Time Course of Post-Traumatic Mitochondrial Oxidative Damage and Dysfunction in a Mouse Model of Focal Traumatic Brain Injury: Implications for Neuroprotective Therapy
Open accessAbstract
In the present study, we investigate the hypothesis that mitochondrial oxidative damage and dysfunction precede the onset of neuronal loss after controlled cortical impact traumatic brain injury (TBI) in mice. Accordingly, we evaluated the time course of post-traumatic mitochondrial dysfunction in the injured cortex and hippocampus at 30 mins, 1, 3, 6, 12, 24, 48, and 72 h after severe TBI. A significant decrease in the coupling of the electron transport system with oxidative phosphorylation was observed as early as 30 mins after injury, followed by a recovery to baseline at 1 h after injury. A statistically significant ( P < 0.0001) decline in the respiratory control ratio was noted at 3 h, which persisted at all subsequent time-points up to 72 h after injury in both cortical and hippocampal mitochondria. Structural damage seen in purified cortical mitochondria included severely swollen mitochondria, a disruption of the cristae and rupture of outer membranes, indicative of mitochondrial permeability transition. Consistent with this finding, cortical mitochondrial calcium-buffering capacity was severely compromised by 3h after injury, and accompanied by significant increases in mitochondrial protein oxidation and lipid peroxidation. A possible causative role for reactive nitrogen species was suggested by the rapid increase in cortical mitochondrial 3-nitrotyrosine levels shown as early as 30 mins after injury. These findings indicate that post-traumatic oxidative lipid and protein damage, mediated in part by peroxynitrite, occurs in mitochondria with concomitant ultrastructural damage and impairment of mitochondrial bioenergetics. The data also indicate that compounds which specifically scavenge peroxynitrite (ONOO) or ONOO−derived radicals (e.g. ONOO− + H+ → ONOOH → †NO 2 + †OH) may be particularly effective for the treatment of TBI, although the therapeutic window for this neuroprotective approach might only be 3 h.
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Immediately following mTBI there is a significant increase of oxidative stress.
“immediately following mTBI there is a significant increase of oxidative stress [52, 140].”
From Early onset senescence and cognitive impairment in a murine model of repeated mTBI (2021) · cites this paper as [140]
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- Authors
- Singh, I. N., Sullivan, P. G., Deng, Y., Mbye, L. H., & Hall, E. D.
- Affiliations
- University of Kentucky HealthCare (US)
- Spinal Cord & Brain Injury Research Center and Department of Anatomy & Neurobiology, University of Kentucky Medical Center, Lexington, Kentucky, USA
- Corresponding author
- Hall, Edward D
- ORCID
- Sullivan, Patrick G
- Venue
- Journal of Cerebral Blood Flow & Metabolism
- Publisher
- SAGE Publications
- Published
- 2006-11
- Volume
- 26
- Issue
- 11
- Pages
- 1407-1418
- ISSN
- 0271-678X (ISSN-L)
- 1559-7016
- OpenAlex
- W2101577668
- Cited by
- 367
- References
- 65
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 20 · 2023: 20 · 2022: 10 · 2021: 14 · 2020: 21 · 2019: 23 · 2018: 22 · 2017: 13 · 2016: 26 · 2015: 21 · 2014: 15 · 2013: 19 · 2012: 11
- FWCI
- 12.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS048191, R01NS046566, NS 1R01 NS46566, NS 048191)
- Topics
- Health Sciences › Medicine › Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Epidemiology › Traumatic Brain Injury Research
- Keywords
- traumatic brain injury, mitochondrial oxidative damage, mitochondrial dysfunction, controlled cortical impact, respiratory control ratio, mitochondrial permeability transition, mitochondrial calcium buffering, lipid peroxidation, nitrotyrosine, peroxynitrite, reactive nitrogen species, neuroprotection, therapeutic window, hippocampus, cortex, mitochondrial ultrastructure
- MeSH terms
- Animals, Calpain, Cytoskeleton, Male, Membrane Lipids, Membrane Proteins, Microscopy, Electron, Mitochondria, Nerve Degeneration, Oxygen Consumption, Tyrosine, Blotting, Northern, Reactive Oxygen Species, Oxidative Stress, Neuroprotective Agents, Brain Hemorrhage, Traumatic, Peroxynitrous Acid, Mice
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