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Transformation by different oncogenes relies on specific metabolic adaptations

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Pages 2656-2668 | Received 06 Apr 2016, Accepted 15 Jul 2016, Published online: 17 Aug 2016

References

  • Parra M. Class IIa HDACs - new insights into their functions in physiology and pathology. FEBS J 2015; 282:1736-44; PMID:25244360; http://dx.doi.org/10.1111/febs.13061
  • Di Giorgio E, Brancolini C. Regulation of class IIa HDAC activities: it is not only matter of subcellular localization. Epigenomics 2016; 8(2):51-69; http://dx.doi.org/10.2217/epi.15.106
  • Clocchiatti A, Florean C, Brancolini C. Class IIa HDACs: from important roles in differentiation to possible implications in tumourigenesis. J Cell Mol Med 2011; 15:1833-46; PMID:21435179; http://dx.doi.org/10.1111/j.1582-4934.2011.01321.x
  • Martin M, Kettmann R, Dequiedt F. Class IIa histone deacetylases: conducting development and differentiation. Int J Dev Biol 2009; 53:291-301; PMID:19412888; http://dx.doi.org/10.1387/ijdb.082698mm
  • Cernotta N, Clocchiatti A, Florean C, Brancolini C. Ubiquitin-dependent degradation of HDAC4, a new regulator of random cell motility. Mol Biol Cell 2011; 22:278-89; PMID:21118993; http://dx.doi.org/10.1091/mbc.E10-07-0616
  • Ishikawa F, Miyoshi H, Nose K, Shibanuma M. Transcriptional induction of MMP-10 by TGF-beta, mediated by activation of MEF2A and downregulation of class IIa HDACs. Oncogene 2010; 29:909-19; PMID:19935709; http://dx.doi.org/10.1038/onc.2009.387
  • Di Giorgio E, Gagliostro E, Clocchiatti A, Brancolini C. The control operated by the cell cycle machinery on MEF2 stability contributes to the downregulation of CDKN1A and entry into S phase. Mol Cell Biol 2015; 35:1633-47; PMID:25733682; http://dx.doi.org/10.1128/MCB.01461-14
  • Paroni G, Mizzau M, Henderson C, Del Sal G, Schneider C, Brancolini C. Caspase-dependent regulation of histone deacetylase 4 nuclear-cytoplasmic shuttling promotes apoptosis. Mol Biol Cell 2004; 15:2804-18; PMID:15075374; http://dx.doi.org/10.1091/mbc.E03-08-0624
  • McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M. Diabetes. AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. 2008; 57:860-7; PMID:18184930
  • Wang B, Liu TY, Lai CH, Rao YH, Choi MC, Chi JT, Dai JW, Rathmell JC, Yao TP. Glycolysis-dependent histone deacetylase 4 degradation regulates inflammatory cytokine production. Mol Biol Cell 2014; 25:3300-7; PMID:25187650; http://dx.doi.org/10.1091/mbc.E13-12-0757
  • Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, Shaw RJ, Yates JR 3rd, Fischer WH, Thomas JB, Montminy M. A hormone-dependent module regulating energy balance. Cell 2011; 145:596-606; PMID:21565616; http://dx.doi.org/10.1016/j.cell.2011.04.013
  • Henriksson E, Säll J, Gormand A, Wasserstrom S, Morrice NA, Fritzen AM, Foretz M, Campbell DG, Sakamoto K, Ekelund M, Degerman E, Stenkula KG, Göransson O. SIK2 regulates CRTCs, HDAC4 and glucose uptake in adipocytes. J Cell Sci 2015; 128:472-86; PMID:25472719; http://dx.doi.org/10.1242/jcs.153932
  • Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M, Shaw RJ. Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 2011; 145:607-21; PMID:21565617; http://dx.doi.org/10.1016/j.cell.2011.03.043
