Mechanisms and Implications of Metabolic Heterogeneity in Cancer
Open accessAbstract
Tumors display reprogrammed metabolic activities that promote cancer progression. We currently possess a limited understanding of the processes governing tumor metabolism in vivo and of the most efficient approaches to identify metabolic vulnerabilities susceptible to therapeutic targeting. While much of the literature focuses on stereotyped, cell-autonomous pathways like glycolysis, recent work emphasizes heterogeneity and flexibility of metabolism between tumors and even within distinct regions of solid tumors. Metabolic heterogeneity is important because it influences therapeutic vulnerabilities and may predict clinical outcomes. This Review describes current concepts about metabolic regulation in tumors, focusing on processes intrinsic to cancer cells and on factors imposed upon cancer cells by the tumor microenvironment. We discuss experimental approaches to identify subtype-selective metabolic vulnerabilities in preclinical cancer models. Finally, we describe efforts to characterize metabolism in primary human tumors, which should produce new insights into metabolic heterogeneity in the context of clinically relevant microenvironments.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Metabolic features and liabilities are selective for subtypes rather than uniform across all cancers.
“As a result, metabolic features and liabilities are subtype-selective rather than uniform across all cancers (2).”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [2]
Human tumors are metabolically heterogeneous.
“Second, as the approaches used to assess metabolic phenotypes have become more informative, it has become clear that human tumors are metabolically heterogeneous.”
From Metabolic reprogramming and cancer progression (2020) · cites this paper as [2]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
Mitochondrial Autophagy Is an HIF-1-dependent Adaptive Metabolic Response to Hypoxia
Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., & Semenza, G. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800102200 · Cited by 1,601 · see citing works
RetractedHallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
Molecular portraits of human breast tumours
Perou, C., Sørlie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Rees, C. A., Pollack, J., Ross, D., Johnsen, H., Akslen, L., et al. (2000) · Nature · doi:10.1038/35021093 · Cited by 16,551 · see citing works
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425 · see citing works
Nishimura, R., Osako, T., Nishiyama, Y., Tashima, R., Nakano, M., Fujisue, M., Toyozumi, Y., & Arima, N. (2013) · Oncology · doi:10.1159/000353099 · Cited by 13,239 · see citing works
Comprehensive molecular profiling of lung adenocarcinoma
The Cancer Genome Atlas Research Network (2014) · Nature · doi:10.1038/nature13385 · Cited by 5,732 · see citing works
The fundamental role of epigenetic events in cancer
Jones, P. A., & Baylin, S. B. (2002) · Nature Reviews Genetics · doi:10.1038/nrg816 · Cited by 5,648 · see citing works
Ki67 expression in breast cancer
Elkablawy, M. A., Albasri, A. M., Mohammed, R. A., Hussainy, A. S., Nouh, M. M., & Alhujaily, A. S. (2016) · Saudi Medical Journal · doi:10.15537/smj.2016.2.12285 · Cited by 4,382 · see citing works
Cancer-associated IDH1 mutations produce 2-hydroxyglutarate
Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., et al. (2009) · Nature · doi:10.1038/nature08617 · Cited by 4,154 · see citing works
Otto Warburg's contributions to current concepts of cancer metabolism
Koppenol, W. H., Bounds, P. L., & Dang, C. V. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3038 · Cited by 3,427 · see citing works
Metabolic Competition in the Tumor Microenvironment Is a Driver of Cancer Progression
Chang, C.-H., Qiu, J., O’Sullivan, D., Buck, M. D., Noguchi, T., Curtis, J. D., Chen, Q., Gindin, M., Gubin, M. M., van der Windt, G. J. W., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.016 · Cited by 3,331 · see citing works
Functional Polarization of Tumour-Associated Macrophages by Tumour-Derived Lactic Acid
Colegio, O. R., Chu, N.-Q., Szabo, A. L., Chu, T., Rhebergen, A. M., Jairam, V., Cyrus, N., Brokowski, C. E., Eisenbarth, S. C., Phillips, G. M., et al. (2014) · Nature · doi:10.1038/nature13490 · Cited by 3,046 · see citing works
Fundamentals of Cancer Metabolism
DeBerardinis, R. J., & Chandel, N. S. (2016) · Science Advances · doi:10.1126/sciadv.1600200 · Cited by 3,013 · see citing works
Self-citationThe molecular hallmarks of epigenetic control
Allis, C. D., & Jenuwein, T. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.59 · Cited by 2,809 · see citing works
ATP-citrate lyase links cellular metabolism to histone acetylation
Wellen, K. E., Hatzivassiliou, G., Sachdeva, U. M., Bui, T. V., Cross, J. R., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1164097 · Cited by 2,298 · see citing works
Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth
Nieman, K. M., Kenny, H. A., Penicka, C. V., Ladanyi, A., Buell-Gutbrod, R., Zillhardt, M. R., Romero, I. L., Carey, M. S., Mills, G. B., Hotamisligil, G. S., et al. (2011) · Nature Medicine · doi:10.1038/nm.2492 · Cited by 2,279 · see citing works
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 · see citing works
Hypoxia in cancer: significance and impact on clinical outcome
Vaupel, P., & Mayer, A. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9055-1 · Cited by 2,240 · see citing works
Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression
Sreekumar, A., Poisson, L., Rajendiran, T. M., Khan, A. P., Cao, Q., Yu, J., Laxman, B., Mehra, R., Lonigro, R. J., Li, Y., et al. (2009) · Nature · doi:10.1038/nature07762 · Cited by 2,238 · see citing works
Gao, P., Tchernyshyov, I., Chang, T.-C., Lee, Y.-S., Kita, K., Ochi, T., Zeller, K. I., De Marzo, A. M., Van Eyk, J. E., Mendell, J. T., et al. (2009) · Nature · doi:10.1038/nature07823 · Cited by 2,124 · see citing works
LDHA-Associated Lactic Acid Production Blunts Tumor Immunosurveillance by T and NK Cells
Brand, A., Singer, K., Koehl, G. E., Kolitzus, M., Schoenhammer, G., Thiel, A., Matos, C., Bruss, C., Klobuch, S., Peter, K., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.011 · Cited by 2,039 · see citing works
Ward, P. S., Patel, J., Wise, D. R., Abdel-Wahab, O., Bennett, B. D., Coller, H. A., Cross, J. R., Fantin, V. R., Hedvat, C. V., Perl, A. E., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.01.020 · Cited by 2,020 · cited 1× · see citing works
“Examples of divergent pathways include (R)-2HG accumulation in tumors with IDH1 or IDH2 mutations, or metabolic preferences that differentiate tumors with distinct oncogenotypes (Dang et al., 2009; Shackelford et al., 2013; Ward et al., 2010).”
