Aldehyde dehydrogenase 3a2 protects AML cells from oxidative death and the synthetic lethality of ferroptosis inducers
Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would...
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| Published in | Blood Vol. 136; no. 11; pp. 1303 - 1316 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
10.09.2020
American Society of Hematology |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would define distinctive vulnerabilities in acute myeloid leukemia (AML). Leukemic cells, but not their normal myeloid counterparts, depended on the aldehyde dehydrogenase 3a2 (Aldh3a2) enzyme that oxidizes long-chain aliphatic aldehydes to prevent cellular oxidative damage. Aldehydes are by-products of increased oxidative phosphorylation and nucleotide synthesis in cancer and are generated from lipid peroxides underlying the non–caspase-dependent form of cell death, ferroptosis. Leukemic cell dependence on Aldh3a2 was seen across multiple mouse and human myeloid leukemias. Aldh3a2 inhibition was synthetically lethal with glutathione peroxidase-4 (GPX4) inhibition; GPX4 inhibition is a known trigger of ferroptosis that by itself minimally affects AML cells. Inhibiting Aldh3a2 provides a therapeutic opportunity and a unique synthetic lethality to exploit the distinctive metabolic state of malignant cells.
•In vivo metabolic dependencies of malignant (vs normal counterpart) cells can be defined by ex vivo screening.•Aldh3a2 is synthetically lethal with GPX4 inhibition, providing a combination therapy approach based solely on metabolic state.
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| AbstractList | Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would define distinctive vulnerabilities in acute myeloid leukemia (AML). Leukemic cells, but not their normal myeloid counterparts, depended on the aldehyde dehydrogenase 3a2 (Aldh3a2) enzyme that oxidizes long-chain aliphatic aldehydes to prevent cellular oxidative damage. Aldehydes are by-products of increased oxidative phosphorylation and nucleotide synthesis in cancer and are generated from lipid peroxides underlying the non–caspase-dependent form of cell death, ferroptosis. Leukemic cell dependence on Aldh3a2 was seen across multiple mouse and human myeloid leukemias. Aldh3a2 inhibition was synthetically lethal with glutathione peroxidase-4 (GPX4) inhibition; GPX4 inhibition is a known trigger of ferroptosis that by itself minimally affects AML cells. Inhibiting Aldh3a2 provides a therapeutic opportunity and a unique synthetic lethality to exploit the distinctive metabolic state of malignant cells.
•In vivo metabolic dependencies of malignant (vs normal counterpart) cells can be defined by ex vivo screening.•Aldh3a2 is synthetically lethal with GPX4 inhibition, providing a combination therapy approach based solely on metabolic state.
[Display omitted] Abstract Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would define distinctive vulnerabilities in acute myeloid leukemia (AML). Leukemic cells, but not their normal myeloid counterparts, depended on the aldehyde dehydrogenase 3a2 (Aldh3a2) enzyme that oxidizes long-chain aliphatic aldehydes to prevent cellular oxidative damage. Aldehydes are by-products of increased oxidative phosphorylation and nucleotide synthesis in cancer and are generated from lipid peroxides underlying the non–caspase-dependent form of cell death, ferroptosis. Leukemic cell dependence on Aldh3a2 was seen across multiple mouse and human myeloid leukemias. Aldh3a2 inhibition was synthetically lethal with glutathione peroxidase-4 (GPX4) inhibition; GPX4 inhibition is a known trigger of ferroptosis that by itself minimally affects AML cells. Inhibiting Aldh3a2 provides a therapeutic opportunity and a unique synthetic lethality to exploit the distinctive metabolic state of malignant cells. Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would define distinctive vulnerabilities in acute myeloid leukemia (AML). Leukemic cells, but not their normal myeloid counterparts, depended on the aldehyde dehydrogenase 3a2 (Aldh3a2) enzyme that oxidizes long-chain aliphatic aldehydes to prevent cellular oxidative damage. Aldehydes are by-products of increased oxidative phosphorylation and nucleotide synthesis in cancer and are generated from lipid peroxides underlying the non-caspase-dependent form of cell death, ferroptosis. Leukemic cell dependence on Aldh3a2 was seen across multiple mouse and human myeloid leukemias. Aldh3a2 inhibition was synthetically lethal with glutathione peroxidase-4 (GPX4) inhibition; GPX4 inhibition is a known trigger of ferroptosis that by itself minimally affects AML cells. Inhibiting Aldh3a2 provides a therapeutic opportunity and a unique synthetic lethality to exploit the distinctive metabolic state of malignant cells. There is a Blood Commentary on this article in this issue. In vivo metabolic dependencies of malignant (vs normal counterpart) cells can be defined by ex vivo screening. Aldh3a2 is synthetically lethal with GPX4 inhibition, providing a combination therapy approach based solely on metabolic state. Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing normal primary mouse hematopoietic cells and their malignant counterparts in an ex vivo system mimicking the bone marrow microenvironment, would define distinctive vulnerabilities in acute myeloid leukemia (AML). Leukemic cells, but not their normal myeloid counterparts, depended on the aldehyde dehydrogenase 3a2 (Aldh3a2) enzyme that oxidizes long-chain aliphatic aldehydes to prevent cellular oxidative damage. Aldehydes are by-products of increased oxidative phosphorylation and nucleotide synthesis in cancer and are generated from lipid peroxides underlying the non–caspase-dependent form of cell death, ferroptosis. Leukemic cell dependence on Aldh3a2 was seen across multiple mouse and human myeloid leukemias. Aldh3a2 inhibition was synthetically lethal with glutathione peroxidase-4 (GPX4) inhibition; GPX4 inhibition is a known trigger of ferroptosis that by itself minimally affects AML cells. Inhibiting Aldh3a2 provides a therapeutic opportunity and a unique synthetic lethality to exploit the distinctive metabolic state of malignant cells. |
