Oxidative Damage and Antioxidant Response in Frontal Cortex of Demented and Nondemented Individuals with Alzheimer’s Neuropathology
Open accessAbstract
Alzheimer's disease (AD) is characterized by progressive neurodegeneration in the cerebral cortex, histopathologically hallmarked by amyloid β (Aβ) extracellular plaques and intracellular neurofibrillary tangles, constituted by hyperphosphorylated tau protein. Correlation between these pathologic features and dementia has been challenged by the emergence of "nondemented with Alzheimer's neuropathology" (NDAN) individuals, cognitively intact despite displaying pathologic features of AD. The existence of these subjects suggests that some unknown mechanisms are triggered to resist Aβ-mediated detrimental events. Aβ accumulation affects mitochondrial redox balance, increasing oxidative stress status, which in turn is proposed as a primary culprit in AD pathogenesis. To clarify the relationship linking Aβ, oxidative stress, and cognitive impairment, we performed a comparative study on AD, NDAN, and aged-matched human postmortem frontal cortices of either sex. We quantitatively analyzed immunofluorescence distribution of oxidative damage markers, and of SOD2 (superoxide dismutase 2), PGC1α [peroxisome proliferator-activated receptor (PPAR) γ-coactivator 1α], PPARα, and catalase as key factors in antioxidant response, as well as the expression of miRNA-485, as a PGC1α upstream regulator. Our results confirm dramatic redox imbalance, associated with impaired antioxidant defenses in AD brain. By contrast, NDAN individuals display low oxidative damage, which is associated with high levels of scavenging systems, possibly resulting from a lack of PGC1α miRNA-485-related inhibition. Comparative analyses in neurons and astrocytes further highlighted cell-specific mechanisms to counteract redox imbalance. Overall, our data emphasize the importance of transcriptional and post-transcriptional regulation of antioxidant response in AD. This suggests that an efficient PGC1α-dependent "safety mechanism" may prevent Aβ-mediated oxidative stress, supporting neuroprotective therapies aimed at ameliorating defects in antioxidant response pathways in AD patients.
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NDAN individuals display low oxidative damage associated with high levels of antioxidant response (SOD2, PGC1α, PPARα, CAT).
“These individuals display low oxidative damage, associated with high levels of antioxidant response (SOD2, PGC1α, PPARα, CAT).”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
PGC1α expression was lower in AD and similar to control levels in NDAN individuals, while expression of miRNA-485 was significantly increased in AD cortex compared to control and NDAN subjects.
“PGC1α expression, as a key regulator of antioxidant response, was lower in AD and similar to control levels in NDAN individuals, while expression of miRNA-485, a PGC1α upstream regulator, was significantly increased in AD cortex as compared to the control and NDAN subjects [154].”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
NDAN patients show cell-specific mechanisms to counteract redox imbalance.
“Further, NDAN patients show cell-specific mechanisms to counteract redox imbalance [154].”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
NDAN patients display amyloid and tau pathology but resist dementia.
“NDAN patients display amyloid and tau pathology, but they resist to dementia [154].”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
Levels of 8-oxo-dG and 4-HNE in relation to accumulation of neurotoxic Aβ peptide were increased in cortices of AD patients compared to NDAN.
“The levels of 8-oxo-dG and 4-HNE in relation to the accumulation of neurotoxic Aβ peptide were increased in cortices of AD patients in comparison to NDAN.”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
Activation of PGC1α-mediated antioxidant pathway may prevent OS in AD.
“Activation of PGC1α-mediated antioxidant pathway may prevent OS in AD [154].”
From Role of Oxidative Damage in Alzheimer’s Disease and Neurodegeneration: From Pathogenic Mechanisms to Biomarker Discovery (2021) · cites this paper as [154]
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Self-citation
- Authors
- Fracassi, A., Marcatti, M., Zolochevska, O., Tabor, N., Woltjer, R., Moreno, S., & Taglialatela, G.
- Affiliations
- The University of Texas Medical Branch at Galveston (US)
- Oregon Health & Science University (US)
- Roma Tre University (IT)
- Corresponding author
- Moreno, Sandra
- Taglialatela, Giulio
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2020-11-25
- Volume
- 41
- Issue
- 3
- Pages
- 538-554
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC7821866
- OpenAlex
- W3108616759
- Cited by
- 81
- References
- 85
- Citations by year
- 2026: 12 · 2025: 11 · 2024: 15 · 2023: 12 · 2022: 21 · 2021: 10
- FWCI
- 6.46
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Iris (Roma Tre University) (submittedVersion, other-oa)
- Funders
- NIA/NIH (R01AG042890, R01AG060718, P30AG008017)
- Robert J. and Helen C. Kleberg Foundation
- Ministero dell'Istruzione, dell'Università e della Ricerca (The Grant of Excellence Departments)
- The Company of Biologists
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- Alzheimer's disease, amyloid-beta, oxidative stress, antioxidant response, frontal cortex, PGC-1α, manganese superoxide dismutase, catalase, PPARα, redox imbalance, neurofibrillary tangles, tau hyperphosphorylation, astrocytes, neurons, neuroprotection
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Aged, Aged, 80 and over, Alzheimer Disease, Antioxidants, Astrocytes, Autopsy, Dementia, Female, Humans, Male, Neurons, Oxidation-Reduction, Free Radical Scavengers, Amyloid beta-Peptides, Prefrontal Cortex, Oxidative Stress, MicroRNAs, PPAR gamma
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