Aging-dependent mitochondrial dysfunction mediated by ceramide signaling inhibits antitumor T cell response
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We lack a mechanistic understanding of aging-mediated changes in mitochondrial bioenergetics and lipid metabolism that affect T cell function. The bioactive sphingolipid ceramide, induced by aging stress, mediates mitophagy and cell death; however, the aging-related roles of ceramide metabolism in regulating T cell function remain unknown. Here, we show that activated T cells isolated from aging mice have elevated C14/C16 ceramide accumulation in mitochondria, generated by ceramide synthase 6, leading to mitophagy/mitochondrial dysfunction. Mechanistically, aging-dependent mitochondrial ceramide inhibits protein kinase A, leading to mitophagy in activated T cells. This aging/ceramide-dependent mitophagy attenuates the antitumor functions of T cells in vitro and in vivo. Also, inhibition of ceramide metabolism or PKA activation by genetic and pharmacologic means prevents mitophagy and restores the central memory phenotype in aging T cells. Thus, these studies help explain the mechanisms behind aging-related dysregulation of T cells' antitumor activity, which can be restored by inhibiting ceramide-dependent mitophagy.
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In response to aging stress, CerS6 localizes to the mitochondria of aging T-cells, producing C14- and C16-ceramides, which induce ceramide-dependent hyperactivated mitophagy, restricting mitochondrial function and inhibiting the T-cell anti-tumor immunity.
“In response to aging stress, CerS6 localizes to the mitochondria of aging T-cells, producing C14- and C16-ceramides, which induce ceramide-dependent hyperactivated mitophagy, restricting mitochondrial function and inhibiting the T-cell anti-tumor immunity (9).”
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 [9]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredCeramide-dependent mitophagy is implicated in aging stress in T-cells, where CerS6 is recruited to mitochondrial membranes to generate C14-/C16-ceramides, which recruit LC3-containing autophagosomes to mitochondria and induce mitophagy.
“Ceramide-dependent mitophagy is implicated in the aging stress observed in T-cells (9), where Ceramide Synthase 6 (CerS6) is recruited to the mitochondrial membranes to mainly generate C14-/C16-ceramides, which recruit LC3-containing autophagosomes to mitochondria and induce mitophagy process (9).”
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 [9]
The Results section (“Aging stress induces ceramide-dependent mitophagy”; page not provided) reports CerS6-dependent mitochondrial C14 ceramide accumulation and mitophagy in aged T cells. The Introduction describes ceramide recruiting autophagosomes through LC3-II. The copy does not show that CerS6 itself is recruited to mitochondrial membranes, and the T-cell results emphasize C14 rather than equally establishing C14 and C16 as the mediators. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe increase in ceramide-dependent mitophagy in aging T-cells is detrimental to their anti-tumor function.
“While the increase in ceramide-dependent mitophagy in aging T-cells is detrimental to their anti-tumor function (9), homeostatic mild mitophagy in aging neurons is essential for healthy aging and mitochondrial quality control.”
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 [9]
Memory T-cell function substantially decreases with aging.
“The changes in the adaptive immune system, namely T-cells, with aging has been reported; memory T-cell function substantially decreases with aging (8,9), with alterations in mitochondrial function and mitochondrial dynamics (8–10).”
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 [9]
Aging is associated with alterations in mitochondrial function and mitochondrial dynamics in memory T cells.
“The changes in the adaptive immune system, namely T-cells, with aging has been reported; memory T-cell function substantially decreases with aging (8,9), with alterations in mitochondrial function and mitochondrial dynamics (8–10).”
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 [9]
The bioactive sphingolipid ceramide is implicated in modulating mitochondrial metabolism and suppressing anti-tumor responses in aging T-cells.
“Memory T-cells depend on mitochondrial and lipid metabolism for function and survival (11), and the bioactive sphingolipid ceramide was implicated in modulating mitochondrial metabolism and suppressing anti-tumor responses in aging T-cells (9).”
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 [9]
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- Authors
- Vaena, S., Chakraborty, P., Lee, H. G., Janneh, A. H., Kassir, M. F., Beeson, G., Hedley, Z., Yalcinkaya, A., Sofi, M. H., Li, H., Husby, M. L., Stahelin, R. V., Yu, X.-Z., Mehrotra, S., & Ogretmen, B.
- Affiliations
- Medical University of South Carolina (US)
- Purdue University West Lafayette (US)
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2021-05
- Volume
- 35
- Issue
- 5
- Pages
- 109076
- ISSN
- 2211-1247 (ISSN-L)
- PMC
- PMC8127241
- OpenAlex
- W3157990394
- Cited by
- 92
- References
- 91
- Citations by year
- 2026: 21 · 2025: 23 · 2024: 18 · 2023: 17 · 2022: 12 · 2021: 1
- FWCI
- 3.77
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (P01 CA203628, DE016572, AG069769, C06 RR015455, CA214461-03S1)
- Medical University of South Carolina
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- aging, mitochondrial dysfunction, ceramide signaling, mitophagy, T cell function, antitumor immunity, ceramide synthase 6, protein kinase A, sphingolipids, central memory T cells, mitochondrial bioenergetics, lipid metabolism
- MeSH terms
- Aging, Animals, Ceramides, Humans, Mitochondria, T-Lymphocytes, Signal Transduction, Mice
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