Supramolecular organization of protein complexes in the mitochondrial inner membrane

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 1, 2009, Pages 117-124

  Vonck, Janet ^a   Schäfer, Eva ^b  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Electron transfer; Membrane proteins; Mitochondria; Protein structure; Respiratory chain; Supercomplexes

Indexed keywords

CYTOCHROME C; CYTOCHROME C OXIDASE; DIGITONIN; MITOCHONDRIAL PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE;

BINDING SITE; ELECTRON MICROSCOPY; ENZYME ISOLATION; HUMAN; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RESPIRATORY CHAIN; REVIEW; SUPRAMOLECULAR CHEMISTRY;

ANIMALS; ATP SYNTHETASE COMPLEXES; DIMERIZATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ELECTRON TRANSPORT COMPLEX III; HUMANS; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; PROTEIN SUBUNITS;

EID: 56349087328     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.05.019     Document Type: Review

References (112)

1. Hatefi Y., and Rieske J.S. The preparation and properties of DPNH-cytochrome c reductase (Complex I-III of the respiratory chain). Methods Enzymol 10 (1967) 225-231
2. Gabaldón T., Rainey D., and Huynen M.A. Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). J. Mol. Biol. 348 (2005) 857-870
3. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
4. Friedrich T., and Böttcher B. The gross structure of the respiratory complex I: a Lego System. Biochim. Biophys. Acta 1608 (2004) 1-9
5. Radermacher M., Ruiz T., Clason T., Benjamin S., Brandt U., and Zickermann V. The three-dimensional structure of complex I from Yarrowia lipolytica: a highly dynamic protein. J. Struct. Biol. 254 (2006) 269-279
6. Grigorieff N. Three-dimensional structure of bovine NADH:ubiquinone oxidoreductase (complex I) at 22 Å in ice. J. Mol. Biol. 277 (1998) 1033-1046
7. Xia D., Yu C.A., Kim H., Xia J., Kachurin A.M., Zhang L., Yu L., and Deisenhofer J. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 281 (1997) 64-71
8. 1 complex. Science 281 (1998) 64-71
9. 1. Nature 392 (1998) 677-684
10. 1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment. Structure 8 (2000) 669-684
11. V fragment. Proc. Natl. Acad. Sci. USA 94 (1997) 10547-10553
12. Iwata S., Ostermeier C., Ludwig B., and Michel H. Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376 (2002) 660-669
13. Svensson-Ek M., Abramson J., Larsson G., Tornroth S., Brzezinski P., and Iwata S. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321 (2002) 329-339
14. Tsukihara T., Aoyama H., Yamashita E., Tomizaki T., Yamaguchi H., Shinzawa-Itoh K., Nakashima R., Yaono R., and Yoshikawa S. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science 272 (1996) 1136-1144
15. Yoshikawa S., Shinzawa-Itoh K., Nakashima R., Yaono R., Yamashita E., Inoue N., Yao M., Fei M.J., Libeu C.P., Mizushima T., Yamaguchi H., Tomizaki T., and Tsukihara T. Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase. Science 280 (1998) 1723-1729
16. Tsukihara T., Shimokata K., Katayama Y., Shimada H., Muramoto K., Aoyama H., Mochizuki M., Shinzawa-Itoh K., Yamashita E., Yao M., Ishimura Y., and Yoshikawa S. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. USA 100 (2003) 15304-15309
17. Muramoto K., Hirata K., Shinzawa-Itoh K., Yoko-O S., Yamashita E., Aoyama H., Tsukihara T., and Yoshikawa S. A histidine residue acting as a controlling site for dioxygen reduction and proton pumping by cytochrome c oxidase. Proc. Natl. Acad. Sci. USA 104 (2007) 7881-7886
18. 1 ATPase from bovine heart mitochondria. Nature 370 (1994) 621-628
19. Boyer P.D. The ATP synthase: a splendid molecular machine. Ann. Rev. Biochem. 66 (1997) 717-749