  • Chen J, Wang N, Dong M, Guo M, Zhao Y, Zhuo Z, Zhang C, Chi X, Pan Y, Jiang J, et al. The Metabolic Regulator Histone Deacetylase 9 Contributes to Glucose Homeostasis Abnormality Induced by Hepatitis C Virus Infection. Diabetes 2015; 64:4088-98; PMID:26420860; http://dx.doi.org/10.2337/db15-0197
  • Choi S, Lim DS, Chung J. Feeding and Fasting Signals Converge on the LKB1-SIK3 Pathway to Regulate Lipid Metabolism in Drosophila. PLoS Genet 2015; 11:e1005263; PMID:25996931; http://dx.doi.org/10.1371/journal.pgen.1005263
  • Tang H, Macpherson P, Marvin M, Meadows E, Klein WH, Yang XJ, Goldman D. A histone deacetylase 4/myogenin positive feedback loop coordinates denervation-dependent gene induction and suppression. Mol Biol Cell 2009; 20:1120-31; PMID:19109424; http://dx.doi.org/10.1091/mbc.E08-07-0759
  • Potthoff MJ, Wu H, Arnold MA, Shelton JM, Backs J, McAnally J, Richardson JA, Bassel-Duby R, Olson EN. Histone deacetylase degradation and MEF2 activation promote the formation of slow-twitch myofibers. J Clin Invest 2007; 117:2459-67; PMID:17786239; http://dx.doi.org/10.1172/JCI31960
  • Geng H, Harvey CT, Pittsenbarger J, Liu Q, Beer TM, Xue C, Qian DZ. HDAC4 protein regulates HIF1α protein lysine acetylation and cancer cell response to hypoxia. J Biol Chem 2011; 286:38095-102; PMID:21917920; http://dx.doi.org/10.1074/jbc.M111.257055
  • Di Giorgio E, Clocchiatti A, Piccinin S, Sgorbissa A, Viviani G, Peruzzo P, Romeo S, Rossi S, Dei Tos AP, Maestro R, Brancolini C. MEF2 is a converging hub for histone deacetylase 4 and phosphatidylinositol 3-kinase/Akt-induced transformation. Mol Cell Biol 2013; 33:4473-91; PMID:24043307; http://dx.doi.org/10.1128/MCB.01050-13
  • Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
  • Kimmelman AC. Metabolic Dependencies in RAS-Driven Cancers. Clin Cancer Res 2015; 21:1828-34; PMID:25878364; http://dx.doi.org/10.1158/1078-0432.CCR-14-2425
  • Ramanathan A, Wang C, Schreiber SL. Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc Natl Acad Sci U S A 2005; 102:5992-7; PMID:15840712; http://dx.doi.org/10.1073/pnas.0502267102
  • Yang D, Wang MT, Tang Y, Chen Y, Jiang H, Jones TT, Rao K, Brewer GJ, Singh KK, Nie D. Impairment of mitochondrial respiration in mouse fibroblasts by oncogenic H-RAS(Q61L). Cancer Biol Ther 2010; 9:122-33; PMID:19923925; http://dx.doi.org/10.4161/cbt.9.2.10379
  • Gaglio D, Metallo CM, Gameiro PA, Hiller K, Danna LS, Balestrieri C, Alberghina L, Stephanopoulos G, Chiaradonna F. Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth. Mol Syst Biol 2011; 7:523; PMID:21847114; http://dx.doi.org/10.1038/msb.2011.56
  • Quijano C, Cao L, Fergusson MM, Romero H, Liu J, Gutkind S, Rovira II, Mohney RP, Karoly ED, Finkel T. Oncogene-induced senescence results in marked metabolic and bioenergetic alterations. Cell Cycle 2012; 11:1383-92; PMID:22421146; http://dx.doi.org/10.4161/cc.19800
  • Newell K, Franchi A, Pouysségur J, Tannock I. Studies with glycolysis-deficient cells suggest that production of lactic acid is not the only cause of tumor acidity. Proc Natl Acad Sci U S A 1993; 90:1127-31; PMID:8430084; http://dx.doi.org/10.1073/pnas.90.3.1127
  • Hu Y, Lu W, Chen G, Wang P, Chen Z, Zhou Y, Ogasawara M, Trachootham D, Feng L, Pelicano H, Chiao PJ, Keating MJ, Garcia-Manero G, Huang P. K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res 2012; 22:399-412; PMID:21876558; http://dx.doi.org/10.1038/cr.2011.145
