Respiratory supercomplexes: Structure, function and assembly

Protein and Cell

Volumn 4, Issue 8, 2013, Pages 582-590

  Vartak, Rasika ^a   Porras, Christina Ann Marie ^a   Bai, Yidong ^a  

^a Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

mitochondrial; respiration; supercomplex

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CARDIOLIPIN; CYTOCHROME C; CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; OXIDOREDUCTASE; PROHIBITIN; PROTEIN AAC1; PROTEIN AAC2; PROTEIN RCF 1; PROTEIN RCF 2; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE; UNCLASSIFIED DRUG;

AGING; BARTH SYNDROME; COMPLEX FORMATION; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; ELECTRON MICROSCOPY; ELECTRON TRANSPORT; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; HUMAN; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RESPIRATORY CHAIN; REVIEW; STRUCTURE ACTIVITY RELATION;

EID: 84880809979     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-013-3032-y     Document Type: Review

References (77)

1. Acin-Perez, R., Bayona-Bafaluy, M. P., Fernandez-Silva, P., Moreno-Loshuertos, R., Perez-Martos, A., Bruno, C., Moraes, C. T., and Enriquez, J. A. (2004). Respiratory complex III is required to maintain complex i in mammalian mitochondria. Mol Cell 13, 805-815.
2. Acín-Pérez, R., Fernández-Silva, P., Peleato, M. L., Pérez-Martos, A., and Enriquez, J. A. (2008). Respiratory active mitochondrial supercomplexes. Mol Cell 32, 529-539.
3. Ahn, C. S., Lee, J. H., Reum Hwang, A., Kim, W. T., and Pai, H.-S. (2006). Prohibitin is involved in mitochondrial biogenesis in plants. Plant J 46, 658-667.
4. Althoff, T., Mills, D. J., Popot, J.-L., and Kühlbrandt, W. (2011). Arrangement of electron transport chain components in bovine mitochondrial supercomplex I1III2IV1. EMBO J 30, 4652-4664.
5. Arnarez, C., Mazat, J.-P., Elezgaray, J., Marrink, S.-J., and Periole, X. (2013a). Evidence for cardiolipin binding sites on the membraneexposed surface of the cytochrome bc(1). J Am Chem Soc 135, 3112-3120.
6. Arnarez, C., Marrink, S. J., and Periole, X. (2013b). Identification of cardiolipin binding sites on cytochrome c oxidase at the entrance of proton channels. Sci Rep 3, 1263.
7. Attardi, G., and Schatz, G. (1988). Biogenesis of mitochondria. Annu Rev Cell Biol 4, 289-333.
8. Barth, P. G., Scholte, H. R., Berden, J. A., van der Klei-van Moorsel, J. M., Luyt-Houwen, I. E., Van't Veer-Korthof, E. T., van der Harten, J. J., and Sobotka-Plojhar, M. A. (1983). An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J Neurol Sci 62, 327-355.
9. Bazán, S., Mileykovskaya, E., Mallampalli, V. K. P. S., Heacock, P., Sparagna, G. C., and Dowhan, W. (2013). Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified saccharomyces cerevisiae complexes III and IV. J Biol Chem 288, 401-411.
10. Berger, K. H., and Yaffe, M. P. (1998). Prohibitin family members interact genetically with mitochondrial inheritance components in Saccharomyces cerevisiae. Mol Cell Biol 18, 4043-4052.
11. Berry, E. A., and Trumpower, B. L. (1985). Isolation of ubiquinol oxidase from Paracoccus denitrificans and resolution into cytochrome bc1 and cytochrome c-aa3 complexes. J Biol Chem 260, 2458-2467.
12. Bianchi, C., Genova, M. L., Parenti Castelli, G., and Lenaz, G. (2004). The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem 279, 36562-36569.
