A tale of two lipids: Lipid unsaturation commands ferroptosis sensitivity.
PUFA
ether lipid
ferroptosis
iron
membrane
necrosis
Journal
Proteomics
ISSN: 1615-9861
Titre abrégé: Proteomics
Pays: Germany
ID NLM: 101092707
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
revised:
03
11
2022
received:
12
05
2022
accepted:
08
11
2022
pubmed:
19
11
2022
medline:
17
3
2023
entrez:
18
11
2022
Statut:
ppublish
Résumé
Membrane lipids play important roles in the regulation of cell fate, including the execution of ferroptosis. Ferroptosis is a non-apoptotic cell death mechanism defined by iron-dependent membrane lipid peroxidation. Phospholipids containing polyunsaturated fatty acids (PUFAs) are highly vulnerable to peroxidation and are essential for ferroptosis execution. By contrast, the incorporation of less oxidizable monounsaturated fatty acids (MUFAs) in membrane phospholipids protects cells from ferroptosis. The enzymes and pathways that govern PUFA and MUFA metabolism therefore play a critical role in determining cellular sensitivity to ferroptosis. Here, we review three lipid metabolic processes-fatty acid biosynthesis, ether lipid biosynthesis, and phospholipid remodeling-that can govern ferroptosis sensitivity by regulating the balance of PUFAs and MUFAs in membrane phospholipids.
Identifiants
pubmed: 36398995
doi: 10.1002/pmic.202100308
doi:
Substances chimiques
Phospholipids
0
Fatty Acids, Unsaturated
0
Membrane Lipids
0
Types de publication
Journal Article
Review
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2100308Subventions
Organisme : NIH HHS
ID : 1F31CA265146-01
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM122923
Pays : United States
Organisme : American Cancer Society
Informations de copyright
© 2023 Wiley-VCH GmbH.
Références
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., Annicchiarico-Petruzzelli, M., Antonov, A. V., Arama, E., Baehrecke, E. H., Barlev, N. A., Bazan, N. G., Bernassola, F., Bertrand, M. J. M., Bianchi, K., … Kroemer, G. (2018). Molecular mechanisms of cell death: Recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death & Differentiation, 25, 486-541. https://doi.org/10.1038/s41418-017-0012-4
Dixon, S. J., Lemberg, K. M., Lamprecht, M. R., Skouta, R., Zaitsev, E. M., Gleason, C. E., Patel, D. N., Bauer, A. J., Cantley, A. M., Yang, W. S., Morrison, B., & Stockwell, B. R. (2012). Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 149, 1060-1072.
Yang, W. S., Sri Ramaratnam, R., Welsch, M. E., Shimada, K., Skouta, R., Viswanathan, V. S., Cheah, J. H., Clemons, P. A., Shamji, A. F., Clish, C. B., Brown, L. M., Girotti, A. W., Cornish, V. W., Schreiber, S. L., & Stockwell, B. R. (2014). Regulation of ferroptotic cancer cell death by GPX4. Cell, 156, 317-331. https://doi.org/10.1016/j.cell.2013.12.010
Kagan, V. E., Mao, G., Qu, F., Angeli, J. P., Doll, S., Croix, C. S., Dar, H. H., Liu, B., Tyurin, V. A., Ritov, V. B., Kapralov, A. A., Amoscato, A. A., Jiang, J., Anthonymuthu, T., Mohammadyani, D., Yang, Q., Proneth, B., Klein-Seetharaman, J., Watkins, S., … Bayır, H. (2017). Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nature Chemical Biology, 13, 81-90. https://doi.org/10.1038/nchembio.2238
Wiernicki, B., Dubois, H., Tyurina, Y. Y., Hassannia, B., Bayir, H., Kagan, V. E., Vandenabeele, P., Wullaert, A., & Vanden Berghe, T. (2020). Excessive phospholipid peroxidation distinguishes ferroptosis from other cell death modes including pyroptosis. Cell Death and Disease, 11, 922.
Friedmann Angeli, J. P., Schneider, M., Proneth, B., Tyurina, Y. Y., Tyurin, V. A., Hammond, V. J., Herbach, N., Aichler, M., Walch, A., Eggenhofer, E., Basavarajappa, D., Rãdmark, O., Kobayashi, S., Seibt, T., Beck, H., Neff, F., Esposito, I., Wanke, R., Fãrster, H., … Conrad, M. (2014). Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nature Cell Biology, 16, 1180-1191. https://doi.org/10.1038/ncb3064
Zilka, O., Shah, R., Li, B., Friedmann Angeli, J. P., Griesser, M., Conrad, M., & Pratt, D. A. (2017). On the mechanism of cytoprotection by ferrostatin-1 and liproxstatin-1 and the role of lipid peroxidation in ferroptotic cell death. ACS Central Science, 3, 232-243. https://doi.org/10.1021/acscentsci.7b00028
Zhang, B., Chen, X., Ru, F., Gan, Y., Li, B., Xia, W., Dai, G., He, Y., & Chen, Z. (2021). Liproxstatin-1 attenuates unilateral ureteral obstruction-induced renal fibrosis by inhibiting renal tubular epithelial cells ferroptosis. Cell Death and Disease, 12, 843. https://doi.org/10.1038/s41419-021-04137-1
Doll, S., Proneth, B., Tyurina, Y. Y., Panzilius, E., Kobayashi, S., Ingold, I., Irmler, M., Beckers, J., Aichler, M., Walch, A., Prokisch, H., Trümbach, D., Mao, G., Qu, F., Bayir, H., Füllekrug, J., Scheel, C. H., Wurst, W., Schick, C. H., … Conrad, M. (2017). ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nature Chemical Biology, 13, 91-98. https://doi.org/10.1038/nchembio.2239
Zielinski, Z. A. M., & Pratt, D. A. (2016). Cholesterol autoxidation revisited: Debunking the dogma associated with the most vilified of lipids. Journal of the American Chemical Society, 138, 6932-6935. https://doi.org/10.1021/jacs.6b03344
Forcina, G. C., & Dixon, S. J. (2019). GPX4 at the crossroads of lipid homeostasis and ferroptosis. Proteomics, 19, 1800311. https://doi.org/10.1002/pmic.201800311
