.
Alderfer, B. S., & Allen, M. H. (2003) · PubMed · Cited by 45 · see citing works
Common risk genes for affective and schizophrenic psychoses
Maier, W. (2008) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-008-2008-z · Cited by 44 · see citing works
Monoaminergic dysregulation in glutathione-deficient mice: Possible relevance to schizophrenia?
Jacobsen, J. P. R., Rodriguiz, R. M., Mørk, A., & Wetsel, W. C. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.01.059 · Cited by 41 · see citing works
Volume reduction of ventromedial prefrontal cortex in bipolar II patients with rapid cycling: A voxel-based morphometric study
Narita, K., Suda, M., Takei, Y., Aoyama, Y., Majima, T., Kameyama, M., Kosaka, H., Amanuma, M., Fukuda, M., & Mikuni, M. (2010) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2010.11.030 · Cited by 38 · see citing works
Assessing oxidative pathway genes as risk factors for bipolar disorder
Fullerton, J. M., Tiwari, Y., Agahi, G., Heath, A., Berk, M., Mitchell, P. B., & Schofield, P. R. (2010) · Bipolar Disorders · doi:10.1111/j.1399-5618.2010.00834.x · Cited by 37 · see citing works
Reduced Anterior Cingulate Cognitive Activation Is Associated with Prefrontal–Temporal Cortical Thinning in Schizophrenia
Schultz, C. C., Koch, K., Wagner, G., Nenadić, I., Schachtzabel, C., Güllmar, D., Reichenbach, J. R., Sauer, H., & Schlösser, R. G. M. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.08.015 · Cited by 32 · see citing works
Mice lacking the glutamate-cysteine ligase modifier subunit are susceptible to myocardial ischaemia–reperfusion injury
Kobayashi, T., Watanabe, Y., Saitō, Y., Fujioka, D., Nakamura, T., Obata, J., Kitta, Y., Yano, T., Kawabata, K., Watanabe, K., et al. (2009) · Cardiovascular Research · doi:10.1093/cvr/cvp342 · Cited by 30 · see citing works
A glutathione deficit alters dopamine modulation of L-type calcium channels via D2 and ryanodine receptors in neurons.
Steullet, P., Lavoie, S., Kraftsik, R., Guidi, R., Gysin, R., Cuenod, M., & Do, K. (2008) · Free Radical Biology & Medicine · doi:10.1016/j.freeradbiomed.2007.12.006 · Cited by 29 · see citing works
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Behavioral Characterization ofGCLM-Knockout Mice, a Model for Enhanced Susceptibility to Oxidative Stress
Cole, T. B., Giordano, G., Co, A. L., Mohar, I., Kavanagh, T. J., & Costa, L. G. (2011) · Journal of Toxicology · doi:10.1155/2011/157687 · Cited by 27 · see citing works
Psychomotor Effects of Dopamine Infusion Under Decreased Glutathione Conditions
Shukitt‐Hale, B., Denisova, N. A., Strain, J. G., & Joseph, J. A. (1997) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(97)00094-4 · Cited by 26 · see citing works
Co-occurring manic symptomatology influences HPA axis alterations in depression
Jabben, N., Nolen, W. A., Smit, J. H., Vreeburg, S. A., Beekman, A. T. F., & Penninx, B. W. J. H. (2011) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2011.03.010 · Cited by 23 · see citing works
Arousability in schizophrenia: relationship to emotional and physiological reactivity and symptom severity
Dinzeo, T. J., Cohen, A. S., Nienow, T. M., & Docherty, N. M. (2008) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.2008.01185.x · Cited by 23 · see citing works
No association between glutathione‐synthesis‐related genes and Japanese schizophrenia
Hanzawa, R., Ohnuma, T., Nagai, Y., Shibata, N., Maeshima, H., Baba, H., Hatano, T., Takebayashi, Y., Hotta, Y., Kitazawa, M., et al. (2010) · Psychiatry and Clinical Neurosciences · doi:10.1111/j.1440-1819.2010.02157.x · Cited by 14 · see citing works
Domain‐specific deficits in schizophrenia
Laws, K. R., Leeson, V. C., & McKenna, P. J. (2006) · Cognitive Neuropsychiatry · doi:10.1080/13546800500286429 · Cited by 10 · see citing works
The Treatment of Acute Agitation in Schizophrenia
Battaglia, J., Robinson, D. G., & Citrome, L. (2007) · CNS Spectrums · doi:10.1017/s1092852900026146 · Cited by 8 · see citing works
Accurate performance of a rat model of schizophrenia in the water maze depends on visual cue availability and stability: A distortion in cognitive mapping abilities?
