Active oligomeric ATP synthases in mammalian mitochondria

Biochemical and Biophysical Research Communications

Volumn 329, Issue 2, 2005, Pages 583-590

  Krause, Frank ^a   Reifschneider, Nicole H ^a   Goto, Sataro ^b   Dencher, Norbert A ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b TOHO UNIVERSITY   (Japan)

Author keywords

ATP synthase; Blue native electrophoresis; Colourless native electrophoresis; Membrane protein complex; Mitochondria; Oxidative phosphorylation; Protein protein interactions

Indexed keywords

DIGITONIN; MONOMER; OLIGOMER; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TETRAMER;

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; COLOR; CONTROLLED STUDY; COW; ENZYME ACTIVITY; HEART MITOCHONDRION; INTERMETHOD COMPARISON; KIDNEY; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OLIGOMERIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; STATISTICAL SIGNIFICANCE;

EID: 14644414866     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.02.010     Document Type: Article

References (70)

1. P. Mitchell Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism Nature 191 1961 144 148
2. P.D. Boyer Catalytic site forms and controls in ATP synthase catalysis Biochim. Biophys. Acta 1458 2000 252 262
3. K.N. Truscott, K. Brandner, and N. Pfanner Mechanisms of protein import into mitochondria Curr. Biol. 13 2003 R326 R337
4. 1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
5. D. Stock, A.G. Leslie, and J.E. Walker Molecular architecture of the rotary motor in ATP synthase Science 286 1999 1700 1705
6. H. Seelert, A. Poetsch, N.A. Dencher, A. Engel, H. Stahlberg, and D.J. Müller Structural biology: proton-powered turbine of a plant motor Nature 405 2000 418 419
7. H. Seelert, N.A. Dencher, and D.J. Müller Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase J. Mol. Biol. 333 2003 337 344
8. +-ATP synthase has an undecameric rotor EMBO Rep. 2 2001 229 233
9. 1-ATPase Nature 381 1996 623 625
10. 1-ATPase Nature 386 1997 299 302
11. 1): direct observation Science 286 1999 1722 1724
12. O-ATP synthase Proc. Natl. Acad. Sci. USA 98 2001 898 902
13. O sector of Escherichia coli ATP synthase Proc. Natl. Acad. Sci. USA 98 2001 8519 8524
14. +/ATP ratio and permissive elastic coupling Proc. Natl. Acad. Sci. USA 101 2004 12159 12164
15. R.D. Allen, C.C. Schroeder, and A.K. Fok An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques J. Cell Biol. 108 1989 2233 2240
16. D. Nicastro, A.S. Frangakis, D. Typke, and W. Baumeister Cryo-electron tomography of Neurospora mitochondria J. Struct. Biol. 129 2000 48 56
17. O-ATPase: the novel subunit e is identical to Tim11 FEBS Lett. 14 1997 195 200
18. O-ATP synthase exists as a dimer: identification of three dimer-specific subunits EMBO J. 17 1998 7170 7178
19. H. Schägger, and K. Pfeiffer Supercomplexes in the respiratory chains of yeast and mammalian mitochondria EMBO J. 19 2000 1777 1783
20. H. Schägger, and K. Pfeiffer 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
21. H. Schägger Respiratory chain supercomplexes IUBMB Life 2 2001 119 128
22. H. Schägger Respiratory chain supercomplexes of mitochondria and bacteria Biochim. Biophys. Acta 1555 2002 154 159
23. H. Schägger, R. de Coo, M.F. Bauer, S. Hofmann, C. Godinot, and U. Brandt Significance of respirasomes for the assembly/stability of human respiratory chain complex I J. Biol. Chem. 279 2004 36349 36353
24. R. van Lis, A. Atteia, G. Mendoza-Hernández, and D. González-Halphen Identification of novel mitochondrial protein components of Chlamydomonas reinhardtii. A proteomic approach Plant Physiol. 132 2003 318 330
