Deletion of the mitochondrial chaperone TRAP-1 uncovers global reprogramming of metabolic networks

Cell Reports

Volumn 8, Issue 3, 2014, Pages 671-677

  Lisanti, Sofia ^a   Tavecchio, Michele ^a   Chae, Young Chan ^a   Liu, Qin ^a   Brice, Angela K ^b   Thakur, Madhukar L ^c   Languino, Lucia R ^a,c   Altieri, Dario C ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN B1; CYCLIN DEPENDENT KINASE 2; HEAT SHOCK PROTEIN 90; MITOCHONDRIAL COMPLEX II; MITOCHONDRIAL COMPLEX IV; OXIDOREDUCTASE; PROTEIN P21; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTOME; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG; TRAP-1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DYSPLASIA; EMBRYO; ENZYME ACTIVITY; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE DELETION; GLYCOLYSIS; IN VIVO STUDY; INCIDENCE; KNOCKOUT MOUSE; LIVER CELL; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OBESITY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TISSUE DEGENERATION; TRAP 1 GENE; UPREGULATION; WILD TYPE; AGING; ANIMAL; C57BL MOUSE; DNA DAMAGE; GENETICS; METABOLISM; MITOCHONDRION;

MUS;

AGING; ANIMALS; CARCINOGENESIS; CELL PROLIFERATION; CELLULAR REPROGRAMMING; DNA DAMAGE; GENE DELETION; GLYCOLYSIS; HSP90 HEAT-SHOCK PROTEINS; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OBESITY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; TRANSCRIPTOME;

EID: 84924602116     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.06.061     Document Type: Article

References (32)

