Metabolic Constants and Plasticity of Cancer Cells in a Limiting Glucose and Glutamine Microenvironment—A Pyruvate Perspective

The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerou...

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Published in:Frontiers in oncology Vol. 10; p. 596197
Main Author: Otto, Angela M.
Format: Journal Article
Language:English
Published: Switzerland Frontiers Media S.A 08.12.2020
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ISSN:2234-943X, 2234-943X
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Abstract The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate 13 C 6 -glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. 13 C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.
AbstractList The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate 13 C 6 -glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. 13 C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.
The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate 13C6-glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. 13C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.
The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate C -glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.
The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate 13C6-glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. 13C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their vitality and propagation. Glucose and glutamine are central metabolites for catabolic and anabolic metabolism, which is in the limelight of numerous diagnostic methods and therapeutic targeting. Understanding tumor metabolism in conditions of nutrient depletion is important for such applications and for interpreting the readouts. To exemplify the metabolic network of tumor cells in a model system, the fate 13C6-glucose was tracked in a breast cancer cell line growing in variable low glucose/low glutamine conditions. 13C-glucose-derived metabolites allowed to deduce the engagement of metabolic pathways, namely glycolysis, the TCA-cycle including glutamine and pyruvate anaplerosis, amino acid synthesis (serine, glycine, aspartate, glutamate), gluconeogenesis, and pyruvate replenishment. While the metabolic program did not change, limiting glucose and glutamine supply reduced cellular metabolite levels and enhanced pyruvate recycling as well as pyruvate carboxylation for entry into the TCA-cycle. Otherwise, the same metabolic pathways, including gluconeogenesis, were similarly engaged with physiologically saturating as with limiting glucose and glutamine. Therefore, the metabolic plasticity in precarious nutritional microenvironment does not require metabolic reprogramming, but is based on dynamic changes in metabolite quantity, reaction rates, and directions of the existing metabolic network.
Author Otto, Angela M.
AuthorAffiliation Munich School of BioEngineering, Technical University of Munich , Garching , Germany
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Cites_doi 10.1111/j.1432-1033.1982.tb05851.x
10.1111/eva.12015
10.1208/s12248-008-9022-y
10.1002/mc.2940080112
10.1038/nature10350
10.1038/nrc.2016.81
10.1016/j.ymben.2017.02.002
10.1016/j.cell.2016.12.039
10.1158/0008-5472.CAN-09-3556
10.1016/j.cell.2011.02.013
10.1007/s11306-007-0094-y
10.1007/BF01372723
10.1007/BF00396375
10.1016/j.molcel.2015.08.013
10.1083/jcb.200703099
10.1111/febs.12864
10.1016/0005-2744(71)90211-7
10.3390/cells8101113
10.1038/nature11540
10.1016/j.cmet.2011.12.009
10.1016/j.cels.2018.06.003
10.1016/j.molcel.2014.09.024
10.1016/j.copbio.2015.02.003
10.1042/bj1480085
10.1016/j.bbadis.2016.11.021
10.2174/1574892811308010085
10.1002/jcb.25038
10.1073/pnas.70.6.1775
10.3892/ijmm_00000173
10.1074/jbc.271.25.14883
10.1016/j.molcel.2015.09.025
10.1042/bj1900705
10.1186/s12964-019-0332-8
10.1074/jbc.RA119.009093
10.1073/pnas.93.5.1847
10.1079/BJN2001454
10.4161/cc.9.19.13302
10.1016/j.bbcan.2012.07.001
10.1074/jbc.M114.566927
10.1002/glia.1054
10.1016/j.biochi.2015.09.017
10.1038/msb.2011.56
10.1038/onc.2014.47
10.1016/j.tcb.2017.05.001
10.4161/cc.9.24.14230
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Keywords pyruvate replenishment
13C-glucose tracing
TCA-cycle
anaplerosis
nutrient deprivation
glycolysis
glutamine
metabolic network
Language English
License Copyright © 2020 Otto.
