The mitochondrial bioenergetic capacity of carcinomas

IUBMB Life

Volumn 62, Issue 7, 2010, Pages 554-560

  Formentini, Laura ^a   Martínez Reyes, Inmaculada ^a   Cuezva, Jose M ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Cancer; Energetic metabolism.; Glycolysis; Mitochondria; Warburg phenotype

Indexed keywords

ADENOSINE TRIPHOSPHATASE;

BIOENERGY; BIOGENESIS; CANCER CELL; CANCER THERAPY; CARCINOMA; CELL PROLIFERATION; ENZYME PHOSPHORYLATION; EPIGENETICS; EPITHELIUM TUMOR; GLYCOLYSIS; HUMAN; METABOLISM; MITOCHONDRION; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REVIEW; TREATMENT RESPONSE; TUMOR CELL; TUMOR GENE;

EID: 77955906912     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.00352     Document Type: Review

References (57)

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. Hanahan, D., and Weinberg, R. A. (2000) The hallmarks of cancer. Cell 100, 57-70.
3. Schulz, T. J., Thierbach, R., Voigt, A., Drewes, G., Mietzner, B., Steinberg, P., Pfeiffer, A. F., and Ristow, M. (2006) Induction of oxidative metabolism by mitochondrial frataxin inhibits cancer growth: Otto Warburg revisited. J. Biol. Chem. 281, 977-981.
4. Kroemer, G., and Pouyssegur, J. (2008) Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13, 472-482.
5. 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.
6. Thierbach, R., Schulz, T. J., Isken, F., Voigt, A., Mietzner, B., Drewes, G., von Kleist-Retzow, J. C., Wiesner, R. J., Magnuson, M. A., Puccio, H., Pfeiffer, A. F., Steinberg, P., and Ristow, M. (2005) Targeted disruption of hepatic frataxin expression causes impaired mitochondrial function, decreased life span and tumor growth in mice. Hum. Mol. Genet. 14, 3857-3864.
7. Kroemer, G. (2006) Mitochondria in cancer. Oncogene 25, 4630-4632.
8. Vander Heiden, M. G., Cantley, L. C., and Thompson, C. B. (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033.
9. Warburg, O., Wind, F., Negelein, E. (1927) The metabolism of tumors in the body. J. Gen. Physiol. 8, 519-530.
10. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314.
11. Warburg, O. (1956) On respiratory impairment in cancer cells. Science 124, 269-270.
12. Cuezva, J. M., Sanchez-Arago, M., Sala, S., Blanco-Rivero, A., Ortega, A. D. (2007) A message emerging from development: the repression of mitochondrial beta-F1-ATPase expression in cancer. J. Bioenerg. Biomembr. 39, 259-265.
13. Tu, B. P., and McKnight, S. L. (2006) Metabolic cycles as an underlying basis of biological oscillations. Nat. Rev. Mol. Cell Biol. 7, 696-701.
14. Schieke, S. M., McCoy, J. P., Jr., and Finkel, T. (2008) Coordination of mitochondrial bioenergetics with G1 phase cell cycle progression. Cell Cycle 7, 1782-1787.
15. Wang, C., Li, Z., Lu, Y., Du, R., Katiyar, S., Yang, J., Fu, M., Leader, J.E., Quong, A., Novikoff, P. M., and Pestell, R. G. (2006) Cyclin D1 repression of nuclear respiratory factor 1 integrates nuclear DNA synthesis and mitochondrial function. Proc. Natl. Acad. Sci. USA 103, 11567-11572.
16. Morrish, F., Neretti, N., Sedivy, J. M., and Hockenbery, D. M. (2008) The oncogene c-Myc coordinates regulation of metabolic networks to enable rapid cell cycle entry. Cell Cycle 7, 1054-1066.
17. 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.
18. Kovacevic, Z., and Morris, H. P. (1972) The role of glutamine in the oxidative metabolism of malignant cells. Cancer Res. 32, 326-333.
19. Valcarce, C., Navarrete, R. M., Encabo, P., Loeches, E., Satrustegui, J., and Cuezva, J. M. (1988) Postnatal development of rat liver mitochondrial functions. The roles of protein synthesis and of adenine nucleotides. J. Biol. Chem. 263, 7767-7775.