Preissmann, D., Bertholet, L., Sierro, G., Cabungcal, J.-H., & Schenk, F. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.034 · Cited by 6 · see citing works
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Editorial Board
(2011) · Biological Psychiatry · doi:10.1016/s0006-3223(11)00174-0 · Cited by 1 · see citing works
Untitled work
(1998) · doi:10.1002/(sici)1098-1063(1998)8:6

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Perineuronal nets protect fast-spiking interneurons against oxidative stress
Cabungcal, J.-H., Steullet, P., Morishita, H., Kraftsik, R., Cuenod, M., Hensch, T. K., & Do, K. Q. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300454110 · Cited by 512 · see citing works
“, proline dehydrogenase (oxidase) 1 (PRODH), disrupted in schizophrenia 1 (DISC1), D-amino acid oxidase activator (DAOA or G72), dystrobrevin binding protein 1 (DTNBP1)] (23–27) could, together with oxidative stress generated by environmental insults, contribute to the pathophysiology of these disorders (28, 29).”
BackgroundSelf-citation
Oxidative stress-driven parvalbumin interneuron impairment as a common mechanism in models of schizophrenia
Steullet, P., Cabungcal, J.-H., Coyle, J., Didriksen, M., Gill, K., Grace, A. A., Hensch, T. K., LaMantia, A.-S., Lindemann, L., Maynard, T. M., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.47 · Cited by 360 · see citing works
Self-citation
Markers of Oxidative Stress and Neuroprogression in Depression Disorder
Vaváková, M., Ďuračková, Z., & Trebatická, J. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/898393 · Cited by 324 · see citing works
“Appraisal of antioxidant activity of natural substances is hindered by disagreement between results observed in vivo and in vitro [4, 7, 13, 61, 91].”
Background
ROS and Brain Diseases: The Good, the Bad, and the Ugly
Popa-Wagner, A., Mitran, S., Sivanesan, S., Chang, E., & Buga, A.-M. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/963520 · Cited by 427 · see citing works
“Glutathione deficiency also contributes to abnormalities seen in autistic behavior [40, 103] as well as schizophrenia and bipolar disorders [104].”
Background
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
Self-citation
Glutathione redox imbalance in brain disorders
Gu, F., Chauhan, V. P. S., & Chauhan, A. (2014) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0000000000000134 · Cited by 233 · see citing works
Oxidative Stress‐Related Mechanisms in Schizophrenia Pathogenesis and New Treatment Perspectives
Ermakov, E. A., Dmitrieva, E. M., Parshukova, D. A., Kazantseva, D. V., Vasilieva, A. R., & Smirnova, L. P. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/8881770 · Cited by 252 · see citing works
“Nevertheless, there is a decrease of canonical antioxidant systems, including peroxidases, oxidoreductases, oxidases, and dismutases, confirmed by multiple studies in schizophrenia [281, 282].”
Background
Vitamin D cell signalling in health and disease
Berridge, M. J. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.01.008 · Cited by 214 · see citing works
Translational evaluation of translocator protein as a marker of neuroinflammation in schizophrenia
Notter, T., Coughlin, J. M., Gschwind, T., Weber-Stadlbauer, U., Wang, Y.-C., Kassiou, M., Vernon, A., Benke, D., Pomper, M., Sawa, A., et al. (2018) · Molecular Psychiatry · doi:10.1038/mp.2016.248 · Cited by 195 · see citing works
Glutathione-Dependent Detoxification Processes in Astrocytes
Dringen, R., Brandmann, M., Hohnholt, M. C., & Blumrich, E. (2014) · Neurochemical Research · doi:10.1007/s11064-014-1481-1 · Cited by 184 · see citing works
Vitamin D and Depression: Cellular and Regulatory Mechanisms
Berridge, M. J. (2017) · Pharmacological Reviews · doi:10.1124/pr.116.013227 · Cited by 186 · see citing works
“The elevation of ROS is enhanced by the fact that neurons from patients with depression have much reduced antioxidants such as glutathione (GSH) (Gawryluk et al., 2011; Kulak et al., 2013).”
Background
Assessing Brain Metabolism With 7-T Proton Magnetic Resonance Spectroscopy in Patients With First-Episode Psychosis
Wang, A. M., Pradhan, S., Coughlin, J. M., Trivedi, A. M., DuBois, S. L., Crawford, J. L., Sedlak, T. W., Nucifora, F. C., Nestadt, G., Nucifora, L. G., et al. (2019) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2018.3637 · Cited by 158 · 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 159 · see citing works
Targeting Oxidative Stress and Aberrant Critical Period Plasticity in the Developmental Trajectory to Schizophrenia
Do, K. Q., Cuenod, M., & Hensch, T. K. (2015) · Schizophrenia Bulletin · doi:10.1093/schbul/sbv065 · Cited by 158 · 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
“The genetic associations with GCLC are particularly intriguing in the light of studies that show disease-relevant phenotypes in mouse models of GSH deﬁciency, triggered by both genetic and pharmacological means 5 .”
Influential
Oxidative Stress and Mitochondrial Dysfunction across Broad-Ranging Pathologies: Toward Mitochondria-Targeted Clinical Strategies
Pagano, G., Talamanca, A. A., Castello, G., Cordero, M. D., d’Ischia, M., Gadaleta, M. N., Pallardó, F. V., Petrović, S. Ž., Tiano, L., & Zatterale, A. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/541230 · Cited by 137 · see citing works
“E, GSH, and melatonin) were observed in SZ patients, along with autoimmune responses, as excess IL-6 and PCC levels [184–186].”
