Cited by 341Cancer, Hypoxia, and MetabolismGlioma Diagnosis and TreatmentMetabolomics and Mass Spectrometry Studies

The DOI matches its Crossref record; 49 of the 49 references it cites were found in a registry or an index.

Metabolism of [U‐ 13 C]glucose in human brain tumors in vivo

Open access

Maher, Elizabeth A., Marin‐Valencia, Isaac, Bachoo, Robert M., Mashimo, Tomoyuki, Raisanen, Jack, Hatanpaa, Kimmo J., Jindal, Ashish, Jeffrey, F. Mark, Choi, Changho, Madden, Christopher, Mathews, Dana, Pascual, Juan M., Mickey, Bruce E., Malloy, Craig R., DeBerardinis, Ralph J.·2012·NMR in Biomedicine

DOI 10.1002/nbm.2794PMC PMC3406255

Open this paper in CoChat — free account

Abstract

Glioblastomas and brain metastases demonstrate avid uptake of 2-[(18) F]fluoro-2-deoxyglucose by positron emission tomography and display perturbations of intracellular metabolite pools by (1) H MRS. These observations suggest that metabolic reprogramming contributes to brain tumor growth in vivo. The Warburg effect, excess metabolism of glucose to lactate in the presence of oxygen, is a hallmark of cancer cells in culture. 2-[(18) F]Fluoro-2-deoxyglucose-positive tumors are assumed to metabolize glucose in a similar manner, with high rates of lactate formation relative to mitochondrial glucose oxidation, but few studies have specifically examined the metabolic fates of glucose in vivo. In particular, the capacity of human brain cancers to oxidize glucose in the tricarboxylic acid cycle is unknown. Here, we studied the metabolism of human brain tumors in situ. [U-(13) C]Glucose (uniformly labeled glucose, i.e. d-glucose labeled with (13) C in all six carbons) was infused during surgical resection, and tumor samples were subsequently subjected to (13) C NMR spectroscopy. The analysis of tumor metabolites revealed lactate production, as expected. We also determined that pyruvate dehydrogenase, turnover of the tricarboxylic acid cycle, anaplerosis and de novo glutamine and glycine synthesis contributed significantly to the ultimate disposition of glucose carbon. Surprisingly, less than 50% of the acetyl-coenzyme A pool was derived from blood-borne glucose, suggesting that additional substrates contribute to tumor bioenergetics. This study illustrates a convenient approach that capitalizes on the high information content of (13) C NMR spectroscopy and enables the analysis of intermediary metabolism in diverse cancers growing in their native microenvironment.

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

Crossref · 10.1002/nbm.2794

Cites

49 of 49 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197
On the origin of cancer cells
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425
IDH1 and IDH2 Mutations in Gliomas
Yan, H., Parsons, D. W., Jin, G., McLendon, R., Rasheed, B. A., Yuan, W., Kos, I., Batinic-Haberle, I., Jones, S., Riggins, G. J., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808710 · Cited by 5,847
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-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
The Biology of Cancer: Metabolic Reprogramming Fuels Cell Growth and Proliferation
DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G., & Thompson, C. B. (2008) · Cell Metabolism · doi:10.1016/j.cmet.2007.10.002 · Cited by 4,088
On Respiratory Impairment in Cancer Cells
Warburg, O. H. (1956) · Science · doi:10.1126/science.124.3215.269 · Cited by 3,472
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
Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis
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