Liang, D., Minikes, A. M., & Jiang, X. (2022). Ferroptosis at the intersection of lipid metabolism and cellular signaling. Molecular Cell, https://doi.org/10.1016/j.molcel.2022.03.022
Wagner, B. A., Buettner, G. R., & Burns, C. P. (1994). Free radical-mediated lipid peroxidation in cells: Oxidizability is a function of cell lipid bis-allylic hydrogen content. Biochemistry, 33, 4449-4453. https://doi.org/10.1021/bi00181a003
Yang, W. S., Kim, K. J., Gaschler, M. M., Patel, M., Shchepinov, M. S., & Stockwell, B. R. (2016). Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proceedings of the National Academy of Sciences USA, 113, E4966-E4975. https://doi.org/10.1073/pnas.1603244113
Catalá, A. (2009). Lipid peroxidation of membrane phospholipids generates hydroxy-alkenals and oxidized phospholipids active in physiological and/or pathological conditions. Chemistry and Physics of Lipids, 157, 1-11. https://doi.org/10.1016/j.chemphyslip.2008.09.004
Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity, 2014, 360438. https://doi.org/10.1155/2014/360438
Zou, Y., Li, H., Graham, E. T., Deik, A. A., Eaton, J. K., Wang, W., Sandoval-Gomez, G., Clish, C. B., Doench, J. G., & Schreiber, S. L. (2020). Cytochrome P450 oxidoreductase contributes to phospholipid peroxidation in ferroptosis. Nature Chemical Biology, 16, 302-309. https://doi.org/10.1038/s41589-020-0472-6
Yan, B., Ai, Y., Sun, Q., Ma, Y., Cao, Y., Wang, J., Zhang, Z., & Wang, X. (2021). Membrane damage during ferroptosis is caused by oxidation of phospholipids catalyzed by the oxidoreductases POR and CYB5R1. Molecular Cell, 81, 355-369. https://doi.org/10.1016/j.molcel.2020.11.024
Lee, J.-Y., Kim, W. K., Bae, K.-H., Lee, S. C., & Lee, E.-W. (2021). Lipid metabolism and ferroptosis. Biology, 10, 184.
Jiang, X., Stockwell, B. R., & Conrad, M. (2021). Ferroptosis: Mechanisms, biology and role in disease. Nature Reviews Molecular Cell Biology, 22, 266-282. https://doi.org/10.1038/s41580-020-00324-8
Eaton, J. K., Furst, L., Ruberto, R. A., Moosmayer, D., Hilpmann, A., Ryan, M. J., Zimmermann, K., Cai, L. L., Niehues, M., Badock, V., Kramm, A., Chen, S., Hillig, R. C., Clemons, P. A., Gradl, S., Montagnon, C., Lazarski, K. E., Christian, S., Bajrami, B., … Schreiber, S. L. (2020). Selective covalent targeting of GPX4 using masked nitrile-oxide electrophiles. Nature Chemical Biology, 16, 497-506. https://doi.org/10.1038/s41589-020-0501-5
Bannai, S., Tsukeda, H., & Okumura, H. (1977). Effect of antioxidants on cultured human diploid fibroblasts exposed to cystine-free medium. Biochemical and Biophysical Research Communications, 74, 1582-1588. https://doi.org/10.1016/0006-291X(77)90623-4
Badgley, M. A., Kremer, D. M., Maurer, H. C., DelGiorno, K. E., Lee, H. J., Purohit, V., Sagalovskiy, I. R., Ma, A., Kapilian, J., Firl, C. E. M., Decker, A. R., Sastra, S. A., Palermo, C. F., Andrade, L. R., Sajjakulnukit, P., Zhang, L., Tolstyka, Z. P., Hirschhorn, T., Lamb, C., … Olive, K. P. (2020). Cysteine depletion induces pancreatic tumor ferroptosis in mice. Science, 368, 85-89. https://doi.org/10.1126/science.aaw9872
Barayeu, U., Schilling, D., Eid, M., Xavier da Silva, T. N., Schlicker, L., Mitreska, N., Zapp, C., Gräter, F., Miller, A. K., Kappl, R., Schulze, A., Friedmann Angeli, J. P., & Dick, T. P. (2022). Hydropersulfides inhibit lipid peroxidation and ferroptosis by scavenging radicals. Nature Chemical Biology, 1-10.
Wu, Z., Khodade, V. S., Chauvin, J.-P. R., Rodriguez, D., Toscano, J. P., & Pratt, D. A. (2022). Hydropersulfides inhibit lipid peroxidation and protect cells from ferroptosis. Journal of the American Chemical Society, 144(34), 15825-15837. https://pubmed.ncbi.nlm.nih.gov/35977425/
Kajarabille, N., & Latunde-Dada, G. O. (2019). Programmed cell-death by ferroptosis: Antioxidants as mitigators. International Journal of Molecular Sciences, 20, 4968. https://doi.org/10.3390/ijms20194968
Bersuker, K., Hendricks, J. M., Li, Z., Magtanong, L., Ford, B., Tang, P. H., Roberts, M. A., Tong, B., Maimone, T. J., Zoncu, R., Bassik, M. C., Nomura, D. K., Dixon, S. J., & Olzmann, J. A. (2019). The CoQ oxidoreductase FSP1 acts in parallel to GPX4 to inhibit ferroptosis. Nature, 575, 688-692. https://doi.org/10.1038/s41586-019-1705-2
Doll, S., Freitas, F. P., Shah, R., Aldrovandi, M., da Silva, M. C., Ingold, I., Goya, G. A., Xavier da Silva, T. N., Panzilius, E., Scheel, C. H., Mourão, A., Buday, K., Sato, M., Wanninger, J., Vignane, T., Mohana, V., Rehberg, M., Flatley, A., Schepers, A., & Conrad, M. (2019). FSP1 is a glutathione-independent ferroptosis suppressor. Nature, 575, 693-698. https://doi.org/10.1038/s41586-019-1707-0
Kraft, V. A. N., Bezjian, C. T., Pfeiffer, S., Ringelstetter, L., Müller, C., Zandkarimi, F., Merl-Pham, J., Bao, X., Anastasov, N., Kössl, J., Brandner, S., Daniels, J. D., Schmitt-Kopplin, P., Hauck, S. M., Stockwell, B. R., Hadian, K., & Schick, J. A. (2020). GTP cyclohydrolase 1/tetrahydrobiopterin counteract ferroptosis through lipid remodeling. ACS Central Science, 6, 41-53. https://doi.org/10.1021/acscentsci.9b01063
Soula, M., Weber, R. A., Zilka, O., Alwaseem, H., La, K., Yen, F., Molina, H., Garcia-Bermudez, J., Pratt, D. A., & Birsoy, K. (2020). Metabolic determinants of cancer cell sensitivity to canonical ferroptosis inducers. Nature Chemical Biology, 1-10.