  • Goldberg EB, Colowick SP. The role of glycolysis in the growth of tumor cells. 3. lactic dehydrogenase as the site of action of oxamate on the growth of cultured cells. J Biol Chem 1965; 240:2786-90; PMID:14342295
  • Xie H, Valera VA, Merino MJ, Amato AM, Signoretti S, Linehan WM, Sukhatme VP, Seth P. LDH-A inhibition, a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Mol Cancer Ther 2009; 8:626-35; PMID:19276158; http://dx.doi.org/10.1158/1535-7163.MCT-08-1049
  • Zhang D, Li J, Wang F, Hu J, Wang S, Sun Y. 2-Deoxy-D-glucose targeting of glucose metabolism in cancer cells as a potential therapy. Cancer Lett 2014; 355:176-83; PMID:25218591; http://dx.doi.org/10.1016/j.canlet.2014.09.003
  • Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E. Energy metabolism in tumor cells. FEBS J 2007; 274:1393-418; PMID:Can't; http://dx.doi.org/10.1111/j.1742-4658.2007.05686.x
  • Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21:297-308; PMID:22439925; http://dx.doi.org/10.1016/j.ccr.2012.02.014
  • Chiaradonna F, Gaglio D, Vanoni M, Alberghina L. Expression of transforming K-Ras oncogene affects mitochondrial function and morphology in mouse fibroblasts. Biochim Biophys Acta 2006; 1757:1338-56; PMID:16987493; http://dx.doi.org/10.1016/j.bbabio.2006.08.001
  • Domenis R, Bisetto E, Rossi D, Comelli M, Mavelli I. Glucose-modulated mitochondria adaptation in tumor cells: a focus on ATP synthase and inhibitor Factor 1. Int J Mol Sci 2012; 13:1933-50; PMID:22408432; http://dx.doi.org/10.3390/ijms13021933
  • Baracca A, Chiaradonna F, Sgarbi G, Solaini G, Alberghina L, Lenaz G. Mitochondrial Complex I decrease is responsible for bioenergetic dysfunction in K-ras transformed cells. Biochim Biophys Acta 2010; 1797:314-23; PMID:19931505; http://dx.doi.org/10.1016/j.bbabio.2009.11.006
  • Subramanian A, Kuehn H, Gould J, Tamayo P, Mesirov JP. GSEA-P: a desktop application for Gene Set Enrichment Analysis. Bioinformatics 2007; 23:3251-3; PMID:17644558; http://dx.doi.org/10.1093/bioinformatics/btm369
  • Clocchiatti A, Di Giorgio E, Ingrao S, Meyer-Almes FJ, Tripodo C, Brancolini C. Class IIa HDACs repressive activities on MEF2-depedent transcription are associated with poor prognosis of ER+ breast tumors. FASEB J 2013; 27:942-54; PMID:23159930; http://dx.doi.org/10.1096/fj.12-209346
  • Kerr EM, Gaude E, Turrell FK, Frezza C, Martins CP. Mutant Kras copy number defines metabolic reprogramming and therapeutic susceptibilities. Nature 2016; 531:110-3; PMID:26909577; http://dx.doi.org/10.1038/nature16967
  • Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM, Royer RE, Vander Jagt DL, Semenza GL, Dang CV. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci U S A 2010; 107:2037-42; PMID:20133848; http://dx.doi.org/10.1073/pnas.0914433107
  • Zhai X, Yang Y, Wan J, Zhu R, Wu Y. Inhibition of LDH-A by oxamate induces G2/M arrest, apoptosis and increases radiosensitivity in nasopharyngeal carcinoma cells. Oncol Rep 2013; 30:2983-91; PMID:24064966
  • Fiume L, Manerba M, Vettraino M, Di Stefano G. Impairment of aerobic glycolysis by inhibitors of lactic dehydrogenase hinders the growth of human hepatocellular carcinoma cell lines. Pharmacology 2010; 86:157-62; PMID:20699632; http://dx.doi.org/10.1159/000317519