Flagged first, then by citations

Show all 49 references

Sorted by citations

The emerging hallmarks of cancer metabolism
Pavlova, N. N., & Thompson, C. B. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2015.12.006 · Cited by 5,926
Fundamentals of Cancer Metabolism
DeBerardinis, R. J., & Chandel, N. S. (2016) · Science Advances · doi:10.1126/sciadv.1600200 · Cited by 3,013
Self-citation
Understanding the Intersections between Metabolism and Cancer Biology
Heiden, M. G. V., & DeBerardinis, R. J. (2017) · Cell · doi:10.1016/j.cell.2016.12.039 · Cited by 2,369
Metabolic pathways promoting cancer cell survival and growth
Boroughs, L. K., & DeBerardinis, R. J. (2015) · Nature Cell Biology · doi:10.1038/ncb3124 · Cited by 1,499
Mitochondria and Cancer
Zong, W., Rabinowitz, J. D., & White, E. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.011 · Cited by 1,330
Glutamine 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
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
Regulation of mammalian nucleotide metabolism and biosynthesis
Lane, A. N., & Fan, T. W.-M. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv047 · Cited by 959
The metabolism of cancer cells during metastasis
Bergers, G., & Fendt, S. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-020-00320-2 · Cited by 974
We need to talk about the Warburg effect
DeBerardinis, R. J., & Chandel, N. S. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0172-2 · Cited by 887
Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression
Li, Z., & Zhang, H. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-2070-4 · Cited by 840
Metabolic reprogramming and epigenetic modifications on the path to cancer
Sun, L., Zhang, H., & Gao, P. (2021) · Protein & Cell · doi:10.1007/s13238-021-00846-7 · Cited by 818
Environment impacts the metabolic dependencies of Ras-driven non-small cell lung cancer
Davidson, S. M., Papagiannakopoulos, T., Olenchock, B. A., Heyman, J. E., Keibler, M. A., Luengo, A., Bauer, M. R., Jha, A. K., O’Brien, J. P., Pierce, K. A., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.01.007 · Cited by 737
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
Self-citation
Mitochondrial Metabolism as a Target for Cancer Therapy
Vasan, K., Werner, M., & Chandel, N. S. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.06.019 · Cited by 762
Metabolites and the Tumour Microenvironment: From Cellular Mechanisms to Systemic Metabolism
Elia, I., & Haigis, M. C. (2021) · Nature Metabolism · doi:10.1038/s42255-020-00317-z · Cited by 651
Mechanisms and Implications of Metabolic Heterogeneity in Cancer
Kim, J., & DeBerardinis, R. J. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.08.013 · Cited by 606
Tissue of origin dictates branched-chain amino acid metabolism in mutant Kras -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
Glutamine synthetase activity fuels nucleotide biosynthesis and supports growth of glutamine-restricted glioblastoma
Tardito, S., Oudin, A., Ahmed, S. U., Fack, F., Keunen, O., Zheng, L., Miletic, H., Sakariassen, P. Ø., Weinstock, A., Wagner, A., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3272 · Cited by 557
Analysis of tumor metabolism reveals mitochondrial glucose oxidation in genetically diverse human glioblastomas in the mouse brain in vivo
Marin-Valencia, I., Yang, C., Mashimo, T., Cho, S., Baek, H., Yang, X.-L., Rajagopalan, K. N., Maddie, M., Vemireddy, V., Zhao, Z., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.05.001 · Cited by 529
Fatty acid oxidation: An emerging facet of metabolic transformation in cancer
Ma, Y., Temkin, S. M., Hawkridge, A. M., Guo, C., Wang, W., Wang, X., & Fang, X. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.08.006 · Cited by 554
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
Tumor glycolysis, an essential sweet tooth of tumor cells
Paul, S., Ghosh, S., & Kumar, S. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.09.007 · Cited by 449
HIFs, angiogenesis, and metabolism: Elusive enemies in breast cancer
de Heer, E. C., Jalving, M., & Harris, A. L. (2020) · Journal of Clinical Investigation · doi:10.1172/jci137552 · Cited by 372
Therapeutic Targeting of the Pyruvate Dehydrogenase Complex/Pyruvate Dehydrogenase Kinase (PDC/PDK) Axis in Cancer
Stacpoole, P. W. (2017) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djx071 · Cited by 418
