Biochemical and electron microscopic characterization of the F1F0 ATP Synthase from the hyperthermophilic eubacterium Aquifex aeolicus

FEBS Letters

Volumn 580, Issue 25, 2006, Pages 5934-5940

  Peng, Guohong ^a,b   Bostina, Mihnea ^a   Radermacher, Michael ^c   Rais, Isam ^d   Karas, Michael ^d   Michel, Hartmut ^a  

^a MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

^b INSTITUTE OF OCEANOLOGY   (China)

^c UNIVERSITY OF VERMONT   (United States)

^d GOETHE UNIVERSITY   (Germany)

Author keywords

Aquifex aeolicus; b Subunit; Electron microscopic single particle analysis; F1F0 ATPase; Mass spectrometric identification

Indexed keywords

PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AQUIFEX; ARTICLE; CHEMICAL ANALYSIS; ELECTRON MICROSCOPY; EUBACTERIUM; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTON-TRANSLOCATING ATPASES; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY;

AQUIFEX AEOLICUS;

EID: 33750073577     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2006.09.062     Document Type: Article

References (52)

1. Sone N., Yoshida M., Hirata H., and Kagawa Y. Reconstitution of adenosine-triphosphate synthesis by electrochemical proton gradient in vesicles reconstituted from purified adenosine-triphosphatase and phospholipids of thermophilic bacterium. J. Biol. Chem. 252 (1977) 2956-2960
2. Boyer P.D. The ATP synthase - a splendid molecular machine. Annu. Rev. Biochem. 66 (1997) 717-749
3. 0-ATP synthase. Biochim. Biophys. Acta 1553 (2002) 188-211
4. Walker J.E., Saraste M., and Gay N.J. The unc operon-nucleotide-sequence, regulation and structure of ATP-synthase. Biochim. Biophys. Acta 768 (1984) 164-200
5. 0-ATP synthases: Glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200 (1997) 217-224
6. Senior A.E. ATP synthesis by oxidative-phosphorylation. Physiol. Rev. 68 (1988) 177-231
7. Walker J.E., and Dickson V.K. The peripheral stalk of the mitochondrial ATP synthase. Biochim. Biophys. Acta 1757 (2006) 286-296
8. Abrahams J.P., Leslie A.G.W., Lutter R., and Walker J.E. Structure at 2.8-Angstrom resolution of F1-ATPase from bovine heart mitochondria. Nature 370 (1994) 621-628
9. Dunn S.D., Revington M., Cipriano D.J., and Shilton B.H. The b subunit of Escherichia coli ATP synthase. J. Bioenerg. Biomemb. 32 (2000) 347-355
10. 1 ATP synthase. J. Biol. Chem. 274 (1999) 15598-15604
11. Del Rizzo P.A., Bi Y., Dunn S.D., and Shilton B.H. The second stalk of Escherichia coli ATP synthase: structure of the isolated dimerization domain. Biochemistry 41 (2002) 6875-6884
12. 1-ATP synthase of Escherichia coli. Biochemistry 39 (2000) 3856-3860
13. 0 ATP synthase b subunit membrane domain. Bioenerg Biomemb. 35 (2003) 389-397
14. Grabar T.B., and Cain B.D. Genetic complementation between mutant b subunits in F1F0 ATP synthase. J. Biol. Chem. 279 (2004) 31205-31211
15. Ono S., Sone N., Yoshida M., and Suzuki T. ATP synthase that lacks F-o alpha-subunit - Isolation, properties, and indication of F(0)b(2)-subunits as an anchor rail of a rotating c-ring. J. Biol. Chem. 279 (2004) 33409-33412
16. Krebstakies T., Zimmermann B., Graber P., Altendorf K., Borsch M., and Greie J.C. Both rotor and stator subunits are necessary for efficient binding of F-1 to F-0 in functionally assembled Escherichia coli ATP synthase. J. Biol. Chem. 280 (2005) 33338-33345
17. Cherepanov D.A., Mulkidjanian A.Y., and Junge W. Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett. 449 (1999) 1-6
18. Wang H.Y., and Oster G. Energy transduction in the F-1 motor of ATP synthase. Nature 396 (1998) 279-282
19. Stock D., Leslie A.G., and Walker J.E. Molecular architecture of the rotary motor in ATP synthase. Science 286 (1999) 1700-1705
20. Rubinstein J.L., Walker J.E., and Henderson R. Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J. 22 (2003) 6182-6192
21. Mellwig C., and Böttcher B. A unique resting position of the ATP-synthase from chloroplasts. J. Biol. Chem. 278 (2003) 18544-18549