  • Martinez-Outschoorn UE, Curry JM, Ko YH, Lin Z, Tuluc M, Cognetti D, Birbe RC, Pribitkin E, Bombonati A, Pestell RG, Howell A, Sotgia F, Lisanti MP. Oncogenes and inflammation rewire host energy metabolism in the tumor microenvironment: RAS and NFκB target stromal MCT4. Cell Cycle 2013; 12:2580-97; PMID:23860378; http://dx.doi.org/10.4161/cc.25510
  • Warburg O. On the origin of cancer cells. Science 1956; 123:309-14
  • Hsu PP, Sabatini DM. Cancer cell metabolism: Warburg and beyond. Cell 2008; 134:703-7; PMID:18775299; http://dx.doi.org/10.1016/j.cell.2008.08.021
  • Palorini R, De Rasmo D, Gaviraghi M, Sala Danna L, Signorile A, Cirulli C, Chiaradonna F, Alberghina L, Papa S. Oncogenic K-ras expression is associated with derangement of the cAMP/PKA pathway and forskolin-reversible alterations of mitochondrial dynamics and respiration. Oncogene 2013; 32:352-62; PMID:22410778; http://dx.doi.org/10.1038/onc.2012.50
  • de Candia P, Minopoli G, Verga V, Gargiulo A, Vanoni M, Alberghina L. Nutritional limitation sensitizes mammalian cells to GSK-3β inhibitors and leads to growth impairment. Am J Pathol 2011; 178:1814-23; PMID:21435461; http://dx.doi.org/10.1016/j.ajpath.2010.12.047
  • Wang S, Jiang B, Zhang T, Liu L, Wang Y, Wang Y, Chen X, Lin H, Zhou L, Xia Y, Chen L, Yang C, Xiong Y, Ye D, Guan KL. Insulin and mTOR Pathway Regulate HDAC3-Mediated Deacetylation and Activation of PGK1. PLoS Biol 2015; 13:e1002243
  • Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, Mazure NM. The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1alpha. Cancer Res 2006; 66:3688-98; PMID:16585195; http://dx.doi.org/10.1158/0008-5472.CAN-05-4564
  • Konieczna A, Szczepańska A, Sawiuk K, Węgrzyn G, Łyżeń R. Effects of partial silencing of genes coding for enzymes involved in glycolysis and tricarboxylic acid cycle on the enterance of human fibroblasts to the S phase. BMC Cell Biol 2015; 16:16; PMID:26017754; http://dx.doi.org/10.1186/s12860-015-0062-8
  • Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324:1029-33; PMID:19460998; http://dx.doi.org/10.1126/science.1160809
  • Viale A, Pettazzoni P, Lyssiotis CA, Ying H, Sánchez N, Marchesini M, Carugo A, Green T, Seth S, Giuliani V. et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014; 514:628-32; PMID:25119024; http://dx.doi.org/10.1038/nature13611
  • Hu J, Locasale JW, Bielas JH, O'Sullivan J, Sheahan K, Cantley LC, Vander Heiden MG, Vitkup D. Heterogeneity of tumor-induced gene expression changes in the human metabolic network. Nat Biotechnol 2013; 31:522-9; PMID:23604282; http://dx.doi.org/10.1038/nbt.2530
  • Cavalli LR, Varella-Garcia M, Liang BC. Diminished tumorigenic phenotype after depletion of mitochondrial DNA. Cell Growth Differ 1997; 8:1189-98; PMID:9372242
  • Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J, Bajzikova M, Kovarova J, Peterka M, Yan B, et al. Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 2015; 21:81-94; PMID:25565207; http://dx.doi.org/10.1016/j.cmet.2014.12.003
  • LeBleu VS, O'Connell JT, Gonzalez Herrera KN, Wikman H, Pantel K, Haigis MC, de Carvalho FM, Damascena A, Domingos Chinen LT, Rocha RM, et al. PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat Cell Biol 2014; 16:992-1003; PMID:25241037; http://dx.doi.org/10.1038/ncb3039
  • Barrientos A. In vivo and in organello assessment of OXPHOS activities. Methods 2002; 26:307-16; PMID:12054921; http://dx.doi.org/10.1016/S1046-2023(02)00036-1

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