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This article was submitted to Cancer Metabolism, a section of the journal Frontiers in Oncology
Reviewed by: Khalid Omer Alfarouk, Alfarouk Biomedical Research LLC, United States; Angela Ostuni, University of Basilicata, Italy
Edited by: Fatima Baltazar, University of Minho, Portugal
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References Glinghammar (B37) 2009; 23
Vacanti Nathaniel (B36) 2014; 56
Zhang (B35) 2019; 17
Gkiouli (B27) 2019; 8
Zwingmann (B42) 2001; 34
Icard (B4) 2012; 1826
Groen (B41) 1982; 122
Leithner (B43) 2015; 34
Yang (B47) 2016; 16
Vander Heiden (B3) 2017; 168
Otto (B15) 2015; 116
Jimenez de Asua (B34) 1971; 235
Buescher (B20) 2015; 34
Takahashi (B16) 1993; 8
Dang (B28) 2010; 70
Alfarouk (B5) 2013; 6
Felig (B8) 1973; 70
Tanner (B24) 2018; 7
Kallinowski (B1) 1987; 113
Reshkin (B6) 2013; 8
Marín-Hernández (B22) 2014; 281
Dubik (B17) 1987; 47
Gullino (B7) 1964; 24
Stark (B10) 2015; 118
Mazurek (B33) 2002; 87
Dong (B21) 2017; 43
Schaefer (B2) 1993; 119
Hanahan (B9) 2011; 144
Halestrap (B38) 1975; 148
Méndez-Lucas (B44) 2014; 289
Yang (B18) 2008; 4
Ganapathy (B25) 2008; 10
Yuneva (B13) 2007; 178
Vincent (B46) 2015; 60
Chen (B12) 2010; 9
Contreras-Baeza (B26) 2019; 294
Newman (B32) 2017; 27
Dang (B11) 2010; 9
Possemato (B31) 2011; 476
Lazo (B39) 1980; 190
Zamora-Leon (B23) 1996; 93
UtsunomiyaTate (B30) 1996; 271
Montal Emily (B45) 2015; 60
Le (B19) 2012; 15
Gaglio (B14) 2011; 7
Phannasil (B40) 2017; 1863
Chaneton (B29) 2012; 491
References_xml – volume: 122
  start-page: 87
  year: 1982
  ident: B41
  article-title: Intracellular Compartmentation and Control of Alanine Metabolism in Rat Liver Parenchymal Cells
  publication-title: Eur J Biochem
  doi: 10.1111/j.1432-1033.1982.tb05851.x
– volume: 6
  start-page: 46
  year: 2013
  ident: B5
  article-title: Riparian ecosystems in human cancers
  publication-title: Evol Appl
  doi: 10.1111/eva.12015
– volume: 10
  year: 2008
  ident: B25
  article-title: Sodium-coupled monocarboxylate transporters in normal tissues and in cancer
  publication-title: AAPS J
  doi: 10.1208/s12248-008-9022-y
– volume: 8
  start-page: 58
  year: 1993
  ident: B16
  article-title: Protein-synthesis dependent cytoplasmic translocation of p53 protein after serum stimulation of growth-arrested MCF-7 cells
  publication-title: Mol Carcinogenesis
  doi: 10.1002/mc.2940080112
– volume: 476
  start-page: 346
  year: 2011
  ident: B31
  article-title: Functional genomics reveal that the serine synthesis pathway is essential in breast cancer
  publication-title: Nature
  doi: 10.1038/nature10350
– volume: 16
  start-page: 650
  year: 2016
  ident: B47
  article-title: Serine and one-carbon metabolism in cancer
  publication-title: Nat Rev Cancer
  doi: 10.1038/nrc.2016.81
– volume: 43
  year: 2017
  ident: B21
  article-title: Review of metabolic pathways activated in cancer cells as determined through isotopic labeling and network analysis
  publication-title: Metab Eng
  doi: 10.1016/j.ymben.2017.02.002
– volume: 168
  year: 2017
  ident: B3
  article-title: Understanding the Intersections between Metabolism and Cancer Biology
  publication-title: Cell
  doi: 10.1016/j.cell.2016.12.039
– volume: 70
  year: 2010
  ident: B28
  article-title: Rethinking the Warburg Effect with Myc Micromanaging Glutamine Metabolism
  publication-title: Cancer Res
  doi: 10.1158/0008-5472.CAN-09-3556
– volume: 144
  year: 2011
  ident: B9
  article-title: Hallmarks of cancer: the next generation
  publication-title: Cell
  doi: 10.1016/j.cell.2011.02.013
– volume: 4
  start-page: 13
  year: 2008
  ident: B18
  article-title: Profiling of central metabolism in human cancer cells by two-dimensional NMR, GC-MS analysis, and isotopomer modeling
  publication-title: Metabolomics
  doi: 10.1007/s11306-007-0094-y
– volume: 119
  start-page: 599
  year: 1993
  ident: B2
  article-title: Microregional distributions of glucose, lactate, ATP and tissue pH in experimental tumours upon local hyperthermia and/or hyperglycaemia
  publication-title: J Cancer Res Clin Oncol
