Decrease in cytochrome c oxidase reserve capacity diminishes robustness of Drosophila melanogaster and shortens lifespan

Biochemical Journal

Volumn 459, Issue 1, 2014, Pages 127-135

  Klichko, Vladimir ^a   Sohal, Barbara H ^b   Radyuk, Svetlana N ^a   Orr, William C ^a   Sohal, Rajindar S ^b  

^a SOUTHERN METHODIST UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aging; Cytochrome c oxidase (CcO); Drosophila melanogaster; Lifespan; Mitochondrion

Indexed keywords

CYTOCHROME C OXIDASE; HOLOENZYME; MESSENGER RNA;

AGING; ARTICLE; CONTROLLED STUDY; DROSOPHILA; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; IMMUNOBLOTTING; LIFESPAN; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SURVIVAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; LONGEVITY; MALE; MOTOR ACTIVITY;

EID: 84896131739     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131370     Document Type: Article

References (51)

1. Muller-Hocker, J., Schafer, S., Link, T. A., Possekel, S. and Hammer, C. (1996) Defects of the respiratory chain in various tissues of old monkeys: a cytochemicalimmunocytochemical study. Mech. Ageing Dev. 86, 197-213 (Pubitemid 26134555)
2. Andreu, A. L., Arbos, M. A., Perez-Martos, A., Lopez-Perez, M. J., Asin, J., Lopez, N., Montoya, J. and Schwartz, S. (1998) Reduced mitochondrial DNA transcription in senescent rat heart. Biochem. Biophys. Res. Commun. 252, 577-581 (Pubitemid 28556819)
3. Navarro, A. and Boveris, A. (2004) Rat brain and liver mitochondria develop oxidative stress and lose enzymatic activities on aging. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1244-R1249 (Pubitemid 39391072)
4. Kwong, L. K. and Sohal, R. S. (2000) Age-related changes in activities of mitochondrial electron transport complexes in various tissues of the mouse. Arch. Biochem. Biophys. 373, 16-22 (Pubitemid 30046485)
5. Ferrandiz, M. L., Martinez, M., De Juan, E., Diez, A., Bustos, G. and Miquel, J. (1994) Impairment of mitochondrial oxidative phosphorylation in the brain of aged mice. Brain Res. 644, 335-338 (Pubitemid 24127992)
6. Morel, F., Mazet, F., Touraille, S. and Alziari, S. (1995) Changes in the respiratory chain complexes activities and in the mitochondrial DNA content during ageing in D. subobscura . Mech. Ageing Dev. 84, 171-181 (Pubitemid 26012444)
7. Ferguson, M., Mockett, R. J., Shen, Y., Orr, W. C. and Sohal, R. S. (2005) Age-associated decline in mitochondrial respiration and electron transport in Drosophila melanogaster . Biochem. J. 390, 501-511 (Pubitemid 41337112)
8. Capaldi, R. A. (1990) Structure and function of cytochrome c oxidase. Annu. Rev. Biochem. 59, 569-596
9. Szuplewski, S. and Terracol, R. (2001) The cyclope gene of Drosophila encodes a cytochrome c oxidase subunit VIc homolog. Genetics 158, 1629-1643 (Pubitemid 32783145)
10. Kadenbach, B., Huttemann, M., Arnold, S., Lee, I. and Bender, E. (2000) Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase. Free Radic. Biol. Med. 29, 211-221
11. Richter, O. M. and Ludwig, B. (2003) Cytochrome c oxidase: structure, function, and physiology of a redox-driven molecular machine. Rev. Physiol. Biochem. Pharmacol. 147, 47-74
12. Fornuskova, D., Stiburek, L., Wenchich, L., Vinsova, K., Hansikova, H. and Zeman, J. (2010) Novel insights into the assembly and function of human nuclear-encoded cytochrome c oxidase subunits 4, 5a, 6a, 7a and 7b. Biochem. J. 428, 363-374
13. Tzagoloff, A. and Dieckmann, C. L. (1990) PET genes of Saccharomyces cerevisiae. Microbiol. Rev. 54, 211-225