Mao, C., Liu, X., Zhang, Y., Lei, G., Yan, Y., Lee, H., Koppula, P., Wu, S., Zhuang, L., Fang, B., Poyurovsky, M. V., Olszewski, K., & Gan, B. (2021). DHODH-mediated ferroptosis defence is a targetable vulnerability in cancer. Nature, 593, 586-590. https://doi.org/10.1038/s41586-021-03539-7
Mishima, E., Nakamura, T., Zheng, J., Zhang, W., Mourão, A. S. D., Sennhenn, P., & Conrad, M. (2022). DHODH inhibitors sensitize cancer cells to ferroptosis via FSP1 inhibition. https://assets.researchsquare.com/files/rs-2190326/v1_covered.pdf?c=1666633598
Kapralov, A. A., Yang, Q., Dar, H. H., Tyurina, Y. Y., Anthonymuthu, T. S., Kim, R., St Croix, C. M., Mikulska-Ruminska, K., Liu, B., Shrivastava, I. H., Tyurin, V. A., Ting, H. C., Wu, Y. L., Gao, Y., Shurin, G. V., Artyukhova, M. A., Ponomareva, L. A., Timashev, P. S., Domingues, R. M., & Kagan, V. E. (2020). Redox lipid reprogramming commands susceptibility of macrophages and microglia to ferroptotic death. Nature Chemical Biology, 16, 278-290. https://doi.org/10.1038/s41589-019-0462-8
Mikulska-Ruminska, K., Anthonymuthu, T. S., Levkina, A., Shrivastava, I. H., Kapralov, A. A., Bayır, H., Kagan, V. E., & Bahar, I. (2021). NO. represses the oxygenation of arachidonoyl PE by 15LOX/PEBP1: Mechanism and role in ferroptosis. International Journal of Molecular Sciences, 22, 5253. https://doi.org/10.3390/ijms22105253
Shimada, K., Hayano, M., Pagano, N. C., & Stockwell, B. R. (2016). Cell-line selectivity improves the predictive power of pharmacogenomic analyses and helps identify NADPH as biomarker for ferroptosis sensitivity. Cell Chemical Biology, 23, 225-235. https://doi.org/10.1016/j.chembiol.2015.11.016
Llabani, E., Hicklin, R. W., Lee, H. Y., Motika, S. E., Crawford, L. A., Weerapana, E., & Hergenrother, P. J. (2019). Diverse compounds from pleuromutilin lead to a thioredoxin inhibitor and inducer of ferroptosis. Nature Chemistry, 11, 521-532. https://doi.org/10.1038/s41557-019-0261-6
Cui, S., Glenn Jr, S., Vale, G., Deng, Y., Kim, J., Kim, H., Zhang, R., McDonald, J. G., & Ye, J. (2022). FAF1 blocks ferroptosis by inhibiting peroxidation of polyunsaturated fatty acids. Proceedings of the National Academy of Sciences USA, 119, e2107189119. https://doi.org/10.1073/pnas.2107189119
Devisscher, L., Van Coillie, S., Hofmans, S., Van Rompaey, D., Goossens, K., Meul, E., Maes, L., De Winter, H., Van Der Veken, P., Vandenabeele, P., Berghe, T. V., & Augustyns, K. (2018). Discovery of novel, drug-like ferroptosis inhibitors with in vivo efficacy. Journal of Medicinal Chemistry, 61, 10126-10140. https://doi.org/10.1021/acs.jmedchem.8b01299
Hambright, W. S., Fonseca, R. S., Chen, L., Na, R., & Ran, Q. (2017). Ablation of ferroptosis regulator glutathione peroxidase 4 in forebrain neurons promotes cognitive impairment and neurodegeneration. Redox Biology, 12, 8-17. https://doi.org/10.1016/j.redox.2017.01.021
Tang, Q., Bai, L., Zou, Z., & Meng, P. (2018). Ferroptosis is newly characterized form of neuronal cell death in response to arsenite exposure. Neurotoxicology, 67, 27-36. https://doi.org/10.1016/j.neuro.2018.04.012
Liebisch, G., Vizcaíno, J. A., Köfeler, H., Trötzmüller, M., Griffiths, W. J., Schmitz, G., Spener, F., & Wakelam, M. J. O. (2013). Shorthand notation for lipid structures derived from mass spectrometry. Journal of Lipid Research, 54, 1523-1530. https://doi.org/10.1194/jlr.M033506
Liebisch, G., Fahy, E., Aoki, J., Dennis, E. A., Durand, T., Ejsing, C. S., Fedorova, M., Feussner, I., Griffiths, W. J., Köfeler, H., Merrill, A. H. Jr, Murphy, R. C., O'Donnell, V. B., Oskolkova, O., Subramaniam, S., Wakelam, M. J. O., & Spener, F. (2020). Update on LIPID MAPS classification, nomenclature, and shorthand notation for MS-derived lipid structures. Journal of Lipid Research, 61, 1539-1555. https://doi.org/10.1194/jlr.S120001025
Yamada, N., Karasawa, T., Kimura, H., Watanabe, S., Komada, T., Kamata, R., Sampilvanjil, A., Ito, J., Nakagawa, K., Kuwata, H., Hara, S., Mizuta, K., Sakuma, Y., Sata, N., & Takahashi, M. (2020). Ferroptosis driven by radical oxidation of n-6 polyunsaturated fatty acids mediates acetaminophen-induced acute liver failure. Cell Death and Disease, 11, 144. https://doi.org/10.1038/s41419-020-2334-2
Lorent, J. H., Levental, K. R., Ganesan, L., Rivera-Longsworth, G., Sezgin, E., Doktorova, M., Lyman, E., & Levental, I. (2020). Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape. Nature Chemical Biology, 1-9.
