AMPK and GCN2-ATF4 signal the repression of mitochondria in colon cancer cells

Biochemical Journal

Volumn 444, Issue 2, 2012, Pages 249-259

  Martínez Reyes, Inmaculada ^a   Sánchez Aragó, María ^a   Cuezva, José M ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

ATP synthase; Cancer; Cellular stress; Glycolysis; Mitochondrion; Translational control

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; GENERAL CONTROL NON DEREPRESSIBLE 2 KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; OLIGOMYCIN; PHOSPHOTRANSFERASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CANCER CELL; COLON CANCER; COPY NUMBER VARIATION; ENZYME REPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GLYCOLYSIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MITOCHONDRIAL GENE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; AMP-ACTIVATED PROTEIN KINASES; AUTOPHAGY; COLONIC NEOPLASMS; DNA, MITOCHONDRIAL; ENERGY METABOLISM; ENZYME ACTIVATION; GENE SILENCING; HCT116 CELLS; HUMANS; MITOCHONDRIA; MOLECULAR MIMICRY; NUCLEAR RECEPTOR SUBFAMILY 6, GROUP A, MEMBER 1; SIGNAL TRANSDUCTION;

EID: 84860849741     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111829     Document Type: Article

References (49)

1. Cuezva, J. M., Ortega, A. D., Willers, I., Sanchez-Cenizo, L., Aldea, M. and Sanchez-Arago, M. (2009) The tumor suppressor function of mitochondria: translation into the clinics. Biochim. Biophys. Acta 1792, 1145-1158
2. Wallace, D. C. (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu. Rev. Genet. 39, 359-407
3. Scarpulla, R. C. (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev. 88, 611-638
4. + -ATP synthase: a key regulator of the metabolic phenotype in cancer. Biochim. Biophys. Acta 1807, 543-551
5. Boyer, P. D. (1997) The ATP synthase: a splendid molecular machine. Annu. Rev. Biochem. 66, 717-749
6. Hanahan, D. and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
7. Bissell, M. J. and Hines, W. C. (2011) Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320-329
8. DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G. and Thompson, C. B. (2008) The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7, 11-20
9. Lopez-Rios, F., Sanchez-Arago, M., Garcia-Garcia, E., Ortega, A. D., Berrendero, J. R., Pozo-Rodriguez, F., Lopez-Encuentra, A., Ballestin, C. and Cuezva, J. M. (2007) Loss of the mitochondrial bioenergetic capacity underlies the glucose avidity of carcinomas. Cancer Res. 67, 9013-9017 (Pubitemid 47535883)
10. Cuezva, J. M., Krajewska, M., de Heredia, M. L., Krajewski, S., Santamaria, G., Kim, H., Zapata, J. M., Marusawa, H., Chamorro, M. and Reed, J. C. (2002) The bioenergetic signature of cancer: a marker of tumor progression. Cancer Res. 62, 6674-6681 (Pubitemid 35364137)
11. o-ATP synthase in human colon cancer cells with induced 5-fluorouracil resistance. Cancer Res. 65, 3162-3170
12. Sanchez-Arago, M. and Cuezva, J. M. (2011) The bioenergetic signature of isogenic colon cancer cells predicts the cell death response to treatment with 3-bromopyruvate, iodoacetate or 5-fluorouracil. J. Transl. Med. 9, 19
13. + -ATP synthase in human tumors mediates the metabolic shift of cancer cells to a Warburg phenotype. J. Biol. Chem. 285, 25308-25313
14. 1-ATPase mRNA depends on the regulation of a protein that binds the 3′ untranslated region of the mRNA. Mol. Cell. Biol. 17, 5255-5268
15. 1-ATPase gene expression during mitochondrial biogenesis in liver. J. Biol. Chem. 270, 10342-10350
16. 1-ATPase β-subunit mRNA largely accounts for the decreased ATPase content in brown adipose tissue mitochondria. FEBS Lett. 313, 23-26
17. Martinez-Diez, M., Santamaria, G., Ortega, A. D. and Cuezva, J. M. (2006) Biogenesis and dynamics of mitochondria during the cell cycle: significance of 3′UTRs. PLoS ONE 1, e107
18. 1-ATPase mRNA between the fetal liver and cancer cells. J. Biol. Chem. 275, 7430-7437
19. 1-ATPase mRNA translation in human tumours. Biochem. J. 426, 319-326
20. Margeot, A., Blugeon, C., Sylvestre, J., Vialette, S., Jacq, C. and Corral-Debrinski, M. (2002) In Saccharomyces cerevisiae, ATP2 mRNA sorting to the vicinity of mitochondria is essential for respiratory function. EMBO J. 21, 6893-6904 (Pubitemid 36014561)
21. 1-ATPase mRNA and inhibits its translation. J. Cell Sci. 123, 2685-2696
22. Sanchez-Arago, M., Chamorro, M. and Cuezva, J. M. (2010) Selection of cancer cells with repressed mitochondria triggers colon cancer progression. Carcinogenesis 31, 567-576
23. Hardie, D. G., Scott, J. W., Pan, D. A. and Hudson, E. R. (2003) Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546, 113-120 (Pubitemid 36782291)
24. Berlanga, J. J., Santoyo, J. and De Haro, C. (1999) Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2α kinase. Eur. J. Biochem. 265, 754-762 (Pubitemid 29489008)
25. Berlanga, J. J., Ventoso, I., Harding, H. P., Deng, J., Ron, D., Sonenberg, N., Carrasco, L. and de Haro, C. (2006) Antiviral effect of the mammalian translation initiation factor 2αkinase GCN2 against RNA viruses. EMBO J. 25, 1730-1740