BackgroundWise, D. R., DeBerardinis, R. J., Mancuso, A., Sayed, N., Zhang, X.-Y., Pfeiffer, H. K., Nissim, I., Daikhin, E., Yudkoff, M., McMahon, S. B., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810199105 · Cited by 2,001 · see citing works
Self-citationIDH mutation impairs histone demethylation and results in a block to cell differentiation
Lu, C., Ward, P. S., Kapoor, G. S., Rohle, D., Turcan, S., Abdel-Wahab, O., Edwards, C. R., Khanin, R., Figueroa, M. E., Melnick, A., et al. (2012) · Nature · doi:10.1038/nature10860 · Cited by 1,985 · see citing works
Inhibitory effect of tumor cell-derived lactic acid on human T cells
Fischer, K., Hoffmann, P., Voelkl, S., Meidenbauer, N., Ammer, J., Edinger, M., Gottfried, E., Schwarz, S., Rothe, G., Hoves, S., et al. (2007) · Blood · doi:10.1182/blood-2006-07-035972 · Cited by 1,946 · see citing works
L-Arginine Modulates T Cell Metabolism and Enhances Survival and Anti-tumor Activity
Geiger, R., Rieckmann, J. C., Wolf, T., Basso, C., Feng, Y., Fuhrer, T., Kogadeeva, M., Picotti, P., Meissner, F., Mann, M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.031 · Cited by 1,775 · see citing works
Functional genomics reveal that the serine synthesis pathway is essential in breast cancer
Possemato, R., Marks, K. M., Shaul, Y. D., Pacold, M. E., Kim, D., Birsoy, K., Sethumadhavan, S., Woo, H.-K., Jang, H. G., Jha, A. K., et al. (2011) · Nature · doi:10.1038/nature10350 · Cited by 1,683 · see citing works
Macropinocytosis of protein is an amino acid supply route in Ras-transformed cells
Commisso, C., Davidson, S. M., Soydaner-Azeloglu, R. G., Parker, S. J., Kamphorst, J. J., Hackett, S., Grabocka, E., Nofal, M., Drebin, J. A., Thompson, C. B., et al. (2013) · Nature · doi:10.1038/nature12138 · Cited by 1,683 · see citing works
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 1,633 · see citing works
Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond
Platten, M., Nollen, E. A. A., Röhrig, U. F., Fallarino, F., & Opitz, C. A. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0016-5 · Cited by 1,586 · see citing works
Kulis, M., & Esteller, M. (2010) · Advances in genetics · doi:10.1016/b978-0-12-380866-0.60002-2 · Cited by 1,575 · see citing works
Phosphoenolpyruvate Is a Metabolic Checkpoint of Anti-tumor T Cell Responses
Ho, P.-C., Bihuniak, J. D., Macintyre, A. N., Staron, M., Liu, X., Amezquita, R., Tsui, Y.-C., Cui, G., Micevic, G., Perales, J. C., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.012 · Cited by 1,462 · see citing works
Metabolic pathways promoting cancer cell survival and growth
Boroughs, L. K., & DeBerardinis, R. J. (2015) · Nature Cell Biology · doi:10.1038/ncb3124 · Cited by 1,459 · see citing works
Self-citationAkt Stimulates Aerobic Glycolysis in Cancer Cells
Elstrom, R. L., Bauer, D. E., Buzzai, M., Karnauskas, R., Harris, M. H., Plas, D. R., Zhuang, H., Cinalli, R. M., Alavi, A., Rudin, C. M., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2904 · Cited by 1,454 · see citing works
Somatic mutation in cancer and normal cells
Martincorena, I., & Campbell, P. J. (2015) · Science · doi:10.1126/science.aab4082 · Cited by 1,396 · see citing works
Stine, Z. E., Walton, Z. E., Altman, B. J., Hsieh, A. L., & Dang, C. V. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-15-0507 · Cited by 1,375 · see citing works
Acetyl Coenzyme A: A Central Metabolite and Second Messenger
Pietrocola, F., Galluzzi, L., Pedro, J. M. B., Madeo, F., & Kroemer, G. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.05.014 · Cited by 1,349 · see citing works
Lactate Metabolism in Human Lung Tumors
Faubert, B., Li, K. Y., Cai, L., Hensley, C. T., Kim, J., Zacharias, L. G., Yang, C., Do, Q. N., Doucette, S., Burguete, D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.019 · Cited by 1,343 · see citing works
Self-citationOxidative stress inhibits distant metastasis by human melanoma cells
Piskounova, E., Agathocleous, M., Murphy, M. M., Hu, Z., Huddlestun, S. E., Zhao, Z., Leitch, A. M., Johnson, T. M., DeBerardinis, R. J., & Morrison, S. J. (2015) · Nature · doi:10.1038/nature15726 · Cited by 1,269 · see citing works
Self-citationGlutamine and cancer: cell biology, physiology, and clinical opportunities
Hensley, C. T., Wasti, A. T., & DeBerardinis, R. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69600 · Cited by 1,262 · see citing works
Self-citationWriting, erasing and reading histone lysine methylations
Hyun, K., Jeon, J., Park, K., & Kim, J. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.11 · Cited by 1,250 · see citing works
Self-citationCpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future
Esteller, M. (2002) · Oncogene · doi:10.1038/sj.onc.1205600 · Cited by 1,235 · see citing works
Xiao, M., Yang, H., Xu, W., Ma, S., Lin, H., Zhu, H., Liu, L., Liu, Y., Yang, C., Xu, Y., et al. (2012) · Genes & Development · doi:10.1101/gad.191056.112 · Cited by 1,188 · see citing works
SIRT1 and other sirtuins in metabolism
