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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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Guan, Y., Wang, Y., Li, B., Shen, K., Li, Q., Ni, Y.-Y., & Huang, L. H. (2021) · Cancer Cell International · doi:10.1186/s12935-021-02065-w · Cited by 97
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Sphingolipids as critical players in retinal physiology and pathology
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Ceramide accumulation induces mitophagy and impairs β-oxidation in PINK1 deficiency
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“Furthermore, ceramide function is dependent on cellular localization, including the stabilization of the Golgi apparatus (49), fluidity of the endoplasmic reticulum (ER) membrane (50), and mitochondrial function (21, 24).”
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Huang, X., Withers, B. R., & Dickson, R. C. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2013.08.006 · Cited by 89
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Sphingolipids and Mitochondrial Dynamic
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Ishaq, M., Ojha, R., Sharma, A. J., & Singh, S. K. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.03.010 · Cited by 75
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“Interestingly, mitophagy might also be cytotoxic if it is excessively induced to degrade even functional mitochondria [23,24].”
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“…insignal transduction andcell regulation,andinawiderangeofotherbiologicalprocesses, including secretion, programmed cell death, autophagy, stress responses, and cell-cell interactions (Liang et al., 2003; Markham et al., 2011; Sentelle et al., 2012; Bi et al., 2014; Li et al., 2015; Wu etal.,2015).”
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“Ceramide, a bioactive sphingolipid, also can interact with LC3B to target autophagolysosomes to mitochondrial membranes and mediate lethal mitophagy (180).”
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BackgroundTargeting Sphingolipid Metabolism as a Therapeutic Strategy in Cancer Treatment
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“Their general function is to catalyze de novo synthesis of ceramides [62,63], which can induce apoptosis [64].”
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“Ceramide can directly interact with LC3B that may facilitate the targeting of lysosomes to APs [51].”
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BackgroundDiabetic Cardiomyopathy: A Brief Summary on Lipid Toxicity
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“Ceramide has also been shown to play a role in autophagy and even mitophagy.(78) Studies of ceramide-induced autoph-”
BackgroundRemodeling of Mitochondrial Plasticity: The Key Switch from NAFLD/NASH to HCC
Longo, M., Paolini, E., Meroni, M., & Dongiovanni, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22084173 · Cited by 61
Colpman, P., Dasgupta, A., & Archer, S. L. (2023) · Cells · doi:10.3390/cells12141897 · Cited by 66
“Ceramide in the OMM interacts with LC3B-II to trigger mitophagy [152].”
BackgroundHPV/E7 induces chemotherapy‐mediated tumor suppression by ceramide‐dependent mitophagy
Thomas, R. J., Oleinik, N. V., Selvam, S. P., Vaena, S. G., Dany, M., Nganga, R., Palma, R. M. D., Baron, K. D., Kim, J., Szulc, Z. M., et al. (2017) · EMBO Molecular Medicine · doi:10.15252/emmm.201607088 · Cited by 62
“D, E Effects of reconstitution of WT CerS1 (CS) versus mutant CerS1 (H138A) on ACO2 degradation (mitophagy marker) and on growth inhibition in response to SS (10 lM, 3 h) were determined using Western blotting (D) and trypan blue exclusion assay (E) in HPV(+) UM-SCC-47 cells, which were transfected with shRNA that tar…”
BackgroundMethodInfluentialSelf-citationCeramide synthases in cancer therapy and chemoresistance
Brachtendorf, S., El-Hindi, K., & Grösch, S. (2019) · Progress in Lipid Research · doi:10.1016/j.plipres.2019.04.002 · Cited by 61
Oleinik, N., Kim, J., Roth, B. M., Selvam, S. P., Gooz, M., Johnson, R. H., Lemasters, J. J., & Ogretmen, B. (2019) · Science Advances · doi:10.1126/sciadv.aax1978 · Cited by 68
“Carey (Department of Otolaryngology/Head and Neck Surgery, University of Michigan, Flint, MI, USA; RRID:CVCL_7707, RRID:CVCL_7759, and RRID: CVCL_7731, respectively); and UM-SCC-22A-Tet On V5-CerS1WT, UM-SCC-22A-Tet On V5-CerS1H138A, and UM-SCC-22A-Tet On V5-CerS6WT were generated as described earlier (14).”