Mitochondria as biosynthetic factories for cancer proliferation
Ahn, C. S., & Metallo, C. M. (2015) · Cancer & Metabolism · doi:10.1186/s40170-015-0128-2 · Cited by 399
Coupling Krebs cycle metabolites to signalling in immunity and cancer
Ryan, D. G., Murphy, M. P., Frezza, C., Prag, H. A., Chouchani, E. T., O’Neill, L. A., & Mills, E. L. (2018) · Nature Metabolism · doi:10.1038/s42255-018-0014-7 · Cited by 398
Similarities and Distinctions of Cancer and Immune Metabolism in Inflammation and Tumors
Andrejeva, G., & Rathmell, J. C. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.06.004 · Cited by 374
Mitochondrial ubiquinol oxidation is necessary for tumour growth
Martínez‐Reyes, I., Cardona, L. R., Kong, H., Vasan, K., McElroy, G. S., Werner, M., Kihshen, H., Reczek, C. R., Weinberg, S. E., Gao, P., et al. (2020) · Nature · doi:10.1038/s41586-020-2475-6 · Cited by 370
Metabolic Reprogramming in Glioma
Strickland, M., & Stoll, E. A. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00043 · Cited by 357
The metabolic fate of acetate in cancer
Schug, Z. T., Vande Voorde, J., & Gottlieb, E. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.87 · Cited by 331
Inhibition of SOAT1 Suppresses Glioblastoma Growth via Blocking SREBP-1–Mediated Lipogenesis
Geng, F., Cheng, X., Wu, X., Yoo, J. Y., Cheng, C., Guo, J. Y., Mo, X. M., Ru, P., Hurwitz, B. S., Kim, S., et al. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-2973 · Cited by 330
Metabolic reprogramming in glioblastoma: the influence of cancer metabolism on epigenetics and unanswered questions
Agnihotri, S., & Zadeh, G. M. (2015) · Neuro-Oncology · doi:10.1093/neuonc/nov125 · Cited by 302
ERGO: A pilot study of ketogenic diet in recurrent glioblastoma
Rieger, J., Bähr, O., Maurer, G. D., Hattingen, E., Franz, K., Brucker, D. P., Walenta, S., Kämmerer, U., Coy, J. F., Weller, M., et al. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2382 · Cited by 284
Isotope tracing of human clear cell renal cell carcinomas demonstrates suppressed glucose oxidation in vivo
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
Self-citation
Breast Cancer-Derived Lung Metastases Show Increased Pyruvate Carboxylase-Dependent Anaplerosis
Christen, S., Lorendeau, D., Schmieder, R., Broekaert, D., Metzger, K., Veys, K., Elia, I., Buescher, J. M., Orth, M. F., Davidson, S. M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.042 · Cited by 258
Mitochondria, Energetics, Epigenetics, and Cellular Responses to Stress
Shaughnessy, D. T., McAllister, K. A., Worth, L., Haugen, A. C., Meyer, J. N., Domann, F. E., Houten, B. V., Mostoslavsky, R., Bultman, S. J., Baccarelli, A., et al. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1408418 · Cited by 272
Oncogenic Myc Induces Expression of Glutamine Synthetase through Promoter Demethylation
Bott, A. J., Peng, I., Fan, Y., Faubert, B., Zhao, L. H., Li, J., Neidler, S., Sun, Y., Jaber, N. L., Krokowski, D., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.09.025 · Cited by 259
Fatty acid oxidation is required for the respiration and proliferation of malignant glioma cells
Lin, H., Patel, S., Affleck, V., Wilson, I., Turnbull, D. M., Joshi, A. R., Maxwell, R. J., & Stoll, E. A. (2016) · Neuro-Oncology · doi:10.1093/neuonc/now128 · Cited by 258
Metabolic Hallmarks of Metastasis Formation
Elia, I., Doglioni, G., & Fendt, S. (2018) · Trends in Cell Biology · doi:10.1016/j.tcb.2018.04.002 · Cited by 253
The Tumor Metabolic Microenvironment: Lessons from Lactate
García‐Cañaveras, J. C., Chen, L., & Rabinowitz, J. D. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3726 · Cited by 252
Wnt and PI3K/Akt/mTOR Survival Pathways as Therapeutic Targets in Glioblastoma
Behrooz, A. B., Talaie, Z., Jusheghani, F., Łoś, M., Klonisch, T. C., & Ghavami, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031353 · Cited by 253
The Warburg effect: a signature of mitochondrial overload
Wang, Y., & Patti, G. J. (2023) · Trends in Cell Biology · doi:10.1016/j.tcb.2023.03.013 · Cited by 250
Nuclear GTPSCS functions as a lactyl-CoA synthetase to promote histone lactylation and gliomagenesis
Liu, R., Ren, X., Park, Y. E., Feng, H., Sheng, X., Song, X., AminiTabrizi, R., Shah, H., Li, L., Zhang, Y., et al. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.11.005 · Cited by 253
Acetate Metabolism in Physiology, Cancer, and Beyond
