The DOI matches its Crossref record; 138 of the 140 references it cites were found in a registry or an index.
The Warburg and Crabtree effects: On the origin of cancer cell energy metabolism and of yeast glucose repression
Open accessAbstract
During the last decades a considerable amount of research has been focused on cancer. Recently, tumor cell metabolism has been considered as a possible target for cancer therapy. It is widely accepted that tumors display enhanced glycolytic activity and impaired oxidative phosphorylation (Warburg effect). Therefore, it seems reasonable that disruption of glycolysis might be a promising candidate for specific anti-cancer therapy. Nevertheless, the concept of aerobic glycolysis as the paradigm of tumor cell metabolism has been challenged, as some tumor cells exhibit high rates of oxidative phosphorylation. Mitochondrial physiology in cancer cells is linked to the Warburg effect. Besides, its central role in apoptosis makes this organelle a promising "dual hit target" to selectively eliminate tumor cells. From a metabolic point of view, the fermenting yeast Saccharomyces cerevisiae and tumor cells share several features. In this paper we will review these common metabolic properties as well as the possible origins of the Crabtree and Warburg effects.
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“Otto Warburg observed that cancer cells rewire glucose metabolism for lactate synthesis even in normoxia, known as the Warburg Effect.14,21”
From The multifaceted contributions of mitochondria to cellular metabolism (2018) · cites this paper as [21]
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Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425
Why Do Cancers Have High Aerobic Glycolysis?
Gatenby, R. A., & Gillies, R. J. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1478 · Cited by 4,784
Cancer genes and the pathways they control
Vogelstein, B., & Kinzler, K. W. (2004) · Nature Medicine · doi:10.1038/nm1087 · Cited by 4,346
Kim, J.-W., Tchernyshyov, I., Semenza, G. L., & Dang, C. V. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.02.002 · Cited by 3,905
DeBerardinis, R. J., Mancuso, A., Daikhin, E., Nissim, I., Yudkoff, M., Wehrli, S., & Thompson, C. B. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709747104 · Cited by 2,622
HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption
Papandreou, I., Cairns, R. A., Fontana, L., Lim, A. L., & Denko, N. C. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.01.012 · Cited by 2,267
Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice
Sonveaux, P., Végran, F., Schroeder, T., Wergin, M., Verrax, J., Rabbani, Z. N., Saedeleer, C. J. D., Kennedy, K. M., Diepart, C., Jordan, B. F., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36843 · Cited by 1,635
Fantin, V. R., St-Pierre, J., & Leder, P. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.04.023 · Cited by 1,635
Glycolysis inhibition for anticancer treatment
Pelicano, H., Martin, D. S., Xu, R., & Huang, P. (2006) · Oncogene · doi:10.1038/sj.onc.1209597 · Cited by 1,546
Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression
Le, A., Cooper, C. R., Gouw, A. M., Dinavahi, R., Maitra, A., Deck, L. M., Royer, R. E., Jagt, D. L. V., Semenza, G. L., & Dang, C. V. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0914433107 · Cited by 1,528
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The multifaceted contributions of mitochondria to cellular metabolism
Spinelli, J. B., & Haigis, M. C. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0124-1 · Cited by 1,935
How the Warburg effect supports aggressiveness and drug resistance of cancer cells?
Icard, P., Shulman, S. D., Farhat, D., Steyaert, J., Alifano, M., & Lincet, H. (2018) · Drug Resistance Updates · doi:10.1016/j.drup.2018.03.001 · Cited by 664
Increased demand for NAD(+) relative to ATP drives aerobic glycolysis
Luengo, A., Li, Z., Gui, D. Y., Sullivan, L. B., Zagorulya, M., Do, B. T., Ferreira, R., Naamati, A., Ali, A., Lewis, C. A., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.012 · Cited by 547
Cancer as a metabolic disease: implications for novel therapeutics
Seyfried, T. N., Flores, R. E., Poff, A. M., & D’Agostino, D. P. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt480 · Cited by 497
Energy metabolism in health and diseases
Liu, H., Wang, S., Wang, J., Guo, X., Song, Y., Fu, K., Gao, Z., Liu, D., He, W., & Yang, L. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02141-x · Cited by 484
Metadata
- Authors
- Diaz-Ruiz, R., Rigoulet, M., & Devin, A.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Devin, Anne
- ORCID
- Devin, Anne
- Venue
- Biochimica et Biophysica Acta (BBA) - Bioenergetics
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 1807
- Issue
- 6
- Pages
- 568-576
- ISSN
- 0005-2728 (ISSN-L)
- OpenAlex
- W2091739490
- Cited by
- 486
- References
- 140
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 15 · 2023: 29 · 2022: 31 · 2021: 38 · 2020: 36 · 2019: 44 · 2018: 45 · 2017: 54 · 2016: 37 · 2015: 37 · 2014: 31 · 2013: 28 · 2012: 18
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biochimica et Biophysica Acta (BBA) - Bioenergetics (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- 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
- Warburg effect, Crabtree effect, cancer cell energy metabolism, aerobic glycolysis, oxidative phosphorylation, mitochondrial physiology, glucose repression, Saccharomyces cerevisiae, cancer metabolism, cancer therapy, apoptosis
- MeSH terms
- Animals, Cells, Energy Metabolism, Biological Evolution, Glucose, Humans, Models, Biological, Models, Theoretical, Neoplasms, Yeasts, Down-Regulation, Gene Expression Regulation, Fungal
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