Venetoclax with azacitidine disrupts energy metabolism and targets leukemia stem cells in patients with acute myeloid leukemia
Open accessAbstract
Acute myeloid leukemia (AML) is the most common acute leukemia in adults. Leukemia stem cells (LSCs) drive the initiation and perpetuation of AML, are quantifiably associated with worse clinical outcomes, and often persist after conventional chemotherapy resulting in relapse 1-5. In this report, we show that treatment of older patients with AML with the B cell lymphoma 2 (BCL-2) inhibitor venetoclax in combination with azacitidine results in deep and durable remissions and is superior to conventional treatments. We hypothesized that these promising clinical results were due to targeting LSCs. Analysis of LSCs from patients undergoing treatment with venetoclax + azacitidine showed disruption of the tricarboxylic acid (TCA) cycle manifested by decreased α-ketoglutarate and increased succinate levels, suggesting inhibition of electron transport chain complex II. In vitro modeling confirmed inhibition of complex II via reduced glutathionylation of succinate dehydrogenase. These metabolic perturbations suppress oxidative phosphorylation (OXPHOS), which efficiently and selectively targets LSCs. Our findings show for the first time that a therapeutic intervention can eradicate LSCs in patients with AML by disrupting the metabolic machinery driving energy metabolism, resulting in promising clinical activity in a patient population with historically poor outcomes.
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The combination of venetoclax and azacitidine targets mitochondrial metabolism through inhibition of glutathionylation of complex II of the electron transport chain and diminishes uptake of global amino acids in primary patient AML stem cells.
“the combination of venetoclax (inhibitor of the anti-apoptopic protein BCL-2) and azacitidine has been shown to target mitochondrial metabolism through inhibition of the glutathionylation of complex II of the electron transport chain (45) and diminishes the uptake of global amino acids in primary patient AML stem cells (46).”
From Eprenetapopt triggers ferroptosis, inhibits NFS1 cysteine desulfurase, and synergizes with serine and glycine dietary restriction (2022) · cites this paper as [45]
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“…of the anti-apoptopic protein BCL-2) and azacitidine has been shown to target mitochondrial metabolism through inhibition of the gluta-thionylation of complex II of the electron transport chain ( 45 ) and diminishes the uptake of global amino acids in primary patient AML stem cells ( 46 ).”
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- Authors
- Pollyea, D. A., Stevens, B. M., Jones, C. L., Winters, A., Pei, S., Minhajuddin, M., D’Alessandro, A., Culp-Hill, R., Riemondy, K. A., Gillen, A. E., Hesselberth, J. R., Abbott, D., Schatz, D., Gutman, J. A., Purev, E., Smith, C., & Jordan, C. T.
- Affiliations
- University of Colorado Anschutz (US)
- Corresponding author
- Jordan, Craig T.
- ORCID
- Venue
- Nature Medicine
- Published
- 2018-11-12
- Volume
- 24
- Issue
- 12
- Pages
- 1859-1866
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC7001730
- OpenAlex
- W2899472109
- Cited by
- 778
- References
- 43
- Citations by year
- 2026: 62 · 2025: 87 · 2024: 129 · 2023: 103 · 2022: 98 · 2021: 120 · 2020: 105 · 2019: 69 · 2018: 4 · 2014: 1
- FWCI
- 53.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA200707)
- National Institute of General Medical Sciences (R35GM119550)
- Topics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Health Sciences › Medicine › Hematology › Chronic Myeloid Leukemia Treatments
- Health Sciences › Medicine › Pharmacology › Flavonoids in Medical Research
- Keywords
- acute myeloid leukemia, venetoclax, azacitidine, leukemia stem cells, energy metabolism, TCA cycle, succinic acid, succinate dehydrogenase, glutathionylation, oxidative phosphorylation, mitochondrial metabolism, BCL-2 inhibition, elderly patients, remission
- MeSH terms
- Aged, Aged, 80 and over, Azacitidine, Energy Metabolism, Female, Humans, Ketoglutaric Acids, Male, Oxidative Phosphorylation, Succinate Dehydrogenase, Sulfonamides, Tricarboxylic Acids, Neoplastic Stem Cells, Leukemia, Myeloid, Acute, Apoptosis, Bridged Bicyclo Compounds, Heterocyclic, Proto-Oncogene Proteins c-bcl-2, Electron Transport Complex II
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