NADPH oxidase in brain injury and neurodegenerative disorders

Ma, Merry W.; Wang, Jing; Zhang, Quanguang; Wang, Ruimin; Dhandapani, Krishnan M.; Vadlamudi, Ratna K.; Brann, Darrell W.

doi:10.1186/s13024-017-0150-7

Cited by 433Redox biology and oxidative stressNitric Oxide and Endothelin EffectsNeutrophil, Myeloperoxidase and Oxidative Mechanisms

NADPH oxidase in brain injury and neurodegenerative disorders

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Ma, Merry W., Wang, Jing, Zhang, Quanguang, Wang, Ruimin, Dhandapani, Krishnan M., Vadlamudi, Ratna K., Brann, Darrell W.·2017·Molecular Neurodegeneration

DOI 10.1186/s13024-017-0150-7PMC PMC5240251

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Abstract

Oxidative stress is a common denominator in the pathology of neurodegenerative disorders such as Alzheimer's disease, Parkinson's disease, Huntington's disease, amyotrophic lateral sclerosis, and multiple sclerosis, as well as in ischemic and traumatic brain injury. The brain is highly vulnerable to oxidative damage due to its high metabolic demand. However, therapies attempting to scavenge free radicals have shown little success. By shifting the focus to inhibit the generation of damaging free radicals, recent studies have identified NADPH oxidase as a major contributor to disease pathology. NADPH oxidase has the primary function to generate free radicals. In particular, there is growing evidence that the isoforms NOX1, NOX2, and NOX4 can be upregulated by a variety of neurodegenerative factors. The majority of recent studies have shown that genetic and pharmacological inhibition of NADPH oxidase enzymes are neuroprotective and able to reduce detrimental aspects of pathology following ischemic and traumatic brain injury, as well as in chronic neurodegenerative disorders. This review aims to summarize evidence supporting the role of NADPH oxidase in the pathology of these neurological disorders, explores pharmacological strategies of targeting this major oxidative stress pathway, and outlines obstacles that need to be overcome for successful translation of these therapies to the clinic.

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Robust activation of NOX isoforms in response to acute neuronal injury and chronic inflammation with oxidative damage has been well documented in post-mortem tissue and models of neurodegeneration.
“The robust activation of NOX isoforms in response to acute neuronal injury and chronic inflammation with oxidative damage has been well documented in post-mortem tissue and models of neurodegeneration (reviewed in [83]).”
From ROS Generation in Microglia: Understanding Oxidative Stress and Inflammation in Neurodegenerative Disease (2020) · cites this paper as [83]