  doi: 10.1007/BF01372723
– volume: 113
  year: 1987
  ident: B1
  article-title: L-glutamine: a major substrate for tumor cells in vivo
  publication-title: J Cancer Res Clin Oncol
  doi: 10.1007/BF00396375
– volume: 60
  start-page: 195
  year: 2015
  ident: B46
  article-title: Mitochondrial Phosphoenolpyruvate Carboxykinase Regulates Metabolic Adaptation and Enables Glucose-Independent Tumor Growth
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2015.08.013
– volume: 178
  start-page: 93
  year: 2007
  ident: B13
  article-title: Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells
  publication-title: J Cell Biol
  doi: 10.1083/jcb.200703099
– volume: 281
  year: 2014
  ident: B22
  article-title: Modeling cancer glycolysis under hypoglycemia, and the role played by the differential expression of glycolytic isoforms
  publication-title: FEBS J
  doi: 10.1111/febs.12864
– volume: 235
  year: 1971
  ident: B34
  article-title: Some kinetic differences between the M isoenzymes of pyruvate kinase from liver and muscle
  publication-title: Biochim Biophys Acta
  doi: 10.1016/0005-2744(71)90211-7
– volume: 8
  year: 2019
  ident: B27
  article-title: Diverse Roads Taken by 13C-Glucose-Derived Metabolites in Breast Cancer Cells Exposed to Limiting Glucose and Glutamine Conditions
  publication-title: Cells
  doi: 10.3390/cells8101113
– volume: 491
  year: 2012
  ident: B29
  article-title: Serine is a natural ligand and allosteric activator of pyruvate kinase M2
  publication-title: Nature
  doi: 10.1038/nature11540
– volume: 15
  year: 2012
  ident: B19
  article-title: Glucose-Independent Glutamine Metabolism via TCA Cycling for Proliferation and Survival in B Cells
  publication-title: Cell Metab
  doi: 10.1016/j.cmet.2011.12.009
– volume: 7
  start-page: 49
  year: 2018
  ident: B24
  article-title: Four Key Steps Control Glycolytic Flux in Mammalian Cells
  publication-title: Cell Syst
  doi: 10.1016/j.cels.2018.06.003
– volume: 56
  year: 2014
  ident: B36
  article-title: Regulation of Substrate Utilization by the Mitochondrial Pyruvate Carrier
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2014.09.024
– volume: 34
  start-page: 189
  year: 2015
  ident: B20
  article-title: A roadmap for interpreting 13C metabolite labeling patterns from cells
  publication-title: Curr Opin Biotechnol
  doi: 10.1016/j.copbio.2015.02.003
– volume: 148
  start-page: 85
  year: 1975
  ident: B38
  article-title: The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors
  publication-title: Biochem J
  doi: 10.1042/bj1480085
– volume: 1863
  year: 2017
  ident: B40
  article-title: Mass spectrometry analysis shows the biosynthetic pathways supported by pyruvate carboxylase in highly invasive breast cancer cells
  publication-title: Biochim Biophys Acta (BBA) - Mol Basis Dis
  doi: 10.1016/j.bbadis.2016.11.021
– volume: 8
  start-page: 85
  year: 2013
  ident: B6
  article-title: Na+-H+ Exchanger, pH Regulation and Cancer
  publication-title: Rec Pat Anti Canc Drug Dis
  doi: 10.2174/1574892811308010085
– volume: 116
  year: 2015
  ident: B15
  article-title: NADH-Linked Metabolic Plasticity of MCF-7 Breast Cancer Cells Surviving in a Nutrient-Deprived Microenvironment
  publication-title: J Cell Biochem
  doi: 10.1002/jcb.25038
– volume: 70
  year: 1973
  ident: B8
  article-title: Evidence of inter-organ amino-acid transport by blood cells in humans
  publication-title: Proc Natl Acad Sci USA
  doi: 10.1073/pnas.70.6.1775
– volume: 23
  year: 2009
  ident: B37
  article-title: Detection of the mitochondrial and catalytically active alanine aminotransferase in human tissues and plasma
  publication-title: Intl J Mol Med
  doi: 10.3892/ijmm_00000173
– volume: 47
  year: 1987
  ident: B17
  article-title: Stimulation of c-myc oncogene expression associated with estrogen-induced proliferation of human breast cancer cells
  publication-title: Cancer Res
– volume: 271
  year: 1996
  ident: B30
  article-title: Cloning and functional characterization of a system ASC-like Na+-dependent neutral amino acid transporter
  publication-title: J Biol Chem
