Structure of a Complete ATP Synthase Dimer Reveals the Molecular Basis of Inner Mitochondrial Membrane Morphology

Molecular Cell

Volumn 63, Issue 3, 2016, Pages 445-456

  Hahn, Alexander ^a   Parey, Kristian ^a   Bublitz, Maike ^b   Mills, Deryck J ^a   Zickermann, Volker ^b   Vonck, Janet ^a   Kühlbrandt, Werner ^a   Meier, Thomas ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

bioenergetics; cryoelectron microscopy; F1Fo ATP synthase dimer; inner membrane morphology; membrane protein complex; mitochondria; rotary ATPase mechanism; X ray crystallography; yeast Yarrowia lipolytica

Indexed keywords

DIMER; HETERODIMER; MONOMER; OLIGOMYCIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATE; F1F0-ATP SYNTHASE; FUNGAL PROTEIN; PROTEIN SUBUNIT;

ARTICLE; CHEMICAL STRUCTURE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DIMERIZATION; ENZYME STRUCTURE; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; NONHUMAN; SURFACE PROPERTY; X RAY CRYSTALLOGRAPHY; YARROWIA LIPOLYTICA; ALPHA HELIX; CATALYSIS; CHEMISTRY; ENZYMOLOGY; METABOLISM; MITOCHONDRION; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; YARROWIA;

ADENOSINE TRIPHOSPHATE; CATALYSIS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MODELS, MOLECULAR; PROTEIN CONFORMATION, ALPHA-HELICAL; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; STRUCTURE-ACTIVITY RELATIONSHIP; YARROWIA;

EID: 84978484141     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.05.037     Document Type: Article

References (66)