Bose, S., Ramesh, V., & Locasale, J. W. (2019) · Trends in Cell Biology · doi:10.1016/j.tcb.2019.05.005 · Cited by 236
Metabolic Reprogramming of Cancer Cells during Tumor Progression and Metastasis
Ohshima, K., & Morii, E. (2021) · Metabolites · doi:10.3390/metabo11010028 · Cited by 236
The Warburg metabolism fuels tumor metastasis
Lu, J. (2019) · Cancer and Metastasis Reviews · doi:10.1007/s10555-019-09794-5 · Cited by 221
Metabolic Imaging of the Human Brain with Hyperpolarized 13C Pyruvate Demonstrates 13C Lactate Production in Brain Tumor Patients
Miloushev, V. Z., Granlund, K. L., Boltyanskiy, R., Lyashchenko, S. K., DeAngelis, L. M., Mellinghoff, I. K., Brennan, C. W., Tabar, V., Yang, J. T., Holodny, A. I., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0221 · Cited by 218
Applications of NMR spectroscopy to systems biochemistry
Fan, T. W. ‐., & Lane, A. N. (2016) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2016.01.005 · Cited by 220
Targeting Cancer Metabolism: Dietary and Pharmacologic Interventions
Vernieri, C., Casola, S., Foiani, M., Pietrantonio, F., de Braud, F., & Longo, V. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0615 · Cited by 202
Glutamine anabolism plays a critical role in pancreatic cancer by coupling carbon and nitrogen metabolism
Bott, A. J., Shen, J., Tonelli, C., Zhan, L., Sivaram, N., Jiang, Y.-P., Yu, X., Bhatt, V., Chiles, E., Zhong, H., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.09.056 · Cited by 185
Interruption of lactate uptake by inhibiting mitochondrial pyruvate transport unravels direct antitumor and radiosensitizing effects
Corbet, C., Bastien, E., Draoui, N., Doix, B., Mignion, L., Jordan, B. F., Marchand, A., Vanherck, J., Chaltin, P., Schakman, O., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03525-0 · Cited by 189
Acyl-CoA-Binding Protein Drives Glioblastoma Tumorigenesis by Sustaining Fatty Acid Oxidation
Duman, C., Yaqubi, K., Hoffmann, A., Açıkgöz, A. A., Korshunov, A., Bendszus, M., Herold‐Mende, C. C., Liu, H., & Alfonso, J. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.04.004 · Cited by 195
Applications 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
Famine versus feast: understanding the metabolism of tumors in vivo
Mayers, J. R., & Heiden, M. G. V. (2015) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2015.01.004 · Cited by 190
Metabolic Heterogeneity of Cancer Cells: An Interplay between HIF-1, GLUTs, and AMPK
Moldogazieva, N. T., Mokhosoev, I. M., & Terentiev, A. A. (2020) · Cancers · doi:10.3390/cancers12040862 · Cited by 181
Metabolic heterogeneity in cancer
Demicco, M., Liu, X., Leithner, K., & Fendt, S. (2024) · Nature Metabolism · doi:10.1038/s42255-023-00963-z · Cited by 186
Harnessing metabolic dependencies in pancreatic cancers
Encarnación-Rosado, J., & Kimmelman, A. C. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-021-00431-7 · Cited by 190
Challenges in the Treatment of Glioblastoma: Multisystem Mechanisms of Therapeutic Resistance
Noch, E., Ramakrishna, R. R., & Magge, R. (2018) · World Neurosurgery · doi:10.1016/j.wneu.2018.04.022 · Cited by 178
Glucose Metabolism on Tumor Plasticity, Diagnosis, and Treatment
Lin, X., Xiao, Z., Chen, T., Liang, S. H., & Guo, H. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00317 · Cited by 185
Cancer cell metabolism and mitochondria: Nutrient plasticity for TCA cycle fueling
Corbet, C., & Féron, O. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.01.002 · Cited by 174
Targeting pyruvate dehydrogenase kinase signaling in the development of effective cancer therapy
Anwar, S., Shamsi, A., Mohammad, T., Islam, A., & Hassan, M. I. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188568 · Cited by 168
Impact of cancer metabolism on therapy resistance – Clinical implications
Gonçalves, A. C., Richiardone, E., Jorge, J., Polónia, B. R. G., Xavier, C. P. R., Salaroglio, I. C., Riganti, C., Vasconcelos, M. H., Corbet, C., & Sarmento‐Ribeiro, A. B. (2021) · Drug Resistance Updates · doi:10.1016/j.drup.2021.100797 · Cited by 176
Mitochondrial Oxidative Stress and “Mito-Inflammation”: Actors in the Diseases
Patergnani, S., Bouhamida, E., Leo, S., Pinton, P., & Rimessi, A. (2021) · Biomedicines · doi:10.3390/biomedicines9020216 · Cited by 178
Hyperpolarized Magnetic Resonance as a Sensitive Detector of Metabolic Function
Comment, A., & Merritt, M. E. (2014) · Biochemistry · doi:10.1021/bi501225t · Cited by 161