13. Bione, S., D'Adamo, P., Maestrini, E., Gedeon, A. K., Bolhuis, P. A., and Toniolo, D. (1996). A novel X-linked gene, G4. 5. is responsible for Barth syndrome. Nat Genet 12, 385-389.
14. Böttinger, L., Horvath, S. E., Kleinschroth, T., Hunte, C., Daum, G., Pfanner, N., and Becker, T. (2012). Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J Mol Biol 423, 677-686.
15. Boumans, H., Grivell, L. A., and Berden, J. A. (1998). The respiratory chain in yeast behaves as a single functional unit. J Biol Chem 273, 4872-4877.
16. Bruel, C., Brasseur, R., and Trumpower, B. L. (1996). Subunit 8 of the Saccharomyces cerevisiae cytochrome bc1 Complex Interacts with succinate-ubiquinone reductase complex. J Bioenerg Biomembr 28, 59-68.
17. Budde, S. M., van den Heuvel, L. P., Janssen, A. J., Smeets, R. J., Buskens, C. A., DeMeirleir, L., van Coster, R., Baethmann, M., Voit, T., Trijbels, J. M., et al. (2000). Combined enzymatic Complex I and III deficiency associated with mutations in the nuclear encoded NDUFS4 gene. Biochem Biophys Res Commun 275, 63-68.
18. Chance, B., and Williams, G. R. (1955). A method for the localization of sites for oxidative phosphorylation. Nature 176, 250-254.
19. Chazotte, B., and Hackenbrock, C. R. (1988). The multicollisional, obstructed, long-range diffusional nature of mitochondrial electron transport. J Biol Chem 263, 14359-14367.
20. Chen, X. J. (2004). Sal1p, a calcium-dependent carrier protein that suppresses an essential cellular function associated With the Aac2 isoform of ADP/ATP translocase in Saccharomyces cerevisiae. Genetics 167, 607-617.
21. Chen, Y.-C., Taylor, E. B., Dephoure, N., Heo, J.-M., Tonhato, A., Papandreou, I., Nath, N., Denko, N. C., Gygi, S. P., and Rutter, J. (2012). Identification of a protein mediating respiratory supercomplex stability. Cell Metab 15, 348-360.
22. D'Aurelio, M., Gajewski, C. D., Lenaz, G., and Manfredi, G. (2006). Respiratory chain supercomplexes set the threshold for respiration defects in human mtDNA mutant cybrids. Hum Mol Genet 15, 2157-2169.
23. Diaz, F., Fukui, H., Garcia, S., and Moraes, C. T. (2006). Cytochrome c oxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol Cell Biol 26, 4872-4881.
24. Dienhart, M. K., and Stuart, R. A. (2008). The yeast Aac2 protein exists in physical association with the cytochrome bc1-COX supercomplex and the TIM23 machinery. Mol Biol Cell 19, 3934-3943.
25. Dudkina, N. V., Eubel, H., Keegstra, W., Boekema, E. J., and Braun, H.-P. (2005). Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. Proc Natl Acad Sci U S A 102, 3225-3229.
26. Dudkina, N. V., Kudryashev, M., Stahlberg, H., and Boekema, E. J. (2011). Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci U S A 108, 15196-15200.
27. Dunning, C. R., McKenzie, M., Sugiana, C., Lazarou, M., Silke, J., Connelly, A., Fletcher, J. M., Kirby, D. M., Thorburn, D. R., and Ryan, M. T. (2007). Human CIA30 is involved in the early assembly of mitochondrial complex I and mutations in its gene cause disease. EMBO J 26, 3227-3237.
28. Eubel, H., Jänsch, L., and Braun, H.-P. (2003). New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of Complex II. Plant Physiol 133, 274-286.
29. Fernandez-Vizarra, E., Bugiani, M., Goffrini, P., Carrara, F., Farina, L., Procopio, E., Donati, A., Uziel, G., Ferrero, I., and Zeviani, M. (2007). Impaired Complex III assembly associated with BCS1L gene mutations in isolated mitochondrial encephalopathy. Hum Mol Genet 16, 1241-1252.
