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

NMR in Biomedicine

Volumn 25, Issue 11, 2012, Pages 1234-1244

  Maher, Elizabeth A ^a,b,c   Marin Valencia, Isaac ^a   Bachoo, Robert M ^a,b,c   Mashimo, Tomoyuki ^a,b,c   Raisanen, Jack ^a,c   Hatanpaa, Kimmo J ^a,c   Jindal, Ashish ^c   Jeffrey, F Mark ^c   Choi, Changho ^c   Madden, Christopher ^a,c   Mathews, Dana ^a   Pascual, Juan M ^a   Mickey, Bruce E ^a,c   Malloy, Craig R ^a,c,d   Deberardinis, Ralph J ^a,b,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^d Veterans Affairs North Texas Healthcare System   (United States)

Author keywords

Cancer; Glioblastoma; Glucose; Glutamine; Metabolism; NMR; Warburg effect

Indexed keywords

BRAIN METASTASIS; BRAIN TUMORS; CANCER; CANCER CELLS; D-GLUCOSE; GLIOBLASTOMAS; GLUCOSE OXIDATION; GLUTAMINE; HIGH RATE; HUMAN BRAIN; HUMAN BRAIN TUMORS; IN-SITU; IN-VIVO; INFORMATION CONTENTS; INTERMEDIARY METABOLISM; INTRACELLULAR METABOLITES; METABOLIC FATE; MICROENVIRONMENTS; PYRUVATES; SURGICAL RESECTION; TRICARBOXYLIC ACID CYCLE; TUMOR SAMPLES; WARBURG EFFECTS;

AMINO ACIDS; BIOCHEMISTRY; BRAIN; DISEASES; ENZYME ACTIVITY; LAKES; METABOLISM; METABOLITES; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHYSIOLOGY; POSITRON EMISSION TOMOGRAPHY; TUMORS;

GLUCOSE;

ACETYL COENZYME A; CARBON 13; FLUORODEOXYGLUCOSE F 18; GLUCOSE; GLUTAMINE; GLYCINE; LACTIC ACID; PYRUVATE DEHYDROGENASE;

AMINO ACID SYNTHESIS; ARTICLE; ASTROCYTOMA; BIOENERGY; BRAIN METASTASIS; BRAIN TUMOR; CANCER CELL; CARBON NUCLEAR MAGNETIC RESONANCE; CITRIC ACID CYCLE; CLINICAL ARTICLE; ENZYME SUBSTRATE; GLIOBLASTOMA; GLUCOSE METABOLISM; GLUCOSE OXIDATION; HUMAN; HUMAN TISSUE; MITOCHONDRIAL RESPIRATION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR MICROENVIRONMENT;

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;

EID: 84868117861     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.2794     Document Type: Article