Chang, H.-C., & Guarente, L. (2014) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2013.12.001 · Cited by 1,138 · see citing works
Metabolic heterogeneity in human lung tumors
Hensley, C. T., Faubert, B., Yuan, Q., Lev-Cohain, N., Jin, E., Kim, J., Jiang, L., Ko, B., Skelton, R., Loudat, L., et al. (2016) · Cell · doi:10.1016/j.cell.2015.12.034 · Cited by 1,138 · see citing works
Self-citationMacintyre, A. N., Gerriets, V. A., Nichols, A., Michalek, R. D., Rudolph, M. C., Deoliveira, D., Anderson, S. M., Abel, E. D., Chen, B. J., Hale, L. P., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.05.004 · Cited by 1,129 · see citing works
Pancreatic stellate cells support tumour metabolism through autophagic alanine secretion
Sousa, C. M., Biancur, D. E., Wang, X., Halbrook, C. J., Sherman, M. H., Zhang, L., Kremer, D., Hwang, R. F., Witkiewicz, A. K., Ying, H., et al. (2016) · Nature · doi:10.1038/nature19084 · Cited by 1,122 · see citing works
Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis
Locasale, J. W., Grassian, A. R., Melman, T., Lyssiotis, C. A., Mattaini, K. R., Bass, A. J., Heffron, G., Metallo, C. M., Muranen, T., Sharfi, H., et al. (2011) · Nature Genetics · doi:10.1038/ng.890 · Cited by 1,120 · see citing works
c-Myc transactivation of <i>LDH-A</i> : Implications for tumor metabolism and growth
Shim, H., Dolde, C., Lewis, B. C., Wu, C.-S., Dang, G., Jungmann, R. A., Dalla-Favera, R., & Dang, C. V. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6658 · Cited by 1,092 · see citing works
Yang, X.-J., & Seto, E. (2007) · Oncogene · doi:10.1038/sj.onc.1210599 · Cited by 1,040 · see citing works
Indoleamine 2,3 dioxygenase and metabolic control of immune responses
Munn, D. H., & Mellor, A. L. (2013) · Trends in Immunology · doi:10.1016/j.it.2012.10.001 · Cited by 1,037 · see citing works
Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment
Schafer, Z. T., Grassian, A. R., Song, L., Jiang, Z., Gerhart-Hines, Z., Irie, H. Y., Gao, S., Puigserver, P., & Brugge, J. S. (2009) · Nature · doi:10.1038/nature08268 · Cited by 1,031 · see citing works
Intracellular α-ketoglutarate maintains the pluripotency of embryonic stem cells
Carey, B. W., Finley, L. W. S., Cross, J. R., Allis, C. D., & Thompson, C. B. (2015) · Nature · doi:10.1038/nature13981 · Cited by 1,007 · see citing works
The Histone Deacetylase Sirt6 Regulates Glucose Homeostasis via Hif1α
Zhong, L., D'Urso, A., Toiber, D., Sebastian, C., Henry, R. E., Vadysirisack, D. D., Guimaraes, A., Marinelli, B., Wikstrom, J. D., Nir, T., et al. (2010) · Cell · doi:10.1016/j.cell.2009.12.041 · Cited by 1,001 · see citing works
Wise, D. R., Ward, P. S., Shay, J. E. S., Cross, J. R., Gruber, J. J., Sachdeva, U. M., Platt, J. M., DeMatteo, R. G., Simon, M. C., & Thompson, C. B. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117773108 · Cited by 975 · see citing works
Commensal Microbiota Promote Lung Cancer Development via γδ T Cells
Jin, C., Lagoudas, G. K., Zhao, C., Bullman, S., Bhutkar, A., Hu, B., Ameh, S., Sandel, D., Liang, X. S., Mazzilli, S., et al. (2019) · Cell · doi:10.1016/j.cell.2018.12.040 · Cited by 964 · see citing works
Influence of Metabolism on Epigenetics and Disease
Kaelin, W. G., & McKnight, S. L. (2013) · Cell · doi:10.1016/j.cell.2013.03.004 · Cited by 920 · see citing works
Cancer Epigenetics: Tumor Heterogeneity, Plasticity of Stem-like States, and Drug Resistance
Easwaran, H., Tsai, H.-C., & Baylin, S. B. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.05.015 · Cited by 915 · see citing works
Tao, R., Coleman, M. C., Pennington, J. D., Ozden, O., Park, S.-H., Jiang, H., Kim, H.-S., Flynn, C. R., Hill, S., Hayes McDonald, W., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.12.013 · Cited by 899 · see citing works
Zhang, H., Gao, P., Fukuda, R., Kumar, G., Krishnamachary, B., Zeller, K. I., Dang, C. V., & Semenza, G. L. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.04.001 · Cited by 885 · see citing works
Loss of FBP1 by Snail-Mediated Repression Provides Metabolic Advantages in Basal-like Breast Cancer
Dong, C., Yuan, T., Wu, Y., Wang, Y., Fan, T. W. ‐., Miriyala, S., Lin, Y., Yao, J., Shi, J., Kang, T., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.01.022 · Cited by 806 · see citing works
HIF and c-Myc: Sibling Rivals for Control of Cancer Cell Metabolism and Proliferation
Gordan, J. D., Thompson, C. B., & Simon, M. C. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.07.006 · Cited by 806 · see citing works
An Integrated Metabolic Atlas of Clear Cell Renal Cell Carcinoma
Hakimi, A. A., Reznik, E., Lee, C., Creighton, C. J., Brannon, A. R., Luna, A., Aksoy, B. A., Liu, E. M., Shen, R., Lee, W., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2015.12.004 · Cited by 791 · see citing works
Flier, J. S., Mueckler, M., Usher, P., & Lodish, H. F. (1987) · Science · doi:10.1126/science.3103217 · Cited by 778 · see citing works
Acetate is a bioenergetic substrate for human glioblastoma and brain metastases
