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Protein & Cell

ISSN 1674-800X

ISSN 1674-8018(Online)

CN 11-5886/Q

Postal Subscription Code 80-984

2018 Impact Factor: 7.575

Prot Cell    2013, Vol. 4 Issue (8) : 582-590    https://doi.org/10.1007/s13238-013-3032-y      PMID: 23828195
RVIEW
Respiratory supercomplexes: structure, function and assembly
Rasika Vartak, Christina Ann-Marie Porras, Yidong Bai()
Department of Cellular and Structural Biology, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA
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Abstract

The mitochondrial respiratory chain consists of 5 enzyme complexes that are responsible for ATP generation. The paradigm of the electron transport chain as discrete enzymes diffused in the inner mitochondrial membrane has been replaced by the solid state supercomplex model wherein the respiratory complexes associate with each other to form supramolecular complexes. Defects in these supercomplexes, which have been shown to be functionally active and required for forming stable respiratory complexes, have been associated with many genetic and neurodegenerative disorders demonstrating their biomedical significance. In this review, we will summarize the functional and structural significance of supercomplexes and provide a comprehensive review of their assembly and the assembly factors currently known to play a role in this process.

Keywords supercomplex      mitochondrial      respiration     
Corresponding Author(s): Bai Yidong,Email:baiy@uthscsa.edu   
Issue Date: 01 August 2013
 Cite this article:   
Yidong Bai,Rasika Vartak,Christina Ann-Marie Porras. Respiratory supercomplexes: structure, function and assembly[J]. Prot Cell, 2013, 4(8): 582-590.
 URL:  
https://academic.hep.com.cn/pac/EN/10.1007/s13238-013-3032-y
https://academic.hep.com.cn/pac/EN/Y2013/V4/I8/582
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 .
doi: 10.1016/S1097-2765(04)00124-8
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 .
doi: 10.1016/j.molcel.2008.10.021
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 .
doi: 10.1111/j.1365-313X.2006.02726.x
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 .
doi: 10.1038/emboj.2011.324
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 .
doi: 10.1021/ja310577u
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 .
doi: 10.1146/annurev.cb.04.110188.001445
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 .
doi: 10.1016/0022-510X(83)90209-5
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 .
doi: 10.1074/jbc.M112.425876
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 fl ux control analysis. J Biol Chem 279, 36562-36569 .
doi: 10.1074/jbc.M405135200
13 Bione, S., D’Adamo, P., Maestrini, E., Gedeon, A.K., Bolhuis, P.A., and Toniolo, D. (1996). Anovel X-linked gene, G4.5. is responsible for Barth syndrome. Nat Genet 12, 385-389 .
doi: 10.1038/ng0496-385
14 B?ttinger, 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 .
doi: 10.1016/j.jmb.2012.09.001
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 .
doi: 10.1074/jbc.273.9.4872
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., . (2000). Combined enzymatic Complex I and III deficiency associated with mutations in the nuclear encoded NDUFS4 gene. Biochem Biophys Res Commun 275, 63-68 .
doi: 10.1006/bbrc.2000.3257
18 Chance, B., and Williams, G.R. (1955). A method for the localization of sites for oxidative phosphorylation. Nature 176, 250-254 .
doi: 10.1038/176250a0
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 .
doi: 10.1534/genetics.103.023655
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 .
doi: 10.1016/j.cmet.2012.02.006
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 .
doi: 10.1093/hmg/ddl141
23 Diaz, F., Fukui, H., Garcia, S., and Moraes, C.T. (2006). Cytochrome coxidase is required for the assembly/stability of respiratory complex I in mouse fibroblasts. Mol Cell Biol 26, 4872-4881 .
doi: 10.1128/MCB.01767-05
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 .
doi: 10.1091/mbc.E08-04-0402
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 USA 102, 3225-3229 .
doi: 10.1073/pnas.0408870102
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 .
doi: 10.1073/pnas.1107819108
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 .
doi: 10.1038/sj.emboj.7601748
28 Eubel, H., J?nsch, 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 .
doi: 10.1104/pp.103.024620
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 .
doi: 10.1093/hmg/ddm072
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 .
doi: 10.1016/j.bbabio.2008.04.007
34 Ghezzi, D., Arzuffi, P., Zordan, M., Da Re, C., Lamperti, C., Benna, C., D’Adamo, P., Diodato, D., Costa, R., Mariotti, C., . (2011). Mutations in TTC19 cause mitochondrial Complex III deficiency and neurological impairment in humans and flies. Nat Genet 43, 259-263 .