| Author | Viswanathan, Vasanthi Acharya, Sanket Doench, John Churchill, Michael Logan, David J. S'aulis, Dana Hutchinson, John N. Schreiber, Stuart Sharda, Azeem Lee, Dongjun Yu, Vionnie W.C. Yusuf, Rushdia Zareen Das, Sudeshna Mercier, Francois Bullinger, Lars Scadden, David T. Scadden, Elizabeth W. Chattophadhyay, Shrikanta Cobert, Julien Sykes, David B. Saez, Borja Stephanopoulos, Gregory Baryawno, Ninib Huang, Cherrie Mukherjee, Siddhartha Keibler, Mark A. van Gastel, Nick Rizzo, William B. |
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H. Chan School of Public Health, Boston, MA – sequence: 18 givenname: Michael orcidid: 0000-0001-7202-3891 surname: Churchill fullname: Churchill, Michael organization: Center for Regenerative Medicine, Massachusetts General Hospital, Boston, MA – sequence: 19 givenname: Siddhartha surname: Mukherjee fullname: Mukherjee, Siddhartha organization: Center for Regenerative Medicine, Massachusetts General Hospital, Boston, MA – sequence: 20 givenname: Dongjun orcidid: 0000-0001-6828-401X surname: Lee fullname: Lee, Dongjun organization: Center for Regenerative Medicine, Massachusetts General Hospital, Boston, MA – sequence: 21 givenname: Francois surname: Mercier fullname: Mercier, Francois organization: Center for Regenerative Medicine, Massachusetts General Hospital, Boston, MA – sequence: 22 givenname: John surname: Doench fullname: Doench, John organization: Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA – sequence: 23 givenname: Lars surname: Bullinger fullname: Bullinger, Lars organization: Department of Hematology, Oncology and Tumor Immunology, Charité University Medicine, Berlin, Germany – sequence: 24 givenname: David J. surname: Logan fullname: Logan, David J. organization: Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA – sequence: 25 givenname: Stuart surname: Schreiber fullname: Schreiber, Stuart organization: Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, MA – sequence: 26 givenname: Gregory surname: Stephanopoulos fullname: Stephanopoulos, Gregory organization: Department of Chemical Engineering, MIT, Cambridge, MA – sequence: 27 givenname: William B. surname: Rizzo fullname: Rizzo, William B. organization: Department of Pediatrics, University of Nebraska Medical Center, Omaha, NE – sequence: 28 givenname: David T. surname: Scadden fullname: Scadden, David T. organization: Center for Regenerative Medicine, Massachusetts General Hospital, Boston, MA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32458004$$D View this record in MEDLINE/PubMed |
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| Copyright | 2020 American Society of Hematology 2020 by The American Society of Hematology. 2020 by The American Society of Hematology 2020 |
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| Notes | R.Z.Y., B.S., and A.S. contributed equally to this work. |
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| Snippet | Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen, comparing... Abstract Metabolic alterations in cancer represent convergent effects of oncogenic mutations. We hypothesized that a metabolism-restricted genetic screen,... There is a Blood Commentary on this article in this issue. In vivo metabolic dependencies of malignant (vs normal counterpart) cells can be defined by ex vivo... |
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| SubjectTerms | Aldehyde Oxidoreductases - genetics Aldehyde Oxidoreductases - physiology Aldehydes - pharmacology Animals Carbolines - pharmacology Cell Line, Tumor Cyclohexylamines - pharmacology Cytarabine - administration & dosage Doxorubicin - administration & dosage Ferroptosis - drug effects Hematopoiesis - physiology Humans Leukemia, Myeloid, Acute - drug therapy Leukemia, Myeloid, Acute - enzymology Leukemia, Myeloid, Acute - pathology Lipid Peroxidation Mice Mice, Inbred C57BL Mice, Knockout Myeloid Neoplasia Myeloid-Lymphoid Leukemia Protein - physiology Neoplasm Proteins - deficiency Neoplasm Proteins - genetics Neoplasm Proteins - physiology Oleic Acid - pharmacology Oncogene Proteins, Fusion - physiology Oxidation-Reduction Oxidative Stress Phenylenediamines - pharmacology Phospholipid Hydroperoxide Glutathione Peroxidase - antagonists & inhibitors Phospholipid Hydroperoxide Glutathione Peroxidase - physiology |
| Title | Aldehyde dehydrogenase 3a2 protects AML cells from oxidative death and the synthetic lethality of ferroptosis inducers |
| URI | https://dx.doi.org/10.1182/blood.2019001808 https://www.ncbi.nlm.nih.gov/pubmed/32458004 https://pubmed.ncbi.nlm.nih.gov/PMC7483435 |
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