Hypoxia and oxygenation induce a metabolic switch between pentose phosphate pathway and glycolysis in glioma stem-like cells

Acta Neuropathologica

Volumn 126, Issue 5, 2013, Pages 763-780

  Kathagen, Annegret ^a   Schulte, Alexander ^a   Balcke, Gerd ^b   Phillips, Heidi S ^c   Martens, Tobias ^a   Matschke, Jakob ^a   Günther, Hauke S ^a   Soriano, Robert ^c   Modrusan, Zora ^c   Sandmann, Thomas ^c   Kuhl, Carsten ^b   Tissier, Alain ^b   Holz, Mareike ^a   Krawinkel, Lutz A ^a   Glatzel, Markus ^a   Westphal, Manfred ^a   Lamszus, Katrin ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c GENENTECH INC   (United States)

Author keywords

Glioblastoma stem cells; Glycolysis; Hypoxia; Invasion; Migration; Pentose phosphate pathway

Indexed keywords

GLUCOSE; PENTOSE PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENERGY YIELD; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GLIOBLASTOMA; GLIOBLASTOMA STEM LIKE CELL; GLIOMA CELL; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL PROLIFERATION; CELLS, CULTURED; FLOW CYTOMETRY; GLIOMA; GLYCOLYSIS; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; OXYGEN; PENTOSE PHOSPHATE PATHWAY; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84888149337     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1173-y     Document Type: Article

References (56)

1. Al-Shahrour F, Minguez P, Tarraga J, Montaner D, Alloza E, Vaquerizas JM, Conde L, Blaschke C, Vera J, Dopazo J (2006) BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments. Nucleic Acids Res 34(Web Server issue):W472-W476
2. Amaral AI, Teixeira AP, Martens S, Bernal V, Sousa MF, Alves PM (2010) Metabolic alterations induced by ischemia in primary cultures of astrocytes: merging 13C NMR spectroscopy and metabolic flux analysis. J Neurochem 113(3):735-748
3. Balcke GU, Kolle SN, Kamp H, Bethan B, Looser R, Wagner S, Landsiedel R, van Ravenzwaay B (2011) Linking energy metabolism to dysfunctions in mitochondrial respiration-a metabolomics in vitro approach. Toxicol Lett 203(3):200-209
4. Bar EE, Lin A, Mahairaki V, Matsui W, Eberhart CG (2010) Hypoxia increases the expression of stem-cell markers and promotes clonogenicity in glioblastoma neurospheres. Am J Pathol 177(3):1491-1502
5. Barrett LE, Granot Z, Coker C, Iavarone A, Hambardzumyan D, Holland EC, Nam HS, Benezra R (2012) Self-renewal does not predict tumor growth potential in mouse models of high-grade glioma. Cancer Cell 21(1):11-24
6. Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Edgar R (2007) NCBI GEO: mining tens of millions of expression profiles-database and tools update. Nucleic Acids Res 35(Database issue):D760-D765
7. Ben-Yoseph O, Camp DM, Robinson TE, Ross BD (1995) Dynamic measurements of cerebral pentose phosphate pathway activity in vivo using [1,6-13C2,6,6-2H2]glucose and microdialysis. J Neurochem 64(3):1336-1342
8. Brahimi-Horn MC, Bellot G, Pouyssegur J (2011) Hypoxia and energetic tumour metabolism. Curr Opin Genet Dev 21(1):67-72
9. Brat DJ, Castellano-Sanchez AA, Hunter SB, Pecot M, Cohen C, Hammond EH, Devi SN, Kaur B, Van Meir EG (2004) Pseudopalisades in glioblastoma are hypoxic, express extracellular matrix proteases, and are formed by an actively migrating cell population. Cancer Res 64(3):920-927
10. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R, Fleming MD, Schreiber SL, Cantley LC (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452(7184):230-233
11. DeLay M, Jahangiri A, Carbonell WS, Hu YL, Tsao S, Tom MW, Paquette J, Tokuyasu TA, Aghi MK (2012) Microarray analysis verifies two distinct phenotypes of glioblastomas resistant to antiangiogenic therapy. Clin Cancer Res 18(10):2930-2942
12. Domanska-Janik K (1988) Hexose monophosphate pathway activity in normal and hypoxic rat brain. Resuscitation 16(2):79-90
13. Eckerich C, Zapf S, Fillbrandt R, Loges S, Westphal M, Lamszus K (2007) Hypoxia can induce c-Met expression in glioma cells and enhance SF/HGF-induced cell migration. Int J Cancer 121(2):276-283
14. Evans SM, Judy KD, Dunphy I, Jenkins WT, Nelson PT, Collins R, Wileyto EP, Jenkins K, Hahn SM, Stevens CW, Judkins AR, Phillips P, Geoerger B, Koch CJ (2004) Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res 64(5):1886-1892
15. 2 tensions and the prevention of differentiation of hES cells. Proc Natl Acad Sci USA 102(13):4783-4788
16. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64(19):7011-7021
17. Gao L, Mejias R, Echevarria M, Lopez-Barneo J (2004) Induction of the glucose-6-phosphate dehydrogenase gene expression by chronic hypoxia in PC12 cells. FEBS Lett 569(1-3):256-260
18. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21(8):1624-1636
19. Griguer CE, Oliva CR, Gobin E, Marcorelles P, Benos DJ, Lancaster JR Jr, Gillespie GY (2008) CD133 is a marker of bioenergetic stress in human glioma. PLoS ONE 3(11):e3655
20. Gunther HS, Schmidt NO, Phillips HS, Kemming D, Kharbanda S, Soriano R, Modrusan Z, Meissner H, Westphal M, Lamszus K (2008) Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 27(20):2897-2909
21. Hakim AM, Moss G, Gollomp SM (1976) The effect of hypoxia on the pentose phosphate pathway in brain. J Neurochem 26(4):683-688
22. Hattingen E, Jurcoane A, Bahr O, Rieger J, Magerkurth J, Anti S, Steinbach JP, Pilatus U (2011) Bevacizumab impairs oxidative energy metabolism and shows antitumoral effects in recurrent glioblastomas: a 31P/1H MRSI and quantitative magnetic resonance imaging study. Neuro Oncol 13(12):1349-1363
23. Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN (2009) The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 8(20):3274-3284
24. Husain J, Juurlink BH (1995) Oligodendroglial precursor cell susceptibility to hypoxia is related to poor ability to cope with reactive oxygen species. Brain Res 698(1-2):86-94
25. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, Thorsen F, Taxt T, Bartos M, Jirik R, Miletic H, Wang J, Stieber D, Stuhr L, Moen I, Rygh CB, Bjerkvig R, Niclou SP (2011) Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci USA 108(9):3749-3754
26. Kingsley-Hickman PB, Ross BD, Krick T (1990) Hexose monophosphate shunt measurement in cultured cells with [1-13C]glucose: correction for endogenous carbon sources using [6-13C] glucose. Anal Biochem 185(2):235-237
27. Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, Westphal M, Lamszus K (2001) Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 61(18):6624-6628
28. Lai A, Kharbanda S, Pope WB, Tran A, Solis OE, Peale F, Forrest WF, Pujara K, Carrillo JA, Pandita A, Ellingson BM, Bowers CW, Soriano RH, Schmidt NO, Mohan S, Yong WH, Seshagiri S, Modrusan Z, Jiang Z, Aldape KD, Mischel PS, Liau LM, Escovedo CJ, Chen W, Nghiemphu PL, James CD, Prados MD, Westphal M, Lamszus K, Cloughesy T, Phillips HS (2011) Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. J Clin Oncol 29(34):4482-4490
29. Lee WN, Boros LG, Puigjaner J, Bassilian S, Lim S, Cascante M (1998) Mass isotopomer study of the nonoxidative pathways of the pentose cycle with [1,2-13C2]glucose. Am J Physiol 274(5 Pt 1):E843-E851
30. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114(2):97-109
31. Makeh I, Thomas M, Hardelin JP, Briand P, Kahn A, Skala H (1994) Analysis of a brain-specific isozyme. Expression and chromatin structure of the rat aldolase C gene and transgenes. J Biol Chem 269(6):4194-4200
32. Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CM, Hubaud A, Stadler B, Choi M, Bar M, Tewari M, Liu A, Vessella R, Rostomily R, Born D, Horwitz M, Ware C, Blau CA, Cleary MA, Rich JN, Ruohola-Baker H (2011) HIF induces human embryonic stem cell markers in cancer cells. Cancer Res 71(13):4640-4652
33. Matsumoto S, Yasui H, Mitchell JB, Krishna MC (2010) Imaging cycling tumor hypoxia. Cancer Res 70(24):10019-10023
34. McCord AM, Jamal M, Shankavaram UT, Lang FF, Camphausen K, Tofilon PJ (2009) Physiologic oxygen concentration enhances the stem-like properties of CD133+ human glioblastoma cells in vitro. Mol Cancer Res 7(4):489-497
35. McLendon RE, Rich JN (2011) Glioblastoma stem cells: a neuropathologist's view. J Oncol 2011:397195
36. Mukherjee J, Phillips JJ, Zheng S, Wiencke J, Ronen SM, Pieper RO (2013) Pyruvate kinase M2 expression, but not pyruvate kinase activity, is up-regulated in a grade-specific manner in human glioma. PLoS ONE 8(2):e57610
37. Osada-Oka M, Hashiba Y, Akiba S, Imaoka S, Sato T (2010) Glucose is necessary for stabilization of hypoxia-inducible factor-1alpha under hypoxia: contribution of the pentose phosphate pathway to this stabilization. FEBS Lett 584(14):3073-3079
38. Phillips HS, Kharbanda S, Chen R, Forrest WF, Soriano RH, Wu TD, Misra A, Nigro JM, Colman H, Soroceanu L, Williams PM, Modrusan Z, Feuerstein BG, Aldape K (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9(3):157-173
39. Pistollato F, Chen HL, Rood BR, Zhang HZ, D'Avella D, Denaro L, Gardiman M, te Kronnie G, Schwartz PH, Favaro E, Indraccolo S, Basso G, Panchision DM (2009) Hypoxia and HIF1alpha repress the differentiative effects of BMPs in high-grade glioma. Stem Cells 27(1):7-17
40. Platet N, Liu SY, Atifi ME, Oliver L, Vallette FM, Berger F, Wion D (2007) Influence of oxygen tension on CD133 phenotype in human glioma cell cultures. Cancer Lett 258(2):286-290
41. Rubenstein JL, Kim J, Ozawa T, Zhang M, Westphal M, Deen DF, Shuman MA (2000) Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2(4):306-314
42. Schulte A, Günther HS, Phillips HS, Kemming D, Martens T, Kharbanda S, Soriano RH, Modrusan Z, Zapf S, Westphal M, Lamszus K (2011) A distinct subset of glioma cell lines with stem cell-like properties reflects the transcriptional phenotype of glioblastomas and overexpresses CXCR4 as therapeutic target. Glia 59(4):590-602
43. Seidel S, Garvalov BK, Wirta V, von Stechow L, Schanzer A, Meletis K, Wolter M, Sommerlad D, Henze AT, Nister M, Reifenberger G, Lundeberg J, Frisen J, Acker T (2010) A hypoxic niche regulates glioblastoma stem cells through hypoxia inducible factor 2 alpha. Brain 133(Pt 4):983-995
44. Semenza GL (2011) HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev 20(1):51-56
45. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432(7015):396-401
46. Soeda A, Park M, Lee D, Mintz A, Androutsellis-Theotokis A, McKay RD, Engh J, Iwama T, Kunisada T, Kassam AB, Pollack IF, Park DM (2009) Hypoxia promotes expansion of the CD133-positive glioma stem cells through activation of HIF-1alpha. Oncogene 28(45):3949-3959
47. Staal GE, Kalff A, Heesbeen EC, van Veelen CW, Rijksen G (1987) Subunit composition, regulatory properties, and phosphorylation of phosphofructokinase from human gliomas. Cancer Res 47(19):5047-5051
48. Stieber D, Abdul Rahim SA, Niclou SP (2011) Novel ways to target brain tumour metabolism. Expert Opin Ther Targets 15(10):1227-1239
49. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324(5930):1029-1033
50. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC (2010) Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329(5998):1492-1499
51. Volker HU, Hagemann C, Coy J, Wittig R, Sommer S, Stojic J, Haubitz I, Vince GH, Kammerer U, Monoranu CM (2008) Expression of transketolase-like 1 and activation of Akt in grade IV glioblastomas compared with grades II and III astrocytic gliomas. Am J Clin Pathol 130(1):50-57
52. Wamelink MM, Struys EA, Jakobs C (2008) The biochemistry, metabolism and inherited defects of the pentose phosphate pathway: a review. J Inherit Metab Dis 31(6):703-717
53. Warburg O (1956) On the origin of cancer cells. Science 123(3191):309-314
54. Ward PS, Thompson CB (2012) Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 21(3):297-308
55. Westphal M, Lamszus K (2011) The neurobiology of gliomas: from cell biology to the development of therapeutic approaches. Nat Rev Neurosci 12(9):495-508
56. Wolf A, Agnihotri S, Micallef J, Mukherjee J, Sabha N, Cairns R, Hawkins C, Guha A (2011) Hexokinase 2 is a key mediator of aerobic glycolysis and promotes tumor growth in human glioblastoma multiforme. J Exp Med 208(2):313-326