20. 1-ATPase. Biochemistry 33 (1994) 7971-7978
21. Devenish R.J., Prescott M., Roucou X., and Nagley P. Insights into ATP synthase assembly and function through the molecular genetic manipulation of subunits of the yeast mitochondrial enzyme complex. BBA-Bioenergetics 1458 (2000) 428-442
22. Kane Dickson V., Silvester J.A., Fearnley I.M., Leslie A.G.W., and Walker J.E. On the structure of the stator of the mitochondrial ATP synthase. EMBO J. 25 (2006) 2911-2918
23. Stock D., Leslie A.G., and Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science 286 (1999) 1700-1705
24. +-ATP synthase has an undecameric rotor. EMBO Reports 2 (2001) 229-233
25. +-ATP synthase. J. Mol. Biol. 321 (2002) 307-316
26. +-ATPase from Ilyobacter tartaricus. Science 308 (2005) 659-662
27. Meier T., Matthey U., von Ballmoos C., Vonck J., Krug von Nidda T., Kühlbrandt W., and Dimroth P. Evidence for structural integrity in the undecameric rotors isolated from sodium ATP synthases. J. Mol. Biol. 325 (2003) 389-397
28. Meier T., Ferguson S.A., Cook G.M., Dimroth P., and Vonck J. Structural investigations of the membrane-embedded rotor ring of the F-ATPase from Clostridium paradoxum. J. Bacteriol. 188 (2006) 7759-7764
29. o ATP synthase. FEBS J. 275 (2008) 1999-2007
30. Meier T., Morgner N., Matthies D., Pogoryelov D., Keis S., Cook G.M., Dimroth P., and Brutschy B. A tridecameric c ring of the adenosine triphosphate (ATP) synthase from the thermoalkaliphilic Bacillus sp. strain TA2.A1 facilitates ATP synthesis at low electrochemical proton potential. Mol. Microbiol. 65 (2007) 1181-1192
31. 0 symmetry mismatch is not obligatory. EMBO Reports 6 (2005) 1045-1052
32. Pogoryelov D., Reichen C., Klyszejko A.L., Brunisholz R., Muller D.J., Dimroth P., and Meier T. The oligomeric state of c rings from cyanobacterial F-ATP synthases varies from 13 to 15. J. Bacteriol. 189 (2007) 5895-5902
33. Seelert H., Dencher N.A., and Muller D.J. Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333 (2003) 337-344
34. Rubinstein J.L., Walker J.E., and Henderson R. Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J. 22 (2003) 6182-6192
35. Frey T.G., and Mannella C.A. The internal structure of mitochondria. Trends Biochem. Sci. 25 (2000) 319-324
36. Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae. Biochim. Biophys. Acta 1763 (2006) 542-548
37. Hackenbrock C.R., Chazotte B., and Gupte S.S. The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J. Bioenerg. Biomembr. 18 (1986) 331-368
38. Chance B., and Williams G.R. A method for the localization of sites for oxidative phosphorylation. Nature 176 (1955) 250-254
39. Ragan C.I., and Heron C. The interaction between mitochondrial NADH-ubiquinone oxidoreductase and ubiquinol-cytochrome c oxidoreductase. Evidence for stoicheiometric association. Biochem. J. 174 (1978) 783-790
40. Hatefi Y. The mitochondrial electron transport and oxidative phosphorylation system. Annu. Rev. Biochem. 54 (1985) 1015-1069
41. Tisdale H.D. Preparation and properties of succinic-cytochrome c reductase (Complex II-III). Methods Enzymol. 10 (1967) 213-216
42. 1 and cytochrome c-aa3 complexes. J. Biol. Chem. 260 (1985) 2458-2467
43. 1 complex and cytochrome oxidase in the thermophilic bacterium PS3. J. Biol. Chem. 262 (1987) 15386-15391
44. Iwasaki T., Wakagi T., Isogai Y., Iizuka T., and Oshima T. 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 c-type cytochromes. J. Biol. Chem. 270 (1995) 30893-30901
45. Boumans H., Grivell L.A., and Berden J.A. The respiratory chain in yeast behaves as a single functional unit. J. Biol. Chem. 273 (1998) 4872-4877