25. +-ATP synthase in the chloroplast of Chlamydomonas reinhardtii Biochim. Biophys. Acta 1658 2004 202 211
26. P. Cardol, F. Vanrobaeys, B. Devreese, J. Van Beeumen, R.F. Matagne, and C. Remacle Higher plant-like subunit composition of mitochondrial complex I from Chlamydomonas reinhardtii: 31 conserved components among eukaryotes Biochim. Biophys. Acta 1658 2004 212 224
27. M. Neboháĉová, D.A. Maslov, A.M. Falick, and L. Simpson The effect of RNA interference down-regulation of RNA editing 3′-terminal uridylyl transferase (TUTase) 1 on mitochondrial de novo protein synthesis and stability of respiratory complexes in Trypanosoma brucei J. Biol. Chem. 279 2004 7819 7825
28. F. Krause, C.Q. Scheckhuber, A. Werner, S. Rexroth, N.H. Reifschneider, N.A. Dencher, and H.D. Osiewacz 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
29. H. Eubel, L. Jänsch, and H.P. Braun New insights into the respiratory chain of plant mitochondria. Supercomplexes and a unique composition of complex II Plant Physiol. 133 2003 274 286
30. F. Krause, N.H. Reifschneider, D. Vocke, H. Seelert, S. Rexroth, and N.A. Dencher Respirasome-like supercomplexes in green leaf mitochondria of spinach J. Biol. Chem. 279 2004 48369 48375
31. P. Paumard, J. Vaillier, B. Coulary, J. Schaeffer, V. Soubannier, D.M. Mueller, D. Brethes, J.P. di Rago, and J. Velours The ATP synthase is involved in generating mitochondrial cristae morphology EMBO J. 21 2002 221 230
32. V. Soubannier, J. Vaillier, P. Paumard, B. Coulary, J. Schaeffer, and J. Velours In the absence of the first membrane-spanning segment of subunit 4(b), the yeast ATP synthase is functional but does not dimerize or oligomerize J. Biol. Chem. 277 2002 10739 10745
33. P. Paumard, G. Arselin, J. Vaillier, S. Chaignepain, K. Bathany, J.M. Schmitter, D. Brethes, and J. Velours Two ATP synthases can be linked through subunits i in the inner mitochondrial membrane of Saccharomyces cerevisiae Biochemistry 41 2002 10390 10396
34. M.F. Giraud, P. Paumard, V. Soubannier, J. Vaillier, G. Arselin, B. Salin, J. Schaeffer, D. Brethes, J.P. di Rago, and J. Velours 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
35. O-ATP synthase dimeric complex does not require the ATPase inhibitor protein, Inh1 J. Biol. Chem. 277 2002 39289 39295
36. O-ATP synthase forms homodimers J. Biol. Chem. 277 2002 48484 48489
37. G. Arselin, M.F. Giraud, A. Dautant, J. Vaillier, D. Brethes, B. Coulary-Salin, J. Schaeffer, and J. Velours 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
38. G. Arselin, J. Vaillier, B. Salin, J. Schaeffer, M.F. Giraud, A. Dautant, D. Brethes, and J. Velours The modulation in subunits e and g amounts of yeast ATP synthase modifies mitochondrial cristae morphology J. Biol. Chem. 279 2004 40392 40399
39. 1 J. Biol. Chem. 275 2000 28353 28355
40. 1 Biochim. Biophys. Acta 1556 2002 133 141
41. K. Pfeiffer, V. Gohil, R.A. Stuart, C. Hunte, U. Brandt, M.L. Greenberg, and H. Schägger Cardiolipin stabilizes respiratory chain supercomplexes J. Biol. Chem. 278 2003 52873 52880
42. O-ATP synthase Biochim. Biophys. Acta 1607 2003 167 179
43. V.K. Mootha, J. Bunkenborg, J.V. Olsen, M. Hjerrild, J.R. Wisniewski, E. Stahl, M.S. Bolouri, H.N. Ray, S. Sihag, M. Kamal, N. Patterson, E.S. Lander, and M. Mann Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria Cell 115 2003 629 640
44. R. Takahashi, and S. Goto Influence of dietary restriction on accumulation of heat-labile enzyme molecules in the liver and brain of mice Arch. Biochem. Biophys. 257 1987 200 206
45. A.L. Smith Preparations, properties and conditions for assay of mitochondria: slaughterhouse material, small scale Methods Enzymol. 10 1967 81 86
46. G.A. Salvador, F.A. López, and N.M. Giusto Age-related changes in central nervous system phosphatidylserine decarboxylase activity J. Neurosci. Res. 70 2002 283 289
47. M. Nagai, R. Takahashi, and S. Goto Dietary restriction initiated late in life can reduce mitochondrial protein carbonyls in rat livers: Western blot studies Biogerontology 1 2000 321 328
48. Z. Radak, M. Sasvari, C. Nyakas, A.W. Taylor, H. Ohno, H. Nakamoto, and S. Goto Regular training modulates the accumulation of reactive carbonyl derivatives in mitochondrial and cytosolic fractions of rat skeletal muscle Arch. Biochem. Biophys. 383 2000 114 118
49. H. Schägger, W.A. Cramer, and G. von Jagow Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis Anal. Biochem. 217 1994 220 230
50. S. Rexroth, J.M.W. Meyer zu Tittingdorf, F. Krause, N.A. Dencher, and H. Seelert Thylakoid membrane at altered metabolic state: challenging the forgotten realms of the proteome Electrophoresis 24 2003 2814 2823
51. E. Zerbetto, L. Vergani, and F. Dabbeni-Sala Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels Electrophoresis 18 1997 2059 2066
52. Y. Hatefi, A.G. Haavik, and D.E. Griffiths Studies on the electron transfer system. XL. Preparation and properties of mitochondrial DPNH-coenzyme Q reductase J. Biol. Chem. 237 1962 1676 1680
53. R. Rossignol, T. Letellier, M. Malgat, C. Rocher, and J.P. Mazat Tissue variation in the control of oxidative phosphorylation: implication for mitochondrial diseases Biochem. J. 347 2000 45 53
54. 1 by blue native electrophoresis Biochem. Biophys. Res. Commun. 259 1999 569 575
55. N.H. Reifschneider, S. Goto, H. Nakamoto, R. Takahashi, M. Sugawa, N.A. Dencher, F. Krause, manuscript in preparation
56. F. Krause, A. Werner, N.A. Dencher, H.D. Osiewacz, manuscript in preparation
57. R.D. Allen Membrane tubulation and proton pumps Protoplasma 189 1995 1 8
58. P.D. Gavin, M. Prescott, S.E. Luff, and R.J. Devenish Cross-linking ATP synthase complexes in vivo eliminates mitochondrial cristae J. Cell Sci. 117 2004 2333 2343
59. M. Grabe, J. Neu, G. Oster, and P. Nollert Protein interactions and membrane geometry Biophys J. 84 2003 854 868
60. R.W. Gilkerson, J.M. Selker, and R.A. Capaldi The crystal membrane of mitochondria is the principal site of oxidative phosphorylation FEBS Lett. 546 2003 355 358
61. R.W. Gilkerson, D.H. Margineantu, R.A. Capaldi, and J.M. Selker Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells FEBS Lett. 474 2000 1 4
62. T.A. Harkness, F.E. Nargang, I. van der Klei, W. Neupert, and R. Lill A crucial role of the mitochondrial protein import receptor MOM19 for the biogenesis of mitochondria J. Cell Biol. 124 1994 637 648
63. G.A. Perkins, C.W. Renken, I.J. van der Klei, M.H. Ellisman, W. Neupert, and T.G. Frey Electron tomography of mitochondria after the arrest of protein import associated with Tom19 depletion Eur. J. Cell Biol. 80 2001 139 150
64. V. Helms Attraction within the membrane. Forces behind transmembrane protein folding and supramolecular complex assembly EMBO Rep. 3 2002 1133 1138
65. G. Vereb, J. Szöllósi, J. Matkó, P. Nagy, T. Farkas, L. Vígh, L. Mátyus, T.A. Waldmann, and S. Damjanovich Dynamic, yet structured: the cell membrane three decades after the Singer-Nicolson model Proc. Natl. Acad. Sci. USA 100 2003 8053 8058
66. i and ADP/ATP J. Biol. Chem. 278 2003 12305 12309
67. i and ADP/ATP J. Biol. Chem. 279 2004 31761 31768
68. + channel activity Proc. Natl. Acad. Sci. USA 101 2004 11880 11885
69. H. Schägger, and G. von Jagow Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form Anal. Biochem. 199 1991 223 231
70. +-ATP synthase purified by blue native electrophoresis Biochim. Biophys. Acta 1466 2000 339 349