14. Sohal, R. S., Toroser, D., Bregere, C., Mockett, R. J. and Orr, W. C. (2008) Age-related decrease in expression of mitochondrial DNA encoded subunits of cytochrome c oxidase in Drosophila melanogaster . Mech. Ageing Dev. 129, 558-561
15. Ren, J. C., Rebrin, I., Klichko, V., Orr, W. C. and Sohal, R. S. (2010) Cytochrome c oxidase loses catalytic activity and structural integrity during the aging process in Drosophila melanogaster . Biochem. Biophys. Res. Commun. 401, 64-68
16. Poyton, R. O. and McEwen, J. E. (1996) Crosstalk between nuclear and mitochondrial genomes. Annu. Rev. Biochem. 65, 563-607 (Pubitemid 26250620)
17. Villani, G. and Attardi, G. (2000) In vivo control of respiration by cytochrome c oxidase in human cells. Free Radic. Biol. Med. 29, 202-210
18. Villani, G., Greco, M., Papa, S. and Attardi, G. (1998) Low reserve of cytochrome c oxidase capacity in vivo in the respiratory chain of a variety of human cell types. J. Biol. Chem. 273, 31829-31836 (Pubitemid 29177118)
19. Khalimonchuk, O. and Rodel, G. (2005) Biogenesis of cytochrome c oxidase. Mitochondrion 5, 363-388 (Pubitemid 43013019)
20. Miwa, S., St-Pierre, J., Partridge, L. and Brand, M. D. (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med. 35, 938-948 (Pubitemid 37211448)
21. Boveris, A., Cadenas, E. and Stoppani, A. O. (1976) Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem. J. 156, 435-444
22. Lee, S. S., Lee, R. Y., Fraser, A. G., Kamath, R. S., Ahringer, J. and Ruvkun, G. (2003) A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity. Nat. Genet. 33, 40-48 (Pubitemid 36068680)
23. Hamilton, B., Dong, Y., Shindo, M., Liu, W., Odell, I., Ruvkun, G. and Lee, S. S. (2005) A systematic RNAi screen for longevity genes in C. elegans. Genes. Dev. 19, 1544-1555 (Pubitemid 41002998)
24. Feng, J., Bussiere, F. and Hekimi, S. (2001) Mitochondrial electron transport is a key determinant of life span in Caenorhabditis elegans. Dev. Cell 1, 633-644 (Pubitemid 33586116)
25. Copeland, J. M., Cho, J., Lo, Jr, T., Hur, J. H., Bahadorani, S., Arabyan, T., Rabie, J., Soh, J. and Walker, D. W. (2009) Extension of Drosophila life span by RNAi of the mitochondrial respiratory chain. Curr. Biol. 19, 1591-1598
26. Nijtmans, L. G., Taanman, J. W., Muijsers, A. O., Speijer, D. and Van den Bogert, C. (1998) Assembly of cytochrome c oxidase in cultured human cells. Eur. J. Biochem. 254, 389-394 (Pubitemid 28289396)
27. Napiwotzki, J. and Kadenbach, B. (1998) Extramitochondrial ATP/ADP ratios regulate cytochrome c oxidase activity via binding to the cytosolic domain of subunit IV. Biol. Chem. 379, 335-339 (Pubitemid 28152098)
28. Arnold, S. and Kadenbach, B. (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome c oxidase. Eur. J. Biochem. 249, 350-354 (Pubitemid 27432632)
29. Bender, E. and Kadenbach, B. (2000) The allosteric ATP-inhibition of cytochrome c oxidase activity is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett. 466, 130-134 (Pubitemid 30050698)
30. Prabu, S. K., Anandatheerthavarada, H. K., Raza, H., Srinivasan, S., Spear, J. F. and Avadhani, N. G. (2006) Protein kinase A-mediated phosphorylation modulates cytochrome c oxidase function and augments hypoxia and myocardial ischemia-related injury. J. Biol. Chem. 281, 2061-2070 (Pubitemid 43845794)
31. Galati, D., Srinivasan, S., Raza, H., Prabu, S. K., Hardy, M., Chandran, K., Lopez, M., Kalyanaraman, B. and Avadhani, N. G. (2009) Role of nuclear-encoded subunit Vb in the assembly and stability of cytochrome c oxidase complex: implications in mitochondrial dysfunction and ROS production. Biochem. J. 420, 439-449