1. Agorreta, J., Hu, J., Liu, D., Delia, D., Turley, H., Ferguson, D.J., Iborra, F., Pajares, M.J., Larrayoz, M., Zudaire, I., et al. (2014). TRAP1 regulates proliferation, mitochondrial function, and has prognostic significance in NSCLC. Mol. Cancer Res. 12, 660-669.
2. Altieri, D.C., Stein, G.S., Lian, J.B., and Languino, L.R. (2012). TRAP-1, the mitochondrial Hsp90. Biochim. Biophys. Acta 1823, 767-773.
3. Balch, W.E., Morimoto, R.I., Dillin, A., and Kelly, J.W. (2008). Adapting proteostasis for disease intervention. Science 319, 916-919.
4. Butler, E.K., Voigt, A., Lutz, A.K., Toegel, J.P., Gerhardt, E., Karsten, P., Falkenburger, B., Reinartz, A., Winklhofer, K.F., and Schulz, J.B. (2012). The mitochondrial chaperone protein TRAP1 mitigates α-Synuclein toxicity. PLoS Genet. 8, e1002488.
5. Butow, R.A., and Avadhani, N.G. (2004). Mitochondrial signaling: the retrograde response. Mol. Cell 14, 1-15.
6. Caino, M.C., Chae, Y.C., Vaira, V., Ferrero, S., Nosotti, M., Martin, N.M., Weeraratna, A., O'Connell, M., Jernigan, D., Fatatis, A., et al. (2013). Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells. J. Clin. Invest. 123, 2907-2920.
7. Chae, Y.C., Caino, M.C., Lisanti, S., Ghosh, J.C., Dohi, T., Danial, N.N., Villanueva, J., Ferrero, S., Vaira, V., Santambrogio, L., et al. (2012). Control of tumor bioenergetics and survival stress signaling by mitochondrial HSP90s. Cancer Cell 22, 331-344.
8. Chae, Y.C., Angelin, A., Lisanti, S., Kossenkov, A.V., Speicher, K.D., Wang, H., Powers, J.F., Tischler, A.S., Pacak, K., Fliedner, S., et al. (2013). Landscape of the mitochondrial Hsp90 metabolome in tumours. Nat. Commun. 4, 2139.
9. Costa, A.C., Loh, S.H., and Martins, L.M. (2013). Drosophila Trap1 protects against mitochondrial dysfunction in a PINK1/parkin model of Parkinson's disease. Cell Death Dis. 4, e467.
10. Ellis, R.J. (2007). Protein misassembly: macromolecular crowding and molecular chaperones. Adv. Exp. Med. Biol. 594, 1-13.
11. Frezza, C., Zheng, L., Folger, O., Rajagopalan, K.N., MacKenzie, E.D., Jerby, L., Micaroni, M., Chaneton, B., Adam, J., Hedley, A., et al. (2011). Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature 477, 225-228.
12. Gorgoulis, V.G., Vassiliou, L.V., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., Ditullio, R.A., Jr., Kastrinakis, N.G., Levy, B., et al. (2005). Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913.
13. Guarente, L. (2008). Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 132, 171-176.
14. Guertin, D.A., and Sabatini, D.M. (2007). Defining the role of mTOR in cancer. Cancer Cell 12, 9-22.
15. Haq, R., Shoag, J., Andreu-Perez, P., Yokoyama, S., Edelman, H., Rowe, G.C., Frederick, D.T., Hurley, A.D., Nellore, A., Kung, A.L., et al. (2013). Oncogenic BRAF regulates oxidative metabolism via PGC1α and MITF. Cancer Cell 23, 302-315.
16. Janiszewska, M., Suvà, M.L., Riggi, N., Houtkooper, R.H., Auwerx, J., Clément-Schatlo, V., Radovanovic, I., Rheinbay, E., Provero, P., and Stamenkovic, I. (2012). Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells. Genes Dev. 26, 1926-1944.
17. Kang, B.H., Plescia, J., Dohi, T., Rosa, J., Doxsey, S.J., and Altieri, D.C. (2007). Regulation of tumor cell mitochondrial homeostasis by an organelle-specific Hsp90 chaperone network. Cell 131, 257-270.
18. Kimmelman, A.C. (2011). The dynamic nature of autophagy in cancer. Genes Dev. 25, 1999-2010.
19. Lavery, L.A., Partridge, J.R., Ramelot, T.A., Elnatan, D., Kennedy, M.A., and Agard, D.A. (2014). Structural asymmetry in the closed state of mitochondrial Hsp90 (TRAP1) supports a two-step ATP hydrolysis mechanism. Mol. Cell 53, 330-343.
20. Liang, J., and Mills, G.B. (2013). AMPK: a contextual oncogene or tumor suppressor? Cancer Res. 73, 2929-2935.
21. Lu, C., Ward, P.S., Kapoor, G.S., Rohle, D., Turcan, S., Abdel-Wahab, O., Edwards, C.R., Khanin, R., Figueroa, M.E., Melnick, A., et al. (2012). IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483, 474-478.
22. Merksamer, P.I., Liu, Y., He, W., Hirschey, M.D., Chen, D., and Verdin, E. (2013). The sirtuins, oxidative stress and aging: an emerging link. Aging (Albany, N.Y. Online) 5, 144-150.
23. Nisoli, E., Tonello, C., Cardile, A., Cozzi, V., Bracale, R., Tedesco, L., Falcone, S., Valerio, A., Cantoni, O., Clementi, E., et al. (2005). Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314-317.
24. Pridgeon, J.W., Olzmann, J.A., Chin, L.S., and Li, L. (2007). PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol. 5, e172.
25. Schulz, T.J., Zarse, K., Voigt, A., Urban, N., Birringer, M., and Ristow, M. (2007). Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab. 6, 280-293.
26. Sciacovelli, M., Guzzo, G., Morello, V., Frezza, C., Zheng, L., Nannini, N., Calabrese, F., Laudiero, G., Esposito, F., Landriscina, M., et al. (2013). The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase. Cell Metab. 17, 988-999.
27. Selak, M.A., Armour, S.M., MacKenzie, E.D., Boulahbel, H., Watson, D.G., Mansfield, K.D., Pan, Y., Simon, M.C., Thompson, C.B., and Gottlieb, E. (2005). Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7, 77-85.
28. Taipale, M., Jarosz, D.F., and Lindquist, S. (2010). HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 11, 515-528.
29. Turcan, S., Rohle, D., Goenka, A., Walsh, L.A., Fang, F., Yilmaz, E., Campos, C., Fabius, A.W., Lu, C., Ward, P.S., et al. (2012). IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483, 479-483.
30. Wallace, D.C. (2012). Mitochondria and cancer. Nat. Rev. Cancer 12, 685-698.
31. Ward, P.S., and Thompson, C.B. (2012). Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 21, 297-308.
32. Yoshida, S., Tsutsumi, S., Muhlebach, G., Sourbier, C., Lee, M.J., Lee, S., Vartholomaiou, E., Tatokoro, M., Beebe, K., Miyajima, N., et al. (2013). Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis. Proc. Natl. Acad. Sci. USA 110, E1604-E1612.