Rapamycin increases mitochondrial efficiency by mtDNAdependent reprogramming of mitochondrial metabolism in Drosophila

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2282-2290

  Villa Cuesta, Eugenia ^a   Holmbeck, Marissa A ^b   Rand, David M ^b  

^a ADELPHI UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

Metabolism; Mitochondrial genotype; Rapamycin

Indexed keywords

HYDROGEN PEROXIDE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; RAPAMYCIN; SUCCINATE DEHYDROGENASE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; DROSOPHILA SIMULANS; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; METABOLOMICS; MITOCHONDRIAL GENOME; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; ANIMAL; DOWN REGULATION; DRUG EFFECTS; GENETICS; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION;

ANIMALS; DNA, MITOCHONDRIAL; DOWN-REGULATION; DROSOPHILA MELANOGASTER; FEMALE; MITOCHONDRIA; OXIDATION-REDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84900823606     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.142026     Document Type: Article

References (48)

1. Balaban, R. S., Nemoto, S. and Finkel, T. (2005). Mitochondria, oxidants, and aging. Cell 120, 483-495.
2. Ballard, J. W. O. and Rand, D. M. (2005). The population biology of mitochondrial dna and its phylogenetic implications. Annu. Rev. Ecol. Evol. Syst. 36, 621-642.
3. Baltzer, C., Tiefenböck, S. K. and Frei, C. (2010). Mitochondria in response to nutrients and nutrient-sensitive pathways. Mitochondrion 10, 589-597.
4. Barrientos, A. (2002). In vivo and in organello assessment of OXPHOS activities. Methods 26, 307-316.
5. Bentzinger, C. F., Romanino, K., Cloëtta, D., Lin, S., Mascarenhas, J. B., Oliveri, F., Xia, J., Casanova, E., Costa, C. F., Brink, M. et al. (2008). Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab. 8, 411-424.
6. Bjedov, I., Toivonen, J. M., Kerr, F., Slack, C., Jacobson, J., Foley, A. and Partridge, L. (2010). Mechanisms of life span extension by rapamycin in the fruit fly Drosophila melanogaster. Cell Metab. 11, 35-46.
7. Bonawitz, N. D., Chatenay-Lapointe, M., Pan, Y. and Shadel, G. S. (2007). Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 5, 265-277.
8. Brière, J.-J., Favier, J., El Ghouzzi, V., Djouadi, F., Bénit, P., Gimenez, A. P. and Rustin, P. (2005). Succinate dehydrogenase deficiency in human. Cell. Mol. Life Sci. 62, 2317-2324.
9. Brown, N. F., Stefanovic-Racic, M., Sipula, I. J. and Perdomo, G. (2007). The mammalian target of rapamycin regulates lipid metabolism in primary cultures of rat hepatocytes. Metabolism 56, 1500-1507.
10. Cecchini, G. (2003). Function and structure of complex II of the respiratory chain. Annu. Rev. Biochem. 72, 77-109.
11. Cheng, Z. and Ristow, M. (2013). Mitochondria and metabolic homeostasis. Antioxid. Redox Signal. 19, 240-242.
12. Csibi, A., Fendt, S.-M., Li, C., Poulogiannis, G., Choo, A. Y., Chapski, D. J., Jeong, S. M., Dempsey, J. M., Parkhitko, A., Morrison, T. et al. (2013). The mTORC1 pathway stimulates glutamine metabolism and cell proliferation by repressing SIRT4. Cell 153, 840-854.
13. Cunningham, J. T., Rodgers, J. T., Arlow, D. H., Vazquez, F., Mootha, V. K. and Puigserver, P. (2007). mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450, 736-740.
14. Dazert, E. and Hall, M. N. (2011). mTOR signaling in disease. Curr. Opin. Cell Biol. 23, 744-755.
15. Düvel, K., Yecies, J. L., Menon, S., Raman, P., Lipovsky, A. I., Souza, A. L., Triantafellow, E., Ma, Q., Gorski, R., Cleaver, S. et al. (2010). Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol. Cell 39, 171-183.
16. Finley, L. W. S. and Haigis, M. C. (2009). The coordination of nuclear and mitochondrial communication during aging and calorie restriction. Ageing Res. Rev. 8, 173-188.
17. Fukui, H. and Moraes, C. T. (2008). The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci. 31, 251-256.
18. Harman, D. (1956). Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
19. Ishii, N., Ishii, T. and Hartman, P. S. (2007). The role of the electron transport SDHC gene on lifespan and cancer. Mitochondrion 7, 24-28.