1. 1-ATPase from bovine heart mitochondria. Nature 370 (1994), 621–628.
2. 1-ATPase complexed with the peptide antibiotic efrapeptin. Proc. Natl. Acad. Sci. USA 93 (1996), 9420–9424.
3. Allegretti, M., Klusch, N., Mills, D.J., Vonck, J., Kühlbrandt, W., Davies, K.M., Horizontal membrane-intrinsic α-helices in the stator a subunit of an F-type ATP synthase. Nature 521 (2015), 237–240.
4. 0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J. 17 (1998), 7170–7178.
5. Arselin, G., Giraud, M.F., Dautant, A., Vaillier, J., Brèthes, D., Coulary-Salin, B., Schaeffer, J., 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.
6. Baker, L.A., Watt, I.N., Runswick, M.J., Walker, J.E., Rubinstein, J.L., Arrangement of subunits in intact mammalian mitochondrial ATP synthase determined by cryo-EM. Proc. Natl. Acad. Sci. USA 109 (2012), 11675–11680.
7. 1-ATPase: configuration of a critical intermediate in ATP synthesis/hydrolysis. Proc. Natl. Acad. Sci. USA 95 (1998), 11065–11070.
8. Bowler, M.W., Montgomery, M.G., Leslie, A.G.W., Walker, J.E., How azide inhibits ATP hydrolysis by the F-ATPases. Proc. Natl. Acad. Sci. USA 103 (2006), 8646–8649.
9. Boyer, P.D., The ATP synthase—a splendid molecular machine. Annu. Rev. Biochem. 66 (1997), 717–749.
10. 0 stator subunits. J. Bioenerg. Biomembr. 32 (2000), 365–371.
11. Daum, B., Nicastro, D., Austin, J. 2nd, McIntosh, J.R., Kühlbrandt, W., Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22 (2010), 1299–1312.
12. Daum, B., Walter, A., Horst, A., Osiewacz, H.D., Kühlbrandt, W., Age-dependent dissociation of ATP synthase dimers and loss of inner-membrane cristae in mitochondria. Proc. Natl. Acad. Sci. USA 110 (2013), 15301–15306.
13. Davies, K.M., Strauss, M., Daum, B., Kief, J.H., Osiewacz, H.D., Rycovska, A., Zickermann, V., Kühlbrandt, W., Macromolecular organization of ATP synthase and complex I in whole mitochondria. Proc. Natl. Acad. Sci. USA 108 (2011), 14121–14126.
14. o-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc. Natl. Acad. Sci. USA 109 (2012), 13602–13607.
15. DeLeon-Rangel, J., Ishmukhametov, R.R., Jiang, W., Fillingame, R.H., Vik, S.B., Interactions between subunits a and b in the rotary ATP synthase as determined by cross-linking. FEBS Lett. 587 (2013), 892–897.
16. Dickson, V.K., Silvester, J.A., Fearnley, I.M., Leslie, A.G.W., Walker, J.E., On the structure of the stator of the mitochondrial ATP synthase. EMBO J. 25 (2006), 2911–2918.
17. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
18. 1) a subunit from Escherichia coli. Arch. Biochem. Biophys. 284 (1991), 71–77.
19. 1-c-ring and b-e-g complex. FEBS Lett. 589:19 Pt B (2015), 2707–2712.
20. 1-c-ring complexes of F-ATP synthase. J. Struct. Biol. 177 (2012), 490–497.
21. 1-ATPase from bovine mitochondria. Proc. Natl. Acad. Sci. USA 104 (2007), 15671–15676.
22. Houstek, J., Pícková, A., Vojtísková, A., Mrácek, T., Pecina, P., Jesina, P., Mitochondrial diseases and genetic defects of ATP synthase. Biochim. Biophys. Acta 1757 (2006), 1400–1405.
23. 0 ATP synthase of Escherichia coli defined by disulfide cross-linking. Proc. Natl. Acad. Sci. USA 95 (1998), 6607–6612.
24. Junge, W., Lill, H., Engelbrecht, S., ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem. Sci. 22 (1997), 420–423.
25. 1 ATPase. EMBO J. 25 (2006), 5433–5442.
26. Kashani-Poor, N., Kerscher, S., Zickermann, V., Brandt, U., Efficient large scale purification of his-tagged proton translocating NADH:ubiquinone oxidoreductase (complex I) from the strictly aerobic yeast Yarrowia lipolytica. Biochim. Biophys. Acta 1504 (2001), 363–370.
27. Kerscher, S., Durstewitz, G., Casaregola, S., Gaillardin, C., Brandt, U., The complete mitochondrial genome of Yarrowia lipolytica. Comp. Funct. Genomics 2 (2001), 80–90.
28. Kucharczyk, R., Zick, M., Bietenhader, M., Rak, M., Couplan, E., Blondel, M., Caubet, S.D., di Rago, J.P., Mitochondrial ATP synthase disorders: molecular mechanisms and the quest for curative therapeutic approaches. Biochim. Biophys. Acta 1793 (2009), 186–199.
29. Kühlbrandt, W., Davies, K.M., Rotary ATPases: A new twist to an ancient machine. Trends Biochem. Sci. 41 (2016), 106–116.
30. Lane, N., Martin, W., The energetics of genome complexity. Nature 467 (2010), 929–934.
31. Lee, J., Ding, S., Walpole, T.B., Holding, A.N., Montgomery, M.G., Fearnley, I.M., Walker, J.E., Organization of subunits in the membrane domain of the bovine F-ATPase revealed by covalent cross-linking. J. Biol. Chem. 290 (2015), 13308–13320.
32. Li, X., Mooney, P., Zheng, S., Booth, C.R., Braunfeld, M.B., Gubbens, S., Agard, D.A., Cheng, Y., Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10 (2013), 584–590.
33. 1-ATPase: a requirement for arginine at position 210 of the a subunit. Biochim. Biophys. Acta 894 (1987), 399–406.
