IDH1 mutation induces reprogramming of pyruvate metabolism

Cancer Research

Volumn 75, Issue 15, 2015, Pages 2999-3009

  Izquierdo Garcia, Jose L ^a   Viswanath, Pavithra ^a   Eriksson, Pia ^a   Cai, Larry ^a   Radoul, Marina ^a   Chaumeil, Myriam M ^a   Blough, Michael ^b   Luchman, H Artee ^c   Weiss, Samuel ^b   Cairncross, J Gregory ^b   Phillips, Joanna J ^a   Pieper, Russell O ^a   Ronen, Sabrina M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DICHLOROACETIC ACID; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOCITRATE DEHYDROGENASE 1; PYRUVATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE KINASE 3; UNCLASSIFIED DRUG; ALPHA-HYDROXYGLUTARATE; GLUTAMIC ACID; GLUTARIC ACID DERIVATIVE; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVIC ACID DERIVATIVE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL PROLIFERATION; CLONOGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME PHOSPHORYLATION; GENE MUTATION; GLIOBLASTOMA CELL LINE; GLUCOSE TRANSPORT; HUMAN; HUMAN CELL; IDH1 GENE; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; ASTROCYTE; DOWN REGULATION; DRUG EFFECTS; GENETICS; GLIOBLASTOMA; METABOLISM; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; TUMOR CELL LINE;

ASTROCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; DICHLOROACETIC ACID; DOWN-REGULATION; GLIOBLASTOMA; GLUTAMIC ACID; GLUTARATES; HUMANS; ISOCITRATE DEHYDROGENASE; MAGNETIC RESONANCE SPECTROSCOPY; MUTATION; PYRUVATE DEHYDROGENASE COMPLEX; PYRUVATES;

EID: 84942909054     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-0840     Document Type: Article

References (53)

1. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
2. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012;21:297-308.
3. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008;13:472-82.
4. Warburg O, Posener K, Negelein E. Ueber den Stoffwechsel der Tumoren. Biochemische Zeitschrift 1924;152:319-44.
5. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004;4:891-9.
6. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009;324:1029-33.
7. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12.
8. Yang H, Ye D, Guan KL, Xiong Y. IDH1 and IDH2 mutations in tumorigenesis: mechanistic insights and clinical perspectives. Clin Cancer Res 2012;18:5562-71.
9. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010;17:225-34.
10. Reitman ZJ, Jin G, Karoly ED, Spasojevic I, Yang J, Kinzler KW, et al. Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome. Proc Natl Acad Sci U S A 2011;108:3270-5.
11. Ohka F, Ito M, Ranjit M, Senga T, Motomura A, Motomura K, et al. Quantitative metabolome analysis profiles activation of glutaminolysis in glioma with IDH1 mutation. Tumour Biol 2014;35:5911-20.
12. Choi C, Ganji S, Hulsey K, Madan A, Kovacs Z, Dimitrov I, et al. A comparative study of short-and long-TE (1)H MRS at 3 T for in vivo detection of 2-hydroxyglutarate in brain tumors. NMR Biomed 2013;26:1242-50.
13. Chaumeil MM, Larson PE, Woods SM, Cai L, Eriksson P, Robinson AE, et al. Hyperpolarized [1-13C] glutamate: a metabolic imaging biomarker of IDH1 mutational status in glioma. Cancer Res 2014;74:4247-57.
14. Esmaeili M, Hamans BC, Navis AC, van Horssen R, Bathen TF, Gribbestad IS, et al. IDH1 R132H mutation generates a distinct phospholipid metabolite profile in glioma. Cancer Res 2014;74:4898-907.
15. Chesnelong C, Chaumeil MM, Blough MD, Al-Najjar M, Stechishin OD, Chan JA, et al. Lactate dehydrogenase A silencing in IDH mutant gliomas. Neuro Oncol 2014;16:686-95.
16. Grassian AR, Parker SJ, Davidson SM, Divakaruni AS, Green CR, Zhang X, et al. IDH1 mutations alter citric acid cycle metabolism and increase dependence on oxidative mitochondrial metabolism. Cancer Res 2014;74:3317-31.
17. Reitman ZJ, Duncan CG, Poteet E, Winters A, Yan LJ, Gooden DM, et al. Cancer-associated isocitrate dehydrogenase 1 (IDH1) R132H mutation and d-2-hydroxyglutaratestimulate glutamine metabolismunder hypoxia. J Biol Chem 2014;289:23318-28.
18. Glunde K, Bhujwalla ZM, Ronen SM. Choline metabolism in malignant transformation. Nat Rev Cancer 2011;11:835-48.
19. Izquierdo-Garcia JL, Viswanath P, Eriksson P, Chaumeil MM, Pieper RO, Phillips JJ, et al. Metabolic Reprogrammingin Mutant IDH1 Glioma Cells. PLoS One 2015;10:e0118781.
20. Ardenkjaer-Larsen JH, Fridlund B, Gram A, Hansson G, Hansson L, Lerche MH, et al. Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR. Proc Natl Acad Sci U S A 2003;100:10158-63.
21. Golman K, in 't Zandt R, Thaning M. Real-time metabolic imaging. Proc Natl Acad Sci U S A 2006;103:11270-5.
22. Kurhanewicz J, Vigneron DB, Brindle K, Chekmenev EY, Comment A, Cunningham CH, et al. Analysis of cancer metabolism by imaging hyperpolarized nuclei: prospects for translation to clinical research. Neoplasia 2011;13:81-97.
23. Nelson SJ, Kurhanewicz J, Vigneron DB, Larson PE, Harzstark AL, Ferrone M, et al. Metabolic imaging of patients with prostate cancer using hyperpolarized [1-(1)(3)C]pyruvate. Sci Transl Med 2013;5: 198ra08.
24. Chaumeil MM, Larson PE, Yoshihara HA, Danforth OM, Vigneron DB, Nelson SJ, et al. Non-invasiveinvivo assessment of IDH1 mutational status in glioma. Nat Commun 2013;4:2429.
25. Izquierdo-Garcia JL, Cai LM, Chaumeil MM, Eriksson P, Robinson AE, Pieper RO, et al. Glioma cells with the IDH1mutation modulate metabolic fractional flux through pyruvate carboxylase. PLoS One 2014;9:e108289.
26. Kelly JJ, Blough MD, Stechishin OD, Chan JA, Beauchamp D, Perizzolo M, et al. Oligodendroglioma cell lines containing t(1;19)(q10;p10). Neuro Oncol 2010;12:745-55.
27. Luchman HA, Stechishin OD, Dang NH, Blough MD, Chesnelong C, Kelly JJ, et al. An in vivo patient-derived model of endogenous IDH1-mutant glioma. Neuro Oncol 2012;14:184-91.
28. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science 1977;197:461-3.
