The mitochondrial calcium regulator cyclophilin d is an essential component of oestrogen-mediated neuroprotection in amyotrophic lateral sclerosis
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Amyotrophic lateral sclerosis is a devastating neurodegenerative disorder that is more prevalent in males than in females. A similar gender difference has been reported in some strains of transgenic mouse models of familial amyotrophic lateral sclerosis harbouring the G93A mutation in CuZn superoxide dismutase. Mitochondrial damage caused by pathological alterations in Ca(2+) accumulation is frequently involved in neurodegenerative diseases, including CuZn superoxide dismutase-related amyotrophic lateral sclerosis, but its association with gender is not firmly established. In this study, we examined the effects of genetic ablation of cyclophilin D on gender differences in mice expressing G93A mutant CuZn superoxide dismutase. Cyclophilin D is a mitochondrial protein that promotes mitochondrial damage from accumulated Ca(2+). As anticipated, we found that cyclophilin D ablation markedly increased Ca(2+) retention in brain mitochondria of both males and females. Surprisingly, cyclophilin D ablation completely abolished the phenotypic advantage of G93A females, with no effect on disease in males. We also found that the 17β-oestradiol decreased Ca(2+) retention in brain mitochondria, and that cyclophilin D ablation abolished this effect. Furthermore, 17β-oestradiol protected G93A cortical neurons and spinal cord motor neurons against glutamate toxicity, but the protection was lost in neurons lacking cyclophilin D. Taken together, these results identify a novel mechanism of oestrogen-mediated neuroprotection in CuZn superoxide dismutase-related amyotrophic lateral sclerosis, whereby Ca(2+) overload and mitochondrial damage are prevented in a cyclophilin D-dependent manner. Such a protective mechanism may contribute to the lower incidence and later onset of amyotrophic lateral sclerosis, and perhaps other chronic neurodegenerative diseases, in females.
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Female brain and heart mitochondria have lower Ca2+ uptake than males.
“Conversely, the female brain and heart mitochondria have lower Ca2+ uptake than males (105, 106).”
From From mitochondria to sarcopenia: role of 17β-estradiol and testosterone (2023) · cites this paper as [105]
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The Protective Effect of Aromatase on NSC-34 Cells with Stably Expressed hSOD1-G93A
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Sex Differences and Gut Microbiota Changes in Parkinson’s Disease
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Sex hormones in neuroprotection and neurodegeneration
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Endocrine Disruption After Brain Injury
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- Authors
- Kim, H. J., Magranè, J., Starkov, A. A., & Manfredi, G.
- Affiliations
- Cornell University (US)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-08-29
- Volume
- 135
- Issue
- 9
- Pages
- 2865-2874
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3437032
- OpenAlex
- W2116110451
- Cited by
- 64
- References
- 42
- Citations by year
- 2025: 2 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 3 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 10 · 2016: 4 · 2015: 3 · 2014: 6 · 2013: 4
- FWCI
- 2.72
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Muscular Dystrophy Association
- National Institutes of Health (5r01ns051419-09, NS062055, NS051419)
- National Institute of Neurological Disorders and Stroke (R01NS062055, R01-NS051419)
- Robert Packard Center for ALS Research, Johns Hopkins University
- Topics
- Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- cyclophilin D, amyotrophic lateral sclerosis, estradiol, sex differences, glutamate excitotoxicity, motor neurons, neurodegeneration, mitochondrial calcium overload
- MeSH terms
- Superoxide Dismutase-1, Peptidyl-Prolyl Isomerase F, Amyotrophic Lateral Sclerosis, Animals, Brain, Calcium, Estradiol, Mitochondria, Neurons, Phenotype, Spinal Cord, Superoxide Dismutase, Mice, Knockout, Neuroprotective Agents, Cyclophilins, Mice, Membrane Potential, Mitochondrial
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