The Mitochondrial Permeability Transition Pore Regulates Nitric Oxide-Mediated Apoptosis of Neurons Induced by Target Deprivation
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Ablation of mouse occipital cortex induces precisely timed and uniform p53-modulated and Bax-dependent apoptosis of thalamocortical projection neurons in the dorsal lateral geniculate nucleus (LGN) by 7 d after lesion. We tested the hypothesis that this neuronal apoptosis is initiated by oxidative stress and the mitochondrial permeability transition pore (mPTP). Preapoptotic LGN neurons accumulate mitochondria, Zn 2+and Ca 2+, and generate higher levels of reactive oxygen species (ROS), including superoxide, nitric oxide (NO), and peroxynitrite, than LGN neurons with an intact cortical target. Preapoptosis of LGN neurons is associated with increased formation of protein carbonyls, protein nitration, and protein S-nitrosylation. Genetic deletion of nitric oxide synthase 1 (nos1) and inhibition of NOS1 with nitroindazole protected LGN neurons from apoptosis, revealing NO as a mediator. Putative components of the mPTP are expressed in mouse LGN, including the voltage-dependent anion channel (VDAC), adenine nucleotide translocator (ANT), and cyclophilin D (CyPD). Nitration of CyPD and ANT in LGN mitochondria occurs by 2 d after cortical injury. Chemical cross-linking showed that LGN neuron preapoptosis is associated with formation of CyPD and VDAC oligomers, consistent with mPTP formation. Mice without CyPD are rescued from neuron apoptosis as are mice treated with the mPTP inhibitors TRO-19622 (cholest-4-en-3-one oxime) and TAT-Bcl-X L-BH4. Manipulation of the mPTP markedly attenuated the early preapoptotic production of reactive oxygen/nitrogen species in target-deprived neurons. Our results demonstrate in adult mouse brain neurons that the mPTP functions to enhance ROS production and the mPTP and NO trigger apoptosis; thus, the mPTP is a target for neuroprotection in vivo.
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In an in vivo model of neuronal apoptosis due to target deprivation, intracellular generation of ROS and NO· promotes protein modifications like S-NO and 3-nitrotyrosine formation in mouse brain.
“intracellular generation of ROS and NO· promotes protein modifications like S-NO and 3-nitrotyrosine formation in mouse brain (277).”
From Redox regulation of mitochondrial function (2012) · cites this paper as [277]
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Lok, J. M., & Martin, L. J. (2002) · Journal of Neurotrauma · doi:10.1089/08977150260190410 · Cited by 51 · see citing works
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Down-regulation of striatin, a neuronal calmodulin-binding protein, impairs rat locomotor activity
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Self-citationZinc accumulation after target loss: an early event in retrograde degeneration of thalamic neurons
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NO production during neuronal cell death can be directly assessed by a chemical reaction in vivo.
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Monitoring Apoptosis with Fluorescent Zn 2+ -Indicators
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Redox regulation of mitochondrial function
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- Authors
- Martin, L. J., Adams, N. A., Pan, Y., Price, A., & Wong, M.
- Affiliations
- Johns Hopkins University (US)
- ORCID
- Martin, Lee J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-01-05
- Volume
- 31
- Issue
- 1
- Pages
- 359-370
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3078575
- OpenAlex
- W2064188898
- Cited by
- 96
- References
- 107
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 2 · 2022: 4 · 2021: 3 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 4 · 2016: 8 · 2015: 4 · 2014: 11 · 2013: 12 · 2012: 9
- FWCI
- 5.46
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Cincinnati Children's Hospital Medical Center
- National Institutes of Health
- U.S. Public Health Service
- National Institute on Aging (AG016282, R01AG016282)
- National Institute of Neurological Disorders and Stroke (R01NS052098)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pharmacological Receptor Mechanisms and Effects
- Keywords
- mitochondrial permeability transition pore, nitric oxide, neuronal apoptosis, dorsal lateral geniculate nucleus, oxidative stress, reactive oxygen species, peroxynitrite, cyclophilin D, adenine nucleotide translocase, voltage-dependent anion channel, nitric oxide synthase 1, protein nitration, S-nitrosylation, protein carbonylation, neuroprotection, thalamocortical neurons
- MeSH terms
- Peptidyl-Prolyl Isomerase F, Mitochondrial Permeability Transition Pore, Mitochondrial ADP, ATP Translocases, Animals, Calcium, Cholestenones, Decerebrate State, Gene Expression Regulation, Geniculate Bodies, Functional Laterality, Mice, Inbred C57BL, Mitochondria, Neurons, Nitric Oxide, Nitroimidazoles, Occipital Lobe, Zinc, Apoptosis, Reactive Oxygen Species, Mice, Knockout, Cyclophilins, Mitochondrial Membrane Transport Proteins, Immunoprecipitation, Voltage-Dependent Anion Channels, bcl-X Protein, Mice, Nitric Oxide Synthase Type I
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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