Mashimo, T., Pichumani, K., Vemireddy, V., Hatanpaa, K. J., Singh, D. K., Sirasanagandla, S., Nannepaga, S., Piccirillo, S. G., Kovacs, Z., Foong, C., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.025 · Cited by 760 · see citing works
Self-citationNRF2 regulates serine biosynthesis in non–small cell lung cancer
DeNicola, G. M., Chen, P.-H., Mullarky, E., Sudderth, J., Hu, Z., Wu, D., Tang, H., Xie, Y., Asara, J. M., Huffman, K. E., et al. (2015) · Nature Genetics · doi:10.1038/ng.3421 · Cited by 747 · see citing works
Self-citationTumor-derived lactic acid modulates dendritic cell activation and antigen expression
Gottfried, E., Kunz-Schughart, L. A., Ebner, S., Mueller-Klieser, W., Hoves, S., Andreesen, R., Mackensen, A., & Kreutz, M. (2006) · Blood · doi:10.1182/blood-2005-05-1795 · Cited by 729 · see citing works
Distinct Regulation of Th17 and Th1 Cell Differentiation by Glutaminase-Dependent Metabolism
Johnson, M. O., Wolf, M. M., Madden, M. Z., Andrejeva, G., Sugiura, A., Contreras, D. C., Maseda, D., Liberti, M. V., Paz, K. G., Kishton, R. J., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.001 · Cited by 702 · see citing works
Cai, L., Sutter, B. M., Li, B., & Tu, B. P. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.05.004 · Cited by 701 · see citing works
Kryukov, G. V., Wilson, F. H., Ruth, J. R., Paulk, J., Tsherniak, A., Marlow, S. E., Vazquez, F., Weir, B. A., Fitzgerald, M. E., Tanaka, M., et al. (2016) · Science · doi:10.1126/science.aad5214 · Cited by 688 · see citing works
McQuade, J. L., Daniel, C. R., Hess, K. R., Mak, C., Wang, D. Y., Rai, R. R., Park, J. J., Haydu, L. E., Spencer, C., Wongchenko, M., et al. (2018) · The Lancet Oncology · doi:10.1016/s1470-2045(18)30078-0 · Cited by 664 · see citing works
The histone deacetylase SIRT6 is a tumor suppressor that controls cancer metabolism
Sebastián, C., Zwaans, B. M. M., Silberman, D. M., Gymrek, M., Goren, A., Zhong, L., Ram, O., Truelove, J., Guimaraes, A. R., Toiber, D., et al. (2012) · Cell · doi:10.1016/j.cell.2012.10.047 · Cited by 660 · see citing works
Serine is an essential metabolite for effector T cell expansion
Ma, E. H., Bantug, G., Griss, T., Condotta, S., Johnson, R. M., Samborska, B., Mainolfi, N., Suri, V., Guak, H., Balmer, M. L., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2016.12.011 · Cited by 657 · see citing works
Keap1 loss promotes Kras-driven lung cancer and results in dependence on glutaminolysis
Romero, R., Sayin, V. I., Davidson, S. M., Bauer, M. R., Singh, S. X., LeBoeuf, S. E., Karakousi, T. R., Ellis, D. C., Bhutkar, A., Sánchez-Rivera, F. J., et al. (2017) · Nature Medicine · doi:10.1038/nm.4407 · Cited by 652 · see citing works
Cancer cell metabolism: the essential role of the nonessential amino acid, glutamine
Zhang, J., Pavlova, N. N., & Thompson, C. B. (2017) · The EMBO Journal · doi:10.15252/embj.201696151 · Cited by 651 · see citing works
The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type
Yuneva, M. O., Fan, T. W. M., Allen, T. D., Higashi, R. M., Ferraris, D. V., Tsukamoto, T., Matés, J. M., Alonso, F. J., Wang, C., Seo, Y., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2011.12.015 · Cited by 639 · see citing works
Antioxidants can increase melanoma metastasis in mice
Le Gal, K., Ibrahim, M. X., Wiel, C., Sayin, V. I., Akula, M. K., Karlsson, C., Dalin, M. G., Akyürek, L. M., Lindahl, P., Nilsson, J., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aad3740 · Cited by 632 · see citing works
Myc Stimulates Nuclearly Encoded Mitochondrial Genes and Mitochondrial Biogenesis
Li, F., Wang, Y., Zeller, K. I., Potter, J. J., Wonsey, D. R., O’Donnell, K. A., Kim, J., Yustein, J. T., Lee, L. A., & Dang, C. V. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.14.6225-6234.2005 · Cited by 615 · see citing works
Self-citationCantor, J. R., Abu-Remaileh, M., Kanarek, N., Freinkman, E., Gao, X., Louissaint, A., Lewis, C. A., & Sabatini, D. M. (2017) · Cell · doi:10.1016/j.cell.2017.03.023 · Cited by 611 · see citing works
Sullivan, M. R., Danai, L. V., Lewis, C. A., Chan, S. H., Gui, D. Y., Kunchok, T., Dennstedt, E. A., Vander Heiden, M. G., & Muir, A. (2019) · eLife · doi:10.7554/elife.44235 · Cited by 588 · see citing works
Fiaschi, T., Marini, A., Giannoni, E., Taddei, M. L., Gandellini, P., Donatis, A. D., Lanciotti, M., Serni, S., Cirri, P., & Chiarugi, P. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-1949 · Cited by 586 · see citing works
Shackelford, D. B., Abt, E., Gerken, L., Vasquez, D. S., Seki, A., Leblanc, M., Wei, L., Fishbein, M. C., Czernin, J., Mischel, P. S., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2012.12.008 · Cited by 585 · see citing works
Reductive carboxylation supports redox homeostasis during anchorage-independent growth
Jiang, L., Shestov, A. A., Swain, P., Yang, C., Parker, S. J., Wang, Q. A., Terada, L. S., Adams, N. D., McCabe, M. T., Pietrak, B., et al. (2016) · Nature · doi:10.1038/nature17393 · Cited by 582 · see citing works
Self-citationTissue of origin dictates branched-chain amino acid metabolism in mutant <i>Kras</i> -driven cancers