InfluentialSelf-citationCrosstalk between autophagy and intracellular radiation response (Review)
Hu, L., Wang, H., Huang, L., Zhao, Y. L., & Wang, J. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3719 · Cited by 58
Dysregulated autophagy in COPD: A pathogenic process to be deciphered
Tan, W. S. D., Shen, H., & Wong, W. S. F. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.04.005 · Cited by 60
The pleiotropic roles of sphingolipid signaling in autophagy
Li, Y., Li, S., Qin, X.-J., Hou, W., Dong, H., Yao, L., & Xiong, L. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.215 · Cited by 61
“A recent study showed that Cer directly interacts with microtubule-associated protein light chain 3 (LC3) on mitochondrial membranes to induce deadly autophagy via an increase in intracellular mitophagy.(44) S1P has emerged as a cell-proliferative lipid messenger.”
BackgroundMitophagy in carcinogenesis and cancer treatment
Denisenko, T. V., Gogvadze, V. G., & Zhivotovsky, B. (2021) · Discover Oncology · doi:10.1007/s12672-021-00454-1 · Cited by 60
del Solar, V., Lizardo, D. Y., Li, N., Hurst, J. J., Brais, C. J., & Atilla‐Gokcumen, G. E. (2015) · Chemistry & Biology · doi:10.1016/j.chembiol.2015.11.004 · Cited by 58
Zheng, W., Wen, L., Zhu, F., Wang, Y., Xie, Q., Chen, Z., & Li, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.21955 · Cited by 58
“showed that CerS1 and C18-ceramide selectively induce non-apoptotic lethal autophagy independent of Bax, Bak, or caspase activity in HNSCC cells and tumors [16].”
BackgroundCPTP: A sphingolipid transfer protein that regulates autophagy and inflammasome activation
Mishra, S. K., Gao, Y., Deng, Y., Chalfant, C. E., Hinchcliffe, E. H., & Brown, R. E. (2017) · Autophagy · doi:10.1080/15548627.2017.1393129 · Cited by 57
Lauterbach, M., Saavedra, V., Mangan, M., Penno, A., Thiele, C., Latz, E., & Kuerschner, L. (2020) · Autophagy · doi:10.1080/15548627.2020.1804677 · Cited by 57
“Indeed, mitochondrial accumulation of various ceramides was described to facilitate recruitment of autophagosomes to damaged mitochondria leading to non-apoptotic lethal mitophagy [36].”
BackgroundLipid-mediated signals that regulate mitochondrial biology
Nielson, J. R., & Rutter, J. P. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.r117.001655 · Cited by 56
“They demonstrate that C18-ceramide directly binds LC3B-II, thereby recruiting the autophagosomal machinery to mitochondria and inducing mitophagy.”
BackgroundInfluentialTargeting lipid mediators in cancer biology
Sulciner, M. L., Gartung, A., Gilligan, M. M., Serhan, C. N., & Panigrahy, D. (2018) · Cancer and Metastasis Reviews · doi:10.1007/s10555-018-9754-9 · Cited by 57
Targeting regulated cell death in aortic aneurysm and dissection therapy
Chen, Y., He, Y., Wei, X., & Jiang, D. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.106048 · Cited by 59
Mitochondrial DNA as inflammatory DAMP: a warning of an aging immune system?
Zanini, G., Selleri, V., Doménech, S. L., Malerba, M., Nasi, M., Mattioli, A. V., & Pinti, M. (2023) · Biochemical Society Transactions · doi:10.1042/bst20221010 · Cited by 56
Stefanović, M., Tutusaus, A., Martínez-Nieto, G., Bárcena, C., de Gregorio, E., Moutinho, C., Barbero‐Camps, E., Villanueva, A., Colell, A., Marı́, M., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.6982 · Cited by 55
“Ceramide accumulation [24] and sorafenib exposure [25] have been reported to promote autophagy.”
