Slow TCA flux and ATP production in primary solid tumours but not metastases
Open accessAbstract
Tissues derive ATP from two pathways-glycolysis and the tricarboxylic acid (TCA) cycle coupled to the electron transport chain. Most energy in mammals is produced via TCA metabolism 1. In tumours, however, the absolute rates of these pathways remain unclear. Here we optimize tracer infusion approaches to measure the rates of glycolysis and the TCA cycle in healthy mouse tissues, Kras-mutant solid tumours, metastases and leukaemia. Then, given the rates of these two pathways, we calculate total ATP synthesis rates. We find that TCA cycle flux is suppressed in all five primary solid tumour models examined and is increased in lung metastases of breast cancer relative to primary orthotopic tumours. As expected, glycolysis flux is increased in tumours compared with healthy tissues (the Warburg effect 2,3), but this increase is insufficient to compensate for low TCA flux in terms of ATP production. Thus, instead of being hypermetabolic, as commonly assumed, solid tumours generally produce ATP at a slower than normal rate. In mouse pancreatic cancer, this is accommodated by the downregulation of protein synthesis, one of this tissue's major energy costs. We propose that, as solid tumours develop, cancer cells shed energetically expensive tissue-specific functions, enabling uncontrolled growth despite a limited ability to produce ATP.
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Bulk fermentative and respiratory rates in primary tumors are lower than previously postulated.
“Intriguingly, a recent study determined that “bulk” fermentative and respiratory rates in primary tumors are lower than previously postulated,4”
From Dynamic IL-6R/STAT3 signaling leads to heterogeneity of metabolic phenotype in pancreatic ductal adenocarcinoma cells (2024) · cites this paper as [4]
The Abstract and Discussion report suppressed TCA flux in primary solid tumour models and lower overall ATP production than the commonly assumed hypermetabolic state. But ‘Tumours make energy slowly’ reports glycolytic flux similar to or higher than that of corresponding healthy tissues; the paper does not establish that fermentative rates are lower than previously postulated. The findings concern the primary tumour models studied, not primary tumours generally. (LLM, conf=0.85)
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Cold and hot tumors: from molecular mechanisms to targeted therapy
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The pentose phosphate pathway in health and disease
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Self-citationTargeting ROS in cancer: rationale and strategies
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Lactate and lactylation in cancer
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Self-citationCD8+ T cells in the cancer-immunity cycle
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Cellular ATP demand creates metabolically distinct subpopulations of mitochondria
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Emerging therapies in cancer metabolism
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Lactate activates the mitochondrial electron transport chain independently of its metabolism
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The Warburg effect: a signature of mitochondrial overload
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Advances in the structure, mechanism and targeting of chemoresistance-linked ABC transporters
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The pleiotropic functions of reactive oxygen species in cancer
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Metabolic heterogeneity in cancer
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Metabolic reprogramming, sensing, and cancer therapy
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Mitochondrial complex I promotes kidney cancer metastasis
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Nanoparticles Synergize Ferroptosis and Cuproptosis to Potentiate Cancer Immunotherapy
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Mitochondrial ATP generation is more proteome efficient than glycolysis
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Self-citationAlberghina, L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115787 · Cited by 120 · see citing works
How protons pave the way to aggressive cancers
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Electron transport chain inhibition increases cellular dependence on purine transport and salvage
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The Multifaceted Roles of NRF2 in Cancer: Friend or Foe?
Glorieux, C., Enriquez-Lara, C., González, C. D., Aguirre-Martínez, G. V., & Calderón, P. B. (2024) · Antioxidants · doi:10.3390/antiox13010070 · Cited by 91 · see citing works
The roles of KRAS in cancer metabolism, tumor microenvironment and clinical therapy
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Lactate homeostasis is maintained through regulation of glycolysis and lipolysis
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Self-citationCell-intrinsic and microenvironmental determinants of metastatic colonization
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Metabolic pathway analysis using stable isotopes in patients with cancer
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Self-citationOXPHOS-targeting drugs in oncology: new perspectives
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Metabolic adaptations in prostate cancer
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Clinical research framework proposal for ketogenic metabolic therapy in glioblastoma
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The Warburg effect on radioresistance: Survival beyond growth
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Targeting metabolism to enhance immunotherapy within tumor microenvironment
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Oncometabolites at the crossroads of genetic, epigenetic and ecological alterations in cancer
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Understanding the Warburg Effect in CancerPreprint
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Mitochondria sense bacterial lactate and drive release of neutrophil extracellular traps
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The immunometabolic ecosystem in cancer
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Emerging diversity in extracellular vesicles and their roles in cancer
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Cancer tissue of origin constrains the growth and metabolism of metastases
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The role of glycolysis in tumorigenesis: From biological aspects to therapeutic opportunities
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Spatial metabolic gradients in the liver and small intestine