Meer, G. V., Voelker, D. R., & Feigenson, G. W. (2008). Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9, 112-124. https://doi.org/10.1038/nrm2330
Sparvero, L. J., Tian, H., Amoscato, A. A., Sun, W. Y., Anthonymuthu, T. S., Tyurina, Y. Y., Kapralov, O., Javadov, S., He, R. R., Watkins, S. C., Winograd, N., Kagan, V. E., & Bayır, H. (2021). Direct mapping of phospholipid ferroptotic death signals in cells and tissues by gas cluster ion beam secondary ion mass spectrometry (GCIB-SIMS). Angewandte Chemie International Edition, 60, 11784-11788. https://doi.org/10.1002/anie.202102001
Wenzel, S. E., Tyurina, Y. Y., Zhao, J., St Croix, C. M., Dar, H. H., Mao, G., Tyurin, V. A., Anthonymuthu, T. S., Kapralov, A. A., Amoscato, A. A., Mikulska-Ruminska, K., Shrivastava, I. H., Kenny, E. M., Yang, Q., Rosenbaum, J. C., Sparvero, L. J., Emlet, D. R., Wen, X., Minami, Y., … Kagan, V. E. (2017). PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell, 171, 628-641.e26.
Sun, W. Y., Tyurin, V. A., Mikulska-Ruminska, K., Shrivastava, I. H., Anthonymuthu, T. S., Zhai, Y. J., Pan, M. H., Gong, H. B., Lu, D. H., Sun, J., Duan, W. J., Korolev, S., Abramov, A. Y., Angelova, P. R., Miller, I., Beharier, O., Mao, G. W., Dar, H. H., Kapralov, A. A., … Kagan, V. E. (2021). Phospholipase iPLA2β averts ferroptosis by eliminating a redox lipid death signal. Nature Chemical Biology, 17, 465-476. https://doi.org/10.1038/s41589-020-00734-x
Anthonymuthu, T. S., Tyurina, Y. Y., Sun, W. Y., Mikulska-Ruminska, K., Shrivastava, I. H., Tyurin, V. A., Cinemre, F. B., Dar, H. H., VanDemark, A. P., Holman, T. R., Sadovsky, Y., Stockwell, B. R., He, R. R., Bahar, I., Bayır, H., & Kagan, V. E. (2021). Resolving the paradox of ferroptotic cell death: Ferrostatin-1 binds to 15LOX/PEBP1 complex, suppresses generation of peroxidized ETE-PE, and protects against ferroptosis. Redox Biology, 38, 101744. https://doi.org/10.1016/j.redox.2020.101744
Lamade, A. M., Wu, L., Dar, H. H., Mentrup, H. L., Shrivastava, I. H., Epperly, M. W., St Croix, C. M., Tyurina, Y. Y., Anthonymuthu, T. S., Yang, Q., Kapralov, A. A., Huang, Z., Mao, G., Amoscato, A. A., Hier, Z. E., Artyukhova, M. A., Shurin, G., Rosenbaum, J. C., Gough, P. J., … Bayır, H. (2022). Inactivation of RIP3 kinase sensitizes to 15LOX/PEBP1-mediated ferroptotic death. Redox Biology, 50, 102232. https://doi.org/10.1016/j.redox.2022.102232
Magtanong, L., Ko, P. J., To, M., Cao, J. Y., Forcina, G. C., Tarangelo, A., Ward, C. C., Cho, K., Patti, G. J., Nomura, D. K., Olzmann, J. A., & Dixon, S. J. (2019). Exogenous monounsaturated fatty acids promote a ferroptosis-resistant cell state. Cell Chemical Biology, 26, 420-432.e9. https://doi.org/10.1016/j.chembiol.2018.11.016
Shah, R., Shchepinov, M. S., & Pratt, D. A. (2018). Resolving the role of lipoxygenases in the initiation and execution of ferroptosis. ACS Central Science, 4, 387-396. https://doi.org/10.1021/acscentsci.7b00589
Chirala, S. S., & Wakil, S. J. (2004). Structure and function of animal fatty acid synthase. Lipids, 39, 1045-1053. https://doi.org/10.1007/s11745-004-1329-9
Song, X., Liu, J., Kuang, F., Chen, X., Zeh, H. J. 3rd, Kang, R., Kroemer, G., Xie, Y., & Tang, D. (2021). PDK4 dictates metabolic resistance to ferroptosis by suppressing pyruvate oxidation and fatty acid synthesis. Cell Reports, 34, 108767. https://doi.org/10.1016/j.celrep.2021.108767
Li, C., Dong, X., Du, W., Shi, X., Chen, K., Zhang, W., & Gao, M. (2020). LKB1-AMPK axis negatively regulates ferroptosis by inhibiting fatty acid synthesis. Signal Transduction and Targeted Therapy, 5, 187. https://doi.org/10.1038/s41392-020-00297-2
Hardie, D. G., & Pan, D. A. (2002). Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochemical Society Transactions, 30, 1064-1070. https://doi.org/10.1042/bst0301064
Lee, H., Zandkarimi, F., Zhang, Y., Meena, J. K., Kim, J., Zhuang, L., Tyagi, S., Ma, L., Westbrook, T. F., Steinberg, G. R., Nakada, D., Stockwell, B. R., & Gan, B. (2020). Energy-stress-mediated AMPK activation inhibits ferroptosis. Nature Cell Biology, 22, 225-234. https://doi.org/10.1038/s41556-020-0461-8
Robichaud, P.-P., Munganyiki, J. E., Boilard, E., & Surette, M. E. (2018). Polyunsaturated fatty acid elongation and desaturation in activated human T-cells: ELOVL5 is the key elongase[S]. Journal of Lipid Research, 59, 2383-2396. https://doi.org/10.1194/jlr.M090050
Lee, J. M., Lee, H., Kang, S., & Park, W. J. (2016). Fatty acid desaturases, polyunsaturated fatty acid regulation, and biotechnological advances. Nutrients, 8, 23. https://doi.org/10.3390/nu8010023
Wood, R., & Harlow, R. D. (1969). Structural studies of neutral glycerides and phosphoglycerides of rat liver. Archives of Biochemistry and Biophysics, 131, 495-501. https://doi.org/10.1016/0003-9861(69)90421-4
