Role of Mitochondria in Ferroptosis

Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one another, whether mitochondria are involved in ferroptosis is under debate. Here, we demonstrate that mitochondria play a crucial role in cysteine-d...

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Veröffentlicht in:	Molecular cell Jg. 73; H. 2; S. 354
Hauptverfasser:	Gao, Minghui, Yi, Junmei, Zhu, Jiajun, Minikes, Alexander M, Monian, Prashant, Thompson, Craig B, Jiang, Xuejun
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	United States 17.01.2019
Schlagworte:	Animals Cell Line, Tumor Citric Acid Cycle - drug effects Electron Transport Electron Transport Chain Complex Proteins - antagonists & inhibitors Electron Transport Chain Complex Proteins - metabolism Enzyme Inhibitors - pharmacology Fibroblasts - drug effects Fibroblasts - enzymology Fibroblasts - pathology Fumarate Hydratase - genetics Fumarate Hydratase - metabolism Glutamine - metabolism Glutathione Peroxidase - genetics Glutathione Peroxidase - metabolism Humans Iron - metabolism Lipid Peroxidation - drug effects Membrane Potential, Mitochondrial Mice Mitochondria - drug effects Mitochondria - enzymology Mitochondria - genetics Mitochondria - pathology Mutation Necrosis Phospholipid Hydroperoxide Glutathione Peroxidase Reactive Oxygen Species - metabolism Signal Transduction
ISSN:	1097-4164, 1097-4164
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Abstract	Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one another, whether mitochondria are involved in ferroptosis is under debate. Here, we demonstrate that mitochondria play a crucial role in cysteine-deprivation-induced ferroptosis but not in that induced by inhibiting glutathione peroxidase-4 (GPX4), the most downstream component of the ferroptosis pathway. Mechanistically, cysteine deprivation leads to mitochondrial membrane potential hyperpolarization and lipid peroxide accumulation. Inhibition of mitochondrial TCA cycle or electron transfer chain (ETC) mitigated mitochondrial membrane potential hyperpolarization, lipid peroxide accumulation, and ferroptosis. Blockage of glutaminolysis had the same inhibitory effect, which was counteracted by supplying downstream TCA cycle intermediates. Importantly, loss of function of fumarate hydratase, a tumor suppressor and TCA cycle component, confers resistance to cysteine-deprivation-induced ferroptosis. Collectively, this work demonstrates the crucial role of mitochondria in cysteine-deprivation-induced ferroptosis and implicates ferroptosis in tumor suppression.
AbstractList	Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one another, whether mitochondria are involved in ferroptosis is under debate. Here, we demonstrate that mitochondria play a crucial role in cysteine-deprivation-induced ferroptosis but not in that induced by inhibiting glutathione peroxidase-4 (GPX4), the most downstream component of the ferroptosis pathway. Mechanistically, cysteine deprivation leads to mitochondrial membrane potential hyperpolarization and lipid peroxide accumulation. Inhibition of mitochondrial TCA cycle or electron transfer chain (ETC) mitigated mitochondrial membrane potential hyperpolarization, lipid peroxide accumulation, and ferroptosis. Blockage of glutaminolysis had the same inhibitory effect, which was counteracted by supplying downstream TCA cycle intermediates. Importantly, loss of function of fumarate hydratase, a tumor suppressor and TCA cycle component, confers resistance to cysteine-deprivation-induced ferroptosis. Collectively, this work demonstrates the crucial role of mitochondria in cysteine-deprivation-induced ferroptosis and implicates ferroptosis in tumor suppression.Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one another, whether mitochondria are involved in ferroptosis is under debate. Here, we demonstrate that mitochondria play a crucial role in cysteine-deprivation-induced ferroptosis but not in that induced by inhibiting glutathione peroxidase-4 (GPX4), the most downstream component of the ferroptosis pathway. Mechanistically, cysteine deprivation leads to mitochondrial membrane potential hyperpolarization and lipid peroxide accumulation. Inhibition of mitochondrial TCA cycle or electron transfer chain (ETC) mitigated mitochondrial membrane potential hyperpolarization, lipid peroxide accumulation, and ferroptosis. Blockage of glutaminolysis had the same inhibitory effect, which was counteracted by supplying downstream TCA cycle intermediates. Importantly, loss of function of fumarate hydratase, a tumor suppressor and TCA cycle component, confers resistance to cysteine-deprivation-induced ferroptosis. Collectively, this work demonstrates the crucial role of mitochondria in cysteine-deprivation-induced ferroptosis and implicates ferroptosis in tumor suppression. Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one another, whether mitochondria are involved in ferroptosis is under debate. Here, we demonstrate that mitochondria play a crucial role in cysteine-deprivation-induced ferroptosis but not in that induced by inhibiting glutathione peroxidase-4 (GPX4), the most downstream component of the ferroptosis pathway. Mechanistically, cysteine deprivation leads to mitochondrial membrane potential hyperpolarization and lipid peroxide accumulation. Inhibition of mitochondrial TCA cycle or electron transfer chain (ETC) mitigated mitochondrial membrane potential hyperpolarization, lipid peroxide accumulation, and ferroptosis. Blockage of glutaminolysis had the same inhibitory effect, which was counteracted by supplying downstream TCA cycle intermediates. Importantly, loss of function of fumarate hydratase, a tumor suppressor and TCA cycle component, confers resistance to cysteine-deprivation-induced ferroptosis. Collectively, this work demonstrates the crucial role of mitochondria in cysteine-deprivation-induced ferroptosis and implicates ferroptosis in tumor suppression.
Author	Gao, Minghui Zhu, Jiajun Minikes, Alexander M Thompson, Craig B Jiang, Xuejun Yi, Junmei Monian, Prashant
Author_xml	– sequence: 1 givenname: Minghui surname: Gao fullname: Gao, Minghui email: gaominghui@hit.edu.cn organization: The HIT Center for Life Sciences, School of Life Science and Technology, Harbin Institute of Technology, Harbin 150080, China; Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA. Electronic address: gaominghui@hit.edu.cn – sequence: 2 givenname: Junmei surname: Yi fullname: Yi, Junmei organization: Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA – sequence: 3 givenname: Jiajun surname: Zhu fullname: Zhu, Jiajun organization: Department of Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA – sequence: 4 givenname: Alexander M surname: Minikes fullname: Minikes, Alexander M organization: Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA; BCMB Allied Program, Weill Cornell Graduate School of Medical Sciences, New York City, NY 10065, USA – sequence: 5 givenname: Prashant surname: Monian fullname: Monian, Prashant organization: Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA – sequence: 6 givenname: Craig B surname: Thompson fullname: Thompson, Craig B organization: Department of Cancer Biology and Genetics, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA – sequence: 7 givenname: Xuejun surname: Jiang fullname: Jiang, Xuejun email: jiangx@mskcc.org organization: Cell Biology Program, Memorial Sloan Kettering Cancer Center, New York City, NY 10065, USA. Electronic address: jiangx@mskcc.org
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/30581146$$D View this record in MEDLINE/PubMed
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Snippet	Ferroptosis is a regulated necrosis process driven by iron-dependent lipid peroxidation. Although ferroptosis and cellular metabolism interplay with one...
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SubjectTerms	Animals Cell Line, Tumor Citric Acid Cycle - drug effects Electron Transport Electron Transport Chain Complex Proteins - antagonists & inhibitors Electron Transport Chain Complex Proteins - metabolism Enzyme Inhibitors - pharmacology Fibroblasts - drug effects Fibroblasts - enzymology Fibroblasts - pathology Fumarate Hydratase - genetics Fumarate Hydratase - metabolism Glutamine - metabolism Glutathione Peroxidase - genetics Glutathione Peroxidase - metabolism Humans Iron - metabolism Lipid Peroxidation - drug effects Membrane Potential, Mitochondrial Mice Mitochondria - drug effects Mitochondria - enzymology Mitochondria - genetics Mitochondria - pathology Mutation Necrosis Phospholipid Hydroperoxide Glutathione Peroxidase Reactive Oxygen Species - metabolism Signal Transduction
Title	Role of Mitochondria in Ferroptosis
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