29. Ronen S, Degani H. Studies of the metabolism of human breast cancer spheroids by NMR. Magn Reson Med 1989;12:274-81.
30. Lodi A, Woods SM, Ronen SM. Treatment with the MEK inhibitor U0126 induces decreased hyperpolarized pyruvate to lactate conversion in breast, but not prostate, cancer cells. NMR Biomed 2013;26:299-306.
31. Ward CS, Venkatesh HS, Chaumeil MM, Brandes AH, Vancriekinge M, Dafni H, et al. Noninvasive detection of target modulation following phosphatidylinositol 3-kinase inhibition using hyperpolarized 13C magnetic resonance spectroscopy. Cancer Res 2010;70:1296-305.
32. Roche TE, Hiromasa Y. Pyruvate dehydrogenase kinase regulatory mechanisms and inhibition in treating diabetes, heart ischemia, and cancer. Cell Mol Life Sci 2007;64:830-49.
33. Semenza GL. HIF-1 mediates metabolic responsestointratumoralhypoxia and oncogenic mutations. J Clin Invest 2013;123:3664-71.
34. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011;19:17-30.
35. Bralten LB, Kloosterhof NK, Balvers R, Sacchetti A, Lapre L, Lamfers M, et al. IDH1 R132H decreases proliferation of glioma cell lines in vitro and in vivo. Ann Neurol 2011;69:455-63.
36. Schroeder MA, Atherton HJ, Ball DR, Cole MA, Heather LC, Griffin JL, et al. Real-time assessment of Krebs cycle metabolism using hyperpolarized 13C magnetic resonance spectroscopy. FASEB J 2009;23: 2529-38.
37. Chen R, Nishimura MC, Kharbanda S, Peale F, Deng Y, Daemen A, et al. Hominoid-specific enzyme GLUD2 promotes growth of IDH1R132H glioma. Proc Natl Acad Sci 2014;111:14217-22.
38. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009;462:739-44.
39. Sanchez WY, McGee SL, Connor T, Mottram B, Wilkinson A, Whitehead JP, et al. Dichloroacetate inhibits aerobic glycolysis in multiple myeloma cells and increases sensitivity to bortezomib. Br J Cancer 2013; 108:1624-33.
40. Tennant DA, Duran RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 2010;10:267-77.
41. Koivunen P, Lee S, Duncan CG, Lopez G, Lu G, Ramkissoon S, et al. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature 2012;483:484-8.
42. Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 2009;324:261-5.
43. Sasaki M, Knobbe CB, Itsumi M, Elia AJ, Harris IS, Chio II, et al. D-2-hydroxyglutarate produced by mutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev 2012;26: 2038-49.
44. Prabhu A, Sarcar B, Miller CR, Kim S-H, Nakano I, Forsyth P, et al. Ras-mediated modulation of pyruvate dehydrogenase activity regulates mitochondrial reserve capacity and contributes to glioblastoma tumorigenesis. Neuro-Oncology 2015. [Epub ahead of print].
45. Sutendra G, Michelakis ED. Pyruvate dehydrogenase kinase as a novel therapeutic target in oncology. Front Oncol 2013;3:38.
46. Michelakis ED, Sutendra G, Dromparis P, Webster L, Haromy A, Niven E, et al. Metabolic modulation of glioblastoma with dichloroacetate. Sci Translat Med 2010;2:31ra34.
47. Seltzer MJ, Bennett BD, Joshi AD, Gao P, Thomas AG, Ferraris DV, et al. Inhibition of glutaminase preferentially slows growth of glioma cells with mutant IDH1. Cancer Res 2010;70:8981-7.
48. Nelson SJ. Assessment of therapeutic response and treatment planning for brain tumors using metabolic and physiological MRI. NMR Biomed 2011;24:734-49.
49. Elkhaled A, Jalbert LE, Phillips JJ, Yoshihara HA, Parvataneni R, Srinivasan R, et al. Magnetic resonance of 2-hydroxyglutarate in IDH1-mutated low-grade gliomas. Sci Transl Med 2012;4:116ra5.
50. Andronesi OC, Kim GS, Gerstner E, Batchelor T, Tzika AA, Fantin VR, et al. Detection of 2-hydroxyglutarate in IDH-mutated glioma patients by in vivo spectral-editing and 2D correlation magnetic resonance spectroscopy. Sci Transl Med 2012;4:116ra4.
51. Choi C, Ganji SK, DeBerardinis RJ, Hatanpaa KJ, Rakheja D, Kovacs Z, et al. 2-hydroxyglutarate detection by magnetic resonance spectroscopy in IDH-mutated patients with gliomas. Nat Med 2012;18:624-9.
52. Pope WB, Prins RM, Albert Thomas M, Nagarajan R, Yen KE, Bittinger MA, et al. Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy. J Neurooncol 2012;107:197-205.
53. Park JM, Josan S, Grafendorfer T, Yen Y-F, Hurd RE, Spielman DM, et al. Measuring mitochondrial metabolism in rat brain in vivo using MR spectros-copy of hyperpolarized [2-13C]pyruvate. NMR in Biomed 2013;26:1197-203.