References (46)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
2. Warburg O. On the origin of cancer cells. Science 1956; 123: 309-314.
3. Warburg O. On respiratory impairment in cancer cells. Science 1956; 124: 269-270.
4. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
5. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 2008; 7: 11-20.
6. Dang CV. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol. Cell. Biol. 1999; 19: 1-11.
7. Semenza GL. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin. Cancer Biol. 2009; 19: 12-16.
8. Lu J, Sharma LK, Bai Y. Implications of mitochondrial DNA mutations and mitochondrial dysfunction in tumorigenesis. Cell Res. 2009; 19: 802-815.
9. Linehan WM, Srinivasan R, Schmidt LS. The genetic basis of kidney cancer: a metabolic disease. Nat. Rev. Urol. 2010; 7: 277-285.
10. Freisinger P, Futterer N, Lankes E, Gempel K, Berger TM, Spalinger J, Hoerbe A, Schwantes C, Lindner M, Santer R, Burdelski M, Schaefer H, Setzer B, Walker UA, Horvath R. Hepatocerebral mitochondrial DNA depletion syndrome caused by deoxyguanosine kinase (DGUOK) mutations. Arch. Neurol. 2006; 63: 1129-1134.
11. Baysal BE, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, van der Mey A, Taschner PE, Rubinstein WS, Myers EN, Richard CW 3rd, Cornelisse CJ, Devilee P, Devlin B. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000; 287: 848-851.
12. Newsholme EA, Crabtree B, Ardawi MS. The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Biosci. Rep. 1985; 5: 393-400.
13. Bui T, Thompson CB. Cancer's sweet tooth. Cancer Cell 2006; 9: 419-420.
14. Pfeiffer T, Schuster S, Bonhoeffer S. Cooperation and competition in the evolution of ATP-producing pathways. Science 2001; 292: 504-507.
15. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat. Rev. Cancer 2004; 4: 891-899.
16. Hawkins RA, Coi Y, Huang SC, Messa C, Hoh CK, Phelps ME. Quantitating tumor glucose metabolism with FDG and PET. J. Nucl. Med. 1992; 33: 339-344.
17. DeBerardinis RJ, Mancuso A, Daikhin E, Nissim I, Yudkoff M, Wehrli S, Thompson CB. Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc. Natl. Acad. Sci. USA 2007; 104: 19 345-19 350.
18. Grassian AR, Metallo CM, Coloff JL, Stephanopoulos G, Brugge JS. Erk regulation of pyruvate dehydrogenase flux through PDK4 modulates cell proliferation. Genes Dev. 2011; 25: 1716-1733.
19. Fogal V, Richardson AD, Karmali PP, Scheffler IE, Smith JW, Ruoslahti E. Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol. Cell. Biol. 2010; 30: 1303-1318.
20. 13C-1-enriched glucose. Magn. Reson. Imaging 2010; 28: 690-697.
21. Petroff OA, Errante LD, Rothman DL, Kim JH, Spencer DD. Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia 2002; 43: 703-710.
22. Fan TW, Lane AN, Higashi RM, Farag MA, Gao H, Bousamra M, Miller DM. Altered regulation of metabolic pathways in human lung cancer discerned by (13)C stable isotope-resolved metabolomics (SIRM). Mol. Cancer 2009; 8: 41.
23. Patronas NJ, Di Chiro G, Kufta C, Bairamian D, Kornblith PL, Simon R, Larson SM. Prediction of survival in glioma patients by means of positron emission tomography. J. Neurosurg. 1985; 62: 816-822.
24. Opstad KS, Ladroue C, Bell BA, Griffiths JR, Howe FA. Linear discriminant analysis of brain tumour (1)H MR spectra: a comparison of classification using whole spectra versus metabolite quantification. NMR Biomed. 2007; 20: 763-770.
25. Yang I, Aghi MK. New advances that enable identification of glioblastoma recurrence. Nat. Rev. Clin. Oncol. 2009; 6: 648-657.
26. 13C mass isotopomer distributions for natural stable isotope abundance. J. Mass Spectrom. 1996; 31: 255-262.
27. 13C isotope isomers. Am. J. Physiol. 1990; 259: H987-H995.
28. 13C NMR under non-steady-state conditions. Biochem. 1990; 29: 6756-6761.