Mayers, J. R., Torrence, M. E., Danai, L. V., Papagiannakopoulos, T., Davidson, S. M., Bauer, M. R., Lau, A. N., Ji, B. W., Dixit, P. D., Hosios, A. M., et al. (2016) · Science · doi:10.1126/science.aaf5171 · Cited by 582 · see citing works
Timmerman, L. A., Holton, T., Yuneva, M., Louie, R. J., Padró, M., Daemen, A., Hu, M., Chan, D. A., Ethier, S. P., van ‘t Veer, L. J., et al. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.08.020 · Cited by 573 · see citing works
What a difference a hydroxyl makes: mutant IDH, (<i>R</i>)-2-hydroxyglutarate, and cancer
Losman, J.-A., & Kaelin, W. G. (2013) · Genes & Development · doi:10.1101/gad.217406.113 · Cited by 570 · see citing works
Akt-dependent metabolic reprogramming regulates tumor cell histone acetylation
Lee, J. V., Carrer, A., Shah, S., Snyder, N. W., Wei, S., Venneti, S., Worth, A. J., Yuan, Z.-F., Lim, H.-W., Liu, S., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.06.004 · Cited by 563 · see citing works
ATP-Citrate Lyase: A Key Player in Cancer Metabolism
Zaidi, N., Swinnen, J. V., & Smans, K. A. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-4112 · Cited by 549 · see citing works
Fructose-1,6-bisphosphatase opposes renal carcinoma progression
Li, B., Qiu, B., Lee, D. S. M., Walton, Z. E., Ochocki, J. D., Mathew, L. K., Mancuso, A., Gade, T. P. F., Keith, B., Nissim, I., et al. (2014) · Nature · doi:10.1038/nature13557 · Cited by 535 · see citing works
Glutathione primes t cell metabolism for inflammation
Mak, T. W., Grusdat, M., Duncan, G. S., Dostert, C., Nonnenmacher, Y., Cox, M., Binsfeld, C., Hao, Z., Brüstle, A., Itsumi, M., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.03.019 · Cited by 511 · see citing works
The landscape of cancer cell line metabolism
Li, H., Ning, S., Ghandi, M., Kryukov, G. V., Gopal, S., Deik, A., Souza, A., Pierce, K. A., Keskula, P., Hernandez, D., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0404-8 · Cited by 511 · see citing works
Pyruvate carboxylase is critical for non–small-cell lung cancer proliferation
Sellers, K., Fox, M. P., Bousamra, M., Slone, S. P., Higashi, R. M., Miller, D. M., Wang, Y., Yan, J., Yuneva, M. O., Deshpande, R., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci72873 · Cited by 497 · see citing works
Mitochondrial complex III is essential for suppressive function of regulatory T cells
Weinberg, S. E., Singer, B. D., Steinert, E. M., Martinez, C. A., Mehta, M., Martínez‐Reyes, I., Gao, P., Helmin, K. A., Abdala‐Valencia, H., Sena, L. A., et al. (2019) · Nature · doi:10.1038/s41586-018-0846-z · Cited by 496 · see citing works
DNA methylation and DNA methyltransferases
Edwards, J. R., Yarychkivska, O., Boulard, M., & Bestor, T. H. (2017) · Epigenetics & Chromatin · doi:10.1186/s13072-017-0130-8 · Cited by 487 · see citing works
Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis
Chicklore, S., Goh, V., Siddique, M. M., Roy, A. S., Marsden, P. K., & Cook, G. (2012) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-012-2247-0 · Cited by 485 · see citing works
MTAP deletions in cancer create vulnerability to targeting of the MAT2A/PRMT5/RIOK1 axis
Marjon, K., Cameron, M. J., Quang, P., Clasquin, M. F., Mandley, E., Kunii, K., McVay, M., Choe, S., Kernytsky, A., Gross, S., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.043 · Cited by 485 · see citing works
The utilization of extracellular proteins as nutrients is suppressed by mTORC1
Palm, W., Park, Y., Wright, K., Pavlova, N. N., Tuveson, D. A., & Thompson, C. B. (2015) · Cell · doi:10.1016/j.cell.2015.06.017 · Cited by 457 · see citing works
NNMT promotes epigenetic remodeling in cancer by creating a metabolic methylation sink
Ulanovskaya, O. A., Zuhl, A. M., & Cravatt, B. F. (2013) · Nature Chemical Biology · doi:10.1038/nchembio.1204 · Cited by 444 · see citing works
Bell, E. L., Emerling, B. M., Ricoult, S. J. H., & Guarente, L. (2011) · Oncogene · doi:10.1038/onc.2011.37 · Cited by 440 · see citing works
Maddocks, O. D. K., Labuschagne, C. F., Adams, P. D., & Vousden, K. H. (2016) · Molecular Cell · doi:10.1016/j.molcel.2015.12.014 · Cited by 440 · see citing works
Fan, T. W. ‐., Lane, A. N., Higashi, R. M., Farag, M. A., Gao, H. T., Bousamra, M., & Miller, D. M. (2009) · Molecular Cancer · doi:10.1186/1476-4598-8-41 · Cited by 438 · see citing works
Heterogeneity of tumor-induced gene expression changes in the human metabolic network
Hu, J., Locasale, J. W., Bielas, J. H., O'Sullivan, J., Sheahan, K., Cantley, L. C., Heiden, M. G. V., & Vitkup, D. (2013) · Nature Biotechnology · doi:10.1038/nbt.2530 · Cited by 407 · see citing works
Daemen, A., Peterson, D., Sahu, N., McCord, R., Du, X., Liu, B., Kowanetz, K., Hong, R., Moffat, J., Gao, M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501605112 · Cited by 398 · see citing works
Improving the metabolic fidelity of cancer models with a physiological cell culture medium
Voorde, J. V., Ackermann, T., Pfetzer, N., Sumpton, D. P., Mackay, G., Kalna, G., Nixon, C., Blyth, K., Gottlieb, E., & Tardito, S. (2019) · Science Advances · doi:10.1126/sciadv.aau7314 · Cited by 389 · see citing works