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Pathogenic mitochondrial DNA mutations inhibit melanoma metastasis
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The Warburg effect: The hacked mitochondrial-nuclear communication in cancer
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Metabolic remodeling in cancer and senescence and its therapeutic implications
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A prismatic view of the epigenetic-metabolic regulatory axis in breast cancer therapy resistance
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Environmental impacts of polymeric flame retardant breakdown
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Mitochondria and CancerPreprint
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Recent advances in fluorescent probes for ATP imaging
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The Ubiquitin–Proteasome System in Tumor Metabolism
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Self-citationTargeting the dynamics of cancer metabolism in the era of precision oncology
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How Bacterial Pathogens Coordinate Appetite with Virulence
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Impact of acute stress on murine metabolomics and metabolic flux
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Self-citationInhibitors of NAD+ Production in Cancer Treatment: State of the Art and Perspectives
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Self-citationMethods to Evaluate Changes in Mitochondrial Structure and Function in Cancer
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Oxidative and Glycolytic Metabolism: Their Reciprocal Regulation and Dysregulation in Cancer
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Detection, mechanisms, and therapeutic implications of oncometabolites
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Cancer-Associated Cachexia: Bridging Clinical Findings with Mechanistic Insights in Human Studies
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Nanoparticles for inducing Gaucher disease-like damage in cancer cells
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Self-citationBeyond glucose and Warburg: finding the sweet spot in cancer metabolism models
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Metabolic adaptations in cancer progression
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Metabolic mechanisms of immunotherapy resistance
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Recent trends in anti-cancer activities of terrestrial plants-based polysaccharides: A review
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Next Generation of Mass Spectrometry Imaging: from Micrometer to Subcellular Resolution
Xing, L., Zhao, C.-L., Mou, H.-Z., Pan, J., Kang, B., Chen, H., & Xu, J. (2023) · Chemical & Biomedical Imaging · doi:10.1021/cbmi.3c00061 · Cited by 21 · see citing works
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Regulation of mitochondrial metabolism by autophagy supports leptin-induced cell migration
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Self-citationAged mice exhibit widespread metabolic changes but preserved major fluxes
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Mito-Nanozyme: Mitochondria-Targeted Nanozyme for Cancer Therapy
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Spatial isotope deep tracing deciphers inter-tissue metabolic crosstalk
Li, X., Zhu, Y., Li, T., Tu, X., Zhu, S., Wang, L., Li, F., Sun, C., Li, X., Zhao, H., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-63243-2 · Cited by 18 · see citing works
Self-citationThe energy resistance principle
Picard, M. A., & Murugan, N. J. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.09.002 · Cited by 17 · see citing works
Cypate-sensitized upconversion nanoprobes for intracellular and in-vivo ATP ratiometric detection
Zhou, W., Gong, J., Lu, S., Li, Z., Long, Y., Li, X., Li, R., Shang, X., Liu, Y., Tu, D., et al. (2024) · Chemical Engineering Journal · doi:10.1016/j.cej.2024.152332 · Cited by 18 · see citing works
Cheng, G., Karoui, H., Hardy, M., & Kalyanaraman, B. (2023) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2023.06.009 · Cited by 17 · see citing works
Li, D., Wen, G., Wang, H., Ren, Q., Wang, D., Dao, A., Huang, H., & Zhang, P. (2025) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.4c02836 · Cited by 17 · see citing works
- Authors
- Bartman, C. R., Weilandt, D. R., Shen, Y., Lee, W. D., Han, Y., TeSlaa, T., Jankowski, C. S. R., Samarah, L., Park, N. R., da Silva-Diz, V., Aleksandrova, M., Gultekin, Y., Marishta, A., Wang, L., Yang, L., Roichman, A., Bhatt, V., Lan, T., Hu, Z., Xing, X., Lu, W., Davidson, S., Wühr, M., Vander Heiden, M. G., Herranz, D., Guo, J. Y., Kang, Y., & Rabinowitz, J. D.
- Affiliations
- Princeton University (US)
- University of California, Los Angeles (US)
- Rutgers, The State University of New Jersey (US)
- Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
- Corresponding author
- Rabinowitz, Joshua D.
- ORCID
- Bartman, Caroline R.
- Weilandt, Daniel R.
- Shen, Yihui
- Lee, Won Dong
- Han, Yujiao
- TeSlaa, Tara
- Jankowski, Connor S. R.
- Samarah, Laith
- Park, Noel R.
- Aleksandrova, Maya
- Wang, Lin
- Yang, Lifeng
- Roichman, Asael
- Bhatt, Vrushank
- Lan, Taijin
- Hu, Zhixian
- Xing, Xi
- Lu, Wenyun
- Davidson, Shawn
- Wühr, Martin
- Vander Heiden, Matthew G.
- Herranz, Daniel
- Guo, Jessie Yanxiang
- Kang, Yibin
- Rabinowitz, Joshua D.
- Venue
- Nature
- Published
- 2023-02-01
- Volume
- 614
- Issue
- 7947
- Pages
- 349-357
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC10288502
- OpenAlex
- W4318771331
- Cited by
- 299
- References
- 83
- Citations by year
- 2026: 49 · 2025: 93 · 2024: 97 · 2023: 60
- FWCI
- 38.49
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Damon Runyon Cancer Research Foundation
- Leukemia and Lymphoma Society (1386-23)
- Ludwig Institute for Cancer Research
- National Institutes of Health
- Stand Up To Cancer (SU2C-AACR-DT-20-16, T32GM007388)
- National Cancer Institute (R01CA236936, K99CA273517, P30CA072720, R01CA237347, R50CA211437, R35CA242379, R01CA163591)
- National Institute of General Medical Sciences (T32GM007388, R35GM128813)
- National Institute of Diabetes and Digestive and Kidney Diseases (F32DK127843, DP1DK113643)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cancer and biochemical research
- Keywords
- TCA cycle, glycolysis, ATP production, cancer metabolism, Warburg effect, lung metastasis, breast cancer, pancreatic cancer, leukemia, tracer infusion, energy metabolism, protein synthesis
- MeSH terms
- Adenosine Triphosphate, Animals, Breast Neoplasms, Citric Acid Cycle, Deceleration, Energy Metabolism, Glycolysis, Lung Neoplasms, Neoplasm Metastasis, Organ Specificity, Pancreatic Neoplasms, Protein Biosynthesis, Proto-Oncogene Proteins p21(ras), Mice
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