26. Fryer, L. G., Foufelle, F., Barnes, K., Baldwin, S. A., Woods, A. and Carling, D. (2002) Characterization of the role of the AMP-activated protein kinase in the stimulation of glucose transport in skeletal muscle cells. Biochem. J. 363, 167-174 (Pubitemid 34280623)
27. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M. and Ron, D. (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6, 1099-1108
28. Acebo, P., Giner, D., Calvo, P., Blanco-Rivero, A., Ortega, A. D., Fernandez, P. L., Roncador, G., Fernandez-Malave, E., Chamorro, M. and Cuezva, J. M. (2009) Cancer abolishes the tissue type-specific differences in the phenotype of energetic metabolism. Transl. Oncol. 2, 138-145
29. Gong, Y. and Agani, F. H. (2005) Oligomycin inhibits HIF-1α expression in hypoxic tumor cells. Am. J. Physiol. Cell Physiol. 288, C1023-C1029 (Pubitemid 40559378)
30. Sarbassov, D. D., Ali, S. M. and Sabatini, D. M. (2005) Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603 (Pubitemid 41540408)
31. Brunn, G. J., Hudson, C. C., Sekulic, A., Williams, J. M., Hosoi, H., Houghton, P. J., Lawrence, Jr, J.C. and Abraham, R. T. (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277, 99-101 (Pubitemid 27450655)
32. Silvera, D., Formenti, S. C. and Schneider, R. J. (2010) Translational control in cancer. Nat. Rev. Cancer 10, 254-266
33. Hao, W., Chang, C. P., Tsao, C. C. and Xu, J. (2010) Oligomycin-induced bioenergetic adaptation in cancer cells with heterogeneous bioenergetic organization. J. Biol. Chem. 285, 12647-12654
34. Kahn, B. B., Alquier, T., Carling, D. and Hardie, D. G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1, 15-25 (Pubitemid 43960587)
35. Jeninga, E. H., Schoonjans, K. and Auwerx, J. (2010) Reversible acetylation of PGC-1: connecting energy sensors and effectors to guarantee metabolic flexibility. Oncogene 29, 4617-4624
36. Schieke, S. M., Phillips, D., McCoy, Jr, J.P., Aponte, A. M., Shen, R. F., Balaban, R. S. and Finkel, T. (2006) The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281, 27643-27652 (Pubitemid 44401789)
37. Ouchi, N., Shibata, R. and Walsh, K. (2005) AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ. Res. 96, 838-846 (Pubitemid 40604967)
38. Ye, J., Kumanova, M., Hart, L. S., Sloane, K., Zhang, H., De Panis, D. N., Bobrovnikova-Marjon, E., Diehl, J. A., Ron, D. and Koumenis, C. (2010) The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J. 29, 2082-2096
39. Baba, Y., Nosho, K., Shima, K., Meyerhardt, J. A., Chan, A. T., Engelman, J. A., Cantley, L. C., Loda, M., Giovannucci, E., Fuchs, C. S. and Ogino, S. (2010) Prognostic significance of AMP-activated protein kinase expression and modifying effect of MAPK3/1 in colorectal cancer. Br. J. Cancer 103, 1025-1033
40. Buckendahl, A. C., Budczies, J., Fiehn, O., Darb-Esfahani, S., Kind, T., Noske, A., Weichert, W., Sehouli, J., Braicu, E., Dietel, M. and Denkert, C. (2011) Prognostic impact of AMP-activated protein kinase expression in ovarian carcinoma: correlation of protein expression and GC/TOF-MS-based metabolomics. Oncol. Rep. 25, 1005-1012
41. Ortega, A. D., Sala, S., Espinosa, E., Gonzalez-Baron, M. and Cuezva, J. M. (2008) HuR and the bioenergetic signature of breast cancer: a low tumor expression of the RNAbinding protein predicts a higher risk of disease recurrence. Carcinogenesis 29, 2053-2061
42. Keene, J. D. (2007) RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8, 533-543
43. Izquierdo, J. M. and Cuezva, J. M. (2005) Epigenetic regulation of the binding activity of translation inhibitory proteins that bind the 3′ untranslated region of β-F1-ATPase mRNA by adenine nucleotides and the redox state. Arch. Biochem. Biophys. 433, 481-486 (Pubitemid 39592803)
44. Wang, W., Fan, J., Yang, X., Furer-Galban, S., Lopez de Silanes, I., von Kobbe, C., Guo, J., Georas, S. N., Foufelle, F., Hardie, D. G. et al. (2002) AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell. Biol. 22, 3425-3436 (Pubitemid 34453982)
45. van Veelen, W., Korsse, S. E., van de Laar, L. and Peppelenbosch, M. P. (2011) The long and winding road to rational treatment of cancer associated with LKB1/AMPK/TSC/mTORC1 signaling. Oncogene 30, 2289-2303
46. Janes, M. R., Limon, J. J., So, L., Chen, J., Lim, R. J., Chavez, M. A., Vu, C., Lilly, M. B., Mallya, S., Ong, S. T. et al. (2010) Effective and selective targeting of leukemia cells using a TORC1/2 kinase inhibitor. Nat. Med. 16, 205-213
47. Kim, H. S., Hwang, J. T., Yun, H., Chi, S. G., Lee, S. J., Kang, I., Yoon, K. S., Choe, W. J., Kim, S. S. and Ha, J. (2008) Inhibition of AMP-activated protein kinase sensitizes cancer cells to cisplatin-induced apoptosis via hyper-induction of p53. J. Biol. Chem. 283, 3731-3742
48. Liu, L., Cash, T. P., Jones, R. G., Keith, B., Thompson, C. B. and Simon, M. C. (2006) Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21, 521-531 (Pubitemid 43228007)
49. Yun, H., Lee, M., Kim, S. S. and Ha, J. (2005) Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J. Biol. Chem. 280, 9963-9972 (Pubitemid 40395845)