Dierge, E., Debock, E., Guilbaud, C., Corbet, C., Mignolet, E., Mignard, L., Bastien, E., Dessy, C., Larondelle, Y., & Feron, O. (2021). Peroxidation of n-3 and n-6 polyunsaturated fatty acids in the acidic tumor environment leads to ferroptosis-mediated anticancer effects. Cell Metabolism, 33, 1701-1715.e5. https://doi.org/10.1016/j.cmet.2021.05.016
Bond, L. M., Miyazaki, M., O'Neill, L. M., Ding, F., & Ntambi, J. M. (2016). Biochemistry of lipids, lipoproteins and membranes (6th ed., Elsevier, pp. 185-208). https://doi.org/10.1016/B978-0-444-63438-2.00006-7
Ubellacker, J. M., Tasdogan, A., Ramesh, V., Shen, B., Mitchell, E. C., Martin-Sandoval, M. S., Gu, Z., McCormick, M. L., Durham, A. B., Spitz, D. R., Zhao, Z., Mathews, T. P., & Morrison, S. J. (2020). Lymph protects metastasizing melanoma cells from ferroptosis. Nature, 585, 113-118. https://doi.org/10.1038/s41586-020-2623-z
Yi, J., Zhu, J., Wu, J., Thompson, C. B., & Jiang, X. (2020). Oncogenic activation of PI3K-AKT-mTOR signaling suppresses ferroptosis via SREBP-mediated lipogenesis. Proceedings of the National Academy of Sciences USA, 117, 31189-31197. https://doi.org/10.1073/pnas.2017152117
Tesfay, L., Paul, B. T., Konstorum, A., Deng, Z., Cox, A. O., Lee, J., Furdui, C. M., Hegde, P., Torti, F. M., & Torti, S. V. (2019). Stearoyl-CoA desaturase 1 protects ovarian cancer cells from ferroptotic cell death. Cancer Research, 79, 5355-5366.
Perez, M. A., Clostio, A. J., Houston, I. R., Ruiz, J., Magtanong, L., Dixon, S. J., & Watts, J. L. (2022). Ether lipid deficiency disrupts lipid homeostasis leading to ferroptosis sensitivity. PLoS Genetics, 18, e1010436. https://doi.org/10.1371/journal.pgen.1010436
Yamane, D., Hayashi, Y., Matsumoto, M., Nakanishi, H., Imagawa, H., Kohara, M., Lemon, S. M., & Ichi, I. (2021). FADS2-dependent fatty acid desaturation dictates cellular sensitivity to ferroptosis and permissiveness for hepatitis C virus replication. Cell Chemical Biology.
Hishikawa, D., Valentine, W., Iizuka-Hishikawa, Y., Shindou, H., & Shimizu, T. (2017). Metabolism and functions of docosahexaenoic acid-containing membrane glycerophospholipids. FEBS Letters, 591, 2730-2744. https://doi.org/10.1002/1873-3468.12825
Lands, W. E. M. (1958). Metabolism of glycerolipides: A comparison of lecithin and triglyceride synthesis. Journal of Biological Chemistry, 231, 883-888. https://doi.org/10.1016/S0021-9258(18)70453-5
Lands, W. E. M. (1960). Metabolism of glycerolipids II. The enzymatic acylation of lysolecithin. Journal of Biological Chemistry, 235, 2233-2237. https://doi.org/10.1016/S0021-9258(18)64604-6
Dennis, E. A. (1994). Diversity of group types, regulation, and function of phospholipase A2. Journal of Biological Chemistry, 269, 13057-13060. https://doi.org/10.1016/S0021-9258(17)36794-7
Beharier, O., Tyurin, V. A., Goff, J. P., Guerrero-Santoro, J., Kajiwara, K., Chu, T., Tyurina, Y. Y., St Croix, C. M., Wallace, C. T., Parry, S., Parks, W. T., Kagan, V. E., & Sadovsky, Y. (2020). PLA2G6 guards placental trophoblasts against ferroptotic injury. Proceedings of the National Academy of Sciences USA, 117, 27319-27328. https://doi.org/10.1073/pnas.2009201117
Chen, D., Chu, B., Yang, X., Liu, Z., Jin, Y., Kon, N., Rabadan, R., Jiang, X., Stockwell, B. R., & Gu, W. (2021). iPLA2β-mediated lipid detoxification controls p53-driven ferroptosis independent of GPX4. Nature Communications, 12, 3644. https://doi.org/10.1038/s41467-021-23902-6
Pap, E. H., Drummen, G. P., Winter, V. J., Kooij, T. W., Rijken, P., Wirtz, K. W., Op den Kamp, J. A., Hage, W. J., & Post, J. A. (1999). Ratio-fluorescence microscopy of lipid oxidation in living cells using C11-BODIPY581/591. FEBS Letters, 453, 278-282. https://doi.org/10.1016/S0014-5793(99)00696-1
Shindou, H., & Shimizu, T. (2009). Acyl-CoA:lysophospholipid acyltransferases*. Journal of Biological Chemistry, 284, 1-5. https://doi.org/10.1074/jbc.R800046200
Hishikawa, D., Shindou, H., Kobayashi, S., Nakanishi, H., Taguchi, R., & Shimizu, T. (2008). Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proceedings of the National Academy of Sciences USA, 105, 2830-2835. https://doi.org/10.1073/pnas.0712245105
O'Donnell, V. B. (2022). New appreciation for an old pathway: The Lands Cycle moves into new arenas in health and disease. Biochemical Society Transactions, 50, 1-11. https://doi.org/10.1042/BST20210579
Dixon, S. J., Winter, G. E., Musavi, L. S., Lee, E. D., Snijder, B., Rebsamen, M., Superti-Furga, G., & Stockwell, B. R. (2015). Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chemical Biology, 10, 1604-1609.