32. 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 (Pubitemid 46507584)
33. Campian, J. L., Gao, X., Qian, M. and Eaton, J. W. (2007) Cytochrome c oxidase activity and oxygen tolerance. J. Biol. Chem. 282, 12430-12438 (Pubitemid 47100605)
34. Brand, A. H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415 (Pubitemid 23214028)
35. Candas, M., Sohal, R. S., Radyuk, S. N., Klichko, V. I. and Orr, W. C. (1997) Molecular organization of the glutathione reductase gene in Drosophila melanogaster. Arch. Biochem. Biophys. 339, 323-334 (Pubitemid 27199977)
36. Mockett, R. J., Orr, W. C. and Sohal, R. S. (2002) Overexpression of Cu,ZnSOD and MnSOD in transgenic Drosophila . Methods Enzymol. 349, 213-220 (Pubitemid 34229508)
37. Mockett, R. J., Orr, W. C., Rahmandar, J. J., Benes, J. J., Radyuk, S. N., Klichko, V. I. and Sohal, R. S. (1999) Overexpression of Mn-containing superoxide dismutase in transgenic Drosophila melanogaster . Arch. Biochem. Biophys. 371, 260-269
38. Klichko, V. I., Radyuk, S. N. and Orr, W. C. (1999) CuZn-SOD promoter-driven expression in the Drosophila central nervous system. Neurobiol. Aging 20, 537-543 (Pubitemid 30001467)
39. Radyuk, S. N., Klichko, V. I. and Orr, W. C. (2000) Catalase expression in Drosophila melanogaster is responsive to ecdysone and exhibits both transcriptional and post-transcriptional regulation. Arch. Insect. Biochem. Physiol. 45, 79-93
40. Orr, W. C., Radyuk, S. N. and Sohal, R. S. (2013) Involvement of redox state in the aging of Drosophila melanogaster . Antioxid. Redox Signal. 19, 788-803
41. Sohal, R. S. and Orr, W. C. (2012) The redox stress hypothesis of aging. Free Radic. Biol. Med. 52, 539-555
42. Rera, M., Monnier, V. and Tricoire, H. (2010) Mitochondrial electron transport chain dysfunction during development does not extend lifespan in Drosophila melanogaster . Mech. Ageing Dev. 131, 156-164
43. Sansbury, B. E., Jones, S. P., Riggs, D. W., Darley-Usmar, V. M. and Hill, B. G. (2011) Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation. Chem. Biol. Interact. 191, 288-295
44. Dillin, A., Hsu, A. L., Arantes-Oliveira, N., Lehrer-Graiwer, J., Hsin, H., Fraser, A. G., Kamath, R. S., Ahringer, J. and Kenyon, C. (2002) Rates of behavior and aging specified by mitochondrial function during development. Science 298, 2398-2401 (Pubitemid 36014215)
45. Curran, S. P. and Ruvkun, G. (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet. 3, e56
46. Chen, D., Pan, K. Z., Palter, J. E. and Kapahi, P. (2007) Longevity determined by developmental arrest genes in Caenorhabditis elegans. Aging Cell 6, 525-533 (Pubitemid 47087057)
47. Hill, B. G., Benavides, G. A., Lancaster, Jr, J. R., Ballinger, S., Dell'Italia, L., Jianhua, Z. and Darley-Usmar, V. M. (2012) Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biol. Chem. 393, 1485-1512
48. Rea, S. L., Ventura, N. and Johnson, T. E. (2007) Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5, e259
49. Suthammarak, W., Yang, Y. Y., Morgan, P. G. and Sedensky, M. M. (2009) Complex I function is defective in complex IV-deficient Caenorhabditis elegans. J. Biol. Chem. 284, 6425-6435
50. Li, Y., D'Aurelio, M., Deng, J. H., Park, J. S., Manfredi, G., Hu, P., Lu, J. and Bai, Y. (2007) An assembled complex IV maintains the stability and activity of complex I in mammalian mitochondria. J. Biol. Chem. 282, 17557-17562 (Pubitemid 47100296)
51. Campian, J. L., Qian, M., Gao, X. and Eaton, J. W. (2004) Oxygen tolerance and coupling of mitochondrial electron transport. J. Biol. Chem. 279, 46580-46587 (Pubitemid 39518302)