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Neuroinflammation: friend and foe for ischemic stroke
Jayaraj, R. L., Azimullah, S., Beiram, R., Jalal, F. Y., & Rosenberg, G. A. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1516-2 · Cited by 1,438 · see citing works
Current Mechanistic Concepts in Ischemia and Reperfusion Injury
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ROS Generation in Microglia: Understanding Oxidative Stress and Inflammation in Neurodegenerative Disease
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“The robust activation of NOX isoforms in response to acute neuronal injury and chronic inflammation with oxidative damage has been well documented in post-mortem tissue and models of neurodegeneration (reviewed in [83]).”
Background
Neuroinflammation in Cerebral Ischemia and Ischemia/Reperfusion Injuries: From Pathophysiology to Therapeutic Strategies
Jurcău, A., & Simion, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010014 · Cited by 515 · see citing works
The Role of NADPH Oxidases and Oxidative Stress in Neurodegenerative Disorders
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Neurodegenerative disorders: Mechanisms of degeneration and therapeutic approaches with their clinical relevance
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Interrelation between ROS and Ca2+ in aging and age-related diseases
Madreiter‐Sokolowski, C. T., Thomas, C., & Ristow, M. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101678 · Cited by 365 · see citing works
Microglia and macrophage metabolism in CNS injury and disease: The role of immunometabolism in neurodegeneration and neurotrauma
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ROS and RNS signalling: adaptive redox switches through oxidative/nitrosative protein modifications
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Blood-Brain Barrier Disruption by Lipopolysaccharide and Sepsis-Associated Encephalopathy
Peng, X., Luo, Z., He, S., Zhang, L., & Li, Y. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.768108 · Cited by 271 · see citing works
Microglia and Neuroinflammation: Crucial Pathological Mechanisms in Traumatic Brain Injury-Induced Neurodegeneration
Shao, F., Wang, X., Wu, H., Wu, Q., & Zhang, J. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.825086 · Cited by 250 · see citing works
Neuroinflammation: An Integrating Overview of Reactive‐Neuroimmune Cell Interactions in Health and Disease
Kölliker-Frers, R., Udovin, L., Otero-Losada, M., Kobiec, T., Herrera, M. I., Palacios, J., Razzitte, G., & Capani, F. (2021) · Mediators of Inflammation · doi:10.1155/2021/9999146 · Cited by 258 · see citing works
Fibrin-targeting immunotherapy protects against neuroinflammation and neurodegeneration
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Excitotoxicity: Still Hammering the Ischemic Brain in 2020
Choi, D. W. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.579953 · Cited by 198 · see citing works
The role of oxidative stress in intervertebral disc degeneration: Mechanisms and therapeutic implications
Chen, X., Zhang, A., Zhao, K., Gao, H., Shi, P., Chen, Y., Cheng, Z., Zhou, W., & Zhang, Y. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102323 · Cited by 194 · see citing works
NADPH Oxidases: From Molecular Mechanisms to Current Inhibitors
Cipriano, A., Viviano, M., Feoli, A., Milite, C., Sarno, G., Castellano, S., & Sbardella, G. (2023) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.3c00770 · Cited by 190 · see citing works
Ferroptosis, a Recent Defined Form of Critical Cell Death in Neurological Disorders
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Pterostilbene Attenuates Astrocytic Inflammation and Neuronal Oxidative Injury After Ischemia-Reperfusion by Inhibiting NF-κB Phosphorylation
Liu, H., Wu, X., Luo, J., Wang, X., Guo, H., Feng, D., Zhao, L., Bai, H., Song, M., Liu, X., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02408 · Cited by 180 · see citing works
Ischemic stroke and mitochondria: mechanisms and targets
Andrabi, S. S., Parvez, S., & Tabassum, H. (2019) · PROTOPLASMA · doi:10.1007/s00709-019-01439-2 · Cited by 180 · see citing works
White matter injury in infants with intraventricular haemorrhage: mechanisms and therapies
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Gram-negative bacteria and their lipopolysaccharides in Alzheimer’s disease: pathologic roles and therapeutic implications
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Oxidative Stress, Neuroinflammation, and NADPH Oxidase: Implications in the Pathogenesis and Treatment of Alzheimer’s Disease
Ganguly, U., Kaur, U., Chakrabarti, S. S., Sharma, P., Agrawal, B. K., Saso, L., & Chakrabarti, S. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/7086512 · Cited by 150 · see citing works
Redox Mechanisms in Neurodegeneration: From Disease Outcomes to Therapeutic Opportunities
Sbodio, J. I., Snyder, S. H., & Paul, B. D. (2018) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7321 · Cited by 143 · see citing works
Mitochondrial Dysfunction and Parkinson’s Disease: Pathogenesis and Therapeutic Strategies
Vastegani, S. M., Nasrolahi, A., Ghaderi, S., Belali, R., Rashno, M., Farzaneh, M., & Khoshnam, S. E. (2023) · Neurochemical Research · doi:10.1007/s11064-023-03904-0 · Cited by 145 · see citing works
Cellular and Molecular Pathophysiology of Traumatic Brain Injury: What Have We Learned So Far?
Freire, M. A. M., Rocha, G. S., Bittencourt, L. O., Falcão, D., Lima, R. R., & Cavalcanti, J. R. L. D. P. (2023) · Biology · doi:10.3390/biology12081139 · Cited by 139 · see citing works
Modulating neuroinflammation and oxidative stress to prevent epilepsy and improve outcomes after traumatic brain injury
Eastman, C. L., D’Ambrosio, R., & Ganesh, T. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107907 · Cited by 137 · see citing works
The Implication of Reactive Oxygen Species and Antioxidants in Knee Osteoarthritis
Tudorachi, N. B., Totu, E. E., Fifere, A., Ardeleanu, V., Mocanu, V., Mircea, C., Işıldak, İ., Smilkov, K., & Cărăușu, E. M. (2021) · Antioxidants · doi:10.3390/antiox10060985 · Cited by 135 · see citing works