30. Fleischer, S., Rouser, G., Fleischer, B., Casu, A., and Kritchevsky, G. (1967). Lipid composition of mitochondria from bovine heart, liver, and kidney. J Lipid Res 8, 170-180.
31. Fry, M., and Green, D. E. (1981). Cardiolipin requirement for electron transfer in Complex I and III of the mitochondrial respiratory chain. J Biol Chem 256, 1874-1880.
32. Gawaz, M., Douglas, M. G., and Klingenberg, M. (1990). Structurefunction studies of adenine nucleotide transport in mitochondria. II. Biochemical analysis of distinct AAC1 and AAC2 proteins in yeast. J Biol Chem 265, 14202-14208.
33. Genova, M. L., Baracca, A., Biondi, A., Casalena, G., Faccioli, M., Falasca, A. I., Formiggini, G., Sgarbi, G., Solaini, G., and Lenaz, G. (2008). Is supercomplex organization of the respiratory chain required for optimal electron transfer activity? Biochim Biophys Acta 1777, 740-746.
34. Ghezzi, D., Arzuffi, P., Zordan, M., Da Re, C., Lamperti, C., Benna, C., D'Adamo, P., Diodato, D., Costa, R., Mariotti, C., et al. (2011). Mutations in TTC19 cause mitochondrial Complex III deficiency and neurological impairment in humans and flies. Nat Genet 43, 259-263.
35. Gohil, V. M., Hayes, P., Matsuyama, S., Schägger, H., Schlame, M., and Greenberg, M. L. (2004). Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem 279, 42612-42618.
36. Gómez, L. A., Monette, J. S., Chavez, J. D., Maier, C. S., and Hagen, T. M. (2009). Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch Biochem Biophys 490, 30-35.
37. Gupte, S. S., and Hackenbrock, C. R. (1988). The role of cytochrome c diffusion in mitochondrial electron transport. J Biol Chem 263, 5248-5253.
38. Hackenbrock, C. R., Chazotte, B., and Gupte, S. S. (1986). The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr 18, 331-368.
39. Hatefi, Y. (1978). Reconstitution of the electron-transport system of bovine heart mitochondria. Meth Enzymol 53, 48-54.
40. Hatefi, Y., Haavik, A. G., and Griffiths, D. E. (1961). Reconstitution of the electron transport system: I. Preparation and properties of the interacting enzyme complexes. Biochem Biophys Res Commun 4, 441-446.
41. Hatefi, Y., Haavik, A. G., and Griffiths, D. E. (1962). Studies on the electron transfer system. XL. Preparation and properties of mitochondrial DPNH-coenzyme Q reductase. J Biol Chem 237, 1676-1680.
42. Heinemeyer, J., Braun, H.-P., Boekema, E. J., and Kouril, R. (2007). A structural model of the cytochrome C reductase/oxidase supercom plex from yeast mitochondria. J Biol Chem 282, 12240-12248.
43. Hess, D. C., Myers, C. L., Huttenhower, C., Hibbs, M. A., Hayes, A. P., Paw, J., Clore, J. J., Mendoza, R. M., Luis, B. S., Nislow, C., et al. (2009). Computationally driven, quantitative experiments discover genes required for mitochondrial biogenesis. PLoS Genet 5, e1000407.
44. Iwasaki, T., Matsuura, K., and Oshima, T. (1995). Resolution of the aerobic respiratory system of the thermoacidophilic archaeon, Sulfolobus sp. strain 7: I. The archaeal terminal oxidase supercomplex is a functional fusion of respiratory complexes III and IV with no ctype cytochromes. J Biol Chem 270, 30881-30892.
45. Jiang, F., Ryan, M. T., Schlame, M., Zhao, M., Gu, Z., Klingenberg, M., Pfanner, N., and Greenberg, M. L. (2000). Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function. J Biol Chem 275, 22387-22394.