How and Why Are Cancers Acidic? Carbonic Anhydrase IX and the Homeostatic Control of Tumour Extracellular pH
Lee, S., & Griffiths, J. R. (2020) · Cancers · doi:10.3390/cancers12061616 · Cited by 163
Glioblastoma Stem-Like Cells, Metabolic Strategy to Kill a Challenging Target
Garnier, D., Renoult, O., Alves‐Guerra, M., Paris, F., & Pecqueur, C. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00118 · Cited by 161
Metabolic Abnormalities in Glioblastoma and Metabolic Strategies to Overcome Treatment Resistance
Zhou, W., & Wahl, D. R. (2019) · Cancers · doi:10.3390/cancers11091231 · Cited by 152
Bevacizumab treatment induces metabolic adaptation toward anaerobic metabolism in glioblastomas
Fack, F., Espedal, H., Keunen, O., Golebiewska, A., Obad, N., Harter, P. N., Mittelbronn, M. G. A., Bähr, O., Weyerbrock, A., Stuhr, L. E. B., et al. (2014) · Acta Neuropathologica · doi:10.1007/s00401-014-1352-5 · Cited by 146
Coordinated Metabolic Transitions During Drosophila Embryogenesis and the Onset of Aerobic Glycolysis
Tennessen, J. M., Bertagnolli, N. M., Evans, J. M., Sieber, M., Cox, J. E., & Thummel, C. S. (2014) · G3 Genes Genomes Genetics · doi:10.1534/g3.114.010652 · Cited by 141
Mitochondrial complex I promotes kidney cancer metastasis
Bezwada, D., Perelli, L., Lesner, N. P., Cai, L., Brooks, B., Wu, Z., Vu, H., Sondhi, V., Cassidy, D. L., Kasitinon, S. Y., et al. (2024) · Nature · doi:10.1038/s41586-024-07812-3 · Cited by 158
mTORC2 in the center of cancer metabolic reprogramming
Masui, K., Cavenee, W. K., & Mischel, P. S. (2014) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2014.04.002 · Cited by 140
Sensitization of Glioblastoma Cells to Irradiation by Modulating the Glucose Metabolism
Shen, H. M., Hau, E. K. C., Joshi, S. M., Dilda, P. J., & McDonald, K. L. (2015) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-15-0247 · Cited by 136
Metabolic Reprogramming in Brain Tumors
Venneti, S., & Thompson, C. B. (2017) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044329 · Cited by 139
Calculation of ATP production rates using the Seahorse XF Analyzer
Desousa, B. R., Kim, K. K. O., Jones, A. E., Ball, A. B., Hsieh, W. Y., Swain, P. M., Morrow, D., Brownstein, A. J., Ferrick, D. A., Shirihai, O. S., et al. (2023) · EMBO Reports · doi:10.15252/embr.202256380 · Cited by 135
Evolving Lessons on the Complex Role of AMPK in Normal Physiology and Cancer
Dasgupta, B., & Chhipa, R. R. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.11.007 · Cited by 121
Non-invasive metabolic imaging of brain tumours in the era of precision medicine
Kim, M. M., Parolia, A., Dunphy, M. P., & Venneti, S. (2016) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.108 · Cited by 121
Nutrient metabolism and cancer in the in vivo context: a metabolic game of give and take
Altea‐Manzano, P., Cuadros, A. M., Broadfield, L. A., & Fendt, S. (2020) · EMBO Reports · doi:10.15252/embr.202050635 · Cited by 123
Noninvasive liquid diet delivery of stable isotopes into mouse models for deep metabolic network tracing
Sun, R. C., Fan, T. W. ‐., Deng, P., Higashi, R. M., Lane, A. N., Le, A.-T., Scott, T. L., Sun, Q., Warmoes, M. O., & Yang, Y. (2017) · Nature Communications · doi:10.1038/s41467-017-01518-z · Cited by 103
Critical role for arginase 2 in obesity-associated pancreatic cancer
Zaytouni, T., Tsai, P.-Y., Hitchcock, D. S., DuBois, C. D., Freinkman, E., Lin, L., Morales‐Oyarvide, V., Lenehan, P. J., Wolpin, B. M., Mino-Kenudson, M. A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00331-y · Cited by 106
Serotonin activates glycolysis and mitochondria biogenesis in human breast cancer cells through activation of the Jak1/STAT3/ERK1/2 and adenylate cyclase/PKA, respectively
Sola‐Penna, M., Paixão, L. P., Branco, J. R., Ochioni, A. C., Albanese, J. M., Mundim, D. M., Baptista‐de‐Souza, D., Figueiredo, C. P., Coelho, W. S., Marcondes, M. C., et al. (2019) · British Journal of Cancer · doi:10.1038/s41416-019-0640-1 · Cited by 103
Exploring cancer metabolism using stable isotope-resolved metabolomics (SIRM)
Bruntz, R. C., Lane, A. N., Higashi, R. M., & Fan, T. W. ‐. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r117.776054 · Cited by 107
Reprogramming metabolism by targeting sirtuin 6 attenuates retinal degeneration
Zhang, L., Du, J., Justus, S., Hsu, C., Bonet‐Ponce, L., Wu, W.-H., Tsai, Y.-T., Wu, W., Jia, Y., Duong, J., et al. (2016) · Journal of Clinical Investigation · doi:10.1172/jci86905 · Cited by 102