20. Sánchez-Aragó , M., Chamorro, M, and Cuezva, J. M. (2010) Selection of cancer cells with repressed mitochondria triggers colon cancer progression. Carcinogenesis 31, 567-576.
21. de Heredia, M. L., Izquierdo, J. M., and Cuezva, J. M. (2000) A conserved mechanism for controlling the translation of beta-F1-ATPase mRNA between the fetal liver and cancer cells. J. Biol. Chem. 275, 7430-7437.
22. Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., Fleming, M. D., Schreiber, S. L., and Cantley, L. C. (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233.
23. LaNoue, K. H., Ohnishi, J. G., Morris, T., and Williamson, H. P., Jr. (1974) Defects of anions and electron transport in morris hepatoma mitochondria. In: Hormones and Cancer (McKerns KW, ed.). pp. 131-165, New York, Academic Press.
24. Pedersen, P. L. (1978) Tumor mitochondria and the bioenergetics of cancer cells. Prog. Exp. Tumor Res. 22, 190-274.
25. Hoberman, H. D. (1975) Is there a role for mitochondrial genes in carcinogenesis? Cancer Res. 35, 3332-3335.
26. Gause, G.F. (1969) Cancer and mitochondrial DNA. Br. Med. J. 3, 413-414.
27. Brandon, M., Baldi, P., and Wallace, D. C. (2006) Mitochondrial mutations in cancer. Oncogene 25, 4647-4662.
28. King, A., Selak, M. A., and Gottlieb, E. (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25, 4675-4682.
29. Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., Marks, K. M., Prins, R. M., Ward, P. S., Yen, K. E., Liau, L. M., Rabinowitz, J. D., Cantley, L. C., Thompson, C. B., Vander Heiden, M. G., and Su, S. M. (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739-744.
30. 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.
31. Lin, P. C., Lin, J. K., Yang, S. H., Wang, H. S., Li, A. F., and Chang, S. C. (2008) Expression of beta-F1-ATPase and mitochondrial transcription factor A and the change in mitochondrial DNA content in colorectal cancer: clinical data analysis and evidence from an in vitro study. Int. J. Colorectal Dis. 23, 1223-1232.
32. 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.
33. 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 RNA-binding protein predicts a higher risk of disease recurrence. Carcinogenesis 29, 2053-2061.
34. Isidoro, A., Casado, E., Redondo, A., Acebo, P., Espinosa, E., Alonso, A. M., Cejas, P., Hardisson, D., Fresno Vara, J. A., Belda-Iniesta, C., Gonzalez-Baron, M., and Cuezva, J. M. (2005) Breast carcinomas fulfill the Warburg hypothesis and provide metabolic markers of cancer prognosis. Carcinogenesis 26, 2095-2104.
35. Cuezva, J. M., Chen, G., Alonso, A. M., Isidoro, A., Misek, D. E., Hanash, S. M., and Beer, D. G. (2004) The bioenergetic signature of lung adenocarcinomas is a molecular marker of cancer diagnosis and prognosis. Carcinogenesis 25, 1157-1163.
36. Santamaria, G., Martinez-Diez, M., Fabregat, I., and Cuezva, J. M. (2006) Efficient execution of cell death in non-glycolytic cells requires the generation of ROS controlled by the activity of mitochondrial H1-ATP synthase. Carcinogenesis 27, 925-935.
37. Shin, Y. K., Yoo, B. C., Chang, H. J., Jeon, E., Hong, S. H., Jung, M. S., Lim, S. J., and Park, J. G. (2005) Down-regulation of mitochondrial F1F0-ATP synthase in human colon cancer cells with induced 5-fluorouracil resistance. Cancer Res. 65, 3162-3170.
38. Izquierdo, J. M., and Cuezva, J. M. (1997) Control of the translational efficiency of beta-F1-ATPase mRNA depends on the regulation of a protein that binds the 30 untranslated region of the mRNA. Mol. Cell Biol. 17, 5255-5268.
39. Martinez-Diez, M., Santamaria, G., Ortega, A. D., and Cuezva, J. M. (2006) Biogenesis and dynamics of mitochondria during the cell cycle: significance of 30UTRs. PLoS ONE 1, e107.