46. Bianchi C., Genova M.L., Parenti Castelli G., and Lenaz G. The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J. Biol. Chem. 279 (2004) 36562-36569
47. Lenaz G., and Genova M.L. Kinetics of integrated electron transfer in the mitochondrial respiratory chain: random collisions vs. solid state electron channeling. Am. J. Physiol. Cell Physiol. 292 (2007) 1221-1239
48. Schägger H., and Pfeiffer K. Supercomplexes in the respiratory chain of yeast and mammalian mitochondria. EMBO J. 19 (2000) 1777-1783
49. Schägger H. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim. Biophys. Acta 1555 (2002) 154-159
50. Eubel H., Jänsch L., and Braun H.P. New insights into the respiratory chain of plant mitochondria. supercomplexes and a unique composition of complex II. Plant Physiol. 133 (2003) 274-286
51. 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. Respiratory complex III is required to maintain complex I in mammalian mitochondria. Mol. Cell 13 (2004) 805-815
52. Eubel H., Heinemeyer J., and Braun H.P. Identification and characterization of respirasomes in potato mitochondria. Plant Physiol. 134 (2004) 1450-1459
53. Krause F., Scheckhuber C.Q., Werner A., Rexroth S., Reifschneider N.H., Dencher N.A., and Osiewacz H.D. Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J. Biol. Chem. 279 (2004) 26453-26461
54. Schägger H., de Coo R., Bauer M.F., Hofmann S., Godinot C., and Brandt U. Significance of respirasomes for the assembly/stability of human respiratory chain complex I. J. Biol. Chem. 279 (2004) 36349-36353
55. Stroh A., Anderka O., Pfeiffer K., Yagi T., Finel M., Ludwig B., and Schägger H. Assembly of respiratory complexes I, III and IV into NADH oxidase supercomplex stabilizes complex I in Paracoccus denitrificans. J. Biol. Chem. 279 (2004) 5000-5007
56. Reifschneider N.H., Goto S., Nakamoto H., Takahashi R., Sugawa M., and Dencher N.A. Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J. Proteome Res. 5 (2006) 1117-1132
57. Schäfer E., Seelert H., Reifschneider N.H., Krause F., Dencher N.A., and Vonck J. Architecture of active mammalian respiratory chain supercomplexes. J. Biol. Chem. 281 (2006) 15370-15375
58. 1 and cytochrome c oxidase complexes associate to form a single supracomplex in yeast mitochondria. J. Biol. Chem. 275 (2000) 18093-18098
59. Krause F., Reifschneider N.H., Vocke D., Seelert H., Rexroth S., and Dencher N.A. "Respirasome"-like supercomplexes in green leaf mitochondria of spinach. J. Biol. Chem. 279 (2004) 48369-48375
60. Krause F., Reifschneider N.H., Goto S., and Dencher N.A. Active oligomeric ATP synthases in mammalian mitochondria. Bioch. Biophys. Res. Comm. 329 (2005) 583-590
61. Boekema E.J., and Braun H.P. Supramolecular structure of the mitochondrial oxidative phosphorylation system. J. Biol. Chem. 282 (2007) 1-4
62. Heinemeyer J., Braun H.P., Boekema E.J., and Kouril R. A structural model of the cytochrome c reductase/oxidase supercomplex from yeast mitochondria. J. Biol. Chem. 282 (2007) 12240-12248
63. Dudkina N.V., Eubel H., Keegstra W., Boekema E.J., and Braun H.P. Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. Proc. Natl. Acad. Sci. USA 102 (2005) 3225-3229
64. 1 from bovine heart mitochondria. Biochemistry 44 (2007) 12579-12585
65. Pfeiffer K., Gohil V., Stuart R.A., Hunte C., Brandt U., Greenberg M.L., and Schägger H. Cardiolipin stabilizes respiratory chain supercomplexes. J. Biol. Chem. 278 (2003) 52873-52880
66. Mileykovskaya E., Zhang M., and Dowhan W. Cardiolipin in energy transducing membranes. Biochemistry (Mosc) 70 (2005) 154-158
67. Zhang M., Mileykovskaya E., and Dowhan W. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J. Biol. Chem. 280 (2005) 29403-29408