Stable isotope tracing to assess tumor metabolism in vivo
Faubert, B., Tasdogan, A., Morrison, S. J., Mathews, T. P., & DeBerardinis, R. J. (2021) · Nature Protocols · doi:10.1038/s41596-021-00605-2 · Cited by 101
The Crosstalk Between Cell Adhesion and Cancer Metabolism
Sousa, B., Pereira, J., & Paredes, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20081933 · Cited by 106
Targeting ACSS2 with a Transition-State Mimetic Inhibits Triple-Negative Breast Cancer Growth
Miller, K. D., Pniewski, K. A., Perry, C. E., Papp, S. B., Shaffer, J. D., Velasco‐Silva, J. N., Casciano, J. C., Aramburu, T. M., Srikanth, Y. V. V., Cassel, J. A., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-20-1847 · Cited by 103
ERGO2: A Prospective, Randomized Trial of Calorie-Restricted Ketogenic Diet and Fasting in Addition to Reirradiation for Malignant Glioma
Voß, M., Wagner, M., von Mettenheim, N., Harter, P. N., Wenger, K. J., Franz, K., Bojunga, J., Vetter, M., Gerlach, R., Glatzel, M., et al. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.06.021 · Cited by 99
Antioxidants in brain tumors: current therapeutic significance and future prospects
Qi, X., Jha, S. K., Jha, N. K., Dewanjee, S., Dey, A., Deka, R., Pritam, P., Ramgopal, K., Liu, W.-T., & Hou, K. (2022) · Molecular Cancer · doi:10.1186/s12943-022-01668-9 · Cited by 100
Analysis of Hypoxia-Induced Metabolic Reprogramming
Yang, C., Jiang, L., Zhang, H., Shimoda, L. A., DeBerardinis, R. J., & Semenza, G. L. (2014) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-416618-9.00022-4 · Cited by 98
Metabolic reprogramming in tumors: Contributions of the tumor microenvironment
Lane, A. N., Higashi, R. M., & Fan, T. W.-M. (2020) · Genes & Diseases · doi:10.1016/j.gendis.2019.10.007 · Cited by 91
Metabolic requirements of pulmonary fibrosis: role of fibroblast metabolism
Hamanaka, R. B., & Mutlu, G. M. (2021) · FEBS Journal · doi:10.1111/febs.15693 · Cited by 94
Both GLS silencing and GLS2 overexpression synergize with oxidative stress against proliferation of glioma cells
Martín‐Rufián, M., Nascimento-Gomes, R., Higuero, A., Crisma, A. R., Campos-Sandoval, J. A., Gómez-García, M. C., Cardona, C., Cheng, T., Lobo, C., Segura, J. A., et al. (2013) · Journal of Molecular Medicine · doi:10.1007/s00109-013-1105-2 · Cited by 88
Rare insights into cancer biology
Adam, J., Yang, M., Soga, T., & Pollard, P. J. (2013) · Oncogene · doi:10.1038/onc.2013.222 · Cited by 90
Metabolic Reprogramming of Non-Hodgkin's B-Cell Lymphomas and Potential Therapeutic Strategies
Ricci, J., & Chiche, J. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00556 · Cited by 87
Modeling the energetic cost of cancer as a result of altered energy metabolism: implications for cachexia
Friesen, D. E., Baracos, V. E., & Tuszyński, J. A. (2015) · Theoretical Biology and Medical Modelling · doi:10.1186/s12976-015-0015-0 · Cited by 86
Magnetic Resonance Spectroscopy and its Clinical Applications: A Review
Faghihi, R., Zeinali-Rafsanjani, B., Mosleh‐Shirazi, M. A., Saeedi-Moghadam, M., Lotfi, M., Jalli, R., & Iravani, V. (2017) · Journal of medical imaging and radiation sciences · doi:10.1016/j.jmir.2017.06.004 · Cited by 85
Metabolic pathway analysis using stable isotopes in patients with cancer
Bartman, C., Faubert, B., Rabinowitz, J. D., & DeBerardinis, R. J. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00632-z · Cited by 93
The evolution of the cancer stem cell state in glioblastoma: emerging insights into the next generation of functional interactions
Mitchell, K., Troike, K. M., Silver, D. J., & Lathia, J. D. (2020) · Neuro-Oncology · doi:10.1093/neuonc/noaa259 · Cited by 84
Brain metabolism modulates neuronal excitability in a mouse model of pyruvate dehydrogenase deficiency
Jakkamsetti, V., Marin‐Valencia, I., Ma, Q., Good, L. B., Terrill, T., Rajasekaran, K., Pichumani, K., Khemtong, C., Hooshyar, M. A., Sundarrajan, C., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aan0457 · Cited by 77
Mitochondria Transfer from Mesenchymal Stem Cells Confers Chemoresistance to Glioblastoma Stem Cells through Metabolic Rewiring
Nakhle, J., Khattar, K., Özkan, T., Boughlita, A., Moussa, D. A., Darlix, A., Lorcy, F., Rigau, V., Bauchet, L., Gerbal‐Chaloin, S., et al. (2023) · Cancer Research Communications · doi:10.1158/2767-9764.crc-23-0144 · Cited by 76