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
Self-citation
Targeting of NMDA receptors in new treatments for schizophrenia
Hashimoto, K. (2014) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2014.934225 · Cited by 115 · see citing works
“It is therefore likely that abnormalities in the synthesis and metabolism of GSH are active in the pathophysiology of schizophrenia, pinpointing this system as a possible new therapeutic target [108-111].”
Background
The role of the habenula in the transition from reward to misery in substance use and mood disorders
Batalla, A., Homberg, J. R., Lipina, T. V., Sescousse, G., Luijten, M., Ivanova, S. А., Schellekens, A., & LOONEN, A. J. M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.019 · Cited by 100 · see citing works
Differentiation of oligodendrocyte precursors is impaired in the prefrontal cortex in schizophrenia
Mauney, S. A., Pietersen, C. Y., Sonntag, K., & Woo, T.-U. W. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.10.042 · Cited by 96 · see citing works
“Oxidative stress is increasingly recognized as an important mechanism that may lead to the cellular insults characteristic of the pathophysiology of schizophrenia (Bitanihirwe and Woo, 2011; Do et al., 2009; Do et al., 2015; Fournier et al., 2014; Kulak et al., 2013).”
Background
Prolonged Period of Cortical Plasticity upon Redox Dysregulation in Fast-Spiking Interneurons
Morishita, H., Cabungcal, J.-H., Chen, Y., Do, K. Q., & Hensch, T. K. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.026 · Cited by 92 · see citing works
Self-citation
Impaired synthesis and antioxidant defense of glutathione in the cerebellum of autistic subjects: Alterations in the activities and protein expression of glutathione-related enzymes
Gu, F., Chauhan, V. P. S., & Chauhan, A. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2013.07.021 · Cited by 88 · see citing works
Mitochondrial, exosomal miR137-COX6A2 and gamma synchrony as biomarkers of parvalbumin interneurons, psychopathology, and neurocognition in schizophrenia
Khadimallah, I., Jenni, R., Cabungcal, J.-H., Cleusix, M., Fournier, M., Béard, E., Klauser, P., Knebel, J., Murray, M. M., Retsa, C., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01313-9 · Cited by 88 · see citing works
Self-citation
A Critical Role for Astrocytes in Hypercapnic Vasodilation in Brain
Howarth, C., Sutherland, B. A., Choi, H. B., Martin, C. J., Lind, B. L., Khennouf, L., LeDue, J. M., Pakan, J. M. P., Ko, R. W. Y., Ellis‐Davies, G. C. R., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0005-16.2016 · Cited by 82 · see citing works
“Alterations in the redox status of brain tissue that are ultimately linked to cellular GSH levels have been observed in numerous neurological and psychiatric disorders (Slivka and Cohen, 1993; Tohgi et al., 1995, 1999; Ansari and Scheff, 2010; Zhang et al., 2012; Kulak et al., 2013).”
Background
Sulforaphane Augments Glutathione and Influences Brain Metabolites in Human Subjects: A Clinical Pilot Study
Sedlak, T. W., Nucifora, L. G., Koga, M., Shaffer, L. S., Higgs, C. P., Tanaka, T., Wang, A. M., Coughlin, J. M., Barker, P. B., Fahey, J. W., et al. (2017) · Complex Psychiatry · doi:10.1159/000487639 · Cited by 77 · see citing works
Vitamin D deficiency: infertility and neurodevelopmental diseases (attention deficit hyperactivity disorder, autism, and schizophrenia)
Berridge, M. J. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00188.2017 · Cited by 74 · see citing works
Synaptic deficits in iPSC-derived cortical interneurons in schizophrenia are mediated by NLGN2 and rescued by N-acetylcysteine
Kathuria, A., Lopez-Lengowski, K., Watmuff, B., McPhie, D. L., Cohen, B. M., & Karmacharya, R. (2019) · Translational Psychiatry · doi:10.1038/s41398-019-0660-x · Cited by 73 · see citing works
Glutathione S -transferases promote proinflammatory astrocyte-microglia communication during brain inflammation
Kano, S., Choi, E. Y., Dohi, E., Agarwal, S., Chang, D. J., Wilson, A. M., Lo, B. D., Rose, I. V. L., Gonzalez, S., Imai, T., et al. (2019) · Science Signaling · doi:10.1126/scisignal.aar2124 · Cited by 72 · see citing works
Oxidation-reduction mechanisms in psychiatric disorders: A novel target for pharmacological intervention
Rossetti, A. C., Paladini, M. S., Riva, M. A., & Molteni, R. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107520 · Cited by 70 · 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
“Although the precise pathophysiological events that lead to the dysfunction of PV neurons remain unknown, there has been increasing evidence suggesting that oxidative injury may be a major culprit (Behrens & Sejnowski, 2009; Bitanihirwe & Woo, 2011; Do et al., 2009; Kulak et al., 2013; Nakazawa et al., 2011; Powell et…”
Background
In Vivo Imaging with Genetically Encoded Redox Biosensors
Kostyuk, A. I., Panova, A. S., Kokova, A. D., Kotova, D. A., Maltsev, D. I., Podgorny, O. V., Belousov, V. V., & Bilan, D. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218164 · Cited by 63 · see citing works
TRPM2, a Susceptibility Gene for Bipolar Disorder, Regulates Glycogen Synthase Kinase-3 Activity in the Brain
Jang, Y., Lee, S., Lee, B., Jung, S., Khalid, A., Uchida, K., Tominaga, M., Jeon, D., & Oh, U. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5251-14.2015 · Cited by 62 · see citing works
“Recently, various animal models, including ge- netically engineered mice, have been used in investigations designed to investigate the pathophysiology of mood disorders (Nestler and Hyman, 2010; Kulak et al., 2013).”
