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Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy
Open accessAbstract
Mechanisms by which autophagy promotes cell survival or death are unclear. We provide evidence that C(18)-pyridinium ceramide treatment or endogenous C(18)-ceramide generation by ceramide synthase 1 (CerS1) expression mediates autophagic cell death, independent of apoptosis in human cancer cells. C(18)-ceramide-induced lethal autophagy was regulated via microtubule-associated protein 1 light chain 3 β-lipidation, forming LC3B-II, and selective targeting of mitochondria by LC3B-II-containing autophagolysosomes (mitophagy) through direct interaction between ceramide and LC3B-II upon Drp1-dependent mitochondrial fission, leading to inhibition of mitochondrial function and oxygen consumption. Accordingly, expression of mutant LC3B with impaired ceramide binding, as predicted by molecular modeling, prevented CerS1-mediated mitochondrial targeting, recovering oxygen consumption. Moreover, knockdown of CerS1 abrogated sodium selenite-induced mitophagy, and stable LC3B knockdown protected against CerS1- and C(18)-ceramide-dependent mitophagy and blocked tumor suppression in vivo. Thus, these data suggest a new receptor function of ceramide for anchoring LC3B-II autophagolysosomes to mitochondrial membranes, defining a key mechanism for the induction of lethal mitophagy.
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“The localization of CerS1 to the mitochondria and the synthesis of ceramide in the outer mitochondrial membrane recruit the autophagic machinery and induce mitophagy (15) by binding autophagosome-associated LC3.”
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 [15]
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“In addition, ceramide is known to induce lethal levels of mitophagy through direct binding to LC3B-II, which recruits the autophagosome to the mitochondria thereby initiating mitophagy and ultimately cell death (78).”
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“Furthermore, CerS1-derived C18:0-ceramides promotes lethal mitophagy, resulting in reduced mitochondrial fatty acid oxidative capacity [75].”
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Ceramide enhances binding of LC3/GABARAP autophagy proteins to cardiolipin-containing membranes
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“36,37 Sphingolipids function in the autophagy and DNA damage response, 17,18,20 and their levels are altered by treatment with autophagy modulators, such as hydroxy-chloroquine.”
BackgroundMethodCeramide synthases: insights into the expression and prognosis of lung cancer
Qian, H.-J., Deng, J., Lu, C., et al. (2020) · Experimental Lung Research · doi:10.1080/01902148.2020.1844345 · Cited by 12
Mandik, F., Kanana, Y., Rody, J., Misera, S., Wilken, B., Laabs, B., Klein, C., & Vos, M. H. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1000553 · Cited by 13
“Hence, ceramide is a key sphingolipid that, upon mitochondrial accumulation, leads to ceramide-induced mitophagy, the autophagy of mitochondria (Sentelle et al., 2012).”
BackgroundMani, S., Ralph, S. J., Swargiary, G., Rani, M., Wasnik, S., Singh, M., & Devi, A. (2023) · Antioxidants and Redox Signaling · doi:10.1089/ars.2023.0379 · Cited by 12
“Eventually, the ceramide-induced mitophagy results in cell death and tumor suppression (Sentelle et al., 2012).”
Metabolomic and lipidomic pathways in aneurysmal subarachnoid hemorrhage
Yang, B. S. K., Blackburn, S., Lorenzi, P. L., Choi, H. A., & Gusdon, A. M. (2024) · Neurotherapeutics · doi:10.1016/j.neurot.2024.e00504 · Cited by 12
“Ceramide has also been shown to interact with light chain 3 beta lipidation to anchor mitochondria and autophagosomes and induce mitophagy [125].”
Rández‐Gil, F., Sánchez‐Adriá, I. E., Estruch, F., et al. (2019) · Microbial Biotechnology · doi:10.1111/1751-7915.13513 · Cited by 12
“Increased Cer levels disturb membrane permeability, induce lethal mitophagy and trigger cell apoptosis (Sentelle et al., 2012), and thus, cells deficient in SLs synthesis are resistant to AbA (Schorling et al.”
BackgroundTargeting Sphingosine Kinase 1 for the Treatment of Pulmonary Arterial Hypertension
Yang, K., Jiang, K., Xu, Z., Song, Y., & Wang, J. (2019) · Future Medicinal Chemistry · doi:10.4155/fmc-2019-0130 · Cited by 10
Natural products as geroprotectors: An autophagy perspective
Raj, S. D., Fann, D. Y., Wong, E. S. P., & Kennedy, B. K. (2021) · Medicinal Research Reviews · doi:10.1002/med.21815 · Cited by 12
Metformin Inhibits Autophagy, Mitophagy and Antagonizes Doxorubicin-Induced Cardiomyocyte Death
Van, J., Hahn, Y., Silverstein, B., Li, C., Cai, F., Wei, J., Katiki, L., Mehta, P. K., Livatova, K., DelPozzo, J., et al. (2023) · International Journal of Drug Discovery and Pharmacology · doi:10.53941/ijddp.0201004 · Cited by 13
“Although mitophagy is believed to be protective in most cases [44], it can be harmful under certain conditions [45, 46], including DOX-induced cardiotoxicity [47].”