Authors: 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., Mathews, D., Pascual, J. M., Mickey, B. E., Malloy, C. R., & DeBerardinis, R. J.
Affiliations: Harold C. Simmons Comprehensive Cancer Center (US)
The University of Texas Southwestern Medical Center (US)
VA North Texas Health Care System (US)
Corresponding author: Maher, Elizabeth A.
DeBerardinis, Ralph J.
ORCID: Maher, Elizabeth A.
Bachoo, Robert M.
Mashimo, Tomoyuki
Hatanpaa, Kimmo J.
Jindal, Ashish
Choi, Changho
Madden, Christopher
Pascual, Juan M.
Mickey, Bruce E.
Malloy, Craig R.
DeBerardinis, Ralph J.
Venue: NMR in Biomedicine
Publisher: Wiley
Published: 2012-03-15
Volume: 25
Issue: 11
Pages: 1234-1244
ISSN: 0952-3480 (ISSN-L)
1099-1492
DOI: 10.1002/nbm.2794
PMC: PMC3406255
OpenAlex: W2114805483
Cited by: 341
References: 49
Citations by year: 2026: 16 · 2025: 22 · 2024: 21 · 2023: 19 · 2022: 28 · 2021: 41 · 2020: 28 · 2019: 30 · 2018: 22 · 2017: 18 · 2016: 34 · 2015: 33 · 2014: 14 · 2013: 11 · 2012: 4
FWCI: 6.54
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: NMR in Biomedicine (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Cancer Prevention and Research Institute of Texas
National Institutes of Health
National Cancer Institute (R01CA154843, R01CA157996)
National Institute of Neurological Disorders and Stroke (RC1NS0760675, RC1NS070675)
National Center for Research Resources (P41RR002584, RR‐02584)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Oncology › Glioma Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
Keywords: brain tumors, glioblastoma, brain metastases, glucose metabolism, Warburg effect, lactic acid production, TCA cycle, pyruvate dehydrogenase, anaplerosis, acetyl-CoA, tumor bioenergetics, metabolic reprogramming
MeSH terms: Acetyl Coenzyme A, Blood Glucose, Brain Neoplasms, Breast Neoplasms, Carbon Isotopes, Carcinoma, Non-Small-Cell Lung, Citric Acid Cycle, Female, Glioblastoma, Glucose, Glycine, Glycolysis, Humans, Oxidation-Reduction

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

Metabolism of [U‐ 13 C]glucose in human brain tumors in vivo

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks