MTOR complex 2 controls glycolytic metabolism in glioblastoma through FoxO acetylation and upregulation of c-Myc

Cell Metabolism

Volumn 18, Issue 5, 2013, Pages 726-739

  Masui, Kenta ^a   Tanaka, Kazuhiro ^a   Akhavan, David ^a   Babic, Ivan ^a   Gini, Beatrice ^a   Matsutani, Tomoo ^a   Iwanami, Akio ^a   Liu, Feng ^a   Villa, Genaro R ^a,b   Gu, Yuchao ^a,b   Campos, Carl ^c   Zhu, Shaojun ^b   Yang, Huijun ^a   Yong, William H ^b   Cloughesy, Timothy F ^b   Mellinghoff, Ingo K ^c   Cavenee, Webster K ^a,d   Shaw, Reuben J ^d,e   Mischel, Paul S ^a,d,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYGLUCOSE; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MICRORNA; MICRORNA 145; MICRORNA 34C; PROTEIN KINASE B; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ACETYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER PATIENT; CANCER SURVIVAL; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GLIOBLASTOMA; GLUCOSE INTAKE; GLYCOLYSIS; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; ONCOGENE C MYC; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TISSUE MICROARRAY; UPREGULATION;

ACETYLATION; ANIMALS; BRAIN NEOPLASMS; CELL DEATH; FORKHEAD TRANSCRIPTION FACTORS; GLIOBLASTOMA; GLUCOSE; GLYCOLYSIS; HISTONE DEACETYLASES; HUMANS; MICE; MICRORNAS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; UP-REGULATION;

EID: 84887430714     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.09.013     Document Type: Article

References (47)

1. A. Albihn, J.I. Johnsen, and M.A. Henriksson MYC in oncogenesis and as a target for cancer therapies Adv. Cancer Res. 107 2010 163 224
2. I. Babic, E.S. Anderson, K. Tanaka, D. Guo, K. Masui, B. Li, S. Zhu, Y. Gu, G.R. Villa, and D. Akhavan EGFR mutation-induced alternative splicing of Max contributes to growth of glycolytic tumors in brain cancer Cell Metab. 17 2013 1000 1008
3. K. Bensaad, A. Tsuruta, M.A. Selak, M.N. Vidal, K. Nakano, R. Bartrons, E. Gottlieb, and K.H. Vousden TIGAR, a p53-inducible regulator of glycolysis and apoptosis Cell 126 2006 107 120
4. W.H. Biggs III, J. Meisenhelder, T. Hunter, W.K. Cavenee, and K.C. Arden Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1 Proc. Natl. Acad. Sci. USA 96 1999 7421 7426
5. C. Bouchard, J. Marquardt, A. Brás, R.H. Medema, and M. Eilers Myc-induced proliferation and transformation require Akt-mediated phosphorylation of FoxO proteins EMBO J. 23 2004 2830 2840
6. A. Brunet, L.B. Sweeney, J.F. Sturgill, K.F. Chua, P.L. Greer, Y. Lin, H. Tran, S.E. Ross, R. Mostoslavsky, and H.Y. Cohen Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase Science 303 2004 2011 2015
7. R.A. Cairns, I.S. Harris, and T.W. Mak Regulation of cancer cell metabolism Nat. Rev. Cancer 11 2011 85 95
8. Cancer Genome Atlas Research Network Comprehensive genomic characterization defines human glioblastoma genes and core pathways Nature 455 2008 1061 1068
9. G. Choe, S. Horvath, T.F. Cloughesy, K. Crosby, D. Seligson, A. Palotie, L. Inge, B.L. Smith, C.L. Sawyers, and P.S. Mischel Analysis of the phosphatidylinositol 3′-kinase signaling pathway in glioblastoma patients in vivo Cancer Res. 63 2003 2742 2746
10. H.R. Christofk, M.G. Vander Heiden, N. Wu, J.M. Asara, and L.C. Cantley Pyruvate kinase M2 is a phosphotyrosine-binding protein Nature 452 2008 181 186
11. C.V. Dang MYC on the path to cancer Cell 149 2012 22 35
12. C.V. Dang Links between metabolism and cancer Genes Dev. 26 2012 877 890
13. C.V. Dang, A. Le, and P. Gao MYC-induced cancer cell energy metabolism and therapeutic opportunities Clin. Cancer Res. 15 2009 6479 6483
14. R.J. DeBerardinis, J.J. Lum, G. Hatzivassiliou, and C.B. Thompson The biology of cancer: metabolic reprogramming fuels cell growth and proliferation Cell Metab. 7 2008 11 20
15. O. Delpuech, B. Griffiths, P. East, A. Essafi, E.W. Lam, B. Burgering, J. Downward, and A. Schulze Induction of Mxi1-SR alpha by FOXO3a contributes to repression of Myc-dependent gene expression Mol. Cell. Biol. 27 2007 4917 4930
16. B. Faubert, G. Boily, S. Izreig, T. Griss, B. Samborska, Z. Dong, F. Dupuy, C. Chambers, B.J. Fuerth, and B. Viollet AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo Cell Metab. 17 2013 113 124
17. E.C. Ferber, B. Peck, O. Delpuech, G.P. Bell, P. East, and A. Schulze FOXO3a regulates reactive oxygen metabolism by inhibiting mitochondrial gene expression Cell Death Differ. 19 2012 968 979
18. L.W. Finley, A. Carracedo, J. Lee, A. Souza, A. Egia, J. Zhang, J. Teruya-Feldstein, P.I. Moreira, S.M. Cardoso, and C.B. Clish SIRT3 opposes reprogramming of cancer cell metabolism through HIF1α destabilization Cancer Cell 19 2011 416 428
19. B. Gan, C. Lim, G. Chu, S. Hua, Z. Ding, M. Collins, J. Hu, S. Jiang, E. Fletcher-Sananikone, and L. Zhuang FoxOs enforce a progression checkpoint to constrain mTORC1-activated renal tumorigenesis Cancer Cell 18 2010 472 484
20. D.A. Guertin, D.M. Stevens, C.C. Thoreen, A.A. Burds, N.Y. Kalaany, J. Moffat, M. Brown, K.J. Fitzgerald, and D.M. Sabatini Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1 Dev. Cell 11 2006 859 871
21. D. Guo, I.J. Hildebrandt, R.M. Prins, H. Soto, M.M. Mazzotta, J. Dang, J. Czernin, J.Y. Shyy, A.D. Watson, and M. Phelps The AMPK agonist AICAR inhibits the growth of EGFRvIII-expressing glioblastomas by inhibiting lipogenesis Proc. Natl. Acad. Sci. USA 106 2009 12932 12937
22. A. Hagiwara, M. Cornu, N. Cybulski, P. Polak, C. Betz, F. Trapani, L. Terracciano, M.H. Heim, M.A. Rüegg, and M.N. Hall Hepatic mTORC2 activates glycolysis and lipogenesis through Akt, glucokinase, and SREBP1c Cell Metab. 15 2012 725 738