Cham, C. M., Driessens, G., O'Keefe, J. P., & Gajewski, T. F. (2008) · European Journal of Immunology · doi:10.1002/eji.200838289 · Cited by 388 · see citing works
Modulating the microbiome to improve therapeutic response in cancer
McQuade, J. L., Daniel, C. R., Helmink, B. A., & Wargo, J. A. (2019) · The Lancet Oncology · doi:10.1016/s1470-2045(18)30952-5 · Cited by 376 · see citing works
Pan, M., Reid, M. A., Lowman, X. H., Kulkarni, R. P., Tran, T. Q., Liu, X., Yang, Y., Hernandez-Davies, J. E., Rosales, K. K., Li, H., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3410 · Cited by 368 · see citing works
Gaude, E., & Frezza, C. (2016) · Nature Communications · doi:10.1038/ncomms13041 · Cited by 366 · see citing works
Stromal control of cystine metabolism promotes cancer cell survival in chronic lymphocytic leukaemia
Zhang, W., Trachootham, D., Liu, J., Chen, G., Pelicano, H., Garcı́a-Prieto, C., Lu, W., Burger, J. A., Croce, C. M., Plunkett, W. K., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2432 · Cited by 357 · see citing works
Yang, A., Herter-Sprie, G., Zhang, H., Lin, E. Y., Biancur, D., Wang, X., Deng, J., Hai, J., Yang, S., Wong, K.-K., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0952 · Cited by 349 · see citing works
Metabolism of [U‐ <sup>13</sup> C]glucose in human brain tumors <i>in vivo</i>
Maher, E. A., Marin‐Valencia, I., Bachoo, R. M., Mashimo, T., Raisanen, J., Hatanpaa, K. J., Jindal, A., Jeffrey, F. M., Choi, C., Madden, C., et al. (2012) · NMR in Biomedicine · doi:10.1002/nbm.2794 · Cited by 341 · see citing works
Mullen, A. R., Hu, Z., Shi, X., Jiang, L., Boroughs, L. K., Kovacs, Z., Boriack, R., Rakheja, D., Sullivan, L. B., Linehan, W. M., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.037 · Cited by 337 · see citing works
Self-citationMetabolic Reprogramming of Cancer-Associated Fibroblasts by IDH3α Downregulation
Zhang, D., Wang, Y., Shi, Z., Liu, J., Sun, P., Hou, X., Zhang, J., Zhao, S., Zhou, B. P., & Mi, J. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.006 · Cited by 334 · see citing works
LC3-Associated Phagocytosis in Myeloid Cells Promotes Tumor Immune Tolerance
Cunha, L. D., Yang, M., Carter, R., Guy, C., Harris, L., Crawford, J. C., Quarato, G., Boada-Romero, E., Kalkavan, H., Johnson, M. D. L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.061 · Cited by 334 · see citing works
Aerobic glycolysis during lymphocyte proliferation
Wang, T., Marquardt, C. A., & Foker, J. E. (1976) · Nature · doi:10.1038/261702a0 · Cited by 333 · see citing works
CPS1 maintains pyrimidine pools and DNA synthesis in KRAS/LKB1-mutant lung cancer cells
Kim, J., Hu, Z., Cai, L., Li, K., Choi, E., Faubert, B., Bezwada, D., Rodriguez-Canales, J., Villalobos, P., Lin, Y.-F., et al. (2017) · Nature · doi:10.1038/nature22359 · Cited by 325 · see citing works
Self-citationThe impact of metabolism on DNA methylation
Ulrey, C. L., Liu, L., Andrews, L. G., & Tollefsbol, T. O. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi100 · Cited by 317 · see citing works
Muir, A., Danai, L. V., Gui, D. Y., Waingarten, C. Y., Lewis, C. A., & Vander Heiden, M. G. (2017) · eLife · doi:10.7554/elife.27713 · Cited by 311 · see citing works
Fumarate and Succinate Regulate Expression of Hypoxia-inducible Genes via TET Enzymes
Laukka, T., Mariani, C. J., Ihantola, T., Cao, J. Z., Hokkanen, J., Kaelin, W. G., Godley, L. A., & Koivunen, P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.688762 · Cited by 307 · see citing works
Valencia, T., Kim, J. Y., Abu-Baker, S., Moscat-Pardos, J., Ahn, C. S., Reina-Campos, M., Duran, A., Castilla, E. A., Metallo, C. M., Diaz-Meco, M. T., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.05.004 · Cited by 304 · see citing works
Self-citationl -Arginine Depletion Blunts Antitumor T-cell Responses by Inducing Myeloid-Derived Suppressor Cells
Fletcher, M., Ramírez, M. E., Sierra, R. A., Raber, P. L., Thevenot, P., Al-Khami, A. A., Sanchez‐Pino, M. D., Hernandez, C., Wyczechowska, D. D., Ochoa, A. C., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-1491 · Cited by 283 · see citing works
<scp>l</scp> -2-Hydroxyglutarate: An Epigenetic Modifier and Putative Oncometabolite in Renal Cancer
Shim, E.-H., Livi, C. B., Rakheja, D., Tan, J., Benson, D., Parekh, V., Kho, E.-Y., Ghosh, A. P., Kirkman, R., Velu, S., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0696 · Cited by 280 · see citing works
Courtney, K. D., Bezwada, D., Mashimo, T., Pichumani, K., Vemireddy, V., Funk, A. M., Wimberly, J., McNeil, S. S., Kapur, P., Lotan, Y., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.07.020 · Cited by 280 · see citing works
Self-citationKung, H.-N., Marks, J. R., & Chi, J.-T. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002229 · Cited by 277 · see citing works
Martinez-Outschoorn, U. E., Pavlides, S., Howell, A., Pestell, R. G., Tanowitz, H. B., Sotgia, F., & Lisanti, M. P. (2011) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2011.01.023 · Cited by 248 · see citing works