Zou, Y., Palte, M. J., Deik, A. A., Li, H., Eaton, J. K., Wang, W., Tseng, Y. Y., Deasy, R., Kost-Alimova, M., Dančík, V., Leshchiner, E. S., Viswanathan, V. S., Signoretti, S., Choueiri, T. K., Boehm, J. S., Wagner, B. K., Doench, J. G., Clish, C. B., Clemons, P. A., & Schreiber, S. L. (2019). A GPX4-dependent cancer cell state underlies the clear-cell morphology and confers sensitivity to ferroptosis. Nature Communications, 10, 1617. https://doi.org/10.1038/s41467-019-09277-9
Zou, Y., Henry, W. S., Ricq, E. L., Graham, E. T., Phadnis, V. V., Maretich, P., Paradkar, S., Boehnke, N., Deik, A. A., Reinhardt, F., Eaton, J. K., Ferguson, B., Wang, W., Fairman, J., Keys, H. R., Dančík, V., Clish, C. B., Clemons, P. A., Hammond, P. T., … Schreiber, S. L. (2020). Plasticity of ether lipids promotes ferroptosis susceptibility and evasion. Nature, 585, 603-608. https://doi.org/10.1038/s41586-020-2732-8
Kuwata, H., & Hara, S. (2019). Role of acyl-CoA synthetase ACSL4 in arachidonic acid metabolism. Prostaglandins & Other Lipid Mediators, 144, 106363.
Dixon, S. J., & Stockwell, B. R. (2018). The hallmarks of ferroptosis. Annual Review of Cancer Biology, 3, 35-54.
Stockwell, B. R., Friedmann, A. J. P., Bayir, H., Bush, A. I., Conrad, M., Dixon, S. J., Fulda, S., Gascón, S., Hatzios, S. K., Kagan, V. E., Noel, K., Jiang, X., Linkermann, A., Murphy, M. E., Overholtzer, M., Oyagi, A., Pagnussat, G. C., Park, J., Ran, Q., … Zhang, D. D. (2017). Ferroptosis: A regulated cell death nexus linking metabolism, redox biology, and disease. Cell, 171, 273-285.
Zheng, J., & Conrad, M. (2020). The metabolic underpinnings of ferroptosis. Cell Metabolism, 32, 920-937. https://doi.org/10.1016/j.cmet.2020.10.011
Hassannia, B., Vandenabeele, P., & Berghe, T. V. (2019). Targeting ferroptosis to iron out cancer. Cancer Cell, 35, 830-849. https://doi.org/10.1016/j.ccell.2019.04.002
Phadnis, V. V., Snider, J., Wong, V., & Vaccaro, K. D. (2022). MMD scaffolds ACSL4 and MBOAT7 to promote polyunsaturated phospholipid synthesis and susceptibility to ferroptosis. Biorxiv, https://doi.org/10.1101/2022.09.01.506096
Wang, K., Lee, C.-W., Sui, X., & Kim, S. (2022). The structure, catalytic mechanism, and inhibitor identification of phosphatidylinositol remodeling MBOAT7. https://doi.org/10.1101/2022.09.01.506096
Zhang, H.-L., Hu, B.-X., Li, Z.-L., Shan, J.-L., Ye, Z.-P., Peng, X.-D., Li, X., Huang, Y., Zhu, X.-Y., Chen, Y.-H., Feng, G.-K., Yang, D., Deng, R., & Zhu, X.-F. (2022). PKCβII phosphorylates ACSL4 to amplify lipid peroxidation to induce ferroptosis Nature Cell Biology, 24, 88-98. https://doi.org/10.1038/s41556-021-00818-3
Rodencal, J., & Dixon, S. J. (2022). Positive feedback amplifies ferroptosis. Nature Cell Biology, 24, 4-5. https://doi.org/10.1038/s41556-021-00824-5
Zhang, Q., Zhou, W., Yu, S., Ju, Y., To, S. K. Y., Wong, A. S. T., Jiao, Y., Poon, T. C. W., Tam, K. Y., & Lee, L. T. O. (2021). Metabolic reprogramming of ovarian cancer involves ACSL1-mediated metastasis stimulation through upregulated protein myristoylation. Oncogene, 40, 97-111. https://doi.org/10.1038/s41388-020-01516-4
Beatty, A., Singh, T., Tyurina, Y. Y., Tyurin, V. A., Samovich, S., Nicolas, E., Maslar, K., Zhou, Y., Cai, K. Q., Tan, Y., Doll, S., Conrad, M., Subramanian, A., Bayır, H., Kagan, V. E., Rennefahrt, U., & Peterson, J. R. (2021). Ferroptotic cell death triggered by conjugated linolenic acids is mediated by ACSL1. Nature Communications, 12, 2244. https://doi.org/10.1038/s41467-021-22471-y
Cui, P., Lin, Q., Fang, D., Zhang, L., Li, R., Cheng, J., Gao, F., Shockey, J., Hu, S., & Lã, S. (2018). Tung tree (Vernicia fordii, Hemsl.) genome and transcriptome sequencing reveals co-ordinate up-regulation of fatty acid beta-oxidation and triacylglycerol biosynthesis pathways during eleostearic acid accumulation in seeds. Plant & Cell Physiology, 59, 1990-2003.