Patra, S., Panigrahi, D. P., Praharaj, P. P., Bhol, C. S., Mahapatra, K. K., Mishra, S. R., Behera, B. P., Jena, M., & Bhutia, S. K. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03098-1 · Cited by 59
Qin, X., Wang, R., Xu, H., Tu, L., Chen, H., Li, H., Liu, N., Wang, J., Li, S., Yin, F., et al. (2022) · Autophagy · doi:10.1080/15548627.2021.2022360 · Cited by 55
Ilnytska, O., Lai, K., Gorshkov, K., Schultz, M. L., Tran, B. N., Jeziorek, M., Kunkel, T. J., Azaria, R. D., McLoughlin, H. S., Waghalter, M., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100813 · Cited by 56
“Ceramide also interacts with LC3-II to mediate cargo recruitment to AP (73, 74).”
BackgroundLiu, Q., Weng, J., Li, C., Feng, Y., Xie, M., Wang, X., Chang, Q., Li, M., Chung, K. F., Adcock, I. M., et al. (2023) · Particle and Fibre Toxicology · doi:10.1186/s12989-023-00534-w · Cited by 57
Local and long-range activation of innate immunity by infection and damage in C. elegans
Ewbank, J. J., & Pujol, N. (2015) · Current Opinion in Immunology · doi:10.1016/j.coi.2015.09.005 · Cited by 56
Fekry, B., Esmaeilniakooshkghazi, A., Krupenko, S. A., & Krupenko, N. I. (2016) · PLoS ONE · doi:10.1371/journal.pone.0146618 · Cited by 52
Ceramides and their roles in programmed cell death
Pilátová, M. B., Solárová, Z., Mezencev, R., & Solár, P. (2023) · Advances in Medical Sciences · doi:10.1016/j.advms.2023.10.004 · Cited by 53
Li, Q., Dong, Z., Lian, W., Cui, J., Wang, J., Shen, H., Liu, W., Yang, J., Zhang, X., & Cui, H. (2019) · Archives of Toxicology · doi:10.1007/s00204-019-02433-6 · Cited by 54
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“It was reported that BNIP3 contributed to ceramide-triggered lethal mitophagy in glioma cells [38].”
BackgroundSphingolipids as cell fate regulators in lung development and disease
Lee, J., Yeganeh, B., Ermini, L., & Post, M. (2015) · APOPTOSIS · doi:10.1007/s10495-015-1112-6 · Cited by 53
PUMA dependent mitophagy by Abrus agglutinin contributes to apoptosis through ceramide generation
Panda, P. K., Naik, P. P., Meher, B. R., Das, D. N., Mukhopadhyay, S., Praharaj, P. P., Maiti, T. K., & Bhutia, S. K. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2017.12.002 · Cited by 50
“Ceramide concentrations were expressed as pmole/million cells [30].”
BackgroundResultInfluentialLiu, Y., Yang, B., Zhang, L., Cong, X., Liu, Z., Hu, Y., Zhang, J., & Hu, H. (2018) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2018.01.091 · Cited by 50
Sphingosine Kinase 1 Cooperates with Autophagy to Maintain Endocytic Membrane Trafficking
Young, M. M., Takahashi, Y., Fox, T. E., Yun, J. K., KESTER, M. A., & Wang, H. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.019 · Cited by 49
Multiple pathways for mitophagy: A neurodegenerative conundrum for Parkinson’s disease
Chu, C. T. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.04.004 · Cited by 50
“In addition to cardiolipin, ceramide has been implicated in targeting autophagosomes to mitochondria to elicit a form of cell death involving mitophagy [65].”
BackgroundRole of Autophagy Pathway in Parkinson’s Disease and Related Genetic Neurological Disorders
Themistokleous, C., Bagnoli, E., Parulekar, R., & Muqit, M. M. K. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2023.168144 · Cited by 51
Zhang, W., Nishimura, T., Gahlot, D., Saito, C., Davis, C. T., Jefferies, H. B. J., Schreiber, A., Thukral, L., & Tooze, S. A. (2023) · eLife · doi:10.7554/elife.89185 · Cited by 45
“, 2007), and direct lipid binding (Chu et al., 2013; Sentelle et al., 2012).”
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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