p62: a versatile multitasker takes on cancer
Moscat, J., & Díaz-Meco, M. T. (2012) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2012.02.008 · Cited by 239 · see citing works
Role of glutamine in human carbohydrate metabolism in kidney and other tissues
Stümvoll, M., Perriello, G., Meyer, C., & Gerich, J. E. (1999) · Kidney International · doi:10.1046/j.1523-1755.1999.055003778.x · Cited by 230 · see citing works
Luo, W., Chang, R., Zhong, J., Pandey, A., & Semenza, G. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217394109 · Cited by 228 · see citing works
Metformin Targets Central Carbon Metabolism and Reveals Mitochondrial Requirements in Human Cancers
Liu, X., Romero, I. L., Litchfield, L. M., Lengyel, E. R., & Locasale, J. W. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.09.005 · Cited by 228 · see citing works
Bonuccelli, G., Whitaker‐Menezes, D., Castelló-Cros, R., Pavlides, S., Pestell, R. G., Fatatis, A., Witkiewicz, A. K., Heiden, M. G. V., Migneco, G., Chiavarina, B., et al. (2010) · Cell Cycle · doi:10.4161/cc.9.10.11601 · Cited by 223 · see citing works
Antigen receptor control of methionine metabolism in T cells
Sinclair, L. V., Howden, A. J. M., Brenes, A. J., Spinelli, L., Hukelmann, J. L., Macintyre, A. N., Liu, X., Thomson, S., Taylor, P. M., Rathmell, J. C., et al. (2019) · eLife · doi:10.7554/elife.44210 · Cited by 222 · see citing works
Hypermethylation of tumor suppressor genes in cancer
Herman, J. G. (1999) · Seminars in Cancer Biology · doi:10.1006/scbi.1999.0138 · Cited by 221 · see citing works
Regulation of Glycolytic Enzyme Phosphoglycerate Mutase-1 by Sirt1 Protein-mediated Deacetylation
Hallows, W. C., Yu, W., & Denu, J. M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.317404 · Cited by 200 · see citing works
Brand, K. (1985) · Biochemical Journal · doi:10.1042/bj2280353 · Cited by 187 · see citing works
Inosine Monophosphate Dehydrogenase Dependence in a Subset of Small Cell Lung Cancers
Huang, F., Ni, M., Chalishazar, M. D., Huffman, K. E., Kim, J., Cai, L., Shi, X., Cai, F., Zacharias, L. G., Ireland, A. S., et al. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.06.005 · Cited by 186 · see citing works
Self-citationAutophagy Regulation of Metabolism Is Required for CD8+ T Cell Anti-tumor Immunity
DeVorkin, L., Pavey, N., Carleton, G., Comber, A., Ho, C., Lim, J., McNamara, E., Huang, H., Kim, P., Zacharias, L. G., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.037 · Cited by 185 · see citing works
Self-citationApplications of metabolomics to study cancer metabolism
Kaushik, A. K., & DeBerardinis, R. J. (2018) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2018.04.009 · Cited by 179 · see citing works
Self-citationTarasenko, T. N., Pacheco, S. E., Koenig, M. K., Gómez‐Rodríguez, J., Kapnick, S. M., Díaz, F., Zerfas, P. M., Barca, E., Sudderth, J., DeBerardinis, R. J., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.007 · Cited by 177 · see citing works
Self-citationSuccinate inhibition of α-ketoglutarate-dependent enzymes in a yeast model of paraganglioma
Smith, E. H., Janknecht, R., & Maher, L. J. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm275 · Cited by 169 · see citing works
Goel, A., Mathupala, S. P., & Pedersen, P. L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300608200 · Cited by 152 · see citing works
Liu, Y., Marks, K. M., Cowley, G. S., Carretero, J., Liu, Q., Nieland, T. J. F., Xu, C., Cohoon, T. J., Gao, P., Zhang, Y., et al. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0015 · Cited by 151 · see citing works
Goodwin, J., Neugent, M. L., Lee, S. Y., Choe, J. H., Choi, H., Jenkins, D. M. R., Ruthenborg, R. J., Robinson, M. W., Jeong, J. Y., Wake, M., et al. (2017) · Nature Communications · doi:10.1038/ncomms15503 · Cited by 151 · see citing works
Self-citationChen, M., Zhang, J., Li, N., Qian, Z., Zhu, M., Li, Q., Zheng, J., Wang, X., & Shi, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025564 · Cited by 150 · see citing works
New Insights into the Regulation of Methyl Group and Homocysteine Metabolism
Williams, K. T., & Schalinske, K. L. (2007) · Journal of Nutrition · doi:10.1093/jn/137.2.311 · Cited by 136 · see citing works
Serine Is an Essential Metabolite for Effector T Cell Expansion
Ma, E. H., Bantug, G. R., Griss, T., Condotta, S. A., Johnson, R. M., Samborska, B., Mainolfi, N., Suri, V., Guak, H., Balmer, M. L., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.01.014 · Cited by 133 · see citing works
Wolf, A., Agnihotri, S., Muñoz, D. M., & Guha, A. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.06.007 · Cited by 118 · see citing works
ATF4-Induced Metabolic Reprograming Is a Synthetic Vulnerability of the p62-Deficient Tumor Stroma
Linares, J. F., Cordes, T., Durán, Á., Reina‐Campos, M., Valencia, T., Ahn, C. S., Castilla, E. A., Moscat, J., Metallo, C. M., & Díaz-Meco, M. T. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.09.001 · Cited by 113 · see citing works