Hishikawa, D., Hashidate, T., Shimizu, T., & Shindou, H. (2014). Diversity and function of membrane glycerophospholipids generated by the remodeling pathway in mammalian cells. Journal of Lipid Research, 55, 799-807. https://doi.org/10.1194/jlr.R046094
Yuki, K., Shindou, H., Hishikawa, D., & Shimizu, T. (2009). Characterization of mouse lysophosphatidic acid acyltransferase 3: An enzyme with dual functions in the testis. Journal of Lipid Research, 50, 860-869. https://doi.org/10.1194/jlr.M800468-JLR200
Hishikawa, D., Yanagida, K., Nagata, K., Kanatani, A., Iizuka, Y., Hamano, F., Yasuda, M., Okamura, T., Shindou, H., & Shimizu, T. (2020). Hepatic levels of DHA-containing phospholipids instruct SREBP1-mediated synthesis and systemic delivery of polyunsaturated fatty acids. iScience, 23, 101495.
Yamashita, A., Hayashi, Y., Matsumoto, N., Nemoto-Sasaki, Y., Oka, S., Tanikawa, T., & Sugiura, T. (2014). Glycerophosphate/acylglycerophosphate acyltransferases. Biology, 3, 801-830. https://doi.org/10.3390/biology3040801
Iizuka-Hishikawa, Y., Hishikawa, D., Sasaki, J., Takubo, K., Goto, M., Nagata, K., Nakanishi, H., Shindou, H., Okamura, T., Ito, C., Toshimori, K., Sasaki, T., & Shimizu, T. (2017). Lysophosphatidic acid acyltransferase 3 tunes the membrane status of germ cells by incorporating docosahexaenoic acid during spermatogenesis. Journal of Biological Chemistry, 292, 12065-12076.
Bebber, C. M., Thomas, E. S., Stroh, J., Chen, Z., Androulidaki, A., Schmitt, A., Höhne, M. N., Stüker, L., de Pádua Alves, C., Khonsari, A., Dammert, M. A., Parmaksiz, F., Tumbrink, H. L., Beleggia, F., Sos, M. L., Riemer, J., George, J., Brodesser, S., Thomas, R. K., … von Karstedt, S. (2021). Ferroptosis response segregates small cell lung cancer (SCLC) neuroendocrine subtypes. Nature Communications, 12, 2048. https://doi.org/10.1038/s41467-021-22336-4
IUPAC-IUB Commission on Biochemical Nomenclature (CBN). (1977). The nomenclature of lipids. European Journal of Biochemistry, 79, 11-21.
Nagan, N., & Zoeller, R. A. (2001). Plasmalogens: biosynthesis and functions. Progress in Lipid Research, 40, 199-229.
Bozelli, J. C., Azher, S., & Epand, R. M. (2021). Plasmalogens and chronic inflammatory diseases. Frontiers in Physiology, 12, 730829. https://doi.org/10.3389/fphys.2021.730829
Braverman, N. E., & Moser, A. B. (2012). Functions of plasmalogen lipids in health and disease. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 1822, 1442-1452. https://doi.org/10.1016/j.bbadis.2012.05.008
Gallego-García, A., Monera-Girona, A. J., Pajares-Martínez, E., Bastida-Martínez, E., Pérez-Castaño, R., Iniesta, A. A., Fontes, M., Padmanabhan, S., & Elías-Arnanz, M. (2019). A bacterial light response reveals an orphan desaturase for human plasmalogen synthesis. Science, 366, 128-132. https://doi.org/10.1126/science.aay1436
Otoki, Y., Kato, S., Kimura, F., Furukawa, K., Yamashita, S., Arai, H., Miyazawa, T., & Nakagawa, K. (2017). Accurate quantitation of choline and ethanolamine plasmalogen molecular species in human plasma by liquid chromatography-tandem mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis, 134, 77-85. https://doi.org/10.1016/j.jpba.2016.11.019
Fujiki, Y., Okumoto, K., Mukai, S., Honsho, M., & Tamura, S. (2014). Peroxisome biogenesis in mammalian cells. Frontiers in Physiology, 5, 307. https://doi.org/10.3389/fphys.2014.00307
Cui, W., Liu, D., Gu, W., & Chu, B. (2021). Peroxisome-driven ether-linked phospholipids biosynthesis is essential for ferroptosis. Cell Death & Differentiation, 28, 2536-2551. https://doi.org/10.1038/s41418-021-00769-0
Jakobsson, A., Westerberg, R., & Jacobsson, A. (2006). Fatty acid elongases in mammals: Their regulation and roles in metabolism. Progress in Lipid Research, 45, 237-249. https://doi.org/10.1016/j.plipres.2006.01.004
Wanders, R. J. A., Waterham, H. R., & Ferdinandusse, S. (2016). Metabolic interplay between peroxisomes and other subcellular organelles including mitochondria and the endoplasmic reticulum. Frontiers in Cell and Developmental Biology, 3, 83. https://doi.org/10.3389/fcell.2015.00083
Magtanong, L., Mueller, G. D., Williams, K. J., Billmann, M., Chan, K., Armenta, D. A., Pope, L. E., Moffat, J., Boone, C., Myers, C. L., Olzmann, J. A., Bensinger, S. J., & Dixon, S. J. (2022). Context-dependent regulation of ferroptosis sensitivity. Cell Chemical Biology, 29, 1409-1418.e6. https://doi.org/10.1016/j.chembiol.2022.06.004
Hardeman, D., & Bosch, H. (1989). Topography of ether phospholipid biosynthesis. Biochimica Et Biophysica Acta (BBA) - Lipids Lipid Metabolism, 1006, 1-8. https://doi.org/10.1016/0005-2760(89)90315-9
Honsho, M., Asaoku, S., Fukumoto, K., & Fujiki, Y. (2013). Topogenesis and homeostasis of fatty Acyl-CoA reductase 1. Journal of Biological Chemistry, 288, 34588-34598. https://doi.org/10.1074/jbc.M113.498345
Cheng, J. B., & Russell, D. W. (2004). Mammalian Wax Biosynthesis I. Identification of two fatty acyl-Coenzyme A reductases with different substrate specificities and tissue distributions. Journal of Biological Chemistry, 279, 37789-37797. https://doi.org/10.1074/jbc.M406225200
Perez, M. A., Magtanong, L., Dixon, S. J., & Watts, J. L. (2020). Dietary lipids induce ferroptosis in caenorhabditis elegans and human cancer cells. Developmental Celll, 54, 447-454.e4. https://doi.org/10.1016/j.devcel.2020.06.019
Dean, J. M., & Lodhi, I. J. (2018). Structural and functional roles of ether lipids. Protein & Cell, 9, 196-206. https://doi.org/10.1007/s13238-017-0423-5105
Morand, O. H., Zoeller, R. A., & Raetz, C. R. (1988). Disappearance of plasmalogens from membranes of animal cells subjected to photosensitized oxidation. Journal of Biological Chemistry, 263, 11597-11606. https://doi.org/10.1016/S0021-9258(18)38001-3
Xin, S., Mueller, C., Pfeiffer, S., Kraft, V. A. N., Merl-Pham, J., Bao, X., Feederle, R., Jin, X., Hauck, S. M., Schmitt-Kopplin, P., & Schick, J. A. (2021). MS4A15 drives ferroptosis resistance through calcium-restricted lipid remodeling. Cell Death & Differentiation, 29, 670-686.