46. Klingenberg, M. (1989). Molecular aspects of the adenine nucleotide carrier from mitochondria. Arch Biochem Biophys 270, 1-14.
47. Lazarou, M., Smith, S. M., Thorburn, D. R., Ryan, M. T., and McKenzie, M. (2009). Assembly of nuclear DNA-encoded subunits into mitochondrial Complex IV, and their preferential integration into supercomplex forms in patient mitochondria. FEBS J 276, 6701-6713.
48. 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.
49. Marques, I., Dencher, N. A., Videira, A., and Krause, F. (2007). Supramolecular organization of the respiratory chain in Neurospora crassa mitochondria. Eukary Cell 6, 2391-2405.
50. McKenzie, M., Lazarou, M., Thorburn, D. R., and Ryan, M. T. (2006). Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J Mol Biol 361, 462-469.
51. Merkwirth, C., Martinelli, P., Korwitz, A., Morbin, M., Brönneke, H. S., Jordan, S. D., Rugarli, E. I., and Langer, T. (2012). Loss of prohibitin membrane scaffolds impairs mitochondrial architecture and leads to tau hyperphosphorylation and neurodegeneration. PLoS Genet 8, e1003021.
52. Mitchell, P., and Moyle, J. (1968). Proton translocation coupled to ATP hydrolysis in rat liver mitochondria. Euro J Biochem 4, 530-539.
53. Morán, M., Marín-Buera, L., Gil-Borlado, M. C., Rivera, H., Blázquez, A., Seneca, S., Vázquez-López, M., Arenas, J., Martín, M. A., and Ugalde, C. (2010). Cellular pathophysiological consequences of BCS1L mutations in mitochondrial Complex III enzyme deficiency. Hum Mutat 31, 930-941.
54. Moreno-Lastres, D., Fontanesi, F., García-Consuegra, I., Martín, M. A., Arenas, J., Barrientos, A., and Ugalde, C. (2012). Mitochondrial complex I plays an essential role in human respirasome assembly. Cell Metab 15, 324-335.
55. Muster, B., Kohl, W., Wittig, I., Strecker, V., Joos, F., Haase, W., Bereiter-Hahn, J., and Busch, K. (2010). Respiratory chain complexes in dynamic mitochondria display a patchy distribution in life cells. PLoS ONE 5, e11910.
56. Ogilvie, I. (2005). A molecular chaperone for mitochondrial Complex I assembly is mutated in a progressive encephalopathy. J Clin Invest 115, 2784-2792.
57. Orstavik, K. H., Orstavik, R. E., Naumova, A. K., D'Adamo, P., Gedeon, A., Bolhuis, P. A., Barth, P. G., and Toniolo, D. (1998). X chromo some inactivation in carriers of Barth syndrome. Am J Hum Genet 63, 1457-1463.
58. Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S.-E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K., et al. (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123.
59. Ramírez-Aguilar, S. J., Keuthe, M., Rocha, M., Fedyaev, V. V., Kramp, K., Gupta, K. J., Rasmusson, A. G., Schulze, W. X., and van Dongen, J. T. (2011). The composition of plant mitochondrial supercomplexes changes with oxygen availability. J Biol Chem 286, 43045-43053.
60. Rosca, M. G., Vazquez, E. J., Kerner, J., Parland, W., Chandler, M. P., Stanley, W., Sabbah, H. N., and Hoppel, C. L. (2008). Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc Res 80, 30-39.
61. Saada, A., Edvardson, S., Rapoport, M., Shaag, A., Amry, K., Miller, C., Lorberboum-Galski, H., and Elpeleg, O. (2008). C6ORF66 is an assembly factor of mitochondrial complex I. Am J Hum Genet 82, 32-38.
62. Santiago, E., López-Moratalla, N., and Segovia, J. F. (1973). Correlation between losses of mitochondrial ATPase activity and cardiolipin degradation. Biochem Biophys Res Commun 53, 439-445.
