Alterations of lipid‐mediated mitophagy result in aging‐dependent sensorimotor defects
Open accessAbstract
The metabolic consequences of mitophagy alterations due to age‐related stress in healthy aging brains versus neurodegeneration remain unknown. Here, we demonstrate that ceramide synthase 1 (CerS1) is transported to the outer mitochondrial membrane by the p17/PERMIT transporter that recognizes mislocalized mitochondrial ribosomes (mitoribosomes) via 39‐FLRN‐42 residues, inducing ceramide‐mediated mitophagy. P17/PERMIT‐CerS1‐mediated mitophagy attenuated the argininosuccinate/fumarate/malate axis and induced d‐glucose and fructose accumulation in neurons in culture and brain tissues (primarily in the cerebellum) of wild‐type mice in vivo. These metabolic changes in response to sodium‐selenite were nullified in the cerebellum of CerS1to/to (catalytically inactive for C18‐ceramide production CerS1 mutant), PARKIN−/− or p17/PERMIT−/− mice that have dysfunctional mitophagy. Whereas sodium selenite induced mitophagy in the cerebellum and improved motor‐neuron deficits in aged wild‐type mice, exogenous fumarate or malate prevented mitophagy. Attenuating ceramide‐mediated mitophagy enhanced damaged mitochondria accumulation and age‐dependent sensorimotor abnormalities in p17/PERMIT−/− mice. Reinstituting mitophagy using a ceramide analog drug with selenium conjugate, LCL768, restored mitophagy and reduced malate/fumarate metabolism, improving sensorimotor deficits in old p17/PERMIT−/− mice. Thus, these data describe the metabolic consequences of alterations to p17/PERMIT/ceramide‐mediated mitophagy associated with the loss of mitochondrial quality control in neurons and provide therapeutic options to overcome age‐dependent sensorimotor deficits and related disorders like amyotrophic lateral sclerosis (ALS).
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Increase in ceramide species as response to aging stress was described.
“The increase in ceramide species as a response to aging stress was described (32).”
From Alzheimer's Disease–Associated Amyloid-β Precursor Protein Prevents Aging Stress–Induced Mitophagy and Fumarate Depletion to Improve Antitumor Immunity (2025) · cites this paper as [32]
Fumarate depletion is a metabolic signature of ceramide-mediated mitophagy in neurons.
“These data are consistent with the recent data, which showed fumarate depletion as a metabolic signature of ceramide-mediated mitophagy in neurons (32).”
From Alzheimer's Disease–Associated Amyloid-β Precursor Protein Prevents Aging Stress–Induced Mitophagy and Fumarate Depletion to Improve Antitumor Immunity (2025) · cites this paper as [32]
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- Authors
- Oleinik, N., Albayram, O., Kassir, M. F., Atilgan, F. C., Walton, C., Karakaya, E., Kurtz, J., Alekseyenko, A., Alsudani, H., Sheridan, M., Szulc, Z. M., & Ogretmen, B.
- Affiliations
- Medical University of South Carolina (US)
- Departments of Pathology and Laboratory Medicine Medical University of South Carolina Charleston South Carolina USA
- Cold Spring Harbor Laboratory (US)
- Department of Biochemistry and Molecular Biology Medical University of South Carolina Charleston South Carolina USA
- Corresponding author
- Oleinik, Natalia
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2023-08-23
- Volume
- 22
- Issue
- 10
- Pages
- e13954-e13954
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC10577547
- OpenAlex
- W4386117017
- Cited by
- 18
- References
- 43
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 7 · 2023: 1
- FWCI
- 3.59
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Aging Cell (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA203628, CA214461)
- National Institute of Dental and Craniofacial Research (DE016572)
- National Institute on Aging (AG069769)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Keywords
- mitophagy, mitochondrial ribosome, ceramide, mitochondrial quality control, sodium selenite, cerebellum, sensorimotor deficits, aging, amyotrophic lateral sclerosis, mitochondrial dysfunction
- MeSH terms
- Animals, Ceramides, Fumarates, Malates, Motor Neurons, Ubiquitin-Protein Ligases, Mice, Mitophagy
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