Copper induces cell death by targeting lipoylated TCA cycle proteins
Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cel...
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| Published in | Science (American Association for the Advancement of Science) Vol. 375; no. 6586; pp. 1254 - 1261 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The American Association for the Advancement of Science
18.03.2022
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0036-8075 1095-9203 1095-9203 |
| DOI | 10.1126/science.abf0529 |
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| Abstract | Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms and is dependent on mitochondrial respiration. We show that copper-dependent death occurs by means of direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss, which leads to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms.
Cell death is an essential, finely tuned process that is critical for the removal of damaged and superfluous cells. Multiple forms of programmed and nonprogrammed cell death have been identified, including apoptosis, ferroptosis, and necroptosis. Tsvetkov
et al
. investigated whether abnormal copper ion elevations may sensitize cells toward a previously unidentified death pathway (see the Perspective by Kahlson and Dixon). By performing CRISPR/Cas9 screens, several genes were identified that could protect against copper-induced cell killing. Using genetically modified cells and a mouse model of a copper overload disorder, the researchers report that excess copper promotes the aggregation of lipoylated proteins and links mitochondrial metabolism to copper-dependent death. —PNK
Lipoylation determines sensitivity to copper-induced cell death. |
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| AbstractList | Copper is an essential co-factor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms, and is dependent on mitochondrial respiration. We show that copper-dependent death occurs via direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss leading to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms.
Copper-induced cell death is regulated by mitochondrial ferredoxin 1-mediated protein lipoylation. Copper induces cell deathCell death is an essential, finely tuned process that is critical for the removal of damaged and superfluous cells. Multiple forms of programmed and nonprogrammed cell death have been identified, including apoptosis, ferroptosis, and necroptosis. Tsvetkov et al. investigated whether abnormal copper ion elevations may sensitize cells toward a previously unidentified death pathway (see the Perspective by Kahlson and Dixon). By performing CRISPR/Cas9 screens, several genes were identified that could protect against copper-induced cell killing. Using genetically modified cells and a mouse model of a copper overload disorder, the researchers report that excess copper promotes the aggregation of lipoylated proteins and links mitochondrial metabolism to copper-dependent death. —PNK Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms and is dependent on mitochondrial respiration. We show that copper-dependent death occurs by means of direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss, which leads to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms. Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms and is dependent on mitochondrial respiration. We show that copper-dependent death occurs by means of direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss, which leads to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms. Cell death is an essential, finely tuned process that is critical for the removal of damaged and superfluous cells. Multiple forms of programmed and nonprogrammed cell death have been identified, including apoptosis, ferroptosis, and necroptosis. Tsvetkov et al . investigated whether abnormal copper ion elevations may sensitize cells toward a previously unidentified death pathway (see the Perspective by Kahlson and Dixon). By performing CRISPR/Cas9 screens, several genes were identified that could protect against copper-induced cell killing. Using genetically modified cells and a mouse model of a copper overload disorder, the researchers report that excess copper promotes the aggregation of lipoylated proteins and links mitochondrial metabolism to copper-dependent death. —PNK Lipoylation determines sensitivity to copper-induced cell death. Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms and is dependent on mitochondrial respiration. We show that copper-dependent death occurs by means of direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss, which leads to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms.Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved homeostatic mechanisms. How excess copper induces cell death, however, is unknown. Here, we show in human cells that copper-dependent, regulated cell death is distinct from known death mechanisms and is dependent on mitochondrial respiration. We show that copper-dependent death occurs by means of direct binding of copper to lipoylated components of the tricarboxylic acid (TCA) cycle. This results in lipoylated protein aggregation and subsequent iron-sulfur cluster protein loss, which leads to proteotoxic stress and ultimately cell death. These findings may explain the need for ancient copper homeostatic mechanisms. |
| Author | Corsello, Steven M. Eaton, John K. Coy, Shannon Tsvetkov, Peter Rossen, Jordan Kocak, Mustafa Dreishpoon, Margaret Golub, Todd R. Kanarek, Naama Santagata, Sandro Lutsenko, Svetlana Humeidi, Ranad Spangler, Ryan D. Verma, Ana Petrova, Boryana Joesch-Cohen, Lena Abdusamad, Mai Frenkel, Evgeni |
| AuthorAffiliation | 7 Whitehead Institute and Massachusetts Institute of Technology, Cambridge, USA 9 Department of Physiology, Johns Hopkins Medical Institutes, Baltimore, MD, USA 12 Division of Pediatric Hematology/Oncology, Boston Children’s Hospital, Boston, MA, USA 5 Harvard Medical School, Boston, MA, USA 3 Ludwig Center at Harvard, Harvard Medical School, Boston, USA 4 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA 10 Department of Pathology, Dana Farber Cancer Institute, Boston, MA, USA 11 Department of Pediatric Oncology, Dana Farber Cancer Institute, Boston, MA, USA 1 Broad Institute of Harvard and MIT, Cambridge, USA 2 Laboratory of Systems Pharmacology, Department of Systems Biology, Boston, USA 8 Department of Medical Oncology, Dana Farber Cancer Institute, Boston, MA, USA 6 Department of Pathology, Boston Children’s Hospital, Boston, MA USA |
| AuthorAffiliation_xml | – name: 5 Harvard Medical School, Boston, MA, USA – name: 4 Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA – name: 10 Department of Pathology, Dana Farber Cancer Institute, Boston, MA, USA – name: 3 Ludwig Center at Harvard, Harvard Medical School, Boston, USA – name: 7 Whitehead Institute and Massachusetts Institute of Technology, Cambridge, USA – name: 8 Department of Medical Oncology, Dana Farber Cancer Institute, Boston, MA, USA – name: 2 Laboratory of Systems Pharmacology, Department of Systems Biology, Boston, USA – name: 9 Department of Physiology, Johns Hopkins Medical Institutes, Baltimore, MD, USA – name: 12 Division of Pediatric Hematology/Oncology, Boston Children’s Hospital, Boston, MA, USA – name: 1 Broad Institute of Harvard and MIT, Cambridge, USA – name: 6 Department of Pathology, Boston Children’s Hospital, Boston, MA USA – name: 11 Department of Pediatric Oncology, Dana Farber Cancer Institute, Boston, MA, USA |
| Author_xml | – sequence: 1 givenname: Peter orcidid: 0000-0002-7577-2342 surname: Tsvetkov fullname: Tsvetkov, Peter organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 2 givenname: Shannon orcidid: 0000-0003-0033-9031 surname: Coy fullname: Coy, Shannon organization: Laboratory of Systems Pharmacology, Department of Systems Biology, Boston, MA, USA., Ludwig Center at Harvard, Harvard Medical School, Boston, MA, USA., Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA., Harvard Medical School, Boston, MA, USA – sequence: 3 givenname: Boryana orcidid: 0000-0001-9996-9353 surname: Petrova fullname: Petrova, Boryana organization: Harvard Medical School, Boston, MA, USA., Department of Pathology, Boston Children’s Hospital, Boston, MA USA – sequence: 4 givenname: Margaret orcidid: 0000-0002-4432-6673 surname: Dreishpoon fullname: Dreishpoon, Margaret organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 5 givenname: Ana orcidid: 0000-0001-9057-171X surname: Verma fullname: Verma, Ana organization: Laboratory of Systems Pharmacology, Department of Systems Biology, Boston, MA, USA., Ludwig Center at Harvard, Harvard Medical School, Boston, MA, USA., Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA., Harvard Medical School, Boston, MA, USA – sequence: 6 givenname: Mai surname: Abdusamad fullname: Abdusamad, Mai organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 7 givenname: Jordan orcidid: 0000-0002-1661-6358 surname: Rossen fullname: Rossen, Jordan organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 8 givenname: Lena orcidid: 0000-0002-9129-6809 surname: Joesch-Cohen fullname: Joesch-Cohen, Lena organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 9 givenname: Ranad surname: Humeidi fullname: Humeidi, Ranad organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 10 givenname: Ryan D. surname: Spangler fullname: Spangler, Ryan D. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 11 givenname: John K. orcidid: 0000-0003-4633-5546 surname: Eaton fullname: Eaton, John K. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 12 givenname: Evgeni surname: Frenkel fullname: Frenkel, Evgeni organization: Whitehead Institute and Massachusetts Institute of Technology, Cambridge, MA, USA – sequence: 13 givenname: Mustafa surname: Kocak fullname: Kocak, Mustafa organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA – sequence: 14 givenname: Steven M. orcidid: 0000-0002-9929-3709 surname: Corsello fullname: Corsello, Steven M. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA., Harvard Medical School, Boston, MA, USA., Department of Medical Oncology, Dana Farber Cancer Institute, Boston, MA, USA – sequence: 15 givenname: Svetlana orcidid: 0000-0001-5275-2587 surname: Lutsenko fullname: Lutsenko, Svetlana organization: Department of Physiology, Johns Hopkins Medical Institutes, Baltimore, MD, USA – sequence: 16 givenname: Naama orcidid: 0000-0002-2068-3908 surname: Kanarek fullname: Kanarek, Naama organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA., Harvard Medical School, Boston, MA, USA., Department of Pathology, Boston Children’s Hospital, Boston, MA USA – sequence: 17 givenname: Sandro orcidid: 0000-0002-7528-9668 surname: Santagata fullname: Santagata, Sandro organization: Laboratory of Systems Pharmacology, Department of Systems Biology, Boston, MA, USA., Ludwig Center at Harvard, Harvard Medical School, Boston, MA, USA., Department of Pathology, Brigham and Women’s Hospital, Boston, MA, USA., Harvard Medical School, Boston, MA, USA., Department of Pathology, Dana Farber Cancer Institute, Boston, MA, USA – sequence: 18 givenname: Todd R. orcidid: 0000-0003-0113-2403 surname: Golub fullname: Golub, Todd R. organization: Broad Institute of Harvard and MIT, Cambridge, MA, USA., Harvard Medical School, Boston, MA, USA., Department of Pediatric Oncology, Dana Farber Cancer Institute, Boston, MA, USA., Division of Pediatric Hematology/Oncology, Boston Children’s Hospital, Boston, MA, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35298263$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Authors contributions: P.T. conceptualized the project, conducted experiments, collected data and analyzed results. M.A. and M.D. assisted with experiments. L.J.C., J.R. and M.K. assisted with data analysis. R.H. and R.S. supervised by S.M.C. performed the whole genome CRISPR/Cas9 screens. S.C. and S.S. performed the TMA staining scoring and visualization and the microscopy assisted by A.V. B.P. and N.K. performed and analyzed the metabolomics experiments. S.L provided study material and experimental advice. J.E. and E.F. provided reagents and experimental advice. T.R.G. supervised the research. P.T. and T.R.G. wrote the manuscript. |
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| Snippet | Copper is an essential cofactor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved... Copper induces cell deathCell death is an essential, finely tuned process that is critical for the removal of damaged and superfluous cells. Multiple forms of... Copper is an essential co-factor for all organisms, and yet it becomes toxic if concentrations exceed a threshold maintained by evolutionarily conserved... |
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| SubjectTerms | Animals Apoptosis Cell death Cell Respiration Citric Acid Cycle Copper Copper - metabolism Copper - toxicity CRISPR Death Dihydrolipoyllysine-Residue Acetyltransferase - metabolism Ferroptosis Genetic modification Hepatolenticular Degeneration - metabolism Homeostasis Humans Hydrazines - toxicity Ionophores - toxicity Iron-Sulfur Proteins - metabolism Lipoylation Metabolic Networks and Pathways Mice Mitochondria Mitochondria - metabolism Mortality Necroptosis Proteins Regulated Cell Death Tricarboxylic acid cycle |
| Title | Copper induces cell death by targeting lipoylated TCA cycle proteins |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/35298263 https://www.proquest.com/docview/2640438165 https://www.proquest.com/docview/2641000917 https://pubmed.ncbi.nlm.nih.gov/PMC9273333 |
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