68. Schägger H., and Pfeiffer K. The ratio of oxidative phosphorylation complexes I-V in bovine heart mitochondria and the composition of respiratory chain supercomplexes. J. Biol. Chem. 276 (2001) 37861-37867
69. Eubel H., Heinemeyer J., Sunderhaus S., and Braun H.P. Respiratory chain supercomplexes in plant mitochondria. Plant Physiol. Biochem. 42 (2004) 937-942
70. Millar A.H., Mittova V., Kiddle G., Heazlewood J.L., Bartoli C.G., Theodoulou F.L., and Foyer C.H. Control of ascorbate synthesis by respiration and its implications for stress responses. Plant Physiol. 133 (2003) 443-447
71. Parisi G., Perales M., Fornasari M., Colaneri A., Schain N., Casati D., Zimmermann S., Brennicke A., Araya A., Ferry J., Echave J., and Zabaleta E. Gamma carbonic anhydrases in plant mitochondria. Plant Mol. Biol. 55 (2004) 193-207
72. Kashani-Poor N., Zwicker K., Kerscher S., and Brandt U. A central functional role for the 49-kDa subunit within the catalytic core of mitochondrial complex I. J. Biol. Chem. 276 (2001) 24082-24087
73. Zickermann V., Bostina M., Hunte C., Ruiz T., Radermacher M., and Brandt U. Functional implications from an unexpected position of the 49-kDa subunit of NADH:ubiquinone oxidoreductase. J. Biol. Chem. 278 (2003) 29072-29078
74. +-sensitive ubisemiquinone species (SQ(Nf)) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44 (2005) 1744-1754
75. 1 complex. J. Biol. Chem. 279 (2004) 15040-15049
76. 1 complex dimer is reduced through center N. J. Biol. Chem. 280 (2005) 22732-22740
77. 1 complex: a new crystal structure reveals an altered intramolecular hydrogen-bonding pattern. J. Mol. Biol. 351 (2005) 573-597
78. 1 complex with its bound substrate cytochrome c. Proc. Natl. Acad. Sci. USA 99 (2002) 2800-2805
79. 1 complex. J. Biol. Chem. 280 (2005) 9251-9257
80. Fernández-Morán H. Low-temperature electron microscopy and X-ray diffraction studies of lipoprotein components in lamellar systems. Circulation 26 (1962) 1039-1065
81. Allen R.D., Schroeder C.C., and Fok A.K. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J. Cell Biol. 108 (1989) 2233-2240
82. Allen R.D. Membrane tubulation and proton pumps. Protoplasma 189 (1995) 1-8
83. Nicastro D., Frangakis A.S., Typke D., and Baumeister W. Cryo-electron tomography of Neurospora mitochondria. J. Struct. Biol. 129 (2000) 48-56
84. 0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17 (1998) 7170-7178
85. Paumard P., Vaillier J., Coulary B., Schaeffer J., Soubannier V., Mueller D.M., Brethes D., di Rago J.-P., and Velours J. The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21 (2002) 221-230
86. Wittig I., and Schägger H. Advantages and limitations of clear-native PAGE. Proteomics 5 (2005) 4338-4346
87. Giraud M.-F., Paumard P., Soubannier V., Vaillier J., Arselin G., Salin B., Schaeffer J., Brethes D., di Rago J.-P., and Velours J. Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae?. Biochim. Biophys. Acta 1555 (2002) 174-180
88. Belogrudov G.I., Tomich J.M., and Hatefi Y. Membrane topography and near-neighbor relationships of the mitochondrial ATP synthase subunits e, f, and g. J. Biol. Chem. 271 (1996) 20340-20345
89. 0-ATPase: the novel subunit e is identical to Tim11. FEBS Lett. 411 (1997) 195-200
90. 0-ATP synthase of the yeast Saccharomyces cerevisiae: importance of the N-terminal membrane anchor region. Eukaryotic Cell 4 (2005) 346-355
91. Arselin G., Giraud M.-F., Dautant A., Vaillier J., Brethes D., Coulary-Salin B., Schaeffer J., and Velours J. The GxxxG motif of the transmembrane domain of subunit e is involved in the dimerization/oligomerization of the yeast ATP synthase complex in the mitochondrial membrane. Eur. J. Biochem. 270 (2003) 1875-1884