  doi: 10.1074/jbc.271.25.14883
– volume: 60
  year: 2015
  ident: B45
  article-title: PEPCK Coordinates the Regulation of Central Carbon Metabolism to Promote Cancer Cell Growth
  publication-title: Mol Cell
  doi: 10.1016/j.molcel.2015.09.025
– volume: 190
  year: 1980
  ident: B39
  article-title: Pyruvate dehydrogenase complex of ascites tumour. Activation by AMP and other properties of potential significance in metabolic regulation
  publication-title: Biochem J
  doi: 10.1042/bj1900705
– volume: 17
  start-page: 23
  year: 2019
  ident: B35
  article-title: Low levels of pyruvate induced by a positive feedback loop protects cholangiocarcinoma cells from apoptosis
  publication-title: Cell Communication Signaling
  doi: 10.1186/s12964-019-0332-8
– volume: 294
  year: 2019
  ident: B26
  article-title: Monocarboxylate transporter 4 (MCT4) is a high affinity transporter capable of exporting lactate in high-lactate microenvironments
  publication-title: J Biol Chem
  doi: 10.1074/jbc.RA119.009093
– volume: 93
  year: 1996
  ident: B23
  article-title: Expression of the fructose transporter GLUT5 in human breast cancer
  publication-title: Proc Natl Acad Sci U States America
  doi: 10.1073/pnas.93.5.1847
– volume: 87
  year: 2002
  ident: B33
  article-title: Pyruvate kinase type M2: a crossroad in the tumor metabolome
  publication-title: Br J Nutr
  doi: 10.1079/BJN2001454
– volume: 9
  year: 2010
  ident: B11
  article-title: Glutaminolysis Supplying carbon or nitrogen or both for cancer cells
  publication-title: Cell Cycle
  doi: 10.4161/cc.9.19.13302
– volume: 1826
  year: 2012
  ident: B4
  article-title: A global view of the biochemical pathways involved in the regulation of the metabolism of cancer cells
  publication-title: Biochim Biophys Acta - Rev Cancer
  doi: 10.1016/j.bbcan.2012.07.001
– volume: 289
  year: 2014
  ident: B44
  article-title: Mitochondrial Phosphoenolpyruvate Carboxykinase (PEPCK-M) Is a Pro-survival, Endoplasmic Reticulum (ER) Stress Response Gene Involved in Tumor Cell Adaptation to Nutrient Availability
  publication-title: J Biol Chem
  doi: 10.1074/jbc.M114.566927
– volume: 34
  year: 2001
  ident: B42
  article-title: 13C isotopomer analysis of glucose and alanine metabolism reveals cytosolic pyruvate compartmentation as part of energy metabolism in astrocytes
  publication-title: Glia
  doi: 10.1002/glia.1054
– volume: 24
  year: 1964
  ident: B7
  article-title: The interstitial fluid of solid tumors
  publication-title: Cancer Res
– volume: 118
  year: 2015
  ident: B10
  article-title: Causes of upregulation of glycolysis in lymphocytes upon stimulation. A comparison with other cell types
  publication-title: Biochimie
  doi: 10.1016/j.biochi.2015.09.017
– volume: 7
  start-page: 523
  year: 2011
  ident: B14
  article-title: Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth
  publication-title: Mol Syst Biol
  doi: 10.1038/msb.2011.56
– volume: 34
  year: 2015
  ident: B43
  article-title: PCK2 activation mediates an adaptive response to glucose depletion in lung cancer
  publication-title: ONCOGENE
  doi: 10.1038/onc.2014.47
– volume: 27
  year: 2017
  ident: B32
  article-title: Serine and Functional Metabolites in Cancer
  publication-title: Trends Cell Biol
  doi: 10.1016/j.tcb.2017.05.001
– volume: 9
  year: 2010
  ident: B12
  article-title: CC3/TIP30 regulates metabolic adaptation of tumor cells to glucose limitation
  publication-title: Cell Cycle
  doi: 10.4161/cc.9.24.14230
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Snippet The metabolism of cancer cells is an issue of dealing with fluctuating and limiting levels of nutrients in a precarious microenvironment to ensure their...
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SubjectTerms 13C-glucose tracing
anaplerosis
glutamine
glycolysis
nutrient deprivation
Oncology
TCA-cycle
Title Metabolic Constants and Plasticity of Cancer Cells in a Limiting Glucose and Glutamine Microenvironment—A Pyruvate Perspective
URI https://www.ncbi.nlm.nih.gov/pubmed/33425750
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