Background
Redox Probing for Chemical Information of Oxidative Stress
Kim, E., Winkler, T. E., Kitchen, C., Kang, M., Banis, G., Bentley, W. E., Kelly, D. L., Reza Ghodssi, A., & Payne, G. F. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.6b03620 · Cited by 57 · see citing works
Oxidation and nitration in dopaminergic areas of the prefrontal cortex from patients with bipolar disorder and schizophrenia
Kim, H. K., Andreazza, A. C., Yeung, P., Isaacs-Trepanier, C., & Young, L. T. (2014) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130155 · Cited by 57 · see citing works
“Previous studies have consistently reported increased markers of oxidative stress for both patients with schizophrenia and BD, where increased levels of protein carbonyl groups and lipid peroxidation have been found.(6,9) Oxidation of thiol groups can alter protein structure and function(49) and may be a contributing…”
Background
Dysfunctional mitochondrial processes contribute to energy perturbations in the brain and neuropsychiatric symptoms
Büttiker, P., Weissenberger, S., Esch, T., Anders, M., Raboch, J., Ptáček, R., Kream, R. M., & Stefano, G. B. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1095923 · Cited by 64 · 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
“In this section, we have focused on ROS as the central player in the pathogenesis of these diseases as many age-related impairments ultimately converge on and negatively impact cell respiration, resulting in the overproduction of ROS.”
Background
Connecting Biology to Electronics: Molecular Communication via Redox Modality
Liu, Y., Li, J., Tschirhart, T., Terrell, J. L., Kim, E., Tsao, C., Kelly, D. L., Bentley, W. E., & Payne, G. F. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201700789 · Cited by 52 · see citing works
Advanced glycation end products and schizophrenia: A systematic review
Kouidrat, Y., Amad, A., Arai, M., Miyashita, M., Lalau, J., Loas, G., & Itokawa, M. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.04.023 · Cited by 51 · see citing works
“…genetic and key biochemical systems involved in the disease and suggest that oxidative stress contributes to the pathophysiology of schizophrenia (Emiliani et al., 2014; Itokawa et al., 2014; Kulak et al., 2013; Wu et al., 2013). logy, University of Picardiefax: þ33 3 22 45 53 34. ouidrat).”
Background
Impaired Metabolic Reactivity to Oxidative Stress in Early Psychosis Patients
Fournier, M., Ferrari, C., Baumann, P. S., Polari, A., Monin, A., Bellier-Teichmann, T., Wulff, J., Pappan, K. L., Cuenod, M., Conus, P., et al. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu053 · Cited by 48 · see citing works
MicroRNA Schizophrenia: Etiology, Biomarkers and Therapeutic Targets.
Zhang, H., Du, Y., Chen, L., Yuan, Z.-Q., & Cheng, Y. (2023) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105064 · Cited by 43 · see citing works
Microglia under psychosocial stressors along the aging trajectory: Consequences on neuronal circuits, behavior, and brain diseases
Tian, L., Hui, C. W., Bisht, K., Tan, Y., Sharma, K. P., Chen, S., Zhang, X., & Tremblay, M. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.01.007 · Cited by 47 · see citing works
Basal low antioxidant capacity correlates with cognitive deficits in early onset psychosis. A 2-year follow-up study
Martínez‐Cengotitabengoa, M., Micó, J. A., Arango, C., Castro‐Fornieles, J., Graell, M., Payá, B., Leza, J. C., Zorrilla, E. P., Parellada, M., López, M. P., et al. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.03.025 · Cited by 45 · see citing works
A developmental redox dysregulation leads to spatio-temporal deficit of parvalbumin neuron circuitry in a schizophrenia mouse model
Cabungcal, J.-H., Steullet, P., Kraftsik, R., Cuénod, M., & Kim, Q. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2019.02.017 · Cited by 45 · see citing works
Self-citation
A multimodal approach to studying the relationship between peripheral glutathione, brain glutamate, and cognition in health and in schizophrenia
Coughlin, J. M., Yang, K., Marsman, A., Pradhan, S., Wang, M., Ward, R. E., Bonekamp, S., Ambinder, E. B., Higgs, C. P., Kim, P. K., et al. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00901-5 · Cited by 43 · see citing works
Thalamic reticular nucleus impairments and abnormal prefrontal control of dopamine system in a developmental model of schizophrenia: prevention by N-acetylcysteine
Zhu, X., Cabungcal, J.-H., Cuénod, M., Uliana, D. L., Kim, Q., & Grace, A. A. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01198-8 · Cited by 44 · see citing works
Self-citation
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
Antioxidant potential of Pediococcus pentosaceus strains from the sow milk bacterial collection in weaned piglets
Wang, L., Liu, Q., Chen, Y., Zheng, X., Wang, C., Qi, Y., Dong, Y., Xiao, Y., Chen, C., Chen, T., et al. (2022) · Microbiome · doi:10.1186/s40168-022-01278-z · Cited by 43 · see citing works
Redox and Immune Signaling in Schizophrenia: New Therapeutic Potential
Dwir, D., Khadimallah, I., Xin, L., Rahman, M., Du, F., Öngür, D., & Kim, Q. (2023) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyad012 · Cited by 40 · see citing works
“PVI circuit alterations constitute a hallmark of SZ (Lewis et al., 2012; Mauney et al., 2013) and have also been reported in bipolar disorders (Kulak et al., 2013) and autism (Zikopoulos and Barbas, 2013).”
Background
Selective dendritic susceptibility to bioenergetic, excitotoxic and redox perturbations in cortical neurons
Hasel, P., Mckay, S., Qiu, J., & Hardingham, G. E. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.12.021 · Cited by 39 · see citing works
“phrenia, bipolar disorder and autistic spectrum disorder [24,30,31,33, 38,43,59,69], associated with more subtle dendritic disturbances such”
Background
Neuroprotection or neurotoxicity? new insights into the effects of Acanthopanax senticosus harms on nervous system through cerebral metabolomics analysis
Zhang, S., Li, X., Wang, Y., et al. (2014) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2014.08.037 · Cited by 39 · see citing works
“In rodent models behavioral, morphological, electrophysiological and neurochemical alternations, which resembles pathologies seen in patients with schizophrenia could be coupled to GSH deficiency (Kulak et al., 2013).”
Background
Riparin II ameliorates corticosterone-induced depressive-like behavior in mice: Role of antioxidant and neurotrophic mechanisms
Lopes, I. S., Oliveira, I. C. M., Capibaribe, V. C. C., Valentim, J. T., da Silva, D. M. A., de Souza, A. G., de Araújo, M. A., Chaves, R. D. C., Gutierrez, S. J. C., Barbosa‐Filho, J. M., et al. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2018.07.007 · Cited by 37 · see citing works
Effects of omega-3 PUFA on the vitamin E and glutathione antioxidant defense system in individuals at ultra-high risk of psychosis
Smesny, S., Milleit, B., Schaefer, M. R., Hipler, U.-C., Milleit, C., Wiegand, C., Hesse, J., Klier, C. M., Holub, M., Holzer, I., et al. (2015) · Prostaglandins, Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2015.07.001 · Cited by 36 · see citing works
“In schizophrenia research, a major target of animal and clinical studies is glutathione (GSH) [17], the major cellular redox regulator and antioxidant [18].”
Background
Decoupling of Brain Temperature and Glutamate in Recent Onset of Schizophrenia: A 7T Proton Magnetic Resonance Spectroscopy Study
Posporelis, S., Coughlin, J. M., Marsman, A., Pradhan, S., Tanaka, T., Wang, H., Varvaris, M., Ward, R. E., Higgs, C. P., Edwards, J. A., et al. (2017) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.04.003 · Cited by 35 · see citing works
Pharmacological targeting of redox regulation systems as new therapeutic approach for psychiatric disorders: A literature overview.
Schiavone, S., & Trabace, L. (2016) · Pharmacological Research · doi:10.1016/j.phrs.2016.03.019 · Cited by 33 · see citing works
Antidepressant-like responses in the forced swimming test elicited by glutathione and redox modulation
Rosa, J. M., Dafré, A. L., & Rodrigues, A. L. S. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.07.009 · Cited by 32 · see citing works
Decreased NOX2 expression in the brain of patients with bipolar disorder: association with valproic acid prescription and substance abuse
Seredenina, T. S., Sorce, S., Herrmann, F. R., Mulone, X.-J. M., Plastre, O., Aguzzi, A., Jaquet, V., & Krause, K.-H. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.175 · Cited by 32 · see citing works
Sleep, mood disorders, and the ketogenic diet: potential therapeutic targets for bipolar disorder and schizophrenia
Choi, J., Kang, J., Kim, T., & Nehs, C. J. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1358578 · Cited by 33 · see citing works
Antimanic-like activity of candesartan in mice: Possible involvement of antioxidant, anti-inflammatory and neurotrophic mechanisms
Gomes, J. A. D. S., de Souza, G. C., Berk, M., Cavalcante, L. M., de Sousa, F. C. F., Budni, J., de Lucena, D. F., Quevedo, J., Carvalho, A. F., & Macêdo, D. S. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.08.005 · Cited by 30 · see citing works
“Deficits in GSH result in oxidative imbalance and subsequent oxidation of phospholipids, proteins, and DNA (Kulak et al., 2013).”
DNA damage and repair in neuropsychiatric disorders. What do we know and what are the future perspectives?
Czarny, P. L., Białek, K. I., Ziółkowska, S., Strycharz, J., & Śliwiński, T. (2019) · Mutagenesis · doi:10.1093/mutage/gez035 · Cited by 30 · see citing works
Absence of parvalbumin increases mitochondria volume and branching of dendrites in inhibitory Pvalb neurons in vivo: a point of convergence of autism spectrum disorder (ASD) risk gene phenotypes
Janickova, L., Rechberger, K. F., Wey, L., & Schwaller, B. (2020) · Molecular Autism · doi:10.1186/s13229-020-00323-8 · Cited by 30 · see citing works
Oxidative/Nitrosative Stress in Psychiatric Disorders: Are We There Yet?
O’Donnell, P., Do, K. Q., & Arango, C. (2014) · Schizophrenia Bulletin · doi:10.1093/schbul/sbu048 · Cited by 29 · see citing works
Self-citation
Glucocorticoids alter neuronal differentiation of human neuroepithelial-like cells by inducing long-lasting changes in the reactive oxygen species balance
Raciti, M., Ong, J., Weis, L., Edoff, K., Battagli, C., Falk, A., & Ceccatelli, S. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.03.022 · Cited by 27 · see citing works
Molecular hydrogen: an overview of its neurobiological effects and therapeutic potential for bipolar disorder and schizophrenia
Ghanizadeh, A. J., & Berk, M. (2013) · Medical Gas Research · doi:10.1186/2045-9912-3-11 · Cited by 28 · see citing works
“pathophysiology of bipolar disorder [22,25,26].”
Disturbed glutathione antioxidative defense is associated with structural brain changes in neuroleptic-naïve first-episode psychosis patients
Langbein, K., Hesse, J., Gussew, A., Milleit, B., Lavoie, S., Amminger, G. P., Christian Gaser, B., Wagner, G., Reichenbach, J. R., Hipler, U. ‐., et al. (2017) · Prostaglandins Leukotrienes and Essential Fatty Acids · doi:10.1016/j.plefa.2017.10.005 · Cited by 29 · see citing works
Taurine and glutathione in plasma and cerebrospinal fluid in olanzapine treated patients with schizophrenia
Samuelsson, M., Skogh, E., Lundberg, K., Vrethem, M., & Öllinger, K. M. (2013) · Psychiatry Research · doi:10.1016/j.psychres.2013.09.014 · Cited by 27 · see citing works
Programmable “Semismart” Sensor: Relevance to Monitoring Antipsychotics
Kim, E., Chocron, S. E., Ben‐Yoav, H., Winkler, T. E., Liu, Y., Glassman, M., Wolfram, C., Kelly, D. L., Reza Ghodssi, A., & Payne, G. F. (2015) · Advanced Functional Materials · doi:10.1002/adfm.201403783 · Cited by 25 · see citing works
The neuroprotective effects of N-acetylcysteine in psychiatric and neurodegenerative disorders: From modulation of glutamatergic transmission to restoration of synaptic plasticity
Chakraborty, S., Rao, S., & Tripathi, S. J. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110527 · Cited by 24 · see citing works
Prospecting for a quinoline containing selenium for comorbidities depression and memory impairment induced by restriction stress in mice
de Oliveira, R. L., Voss, G. T., Rodrigues, K. D. C., Pinz, M. P., Biondi, J. V., Becker, N., Blödorn, E. B., Domingues, W. B., Larroza, A., Campos, V. F., et al. (2022) · Psychopharmacology · doi:10.1007/s00213-021-06039-8 · Cited by 23 · see citing works
“Moreover, SOD, GPx, and GR are the main antioxidant defenses responsible for maintaining the redox balance (Kulak et al. 2013) and an increase in these enzyme activities is an attempt to eliminate the RS generated by ARS in cerebral structures.”
Background
Omega-3 fatty acids during adolescence prevent schizophrenia-related behavioural deficits: Neurophysiological evidences from the prenatal viral infection with PolyI:C
Casquero‐Veiga, M., Romero‐Miguel, D., MacDowell, K. S., Torres-Sánchez, S., Garcia-Partida, J. A., Lamanna‐Rama, N., Gómez‐Rangel, V., Romero‐Miranda, A., Berrocoso, E., Leza, J. C., et al. (2021) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2021.02.001 · Cited by 22 · see citing works
Gene set enrichment analysis of pathophysiological pathways highlights oxidative stress in psychosis
Pistis, G., Vázquez-Bourgón, J., Fournier, M., Jenni, R., Cleusix, M., Papiol, S., Smart, S. E., Pardiñas, A. F., Walters, J., MacCabe, J. H., et al. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01779-1 · Cited by 20 · see citing works
“This is at the basis of neural circuit synchronization impairments and cognitive, emotional, social and sensory de ﬁ cits characteristic of schizophrenia [12, 16, 18, 52].”
Background
Current and Emergent Treatments for Symptoms and Neurocognitive Impairment in Schizophrenia
Javitt, D. C. (2014) · Current Treatment Options in Psychiatry · doi:10.1007/s40501-014-0010-9 · Cited by 23 · see citing works
Dentate gyrus−cornu ammonis (CA) 4 volume is decreased and associated with depressive episodes and lipid peroxidation in bipolar II disorder: Longitudinal and cross‐sectional analyses
Elvsåshagen, T., Zuzarte, P., Westlye, L. T., Bøen, E., Josefsen, D., Boye, B., Hol, P. K., Malt, U. F., Young, L. T., & Andreazza, A. C. (2016) · Bipolar Disorders · doi:10.1111/bdi.12457 · Cited by 21 · see citing works
A Characterization of the Effects of Minocycline Treatment During Adolescence on Structural, Metabolic, and Oxidative Stress Parameters in a Maternal Immune Stimulation Model of Neurodevelopmental Brain Disorders
Romero‐Miguel, D., Casquero‐Veiga, M., MacDowell, K. S., Torres-Sánchez, S., Garcia-Partida, J. A., Lamanna‐Rama, N., Romero‐Miranda, A., Berrocoso, E., Leza, J. C., Desco, M., et al. (2021) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyab036 · Cited by 21 · see citing works
Placebo-Controlled Augmentation Trials of the Antioxidant Nac in Schizophrenia: A Review
Chen, A. T., Chibnall, J. T., & Nasrallah, H. A. (2016) · Annals of Clinical Psychiatry · doi:10.1177/104012371602800308 · Cited by 20 · see citing works
Antioxidants in neuropsychiatric disorder prevention: neuroprotection, synaptic regulation, microglia modulation, and neurotrophic effects
Liu, F., Bai, Q., Tang, W., Zhang, S., Guo, Y. H., Pan, S., Ma, X., Yang, Y., & Fan, H. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1505153 · Cited by 19 · see citing works
Alterations in TRN-anterodorsal thalamocortical circuits affect sleep architecture and homeostatic processes in oxidative stress vulnerable Gclm−/− mice
Czekus, C., Steullet, P., López, A. O., Bozic, I., Rusterholz, T., Bandarabadi, M., Kim, Q., & Herrera, C. G. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01700-w · Cited by 17 · see citing works
Self-citation
De novo expression of parvalbumin in ependymal cells in response to brain injury promotes ependymal remodeling and wound repair
Szabolcsi, V., & Celio, M. R. (2014) · Glia · doi:10.1002/glia.22768 · Cited by 18 · see citing works
“In murine models, treatment regimes that restore the redox balance, such as the administration of the antioxidant N-acetylcysteine, help to correct some of these deficits (Cabungcal et al., 2006; Kulak et al., 2013).”
Background
Fusing Sensor Paradigms to Acquire Chemical Information: An Integrative Role for Smart Biopolymeric Hydrogels
Kim, E., Liu, Y., Ben‐Yoav, H., Winkler, T. E., Yan, K., Shi, X., Shen, J., Kelly, D. L., Reza Ghodssi, A., Bentley, W. E., et al. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201600516 · Cited by 17 · see citing works
Dopamine and Stress
Stanwood, G. D. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813146-6.00009-6 · Cited by 17 · see citing works
Maternal Supplementation with N-Acetylcysteine Modulates the Microbiota-Gut-Brain Axis in Offspring of the Poly I:C Rat Model of Schizophrenia
Romero‐Miguel, D., Casquero‐Veiga, M., Fernández, J., Lamanna‐Rama, N., Gómez‐Rangel, V., Gálvez-Robleño, C., Santa-Marta, C., Villar, C. J., Lombó, F., Abalo, R., et al. (2023) · Antioxidants · doi:10.3390/antiox12040970 · Cited by 18 · see citing works
“In this regard, the likely involvement of inflammation/oxidative stress (IOS) in the pathophysiology of SCZ has raised the potential use of anti-oxidant and anti-inflammatory (anti-IOS) compounds as therapeutic strategies in this disorder [19].”
Background
Therapeutic potential of NOX inhibitors in neuropsychiatric disorders
Kaur, P., Khan, H., Grewal, A. K., Dua, K., & Singh, T. G. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06424-5 · Cited by 15 · see citing works
Dysregulated mitochondrial and chloroplast bioenergetics from a translational medical perspective (Review)
Stefano, G. B., & Kream, R. M. (2016) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2016.2471 · Cited by 15 · see citing works
“Chronic oxidative stress in conjunction with altered NO-mediated signaling pathways has also been proposed as a significant contributing factor in the pathophysiology of SCZ-related behaviors (124,125) and in the etiology of BPD (126).”