34. Meier, T., Matthey, U., Henzen, F., Dimroth, P., Müller, D.J., The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids. FEBS Lett. 505 (2001), 353–356.
35. +-ATPase from Ilyobacter tartaricus. Science 308 (2005), 659–662.
36. Meier, T., Faraldo-Gómez, J.D., Börsch, M., ATP synthase, a paradigmatic molecular machine. Frank, J., (eds.) Molecular Machines in Biology, 2011, Cambridge University Press, 208–238.
37. 0 proton channel. Biochem. J. 430 (2010), 171–177.
38. +-transporting vacuolar ATPase. Proc. Natl. Acad. Sci. USA 108 (2011), 13474–13479.
39. Morales-Rios, E., Montgomery, M.G., Leslie, A.G.W., Walker, J.E., Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallography at 4.0 Å resolution. Proc. Natl. Acad. Sci. USA 112 (2015), 13231–13236.
40. +-ATPase from Enterococcus hirae. Science 308 (2005), 654–659.
41. 1-ATPase. Nature 386 (1997), 299–302.
42. Nübel, E., Wittig, I., Kerscher, S., Brandt, U., Schägger, H., Two-dimensional native electrophoretic analysis of respiratory supercomplexes from Yarrowia lipolytica. Proteomics 9 (2009), 2408–2418.
43. Pagadala, V., Vistain, L., Symersky, J., Mueller, D.M., Characterization of the mitochondrial ATP synthase from yeast Saccharomyces cerevisae. J. Bioenerg. Biomembr. 43 (2011), 333–347.
44. 0 component of the yeast ATP synthase. Biochemistry 39 (2000), 4199–4205.
45. Paumard, P., Vaillier, J., Coulary, B., Schaeffer, J., Soubannier, V., Mueller, D.M., Brèthes, D., di Rago, J.P., Velours, J., The ATP synthase is involved in generating mitochondrial cristae morphology. EMBO J. 21 (2002), 221–230.
46. Pogoryelov, D., Yildiz, O., Faraldo-Gómez, J.D., Meier, T., High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat. Struct. Mol. Biol. 16 (2009), 1068–1073.
47. 0 complex of ATP synthases. Nat. Chem. Biol. 6 (2010), 891–899.
48. Rees, D.M., Leslie, A.G.W., Walker, J.E., The structure of the membrane extrinsic region of bovine ATP synthase. Proc. Natl. Acad. Sci. USA 106 (2009), 21597–21601.
49. 1-ATPase from bovine heart mitochondria. Proc. Natl. Acad. Sci. USA 109 (2012), 11139–11143.
50. Runswick, M.J., Bason, J.V., Montgomery, M.G., Robinson, G.C., Fearnley, I.M., Walker, J.E., The affinity purification and characterization of ATP synthase complexes from mitochondria. Open Biol., 3, 2013, 120160.
51. Satre, M., de Jerphanion, M.B., Huet, J., Vignais, P.V., ATPase inhibitor from yeast mitochondria. Purification and properties. Biochim. Biophys. Acta 387 (1975), 241–255.
52. Scheres, S.H., RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180 (2012), 519–530.
53. Schwem, B.E., Fillingame, R.H., Cross-linking between helices within subunit a of Escherichia coli ATP synthase defines the transmembrane packing of a four-helix bundle. J. Biol. Chem. 281 (2006), 37861–37867.
54. Soubannier, V., Rusconi, F., Vaillier, J., Arselin, G., Chaignepain, S., Graves, P.V., Schmitter, J.M., Zhang, J.L., Mueller, D., Velours, J., The second stalk of the yeast ATP synthase complex: identification of subunits showing cross-links with known positions of subunit 4 (subunit b). Biochemistry 38 (1999), 15017–15024.
55. Soubannier, V., Vaillier, J., Paumard, P., Coulary, B., Schaeffer, J., Velours, J., 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.
56. Stephens, A.N., Roucou, X., Artika, I.M., Devenish, R.J., Nagley, P., Topology and proximity relationships of yeast mitochondrial ATP synthase subunit 8 determined by unique introduced cysteine residues. Eur. J. Biochem. 267 (2000), 6443–6451.
57. 0-ATP synthase probed by cysteine scanning mutagenesis and chemical modification. J. Biol. Chem. 278 (2003), 17867–17875.
58. Stock, D., Leslie, A.G.W., Walker, J.E., Molecular architecture of the rotary motor in ATP synthase. Science 286 (1999), 1700–1705.
59. 1-ATPase. Structure 15 (2007), 904–914.
60. Strauss, M., Hofhaus, G., Schröder, R.R., Kühlbrandt, W., Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J. 27 (2008), 1154–1160.
61. 10 ring of the yeast mitochondrial ATP synthase in the open conformation. Nat. Struct. Mol. Biol. 19 (2012), 485–491, S1.
62. 0 ATP synthases suggested by double mutants of the a subunit. J. Biol. Chem. 269 (1994), 30364–30369.
63. +-ATP synthase. J. Mol. Biol. 321 (2002), 307–316.
64. Xu, T., Pagadala, V., Mueller, D.M., Understanding structure, function, and mutations in the mitochondrial ATP synthase. Microb. Cell 2 (2015), 105–125.
65. Zhao, J., Benlekbir, S., Rubinstein, J.L., Electron cryomicroscopy observation of rotational states in a eukaryotic V-ATPase. Nature 521 (2015), 241–245.
66. Zhou, A., Rohou, A., Schep, D.G., Bason, J.V., Montgomery, M.G., Walker, J.E., Grigorieff, N., Rubinstein, J.L., Structure and conformational states of the bovine mitochondrial ATP synthase by cryo-EM. eLife, 4, 2015, e10180.