doi: 10.1038/ng.761
35 Gohil, V.M., Hayes, P., Matsuyama, S., Sch?gger, H., Schlame, M., and Greenberg, M.L. (2004). Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem 279, 42612-42618 .
doi: 10.1074/jbc.M402545200
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 .
doi: 10.1016/j.abb.2009.08.002
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 .
doi: 10.1007/BF00743010
39 Hatefi, Y. (1978). Reconstitution of the electron-transport system of bovine heart mitochondria. Meth Enzymol 53, 48-54 .
doi: 10.1016/S0076-6879(78)53012-7
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 .
doi: 10.1016/0006-291X(61)90305-9
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 supercomplex from yeast mitochondria. J Biol Chem 282, 12240-12248 .
doi: 10.1074/jbc.M610545200
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., . (2009). Computationally driven, quantitative experiments discover genes required for mitochondrial biogenesis. PLoS Genet 5, e1000407.
doi: 10.1371/journal.pgen.1000407
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 .
doi: 10.1074/jbc.270.52.30881
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 .
doi: 10.1074/jbc.M909868199
46 Klingenberg, M. (1989). Molecular aspects of the adenine nucleotide carrier from mitochondria. Arch Biochem Biophys 270, 1-14 .
doi: 10.1016/0003-9861(89)90001-5
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 .
doi: 10.1111/j.1742-4658.2009.07384.x
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 .
doi: 10.1074/jbc.M701056200
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 .
doi: 10.1128/EC.00149-07
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 .
doi: 10.1016/j.jmb.2006.06.057
51 Merkwirth, C., Martinelli, P., Korwitz, A., Morbin, M., Br?nneke, 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.
doi: 10.1371/journal.pgen.1003021
52 Mitchell, P., and Moyle, J. (1968). Proton translocation coupled to ATP hydrolysis in rat liver mitochondria. Euro J Biochem 4, 530-539 .
doi: 10.1111/j.1432-1033.1968.tb00245.x
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 .
doi: 10.1002/humu.21294
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 .
doi: 10.1016/j.cmet.2012.01.015
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.
doi: 10.1371/journal.pone.0011910
56 Ogilvie, I. (2005). A molecular chaperone for mitochondrial Complex I assembly is mutated in a progressive encephalopathy. J Clin Invest 115, 2784-2792 .
doi: 10.1172/JCI26020
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 .
doi: 10.1086/302095
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., . (2008). A mitochondrial protein compendium elucidates complex I disease biology. Cell 134, 112-123 .
doi: 10.1016/j.cell.2008.06.016
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 .
doi: 10.1074/jbc.M111.252544
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 .
doi: 10.1093/cvr/cvn184
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 .
doi: 10.1016/j.ajhg.2007.08.003
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 .
doi: 10.1016/0006-291X(73)90681-5
63 Sch?fer, 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 .
doi: 10.1074/jbc.M513525200
64 Sch?gger, H., and Pfeiffer, K. (2000). Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19, 1777-1783 .
doi: 10.1093/emboj/19.8.1777
65 Sch?gger, 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 .
doi: 10.1083/jcb.200706072
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 .
doi: 10.1128/MCB.06369-11
69 Stroh, A., Anderka, O., Pfeiffer, K., Yagi, T., Finel, M., Ludwig, B., and Sch?gger, 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 .
doi: 10.1074/jbc.M309505200
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., . (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 .
doi: 10.1096/fj.10-167502
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., . (2008). Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am J Hum Genet 83, 468-478 .
doi: 10.1016/j.ajhg.2008.09.009
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 USA 108, E1027-1034 .
doi: 10.1073/pnas.1109510108
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., . (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 .
doi: 10.1101/gad.408407
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 .
doi: 10.1006/bbrc.2000.3952
75 Wang, J., Cao, Y., Chen, Y., Chen, Y., Gardner, P., and Steiner, D.F. (2006). Pancreatic β cells lack a low glucose and O2-inducible mitochondrial protein that augments cell survival. Proc Natl Acad Sci U S A 103, 10636-10641 .
doi: 10.1073/pnas.0604194103
76 Wenz, T., Hielscher, R., Hellwig, P., Sch?gger, 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 .
doi: 10.1016/j.bbabio.2009.02.012
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 .
doi: 10.1074/jbc.M504955200
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