20. King, A., Selak, M. A. and Gottlieb, E. (2006). Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25, 4675-4682.
21. Lane, N. (2005). Power, Sex, Suicide: Mitochondria and the Meaning of Life. New York, NY: Oxford University Press.
22. Laplante, M. and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
23. Liu, Z. and Butow, R. A. (2006). Mitochondrial retrograde signaling. Annu. Rev. Genet. 40, 159-185.
24. Masoro, E. J., Yu, B. P. and Bertrand, H. A. (1982). Action of food restriction in delaying the aging process. Proc. Natl. Acad. Sci. USA 79, 4239-4241.
25. Mathew, R. and White, E. (2011). Autophagy in tumorigenesis and energy metabolism: friend by day, foe by night. Curr. Opin. Genet. Dev. 21, 113-119.
26. Meiklejohn, C. D., Holmbeck, M. A., Siddiq, M. A., Abt, D. N., Rand, D. M. and Montooth, K. L. (2013). An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9, e1003238.
27. Montooth, K. L., Meiklejohn, C. D., Abt, D. N. and Rand, D. M. (2010). Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to fixed incompatibilities between species of Drosophila. Evolution 64, 3364-3379.
28. Murphy, M. P., Holmgren, A., Larsson, N.-G., Halliwell, B., Chang, C. J., Kalyanaraman, B., Rhee, S. G., Thornalley, P. J., Partridge, L., Gems, D. et al. (2011). Unraveling the biological roles of reactive oxygen species. Cell Metab. 13, 361-366.
29. Paglin, S., Lee, N.-Y., Nakar, C., Fitzgerald, M., Plotkin, J., Deuel, B., Hackett, N., McMahill, M., Sphicas, E., Lampen, N. et al. (2005). Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res. 65, 11061-11070.
30. Pan, Y., Nishida, Y., Wang, M. and Verdin, E. (2012). Metabolic regulation, mitochondria and the life-prolonging effect of rapamycin: a mini-review. Gerontology 58, 524-530.
31. Pesole, G., Allen, J. F., Lane, N., Martin, W., Rand, D. M., Schatz, G. and Saccone, C. (2012). The neglected genome. EMBO Rep. 13, 473-474.
32. Polak, P., Cybulski, N., Feige, J. N., Auwerx, J., Rüegg, M. A. and Hall, M. N. (2008). Adipose-specific knockout of raptor results in lean mice with enhanced mitochondrial respiration. Cell Metab. 8, 399-410.
33. Raffaello, A. and Rizzuto, R. (2011). Mitochondrial longevity pathways. Biochim. Biophys. Acta 1813, 260-268.
34. Ramanathan, A. and Schreiber, S. L. (2009). Direct control of mitochondrial function by mTOR. Proc. Natl. Acad. Sci. USA 106, 22229-22232.
35. Rand, D. M., Haney, R. A. and Fry, A. J. (2004). Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19, 645-653.
36. Richter, J. D. and Sonenberg, N. (2005). Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433, 477-480.
37. Ristow, M. (2006). Oxidative metabolism in cancer growth. Curr. Opin. Clin. Nutr. Metab. Care 9, 339-345.
38. Ristow, M. and Schmeisser, S. (2011). Extending life span by increasing oxidative stress. Free Radic. Biol. Med. 51, 327-336.
39. Scheffler, I. E. (2007). Mitochondria (Scheffler, Mitochondria). Wiley-Liss.
40. Schieke, S. M. and Finkel, T. (2006). Mitochondrial signaling, TOR, and life span. Biol. Chem. 387, 1357-1361.
41. Schieke, S. M., Phillips, D., McCoy, J. P., Jr, 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.
42. Sharp, Z. D. and Richardson, A. (2011). Aging and cancer: can mTOR inhibitors kill two birds with one drug? Target. Oncol. 6, 41-51.
43. Soliman, G. A. (2011). The integral role of mTOR in lipid metabolism. Cell Cycle 10, 861-862.
44. Tatsuta, T. and Langer, T. (2008). Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J. 27, 306-314.
45. Vendelbo, M. H. and Nair, K. S. (2011). Mitochondrial longevity pathways. Biochim. Biophys. Acta 1813, 634-644.
46. Wiederkehr, A. and Wollheim, C. B. (2006). Minireview: implication of mitochondria in insulin secretion and action. Endocrinology 147, 2643-2649.
47. Woodson, J. D. and Chory, J. (2008). Coordination of gene expression between organellar and nuclear genomes. Nat. Rev. Genet. 9, 383-395.
48. Zoncu, R., Efeyan, A. and Sabatini, D. M. (2011). mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol. 12, 21-35.