Zinc in the Brain: Friend or Foe?
Choi, S., Hong, D. K., Choi, B. Y., & Suh, S. W. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21238941 · Cited by 136 · see citing works
Melatonin and the electron transport chain
Hardeland, R. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2615-9 · Cited by 126 · see citing works
NADPH Oxidase 2 Regulates NLRP3 Inflammasome Activation in the Brain after Traumatic Brain Injury
Ma, M. W., Wang, J., Dhandapani, K. M., & Brann, D. W. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/6057609 · Cited by 116 · see citing works
Statins and the Brain: More than Lipid Lowering Agents?
Fracassi, A., Marangoni, M., Rosso, P., Pallottini, V., Fioramonti, M., Siteni, S., & Segatto, M. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666170703101816 · Cited by 116 · see citing works
NADPH oxidases as drug targets and biomarkers in neurodegenerative diseases: What is the evidence?
Sorce, S., Stocker, R., Seredenina, T. S., Holmdahl, R., Aguzzi, A., Chiò, A., Depaulis, A., Heitz, F., Olofsson, P., Olsson, T. P., et al. (2017) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2017.08.006 · Cited by 113 · see citing works
NADPH oxidases in traumatic brain injury – Promising therapeutic targets?
Ma, M. W., Wang, J., Dhandapani, K. M., Wang, R., & Brann, D. W. (2018) · Redox Biology · doi:10.1016/j.redox.2018.03.005 · Cited by 114 · see citing works
The Role of NLRP3 Inflammasome in the Pathogenesis of Traumatic Brain Injury
Irrera, N., Russo, M., Pallio, G., Bitto, A., Mannino, F., Minutoli, L., Altavilla, D., & Squadrito, F. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176204 · Cited by 97 · see citing works
Inhibition of NADPH oxidase by apocynin prevents learning and memory deficits in a mouse Parkinson's disease model
Hou, L., Sun, F., Huang, R., Sun, W., Zhang, D., & Wang, Q. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101134 · Cited by 110 · see citing works
Complement receptor 3 mediates NADPH oxidase activation and dopaminergic neurodegeneration through a Src-Erk-dependent pathway
Hou, L., Wang, K., Zhang, C., Sun, F., Che, Y., Zhao, X., Zhang, D., Li, H., & Wang, Q. (2018) · Redox Biology · doi:10.1016/j.redox.2017.09.017 · Cited by 104 · see citing works
NADPH oxidase regulates paraquat and maneb-induced dopaminergic neurodegeneration through ferroptosis.
Hou, L.-Y., Huang, R.-X., Sun, F., Zhang, L., & Wang, Q.-S. (2019) · Toxicology · doi:10.1016/j.tox.2019.02.011 · Cited by 97 · see citing works
Microglia morphology and proinflammatory signaling in the nucleus accumbens during nicotine withdrawal
Adeluyi, A., Guerin, L. N., Fisher, M. L., Galloway, A. L., Cole, R. D., Chan, S. S. L., Wyatt, M. D., Davis, S. W., Freeman, L. R., Ortinski, P. I., et al. (2019) · Science Advances · doi:10.1126/sciadv.aax7031 · Cited by 107 · see citing works
Molecular pathophysiological mechanisms of ischemia/reperfusion injuries after recanalization therapy for acute ischemic stroke
Jurcău, A., & Ardelean, I. A. (2021) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2003078 · Cited by 103 · see citing works
NADPH oxidases: redox regulation of cell homeostasis and disease
Kračun, D., Lopes, L. R., Cifuentes-Pagano, E., & Pagano, P. J. (2025) · Physiological Reviews · doi:10.1152/physrev.00034.2023 · Cited by 104 · see citing works
Excitotoxicity as a Target Against Neurodegenerative Processes
Binvignat, O., & Olloquequi, J. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200113162641 · Cited by 100 · see citing works
Neurodegenerative Disease: Roles for Sex, Hormones, and Oxidative Stress
Sumien, N., Cunningham, J. T., Davis, D., Engelland, R. E., Fadeyibi, O., Farmer, G. E., Mabry, S., Mensah-Kane, P., Trinh, O. T. P., Vann, P. H., et al. (2021) · Endocrinology · doi:10.1210/endocr/bqab185 · Cited by 102 · see citing works
Pharmacological Modulation of Nrf2/HO-1 Signaling Pathway as a Therapeutic Target of Parkinson’s Disease
Wang, Y., Gao, L., Chen, J., Li, Q., Huo, L., Wang, Y., Wang, H., & Du, J. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.757161 · Cited by 106 · see citing works
Investigations into Hypoxia and Oxidative Stress at the Optic Nerve Head in a Rat Model of Glaucoma
Chidlow, G., Wood, J. P. M., & Casson, R. J. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00478 · Cited by 99 · see citing works
Crosstalk between Rac1-mediated actin regulation and ROS production
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Authors: Ma, M. W., Wang, J., Zhang, Q., Wang, R., Dhandapani, K. M., Vadlamudi, R. K., & Brann, D. W.
Affiliations: Augusta University (US)
The University of Texas at San Antonio Health Science Center (US)
Corresponding author: Brann, Darrell W.
ORCID: Ma, Merry W.
Wang, Jing
Zhang, Quanguang
Wang, Ruimin
Dhandapani, Krishnan M.
Vadlamudi, Ratna K.
Brann, Darrell W.
Venue: Molecular Neurodegeneration
Publisher: Springer Science and Business Media LLC
Published: 2017-01-17
Volume: 12
Issue: 1
Pages: 7-7
ISSN: 1750-1326 (ISSN-L)
DOI: 10.1186/s13024-017-0150-7
PMC: PMC5240251
OpenAlex: W2574254633
Cited by: 432
References: 417
Citations by year: 2026: 21 · 2025: 45 · 2024: 43 · 2023: 59 · 2022: 44 · 2021: 67 · 2020: 49 · 2019: 38 · 2018: 40 · 2017: 26
FWCI: 3.92
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Molecular Neurodegeneration (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: U.S. Department of Veterans Affairs (5l101BX001117)
National Institute of Neurological Disorders and Stroke (5R01NS050730, R01NS088058)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: NADPH oxidase, oxidative stress, neurodegenerative diseases, brain injury, ischemic brain injury, traumatic brain injury, NOX1, NOX2, NOX4, neuroprotection, antioxidant therapy, Alzheimer's disease, Parkinson's disease, Huntington's disease, amyotrophic lateral sclerosis, multiple sclerosis
MeSH terms: Animals, Brain Injuries, Humans, NADPH Oxidases, Neurodegenerative Diseases

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NADPH oxidase in brain injury and neurodegenerative disorders

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