40. Willers, I. M., Isidoro, A., Ortega, A. D., Fernández, P. L., and Cuezva, J. M. (2010) Selective inhibition of beta-F1-ATPase mRNA translation in human tumors. Biochem. J. 426, 319-326.
41. Izquierdo, J. M., and Cuezva, J. M. (2000) Internal-ribosome-entry-site functional activity of the 30-untranslated region of the mRNA for the beta subunit of mitochondrial H1-ATP synthase. Biochem. J. 346(Pt 3), 849-855.
42. Li, R. J., Zhang, G. S., Chen, Y. H., Zhu, J. F., Lu, Q. J., Gong, F. J., and Kuang, W. Y. (2009) Down-regulation of mitochondrial ATPase by hypermethylation mechanism in chronic myeloid leukemia is associated with multidrug resistance. Ann. Oncol. [Epub ahead of print].
43. Osthus, R. C., Shim, H., Kim, S., Li, Q., Reddy, R., Mukherjee, M., Xu, Y., Wonsey, D., Lee, L. A., and Dang, C. V. (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J. Biol. Chem. 275, 21797-21800.
44. Kovacevic, Z., and Morris, H. P. (1972) The role of glutamine in the oxidative metabolism of malignant cells. Cancer Res. 32, 326-333.
45. Gao, P., Tchernyshyov, I., Chang, T. C., Lee, Y. S., Kita, K., Ochi, T., Zeller, K. I., De Marzo, A. M., Van Eyk, J. E., Mendell, J. T., and Dang, C. V. (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458, 762-765.
46. David, C. J., Chen, M., Assanah, M., Canoll, P., and Manley, J. L. (2010) HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 463, 364-368.
47. Semenza, G. L. (2008) Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life. 60, 591-597.
48. Kim, J. W., Gao, P., Liu, Y. C., Semenza, G. L., and Dang, C. V. (2007) Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol. Cell Biol. 27, 7381-7393.
49. Zhang, H., Gao, P., Fukuda, R., Kumar, G., Krishnamachary, B., Zeller, K. I., Dang, C. V., and Semenza, G. L. (2007) HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11, 407-420.
50. Fukuda, R., Zhang, H., Kim, J. W., Shimoda, L., Dang, C. V., and Semenza, G. L. (2007) HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129, 111-122.
51. Govindarajan, B., Sligh, J. E., Vincent, B. J., Li, M., Canter, J. A., Nickoloff, B. J., Rodenburg, R. J., Smeitink, J. A., Oberley, L., Zhang, Y., Slingerland, J., Arnold, R. S., Lambeth, J. D., Cohen, C., Hilenski, L., Griendling, K., Martinez-Diez, M., Cuezva, J. M., and Arbiser, J. L. (2007) Overexpression of Akt converts radial growth melanoma to vertical growth melanoma. J. Clin. Invest. 117, 719-729.
52. Plas, D. R., and Thompson, C. B. (2005) Akt-dependent transformation: there is more to growth than just surviving. Oncogene 24, 7435-7442.
53. Pelicano, H., Xu, R. H., Du, M., Feng, L., Sasaki, R., Carew, J. S., Hu, Y., Ramdas, L., Hu, L., Keating, M. J., Zhang, W., Plunkett, W., and Huang, P. (2006) Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J. Cell Biol. 175, 913-923.
54. Bensaad, K., Tsuruta, A., Selak, M. A., Vidal, M. N., Nakano, K., Bartrons, R., Gottlieb, E., and Vousden, K. H. (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126, 107-120.
55. Matoba, S., Kang, J. G., Patino, W. D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P. J., Bunz, F., and Hwang, P. M. (2006) p53 regulates mitochondrial respiration. Science 312, 1650-1653.
56. Almeida, A., Bolanos, J. P., and Moncada, S. (2010) E3 ubiquitin ligase APC/C-Cdh1 accounts for the Warburg effect by linking glycolysis to cell proliferation. Proc. Natl. Acad. Sci. USA 107, 738-741.
57. Liu, X., Wang, X., Zhang, J., Lam, E. K., Shin, V. Y., Cheng, A. S., Yu, J., Chan, F. K., Sung, J. J., and Jin, H. C. (2010) Warburg effect revisited: an epigenetic link between glycolysis and gastric carcinogenesis. Oncogene 29, 442-450.