Influential
A possible key role of vision in the development of schizophrenia
Császár, N., Kapócs, G., & Bókkon, I. (2018) · Reviews in the Neurosciences · doi:10.1515/revneuro-2018-0022 · Cited by 15 · see citing works
The Pathophysiological Underpinnings of Gamma-Band Alterations in Psychiatric Disorders
Palmisano, A., Pandit, S., Smeralda, C. L., Demchenko, I., Rossi, S., Battelli, L., Rivolta, D., Bhat, V., & Santarnecchi, E. (2024) · Life · doi:10.3390/life14050578 · Cited by 16 · see citing works
“Similar results emerged in transgenic mice with redox dysregulation compared with the wild-type mice [218].”
Result
Pathway-specific contribution of parvalbumin interneuron NMDARs to synaptic currents and thalamocortical feedforward inhibition
Lewis, E. M., Spence, H. E., Akella, N., & Buonanno, A. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01747-9 · Cited by 12 · see citing works
Acoustic Hyper-Reactivity and Negatively Skewed Locomotor Activity in Children With Autism Spectrum Disorders: An Exploratory Study
Takahashi, H., Nakamura, T., Kim, J., Kikuchi, H., Nakahachi, T., Ishitobi, M., Ebishima, K., Yoshiuchi, K., Ando, T., Stickley, A., et al. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00355 · Cited by 12 · see citing works
Behavioral regulation by perineuronal nets in the prefrontal cortex of the CNTNAP2 mouse model of autism spectrum disorder
Gandhi, T., Liu, C., Adeyelu, T. T., Canepa, C. R., & Lee, C. C. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1114789 · Cited by 12 · see citing works
“…important implications in neurodegenerative diseases, addiction and recovery from CNS related injury (Massey et al., 2006; Galtrey and Fawcett, 2007; Kwok et al., 2008; Alilain et al., 2011; Blanchard et al., 2012; Mercier et al., 2012; Xue et al., 2014; Yang et al., 2015; Kasinathan et al., 2016).”
Background
Modeling of Hot Rolling Industrial Process Using Fuzzy Logic.
Sheta, A. F., Öznergiz, E., Abdelrahman, M., & Babuška, R. (2009) · Computer Applications in Industry and Engineering · Cited by 12 · see citing works
Oxidative Stress in the Early Stage of Psychosis
Ventriglio, A., Bellomo, A., Favale, D., Bonfitto, I., Vitrani, G., Dario, D. S., Cuozzo, E., Ilaria, D. G., Pettorruso, M., Perna, G., et al. (2021) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026621666210701105839 · Cited by 11 · see citing works
Manipulations of Glutathione Metabolism Modulate IP3-Mediated Store-Operated Ca2+ Entry on Astroglioma Cell Line
Mokrane, N., Snabi, Y., Cens, T., Guiramand, J., Charnet, P., Bertaud, A., Ménard, C., Rousset, M., Ferreira, M. D. J., Thibaud, J., et al. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.785727 · Cited by 11 · see citing works
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Self-citation

Authors: Kulak, A., Steullet, P., Cabungcal, J.-H., Werge, T., Ingason, A., Cuenod, M., & Do, K. Q.
Affiliations: Centre Hospitalier Universitaire Vaudois (CH)
Sankt Hans Hospital (DK)
Department of Psychiatry, Center for Psychiatric Neuroscience, Lausanne University Hospital, Prilly-Lausanne, Switzerland.
ORCID: Steullet, Pascal
Werge, Thomas
Ingason, Andrés
Venue: Antioxidants & Redox Signaling
Publisher: SAGE Publications
Published: 2013-04-20
Volume: 18
Issue: 12
Pages: 1428-1443
ISSN: 1523-0864 (ISSN-L)
1557-7716
DOI: 10.1089/ars.2012.4858
OpenAlex: W2105730072
Cited by: 124
References: 128
Citations by year: 2026: 6 · 2025: 7 · 2024: 6 · 2023: 6 · 2022: 8 · 2021: 11 · 2020: 7 · 2019: 9 · 2018: 3 · 2017: 14 · 2016: 8 · 2015: 16 · 2014: 15 · 2013: 7
FWCI: 1.64
Type: journal article
Language: en
Open access: closed
Locations: Antioxidants and Redox Signaling (publishedVersion)
PubMed (publishedVersion)
Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
IRIS (submittedVersion)
SERVAL (Université de Lausanne) (submittedVersion)
Funders: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Keywords: schizophrenia, bipolar disorder, redox dysregulation, oxidative stress, glutathione deficiency, NMDA receptor hypofunction, glutamate excitotoxicity, parvalbumin interneurons, prepulse inhibition, stress reactivity, dopamine signaling, myelination, N-acetylcysteine, antioxidant therapy
MeSH terms: Animals, Bipolar Disorder, Brain, Disease Models, Animal, Glutamate-Cysteine Ligase, Glutathione, Humans, Synaptic Transmission, Oxidation-Reduction, Schizophrenia, Polymorphism, Single Nucleotide, Gene Knockout Techniques

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Redox Dysregulation in the Pathophysiology of Schizophrenia and Bipolar Disorder: Insights from Animal Models

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