63. Schäfer, E., Seelert, H., Reifschneider, N. H., Krause, F., Dencher, N. A., and Vonck, J. (2006). Architecture of active mammalian respiratory chain supercomplexes. J Biol Chem 281, 15370-15375.
64. Schägger, H., and Pfeiffer, K. (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19, 1777-1783.
65. Schägger, H., and Pfeiffer, K. (2001). The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J Biol Chem 276, 37861-37867.
66. Schleicher, M., Shepherd, B. R., Suarez, Y., Fernandez-Hernando, C., Yu, J., Pan, Y., Acevedo, L. M., Shadel, G. S., and Sessa, W. C. (2008). Prohibitin-1 maintains the angiogenic capacity of endothelial cells by regulating mitochondrial function and senescence. J Cell Biol 180, 101-112.
67. Sone, N., Sekimachi, M., and Kutoh, E. (1987). Identification and properties of a quinol oxidase super-complex composed of a bc1 complex and cytochrome oxidase in the thermophilic bacterium PS3. J Biol Chem 262, 15386-15391.
68. Strogolova, V., Furness, A., Robb-McGrath, M., Garlich, J., and Stuart, R. A. (2012). Rcf1 and Rcf2, members of the hypoxia-induced gene 1 protein family, are critical components of the mitochondrial cytochrome bc1-cytochrome c oxidase supercomplex. Mol Cell Biol 32, 1363-1373.
69. Stroh, A., Anderka, O., Pfeiffer, K., Yagi, T., Finel, M., Ludwig, B., and Schägger, H. (2004). Assembly of respiratory complexes I, III, and IV into NADH oxidase supercomplex stabilizes Complex I in Paracoccus denitrificans. J Biol Chem 279, 5000-5007.
70. Strub, G. M., Paillard, M., Liang, J., Gomez, L., Allegood, J. C., Hait, N. C., Maceyka, M., Price, M. M., Chen, Q., Simpson, D. C., et al. (2011). Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate Complex IV assembly and respiration. FASEB J 25, 600-612.
71. Sugiana, C., Pagliarini, D. J., McKenzie, M., Kirby, D. M., Salemi, R., Abu-Amero, K. K., Dahl, H.-H. M., Hutchison, W. M., Vascotto, K. A., Smith, S. M., et al. (2008). Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am J Hum Genet 83, 468-478.
72. Trouillard, M., Meunier, B., and Rappaport, F. (2011). Questioning the functional relevance of mitochondrial supercomplexes by timeresolved analysis of the respiratory chain. Proc Natl Acad Sci U S A 108, E1027-1034.
73. Vogel, R. O., Janssen, R. J. R. J., van den Brand, M. A. M., Dieteren, C. E. J., Verkaart, S., Koopman, W. J. H., Willems, P. H. G. M., Pluk, W., van den Heuvel, L. P. W. J., Smeitink, J. A. M., et al. (2007). Cytosolic signaling protein Ecsit also localizes to mitochondria where it interacts with chaperone NDUFAF1 and functions in Complex I assembly. Genes Dev 21, 615-624.
74. Vreken, P., Valianpour, F., Nijtmans, L. G., Grivell, L. A., Plecko, B., Wanders, R. J. A., and Barth, P. G. (2000). Defective remodeling of cardiolipin and phosphatidylglycerol in barth syndrome. Biochem Biophy Res Commun 279, 378-382.
75. 2-inducible mitochondrial protein that augments cell survival. Proc Natl Acad Sci U S A 103, 10636-10641.
76. Wenz, T., Hielscher, R., Hellwig, P., Schägger, H., Richers, S., and Hunte, C. (2009). Role of phospholipids in respiratory cytochrome bc(1) complex catalysis and supercomplex formation. Biochim Biophys Acta 1787, 609-616.
77. Zhang, M., Mileykovskaya, E., and Dowhan, W. (2005). Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem 280, 29403-29408.