BackgroundTranscription factor FOXM1 specifies chromatin DNA to extracellular vesicles
Zhang, Y., Ding, N., Li, Y., Zhao, X., Yang, S., Fu, P., Peng, Y., Cheng, H., Ouyang, M., 王瑞平, et al. (2023) · Autophagy · doi:10.1080/15548627.2023.2284523 · Cited by 15
“On the other hand, because LC3 residues R10, R11, and F52 mediated LC3 binding to its protein partners [10,34], we tested whether the LC3 aa1–28 region (containing R10 and R11) or LC3 aa29–128 region (containing F52) could interact with FOXM1 in GST-affinity-isolation assays.”
BackgroundKarakaya, E., Oleinik, N. V., Edwards, J. M., Tomberlin, J., Barker, R. B., Berber, B., Ericsson, M., Alsudani, H., Ergul, A., Beyaz, S., et al. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae018 · Cited by 13
Self-citationCERS1 is a biomarker of Staphylococcus aureus abundance and atopic dermatitis severity
Kenney, H. M., Yoshida, T., Berdyshev, E. V., Calatroni, A., Gill, S. R., Simpson, E. L., Lussier, S. J., Boguniewicz, M., Hata, T. R., Fuxench, Z. C. C., et al. (2024) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2024.09.017 · Cited by 11
The Role of Autophagy in Excitotoxicity, Synaptic Mitochondrial Stress and Neurodegeneration
Chu, C. T. (2025) · Autophagy Reports · doi:10.1080/27694127.2025.2464376 · Cited by 12
“A third class of selective autophagy mechanisms involves mitochondrial lipids such as cardiolipin or ceramide [79-81].”
Eswaran, S., Mascarenhas, R., & Kabekkodu, S. P. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02218-8 · Cited by 11
Lama, S., Monda, V., Rizzo, M. R., Dacrema, M., Maisto, M., Annunziata, G., Tenore, G. C., Novellino, E., & Stiuso, P. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/2961406 · Cited by 12
“A recent study showed that Cer directly interacts with microtubule-associated protein light chain 3 (LC3) on mitochondrial membranes, inducing autophagy [10].”
BackgroundChemical tools for modulating autophagy
Triola, G. (2014) · Tetrahedron · doi:10.1016/j.tet.2014.10.057 · Cited by 11
Mitophagy: Vps13D Couples Mitochondrial Fission and Autophagic Clearance
Wang, Z., & Zhang, H. (2018) · Current Biology · doi:10.1016/j.cub.2017.12.017 · Cited by 11
Molecular and mesoscopic geometries in autophagosome generation. A review
Iriondo, M. N., Etxaniz, A., Antón, Z., Montes, L. R., & Alonso, A. (2021) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2021.183731 · Cited by 12
Kassir, M. F., Lee, H. G., Oleinik, N. V., Wofford, W., Walton, C., Atilgan, F. C., Janneh, A. H., Chakraborty, P., Calisir, K., Percin, E., et al. (2025) · Cancer Research · doi:10.1158/0008-5472.can-24-4740 · Cited by 10
McCaffrey, J. M., & Ibdah, J. A. (2025) · Nutrients · doi:10.3390/nu17182972 · Cited by 14
“Drp1 is both an essential regulator of fission and a recruiter of ceramides to the OMM [96].”
InfluentialMitochondrial damage and clearance in retinal pigment epithelial cells
Gurubaran, I. S. (2024) · Acta Ophthalmologica · doi:10.1111/aos.16661 · Cited by 11
Mitochondrial abnormalities as a target of intervention in acute myeloid leukemia
Tjahjono, E., Daneman, M. R., Meika, B., Revtovich, A. V., & Kirienko, N. V. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2024.1532857 · Cited by 12
Zhang, L., Yang, S., Cui, H. Z., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-89176-w · Cited by 10
Metabolome-Driven Regulation of Adenovirus-Induced Cell Death
Laevskaya, A., Borovjagin, A. V., Timashev, P. S., Lesniak, M. S., & Ulasov, I. V. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22010464 · Cited by 10
“Several studies showed that the accumulation of C18-ceramides on the surface of the mitochondrial membrane leads to their binding to LC3 protein, which could promote a lethal mitophagy in head and neck squamous cell carcinoma [25,26].”
BackgroundInvolvement of Sphingolipids in Ethanol Neurotoxicity in the Developing Brain
Saito, M., & Saito, M. (2013) · Brain Sciences · doi:10.3390/brainsci3020670 · Cited by 11
“to LC3B-II and anchors LC3B-II-positive autophagolysosomes to mitochondrial membranes to induce mitophagy [231].”
BackgroundSheridan, M., Chowdhury, N., Wellslager, B., Oleinik, N. V., Kassir, M. F., Lee, H. G., Engevik, M. A., Peterson, Y. K., Pandruvada, S. N. M., Szulc, Z. M., et al. (2024) · iScience · doi:10.1016/j.isci.2024.109860 · Cited by 10
“We began with our previous model of C18-ceramide interaction with LC3 (Sentelle et al. 28 ).”