Sakamoto, A., Hino, S., Nagaoka, K., Anan, K., Takase, R., Matsumori, H., Ojima, H., Kanai, Y., Arita, K., & Nakao, M. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-1560 · Cited by 108 · see citing works
Wan, W., Peng, K., Li, M., Qin, L., Tong, Z., Yan, J., Shen, B., & Yu, C. (2017) · Oncogene · doi:10.1038/onc.2017.13 · Cited by 108 · see citing works
Meta‐analysis of clinical metabolic profiling studies in cancer: challenges and opportunities
Goveia, J., Pircher, A., Conradi, L., Kalucka, J. M., Lagani, V., Dewerchin, M. A., Eelen, G., DeBerardinis, R. J., Wilson, I. D., & Carmeliet, P. (2016) · EMBO Molecular Medicine · doi:10.15252/emmm.201606798 · Cited by 106 · see citing works
Self-citationCritical role for PI3-kinase in regulating the use of proteins as an amino acid source
Palm, W., Araki, J., King, B., Dematteo, R. G., & Thompson, C. B. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712726114 · Cited by 79 · see citing works
Stable Isotope Resolved Metabolomics Studies in ex vivo TIssue Slices
Fan, T. W. ‐., Lane, A. N., & Higashi, R. M. (2016) · BIO-PROTOCOL · doi:10.21769/bioprotoc.1730 · Cited by 68 · see citing works
Suppression of Gluconeogenic Gene Expression by LSD1-Mediated Histone Demethylation
Pan, D., Mao, C., & Wang, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066294 · Cited by 55 · see citing works
Shi, X., Tasdogan, A., Huang, F., Hu, Z., Morrison, S. J., & DeBerardinis, R. J. (2017) · Science Advances · doi:10.1126/sciadv.aao5268 · Cited by 47 · see citing works
Self-citationAddressing metabolic heterogeneity in clear cell renal cell carcinoma with quantitative Dixon MRI
Zhang, Y., Udayakumar, D., Cai, L., Hu, Z., Kapur, P., Kho, E.-Y., Pavía-Jiménez, A., Fulkerson, M., de Leon, A. D., Yuan, Q., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.94278 · Cited by 45 · see citing works
Self-citationMachida, K. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.7241 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Metabolic reprogramming and cancer progression
Faubert, B., Solmonson, A., & DeBerardinis, R. J. (2020) · Science · doi:10.1126/science.aaw5473 · Cited by 2,740 · see citing works
Self-citationMetabolism of immune cells in cancer
Leone, R. D., & Powell, J. D. (2020) · Nature Reviews Cancer · doi:10.1038/s41568-020-0273-y · Cited by 877 · see citing works
A non-canonical tricarboxylic acid cycle underlies cellular identity
Arnold, P. K., Jackson, B. T., Paras, K. I., Brunner, J. S., Hart, M. L., Newsom, O. J., Alibeckoff, S. P., Endress, J., Drill, E., Sullivan, L. B., et al. (2022) · Nature · doi:10.1038/s41586-022-04475-w · Cited by 304 · see citing works
Targeting Mitochondrial Complex I Overcomes Chemoresistance in High OXPHOS Pancreatic Cancer
Masoud, R., Reyes-Castellanos, G., Lac, S., Garcia, J., Dou, S., Shintu, L., Abdel Hadi, N., Gicquel, T., El Kaoutari, A., Diémé, B., et al. (2020) · Cell Reports Medicine · doi:10.1016/j.xcrm.2020.100143 · Cited by 175 · see citing works
Keoh, L. Q., Chiu, C.-F., & Ramasamy, T. S. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-10956-y · Cited by 66 · see citing works
Role of the tumor microenvironment in cancer hallmarks and targeted therapy (Review)
Naser, R., Fakhoury, I., El‑Fouani, A., Abi‑Habib, R., & El‑Sibai, M. (2022) · International Journal of Oncology · doi:10.3892/ijo.2022.5471 · Cited by 61 · see citing works
Metabolic impairment of non-small cell lung cancers by mitochondrial HSPD1 targeting
Parma, B., Ramesh, V., Gollavilli, P. N., Siddiqui, A., Pinna, L., Schwab, A., Marschall, S., Zhang, S., Pilarsky, C., Napoli, F., et al. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-02049-8 · Cited by 46 · see citing works
Rocha-Rodrigues, S., Matos, A., Afonso, J., Mendes-Ferreira, M., Abade, E., Teixeira, E., Silva, B., Murawska-Ciałowicz, E., Oliveira, M. J., & Ribeiro, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094469 · Cited by 17 · see citing works
- Authors
- Kim, J., & DeBerardinis, R. J.
- Affiliations
- University of Illinois Chicago (US)
- Children's Medical Center (US)
- Corresponding author
- DeBerardinis, Ralph J.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 30
- Issue
- 3
- Pages
- 434-446
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC6730674
- OpenAlex
- W2971544885
- Cited by
- 606
- References
- 156
- Citations by year
- 2026: 66 · 2025: 96 · 2024: 99 · 2023: 112 · 2022: 98 · 2021: 96 · 2020: 36 · 2019: 1
- FWCI
- 5.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute
- Moody Foundation
- Howard Hughes Medical Institute
- American Lung Association
- 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 › Cancer Research › Cancer, Lipids, and Metabolism
- Keywords
- tumor metabolic heterogeneity, cancer metabolism, tumor metabolic reprogramming, tumor microenvironment, metabolic vulnerability, glycolysis, solid tumors, tumor subtypes
- MeSH terms
- Animals, Glycolysis, Humans, Mitochondria, Neoplasms, T-Lymphocytes, Gene Expression Regulation, Neoplastic, Epigenesis, Genetic, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