Engelmann, B., Brautigam, C., & Thiery, J. (1994). Plasmalogen phospholipids as potential protectors against lipid peroxidation of low-density lipoproteins. Biochemical and Biophysical Research Communications, 204, 1235-1242. https://doi.org/10.1006/bbrc.1994.2595
Zommara, M., Tachibana, N., Mitsui, K., Nakatani, N., Sakono, M., Ikeda, I., & Imaizumi, K. (1995). Inhibitory effect of ethanolamine plasmalogen on iron- and copper-dependent lipid peroxidation. Free Radical Biology and Medicine, 18, 599-602.
Khan, M., Singh, J., & Singh, I. (2008). Plasmalogen deficiency in cerebral adrenoleukodystrophy and its modulation by lovastatin. Journal of Neurochemistry, 106, 1766-1779.
Zoeller, R. A., Grazia, T. J., LaCamera, P., Park, J., Gaposchkin, D. P., & Farber, H. W. (2002). Increasing plasmalogen levels protects human endothelial cells during hypoxia. American Journal of Physiology-Heart and Circulatory Physiology, 283, H671-H679. https://doi.org/10.1152/ajpheart.00524.2001
Khaselev, N., & Murphy, R. C. (1999). Susceptibility of plasmenyl glycerophosphoethanolamine lipids containing arachidonate to oxidative degradation. Free Radical Biology and Medicine, 26, 275-284.
Khaselev, N., & Murphy, R. C. (2000). Structural characterization of oxidized phospholipid products derived from arachidonate-containing plasmenyl glycerophosphocholine. Journal of Lipid Research, 41, 564-572. https://doi.org/10.1016/S0022-2275(20)32404-4
Werner, E. R., Keller, M. A., Sailer, S., Lackner, K., Koch, J., Hermann, M., Coassin, S., Golderer, G., Werner-Felmayer, G., Zoeller, R. A., Hulo, N., Berger, J., & Watschinger, K. (2020). The TMEM189 gene encodes plasmanylethanolamine desaturase which introduces the characteristic vinyl ether double bond into plasmalogens. Proceedings of the National Academy of Sciences USA, 117, 7792-7798. https://doi.org/10.1073/pnas.1917461117
Koslowski, M., Sahin, U., Dhaene, K., Huber, C., & Türeci, Ö. (2008). MS4A12 is a colon-selective store-operated calcium channel promoting malignant cell processes. Cancer Research, 68, 3458-3466. https://doi.org/10.1158/0008-5472.CAN-07-5768
Reed, A., Ware, T., Li, H., Bazan, J. F., & Cravatt, B. F. (2022). TMEM164 is an acyltransferase that forms ferroptotic polyunsaturated ether phospholipids. Biorxiv, https://doi.org/10.1101/2022.07.06.498872
Chen, X., Kang, R., Kroemer, G., & Tang, D. (2021). Broadening horizons: The role of ferroptosis in cancer. Nature Reviews Clinical Oncology, 18, 280-296. https://doi.org/10.1038/s41571-020-00462-0
Messias, M. C. F., Mecatti, G. C., Priolli, D. G., Carvalho, P., & de, O. (2018). Plasmalogen lipids: Functional mechanism and their involvement in gastrointestinal cancer. Lipids in Health and Disease, 17, 41. https://doi.org/10.1186/s12944-018-0685-9
Snyder, F., & Wood, R. (1969). Alkyl and alk-1-enyl ethers of glycerol in lipids from normal and neoplastic human tissues. Cancer Research, 29, 251-257.
Howard, B. V., Morris, H. P., & Bailey, J. M. (1972). Ether-lipids, -glycerol phosphate dehydrogenase, and growth rate in tumors and cultured cells. Cancer Research, 32, 1533-1538.
Albert, D. H., & Anderson, C. E. (1977). Ether-linked glycerolipids in human brain tumors. Lipids, 12, 188-192. https://doi.org/10.1007/BF02533292
Roos, D. S., & Choppin, P. W. (1984). Tumorigenicity of cell lines with altered lipid composition. Proceedings of the National Academy of Sciences USA, 81, 7622-7626. https://doi.org/10.1073/pnas.81.23.7622
Liesenfeld, D. B., Grapov, D., Fahrmann, J. F., Salou, M., Scherer, D., Toth, R., Habermann, N., Böhm, J., Schrotz-King, P., Gigic, B., Schneider, M., Ulrich, A., Herpel, E., Schirmacher, P., Fiehn, O., Lampe, J. W., & Ulrich, C. M. (2015). Metabolomics and transcriptomics identify pathway differences between visceral and subcutaneous adipose tissue in colorectal cancer patients: The ColoCare study. The American Journal of Clinical Nutrition, 102, 433-443. https://doi.org/10.3945/ajcn.114.103804
Patterson, N. H., Alabdulkarim, B., Lazaris, A., Thomas, A., Marcinkiewicz, M. M., Gao, Z. H., Vermeulen, P. B., Chaurand, P., & Metrakos, P. (2016). Assessment of pathological response to therapy using lipid mass spectrometry imaging. Scientific Reports, 6, 36814. https://doi.org/10.1038/srep36814