InfluentialSelf-citationSphingolipids in thyroid eye disease
Gulbins, A., Görtz, G.-E., Gulbins, E., & Eckstein, A. K. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1170884 · Cited by 9
“In addition to re-organizing the cell membrane and to form membrane platforms, ceramide has been also shown to directly regulate several molecules, i.e. cathepsin D (30), phospholipase A2 (31), kinase suppressor of Ras (32), ceramide-activated protein serine-threonine phosphatases [CAPP] (33), protein kinase C isoform…”
BackgroundAgrawal, B., Boulos, S., Khatib, S., Feuermann, Y., Panov, J., & Kaphzan, H. (2024) · Cells · doi:10.3390/cells13030205 · Cited by 9
“A further accumulation of ceramide in mitochondria leads to increased ROS levels [31], decreased ATP production [59], and the induction of apoptosis [60].”
BackgroundA Three‐Step Assay for Ceramide Synthase Activity Using a Fluorescent Substrate and HPLC
Couttas, T. A., Lim, X. Y., & Don, A. S. (2014) · Lipids · doi:10.1007/s11745-014-3969-5 · Cited by 9
“This assay uses commercially available 7-nitro-2-1,3-benzoxadiazole (NBD)-labelled dihydrosphingosine [(2S,3R)2-amino-18((7-nitrobenzo[c][1,2,5]oxadiazol-4-yl) amino)octadecane-1-3-diol] as a substrate in place of the natural dihydrosphingosine substrate [18].”
BackgroundMethodVarela, Y. R., González-Ramírez, E. J., Iriondo, M. N., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065080 · Cited by 9
“Even if the relevance of Cer in the binding of LC3/GABARAP to membranes was suggested [14], CL and Cer are rarely found together in membranes.”
BackgroundTargeting mitophagy for neurological disorders treatment: advances in drugs and non-drug approaches
Yang, X., Zhang, Y., Luo, J.-X., Zhu, T., Zhao, R., Mu, B., & Lu, M. (2023) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-023-02636-w · Cited by 9
“A previous study reported a mechanistic link between ceramide signaling and mitophagy, and found that C18 ceramide cooperates with LC3B to recruit damaged mitochondria to autophagic vesicles after DRP1-mediated mitochondrial fission (Sentelle et al. 2012).”
BackgroundRole of mitophagy in spinal cord ischemia-reperfusion injury
Duan, Y., Yang, F., Zhang, Y., Zhang, M., Shi, Y., Lang, Y., Sun, H., Wang, X., Jin, H., & Kang, X. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00668 · Cited by 8
Chen, J., Zhu, L., Wang, F., Zhu, Y., Chen, J., Liang, C., Liu, B., Pang, A., & Yang, X. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-04765-0 · Cited by 9
“Ceramide triggers the generation of activated lipids and autophagic markers within mitochondria, facilitating the targeting of mitochondria to autophagosomes and promoting ceramide-induced mitophagy [44, 45].”
Endo, T. H., Samokhvalov, V., Darwesh, A. M., et al. (2018) · Cell Death Discovery · doi:10.1038/s41420-018-0090-1 · Cited by 8
Metadata
- Authors
- Sentelle, R. D., Senkal, C. E., Jiang, W., Ponnusamy, S., Gencer, S., Panneer Selvam, S., Ramshesh, V. K., Peterson, Y. K., Lemasters, J. J., Szulc, Z. M., Bielawski, J., & Ogretmen, B.
- Affiliations
- Medical University of South Carolina (US)
- Venue
- Nature Chemical Biology
- Published
- 2012-08-26
- Volume
- 8
- Issue
- 10
- Pages
- 831-838
- ISSN
- 1552-4450 (ISSN-L)
- 1552-4469
- PMC
- PMC3689583
- OpenAlex
- W1981224101
- Cited by
- 539
- References
- 44
- Citations by year
- 2026: 36 · 2025: 44 · 2024: 50 · 2023: 56 · 2022: 35 · 2021: 47 · 2020: 38 · 2019: 37 · 2018: 48 · 2017: 41 · 2016: 32 · 2015: 31 · 2014: 27 · 2013: 15 · 2012: 2
- FWCI
- 17.96
- Type
- journal article
- Language
- en
- Update notices
- erratum (2012-11-26)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Chemical Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (1c06rr015455-01a1)
- National Institute on Alcohol Abuse and Alcoholism (P50AA011605, 1-P50-AA11605)
- National Cancer Institute (CA088932, R01CA088932, CA097165, P30CA138313)
- National Institute of Diabetes and Digestive and Kidney Diseases (5P30 DK 34987, P30DK034987)
- National Institute of Dental and Craniofacial Research (DE-016572, R01DE016572)
- National Center for Research Resources (C06 RR-015455)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- ceramide, mitophagy, autophagy, LC3B-II, LC3B lipidation, CERS1, autophagic cell death, Drp1, mitochondrial fission, autophagolysosomes, mitochondrial targeting, oxygen consumption, sodium selenite, tumor suppression, cancer cells
- MeSH terms
- Autophagy, Ceramides, Humans, Lipids, Phagosomes, Cell Death, Microscopy, Confocal, Cell Line, Tumor, Mitophagy
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