92. Bustos D.M., and Velours J. The modification of the conserved GXXXG motif of the membrane-spanning segment of subunit g destabilizes the supramolecular species of yeast ATP synthase. J. Biol. Chem. 280 (2005) 29004-29010
93. Fronzes R., Weimann T., Vaillier J., Velours J., and Brèthes D. The peripheral stalk participates in the yeast ATP synthase dimerization independently of e and g subunits. Biochemistry 45 (2006) 6715-6723
94. 1, the regulatory subunit of mitochondrial F-ATPase. EMBO J. 20 (2001) 6690-6696
95. 1. Nat. Struct. Biol. 10 (2003) 744-750
96. 0-ATP synthase dimeric complex does not require the ATPase inhibitor protein, Inh1. J. Biol. Chem. 277 (2002) 39289-39295
97. 1. Biochim. Biophys. Acta 1556 (2002) 133-141
98. 0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc. Natl. Acad. Sci. USA 102 (2005) 12356-12358
99. Dudkina N.V., Sunderhaus S., Braun H.P., and Boekema E.J. Characterization of dimeric ATP synthase and cristae membrane ultrastructure from Saccharomyces and Polytomella mitochondria. FEBS Lett. 580 (2006) 3427-3432
100. Dudkina N.V., Heinemeyer J., Keegstra W., Boekema E.J., and Braun H.P. Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett. 579 (2005) 5769-5772
101. van Lis R., Atteia A., Mendoza-Hernandez G., and Gonzalez-Halphen D. Identification of novel mitochondrial protein components of Chlamydomonas reinhardtii. A proteomic approach. Plant Physiol. 132 (2003) 318-330
102. Buzhynshyy N., Sens P., Prima V., Sturgis J., and Scheuring S. Rows of ATP synthase dimers in native mitochondrial inner membranes. Biophys. J. 93 (2007) 2870-2876
103. Strauss M., Hofhaus G., Schröder R.R., and Kühlbrandt W. Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27 (2008) 1154-1160
104. Dudkina N.V., Heinemeyer J., Sunderhaus S., Boekema E.J., and Braun H.-P. Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends in Plant Sci. 11 (2006) 232-240
105. Wittig I., Carrozzo R., Santorelli F.M., and Schägger H. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim. Biophys. Acta - Bioenergetics 1575 (2006) 1066-1072
106. Brass E.P., Hiatt W.R., Gardner A.W., and Hoppel C.L. Decreased NADH dehydrogenase and ubiquinol-cytochrome c oxidoreductase in peripheral arterial disease. Am. J. Physiol. Heart Circ. Physiol. (2001) 603-609
107. Benecke R., Strumper P., and Weiss H. Electron transfer complexes I and IV of platelets are abnormal in Parkinson's disease but normal in Parkinson-plus syndromes. Brain 116 (1993) 1451-1463
108. Cardellach F., Marti M.J., Fernandez-Sola J., Marin C., Hoek J.B., Tolosa E., and Urbano-Marquez A. Mitochondrial respiratory chain activity in skeletal muscle from patients with Parkinson's disease. Neurology 43 (1993) 2170-2172
109. Gu M., Cooper J.M., Taanman J.W., and Schapira A.H.V. Mitochondrial DNA transmission of the mitochondrial defect in Parkinson's disease. Ann. Neurol. 44 (1998) 177-186
110. van Straaten H.L.M., van Tintelen J.P., Trijbels J.M.F., van den Heuvel L.P., Troost D., Rozemuller-Kwakkel J.M., Duran M., de Vries L.S., Schuelke M., and Barth P.G. Neonatal lactic acidosis, complex I/IV deficiency, and fetal cerebral disruption. Neuropediatrics 36 (2005) 193-199
111. Mazzio E.A., and Soliman K.F. Effects of enhancing mitochondrial oxidative phosphorylation with reducing equivalents and ubiquinone on 1-methyl-4-phenylpyridinium toxicity and complex I-IV damage in neuroblastoma cells. Biochem. Pharmacol. 67 (2004) 1167-1184
112. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera: a visualisation system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612