Plasticity of ether lipids promotes ferroptosis susceptibility and evasion
Ferroptosis—an iron-dependent, non-apoptotic cell death process—is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers 1 . The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during c...
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| Published in | Nature (London) Vol. 585; no. 7826; pp. 603 - 608 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
24.09.2020
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/s41586-020-2732-8 |
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| Abstract | Ferroptosis—an iron-dependent, non-apoptotic cell death process—is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers
1
. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions
2
–
5
. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR–Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome–ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis.
The cellular organelles peroxisomes contribute to the sensitivity of cells to ferroptosis by synthesizing polyunsaturated ether phospholipids, and changes in the abundances of these lipids are associated with altered sensitivity to ferroptosis during cell-state transitions. |
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| AbstractList | Ferroptosis--an iron-dependent, non-apoptotic cell death process--is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers.sup.1. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions.sup.2-5. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. Ferroptosis-an iron-dependent, non-apoptotic cell death process-is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers1. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions2-5. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis.Ferroptosis-an iron-dependent, non-apoptotic cell death process-is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers1. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions2-5. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. Ferroptosis, an iron-dependent, non-apoptotic cell death program, is involved in various degenerative diseases and represents a targetable vulnerability in certain cancers 1 . The ferroptosis-susceptible cell state can either preexist in cells arising from certain lineages or be acquired during cell-state transitions 2 – 5 . Precisely how ferroptosis susceptibility is dynamically regulated remains poorly understood. Using genome-wide CRISPR/Cas9 suppressor screens, we identify the peroxisome organelle as a critical contributor to ferroptosis sensitivity in human renal and ovarian carcinoma cells. By lipidomic profiling, we show that peroxisomes contribute to ferroptosis through the synthesis of polyunsaturated ether phospholipids (PUFA-ePLs), an understudied lipid class that provides substrates for lipid peroxidation, resulting in turn in induction of ferroptosis. Moreover, carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo , a state associated with extensive PUFA-ePL downregulation. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including normal neurons and cardiomyocytes. Together, our work reveals important roles for the peroxisome–ether phospholipid axis in driving ferroptosis susceptibility and evasion, highlights PUFA-ePL as a distinct functional lipid group that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases involving ferroptosis. Ferroptosis--an iron-dependent, non-apoptotic cell death process--is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers.sup.1. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions.sup.2-5. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. The cellular organelles peroxisomes contribute to the sensitivity of cells to ferroptosis by synthesizing polyunsaturated ether phospholipids, and changes in the abundances of these lipids are associated with altered sensitivity to ferroptosis during cell-state transitions. Ferroptosis-an iron-dependent, non-apoptotic cell death process-is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers1. The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions2-5. However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CR1SPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation ofPUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. Ferroptosis-an iron-dependent, non-apoptotic cell death process-is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers . The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions . However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR-Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome-ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. Ferroptosis—an iron-dependent, non-apoptotic cell death process—is involved in various degenerative diseases and represents a targetable susceptibility in certain cancers 1 . The ferroptosis-susceptible cell state can either pre-exist in cells that arise from certain lineages or be acquired during cell-state transitions 2 – 5 . However, precisely how susceptibility to ferroptosis is dynamically regulated remains poorly understood. Here we use genome-wide CRISPR–Cas9 suppressor screens to identify the oxidative organelles peroxisomes as critical contributors to ferroptosis sensitivity in human renal and ovarian carcinoma cells. Using lipidomic profiling we show that peroxisomes contribute to ferroptosis by synthesizing polyunsaturated ether phospholipids (PUFA-ePLs), which act as substrates for lipid peroxidation that, in turn, results in the induction of ferroptosis. Carcinoma cells that are initially sensitive to ferroptosis can switch to a ferroptosis-resistant state in vivo in mice, which is associated with extensive downregulation of PUFA-ePLs. We further find that the pro-ferroptotic role of PUFA-ePLs can be extended beyond neoplastic cells to other cell types, including neurons and cardiomyocytes. Together, our work reveals roles for the peroxisome–ether-phospholipid axis in driving susceptibility to and evasion from ferroptosis, highlights PUFA-ePL as a distinct functional lipid class that is dynamically regulated during cell-state transitions, and suggests multiple regulatory nodes for therapeutic interventions in diseases that involve ferroptosis. The cellular organelles peroxisomes contribute to the sensitivity of cells to ferroptosis by synthesizing polyunsaturated ether phospholipids, and changes in the abundances of these lipids are associated with altered sensitivity to ferroptosis during cell-state transitions. |
| Audience | Academic |
| Author | Fairman, Joshua Eaton, John K. Reinhardt, Ferenc Clish, Clary B. Boyer, Laurie A. Ricq, Emily L. Graham, Emily T. Dančík, Vlado Hammond, Paula T. Weinberg, Robert A. Wang, Wenyu Henry, Whitney S. Paradkar, Sateja Deik, Amy A. Ferguson, Bryan Phadnis, Vaishnavi V. Boehnke, Natalie Zou, Yilong Maretich, Pema Schreiber, Stuart L. Clemons, Paul A. Keys, Heather R. |
| AuthorAffiliation | 2 Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138, U.S.A 4 Department of Biology, MIT, MA 02142, U.S.A 6 Department of Chemical Engineering, MIT, MA 02142, U.S.A 3 Whitehead Institute for Biomedical Research, MIT, MA 02142, U.S.A 5 Koch Institute for Integrative Cancer Research, MIT, MA 02142, U.S.A 7 Department of Biological Engineering, MIT, MA 02142, U.S.A 1 Broad Institute, Cambridge, MA 02142, U.S.A |
| AuthorAffiliation_xml | – name: 3 Whitehead Institute for Biomedical Research, MIT, MA 02142, U.S.A – name: 7 Department of Biological Engineering, MIT, MA 02142, U.S.A – name: 4 Department of Biology, MIT, MA 02142, U.S.A – name: 1 Broad Institute, Cambridge, MA 02142, U.S.A – name: 6 Department of Chemical Engineering, MIT, MA 02142, U.S.A – name: 2 Department of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138, U.S.A – name: 5 Koch Institute for Integrative Cancer Research, MIT, MA 02142, U.S.A |
| Author_xml | – sequence: 1 givenname: Yilong orcidid: 0000-0001-8198-6067 surname: Zou fullname: Zou, Yilong email: yzou@broadinstitute.org organization: Broad Institute, Department of Chemistry and Chemical Biology, Harvard University – sequence: 2 givenname: Whitney S. surname: Henry fullname: Henry, Whitney S. organization: Whitehead Institute for Biomedical Research – sequence: 3 givenname: Emily L. surname: Ricq fullname: Ricq, Emily L. organization: Broad Institute, Department of Chemistry and Chemical Biology, Harvard University – sequence: 4 givenname: Emily T. orcidid: 0000-0001-6696-4564 surname: Graham fullname: Graham, Emily T. organization: Broad Institute – sequence: 5 givenname: Vaishnavi V. orcidid: 0000-0001-8452-8512 surname: Phadnis fullname: Phadnis, Vaishnavi V. organization: Whitehead Institute for Biomedical Research – sequence: 6 givenname: Pema surname: Maretich fullname: Maretich, Pema organization: Department of Biology, MIT – sequence: 7 givenname: Sateja surname: Paradkar fullname: Paradkar, Sateja organization: Whitehead Institute for Biomedical Research – sequence: 8 givenname: Natalie surname: Boehnke fullname: Boehnke, Natalie organization: Koch Institute for Integrative Cancer Research, MIT – sequence: 9 givenname: Amy A. surname: Deik fullname: Deik, Amy A. organization: Broad Institute – sequence: 10 givenname: Ferenc surname: Reinhardt fullname: Reinhardt, Ferenc organization: Whitehead Institute for Biomedical Research – sequence: 11 givenname: John K. orcidid: 0000-0003-4633-5546 surname: Eaton fullname: Eaton, John K. organization: Broad Institute – sequence: 12 givenname: Bryan surname: Ferguson fullname: Ferguson, Bryan organization: Broad Institute – sequence: 13 givenname: Wenyu surname: Wang fullname: Wang, Wenyu organization: Broad Institute – sequence: 14 givenname: Joshua surname: Fairman fullname: Fairman, Joshua organization: Whitehead Institute for Biomedical Research – sequence: 15 givenname: Heather R. orcidid: 0000-0003-1371-2288 surname: Keys fullname: Keys, Heather R. organization: Whitehead Institute for Biomedical Research – sequence: 16 givenname: Vlado surname: Dančík fullname: Dančík, Vlado organization: Broad Institute – sequence: 17 givenname: Clary B. orcidid: 0000-0001-8259-9245 surname: Clish fullname: Clish, Clary B. organization: Broad Institute – sequence: 18 givenname: Paul A. orcidid: 0000-0002-1800-5112 surname: Clemons fullname: Clemons, Paul A. organization: Broad Institute – sequence: 19 givenname: Paula T. orcidid: 0000-0002-9835-192X surname: Hammond fullname: Hammond, Paula T. organization: Koch Institute for Integrative Cancer Research, MIT, Department of Chemical Engineering, MIT – sequence: 20 givenname: Laurie A. surname: Boyer fullname: Boyer, Laurie A. organization: Department of Biology, MIT, Department of Biological Engineering, MIT – sequence: 21 givenname: Robert A. orcidid: 0000-0002-0895-3557 surname: Weinberg fullname: Weinberg, Robert A. email: weinberg@wi.mit.edu organization: Whitehead Institute for Biomedical Research – sequence: 22 givenname: Stuart L. orcidid: 0000-0003-1922-7558 surname: Schreiber fullname: Schreiber, Stuart L. email: stuart_schreiber@harvard.edu organization: Broad Institute, Department of Chemistry and Chemical Biology, Harvard University |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32939090$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature Limited 2020 COPYRIGHT 2020 Nature Publishing Group Copyright Nature Publishing Group Sep 24, 2020 |
| Copyright_xml | – notice: The Author(s), under exclusive licence to Springer Nature Limited 2020 – notice: COPYRIGHT 2020 Nature Publishing Group – notice: Copyright Nature Publishing Group Sep 24, 2020 |
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| DOI | 10.1038/s41586-020-2732-8 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Y.Z., W.S.H., and E.L.R. conceived the project, performed the experiments and analyzed data. E.T.G., V.V.P., S.P., B.F., J.F., H.K. assisted the experiments and interpreted data. A.A.D. and C.B.C. performed metabolomics profiling. W.W. and J.K.E. performed chemical synthesis. N.B. prepared the plasmalogen nanoparticles with input from P.T.H.. P.M. and L.B. assisted the cardiomyocyte experiments and data interpretation. J.K.E. performed the DPPH assay. F.R. assisted animal experiments. V.D. and P.A.C. developed GeLiNEA and assisted computational analysis. Y.Z., W.S.H., S.L.S. and R.A.W. wrote the manuscript with input from all authors. These authors contributed equally to this work. Author contributions |
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| Snippet | Ferroptosis—an iron-dependent, non-apoptotic cell death process—is involved in various degenerative diseases and represents a targetable susceptibility in... Ferroptosis-an iron-dependent, non-apoptotic cell death process-is involved in various degenerative diseases and represents a targetable susceptibility in... Ferroptosis--an iron-dependent, non-apoptotic cell death process--is involved in various degenerative diseases and represents a targetable susceptibility in... Ferroptosis, an iron-dependent, non-apoptotic cell death program, is involved in various degenerative diseases and represents a targetable vulnerability in... |
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| Title | Plasticity of ether lipids promotes ferroptosis susceptibility and evasion |
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