23. C.C. Hudson, M. Liu, G.G. Chiang, D.M. Otterness, D.C. Loomis, F. Kaper, A.J. Giaccia, and R.T. Abraham Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin Mol. Cell. Biol. 22 2002 7004 7014
24. N. Ilic, T. Utermark, H.R. Widlund, and T.M. Roberts PI3K-targeted therapy can be evaded by gene amplification along the MYC-eukaryotic translation initiation factor 4E (eIF4E) axis Proc. Natl. Acad. Sci. USA 108 2011 E699 E708
25. W.G. Kaelin Jr., and P.J. Ratcliffe Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway Mol. Cell 30 2008 393 402
26. W.H. Koppenol, P.L. Bounds, and C.V. Dang Otto Warburg's contributions to current concepts of cancer metabolism Nat. Rev. Cancer 11 2011 325 337
27. T.R. Kress, I.G. Cannell, A.B. Brenkman, B. Samans, M. Gaestel, P. Roepman, B.M. Burgering, M. Bushell, A. Rosenwald, and M. Eilers The MK5/PRAK kinase and Myc form a negative feedback loop that is disrupted during colorectal tumorigenesis Mol. Cell 41 2011 445 457
28. A.J. Levine, and A.M. Puzio-Kuter The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes Science 330 2010 1340 1344
29. J. Liu, and D. Levens Making myc Curr. Top. Microbiol. Immunol. 302 2006 1 32
30. K.V. Lu, S. Zhu, A. Cvrljevic, T.T. Huang, S. Sarkaria, D. Ahkavan, J. Dang, E.B. Dinca, S.B. Plaisier, and I. Oderberg Fyn and SRC are effectors of oncogenic epidermal growth factor receptor signaling in glioblastoma patients Cancer Res. 69 2009 6889 6898
31. L.D. Marroquin, J. Hynes, J.A. Dykens, J.D. Jamieson, and Y. Will Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants Toxicol. Sci. 97 2007 539 547
32. M.M. Mihaylova, D.S. Vasquez, K. Ravnskjaer, P.D. Denechaud, R.T. Yu, J.G. Alvarez, M. Downes, R.M. Evans, M. Montminy, and R.J. Shaw Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis Cell 145 2011 607 621
33. M.K. Muellner, I.Z. Uras, B.V. Gapp, C. Kerzendorfer, M. Smida, H. Lechtermann, N. Craig-Mueller, J. Colinge, G. Duernberger, and S.M. Nijman A chemical-genetic screen reveals a mechanism of resistance to PI3K inhibitors in cancer Nat. Chem. Biol. 7 2011 787 793
34. N. Nakamura, S. Ramaswamy, F. Vazquez, S. Signoretti, M. Loda, and W.R. Sellers Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN Mol. Cell. Biol. 20 2000 8969 8982
35. B. Peck, E.C. Ferber, and A. Schulze Antagonism between FOXO and MYC Regulates Cellular Powerhouse Front Oncol. 3 2013 96
36. D.R. Plas, and C.B. Thompson Akt-dependent transformation: there is more to growth than just surviving Oncogene 24 2005 7435 7442
37. M.J. Potthoff, H. Wu, M.A. Arnold, J.M. Shelton, J. Backs, J. McAnally, J.A. Richardson, R. Bassel-Duby, and E.N. Olson Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers J. Clin. Invest. 117 2007 2459 2467
38. D. Rohle, J. Popovici-Muller, N. Palaskas, S. Turcan, C. Grommes, C. Campos, J. Tsoi, O. Clark, B. Oldrini, and E. Komisopoulou An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells Science 340 2013 626 630
39. K. Tanaka, I. Babic, D. Nathanson, D. Akhavan, D. Guo, B. Gini, J. Dang, S. Zhu, H. Yang, and J. De Jesus Oncogenic EGFR signaling activates an mTORC2-NF-κB pathway that promotes chemotherapy resistance Cancer Discov. 1 2011 524 538
40. X. Tong, F. Zhao, and C.B. Thompson The molecular determinants of de novo nucleotide biosynthesis in cancer cells Curr. Opin. Genet. Dev. 19 2009 32 37
41. A. van der Horst, and B.M. Burgering Stressing the role of FoxO proteins in lifespan and disease Nat. Rev. Mol. Cell Biol. 8 2007 440 450
42. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
43. B. Wang, N. Moya, S. Niessen, H. Hoover, M.M. Mihaylova, R.J. Shaw, J.R. Yates III, W.H. Fischer, J.B. Thomas, and M. Montminy A hormone-dependent module regulating energy balance Cell 145 2011 596 606
44. O. Warburg On the origin of cancer cells Science 123 1956 309 314
45. P.S. Ward, and C.B. Thompson Metabolic reprogramming: a cancer hallmark even warburg did not anticipate Cancer Cell 21 2012 297 308
46. Y. Zhao, J. Yang, W. Liao, X. Liu, H. Zhang, S. Wang, D. Wang, J. Feng, L. Yu, and W.G. Zhu Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity Nat. Cell Biol. 12 2010 665 675
47. Y. Zhao, Y. Wang, and W.G. Zhu Applications of post-translational modifications of FoxO family proteins in biological functions J. Mol. Cell Biol. 3 2011 276 282