29. Possemato R, Marks KM, Shaul YD, Pacold ME, Kim D, Birsoy K, Sethumadhavan S, Woo HK, Jang HG, Jha AK, Chen WW, Barrett FG, Stransky N, Tsun ZY, Cowley GS, Barretina J, Kalaany NY, Hsu PP, Ottina K, Chan AM, Yuan B, Garraway LA, Root DE, Mino-Kenudson M, Brachtel EF, Driggers EM, Sabatini DM. Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature, 2011; 476: 346-350.
30. Locasale JW, Grassian AR, Melman T, Lyssiotis CA, Mattaini KR, Bass AJ, Heffron G, Metallo CM, Muranen T, Sharfi H, Sasaki AT, Anastasiou D, Mullarky E, Vokes NI, Sasaki M, Beroukhim R, Stephanopoulos G, Ligon AH, Meyerson M, Richardson AL, Chin L, Wagner G, Asara JM, Brugge JS, Cantley LC, Vander Heiden MG. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 2011; 43: 869-874.
31. Burgess SC, Hausler N, Merritt M, Jeffrey FM, Storey C, Milde A, Koshy S, Lindner J, Magnuson MA, Malloy CR, Sherry AD. Impaired tricarboxylic acid cycle activity in mouse livers lacking cytosolic phosphoenolpyruvate carboxykinase. J. Biol. Chem. 2004; 279: 48 941-48 949.
32. 13C NMR spectroscopy. J. Biol. Chem. 1988; 263: 6964-6971.
33. Grobben B, De Deyn PP, Slegers H. Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion. Cell Tissue Res. 2002; 310: 257-270.
34. Bouzier AK, Quesson B, Valeins H, Canioni P, Merle M. [1-(13)C]glucose metabolism in the tumoral and nontumoral cerebral tissue of a glioma-bearing rat. J. Neurochem. 1999; 72: 2445-2455.
35. Terpstra M, Gruetter R, High WB, Mescher M, DelaBarre L, Merkle H, Garwood M. Lactate turnover in rat glioma measured by in vivo nuclear magnetic resonance spectroscopy. Cancer Res. 1998; 58: 5083-5088.
36. Magnusson I, Schumann WC, Bartsch GE, Chandramouli V, Kumaran K, Wahren J, Landau BR. Noninvasive tracing of Krebs cycle metabolism in liver. J. Biol. Chem. 1991; 266: 6975-6984.
37. 13C-labelled microdialysis and high-resolution nuclear magnetic resonance study. Brain 2009; 132: 2839-2849.
38. Sonveaux P, Végran F, Schroeder T, Wergin MC, Verrax J, Rabbani ZN, De Saedeleer CJ, Kennedy KM, Diepart C, Jordan BF, Kelley MJ, Gallez B, Wahl ML, Feron O, Dewhirst MW. Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J. Clin. Invest. 2008; 118: 3930-3942.
39. Koppenol WH, Bounds PL, Dang CV. Otto Warburg's contributions to current concepts of cancer metabolism. Nat. Rev. Cancer 2011; 11: 325-337.
40. Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E, Maguire C, Gammer TL, Mackey JR, Fulton D, Abdulkarim B, McMurtry MS, Petruk KC. Metabolic modulation of glioblastoma with dichloroacetate. Sci. Transl. Med. 2010; 2: 31ra-34ra.
41. Clarke DD, Sokoloff L. Circulation and energy metabolism of the brain. In Basic Neurochemistry: Molecular, Cellular and Medical Aspects. Siegel GL, Agranoff BW, Albers RW, Fisher SK, Uhler MD (eds). Lippincott-Raven: Philadelphia, PA; 1999: 637-670.
42. Opstad KS, Griffiths JR, Bell BA, Howe FA. Apparent T(2) relaxation times of lipid and macromolecules: a study of high-grade tumor spectra. J. Magn. Reson. Imaging 2008; 27: 178-184.
43. Choi C, Ganji SK, DeBerardinis RJ, Dimitrov IE, Pascual JM, Bachoo R, Mickey BE, Malloy CR, Maher EA. Measurement of glycine in the human brain in vivo by (1)H-MRS at 3T: application in brain tumors. Magn. Reson. Med. 2011; 66: 609-618.
44. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW, He Y, Bigner DD, Vogelstein B, Yan H. Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc. Natl. Acad. Sci. USA 2011; 108: 3270-3275.
45. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, Kos I, Batinic-Haberle I, Jones S, Riggins GJ, Friedman H, Friedman A, Reardon D, Herndon J, Kinzler KW, Velculescu VE, Vogelstein B, Bigner DD. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009; 360: 765-773.
46. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, Fantin VR, Jang HG, Jin S, Keenan MC, Marks KM, Prins RM, Ward PS, Yen KE, Liau LM, Rabinowitz JD, Cantley LC, Thompson CB, Vander Heiden MG, Su SM. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009; 462: 739-744.