22. Perutz M.F., and Raidt H. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature 255 (1975) 256-259
23. Berezovsky I.N., and Shakhnovich E.I. Physics and evolution of thermophilic adaptation. Proc. Natl. Acad. Sci. USA 102 (2005) 12742-12747
24. Deckert G., Warren P.V., Gaasterland T., Young W.G., Lenox A.L., Graham D.E., Overbeek R., Snead M.A., Keller M., Aujay M., Huber R., Feldman R.A., Short J.M., Olsen G.J., and Swanson R.V. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392 (1998) 353-358
25. Peng G.H., Fritzsch G., Zickermann V., Shägger H., Mentele R., Lottspeich F., Bostina M., Radermacher M., Huber R., Stetter K.O., and Michel H. Isolation, characterization and electron microscopic single particle analysis of the NADH : ubiquinone oxidoreductase (complex I) from the hyperthermophilic eubacterium Aquifex aeolicus. Biochemistry 42 (2003) 3032-3039
26. Schägger H., and Gebhard v.J. Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal. Biochem. 199 (1991) 223-231
27. Zerbetto E., Vergani L., and Dabbeni-Sala F. Quantification of muscle mitochondrial oxidative phosphorylation enzymes via histochemical staining of blue native polyacrylamide gels. Electrophoresis 18 (2000) 2059-2064
28. Dabbeni-Sala F., Santo S.D., Franceschini D., Skaper S.D., and Giusti P. Melatonin protects against 6-OHDA-induced neurotoxicity in rats: a role for mitochondrial complex I activity. FASEB J. 15 (2001) 164-170
29. Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227 (1970) 680
30. Rais I., Karas M., and Schägger H. Two-dimensional electrophoresis for the isolation of integral membrane proteins and mass spectrometric identification. Proteomics 4 (2004) 2567-2571
31. Stoops J.K., Baker T.S., Schroeter J.P., Kolodziej S.J., Niu X.D., and Reed L.J. Three-dimensional structure of the truncated core of the Saccharomyces cerevisiae pyruvate dehydrogenase complex determined from negative stain and cryoelectron microscopy images. J. Biol. Chem. 267 (1992) 24769-24775
32. Frank J., Radermacher M., Penczek P., Zhu J., Li Y.H., Ladjadj M., and Leith A. SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
33. Marabini R., Masegosa I.M., SanMartin M.C., Marco S., Fernandez J.J., delaFraga L.G., Vaquerizo C., and Carazo J.M. Xmipp: An image processing package for electron microscopy. J. Struct. Biol. 116 (1996) 237-240
34. Radermacher M., Ruiz T., Wieczorek H., and Grüber G. The structure of the V-1-ATPase determined by three-dimensional electron microscopy of single particles. J. Struct. Biol. 135 (2001) 26-37
35. Radermacher M. Radon transform techniques for alignment and 3D reconstruction from random projections. Scanning Microsc. 11 (1997) 171-177
36. Saxton W.O., and Baumeister W. The correlation averaging of a regularly arranged bacterial-cell envelope protein. J. Microsc. 127 (1982) 127-138
37. Notredame C., Higgins D., and Heringa J. A novel method for multiple sequence alignment. J. Mol. Biol. 302 (2000) 205-217
38. Chang J.F., Hall B.E., Tanny J.C., Moazed D., Filman D., and Ellenberger T. Structure of the coiled-coil dimerization motif of Sir4 and its interaction with Sir3. Structure 11 (2003) 637-649
39. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
40. Sonnhammer E.L.L., von Heijne G., and Krogh A. In: Glasgow J., Littlejohn T., Major F., Lathrop R., Sankoff D., and Sensen C. (Eds). Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (1998), AAA1 Press, Menlo Park, CA 175-182
41. 0-ATP synthase by immune electron microscopy: The subunit delta binds on top of the F-1. J. Mol. Biol. 295 (2000) 387-391
42. Boekema E.J., van Breeemen J.F.L., Brisson A., Ubbink-Kok T., Konings W.N., and Lolkema J. Connecting stalks in V-ATPase. Nature 401 (1999) 37-38
43. Wilkens S., Vasilyeva E., and Forgac M. Structure of the vacuolar ATPase by electron microscopy. J. Biol. Chem. 45 (1999) 31804-31810
44. 1-catalytic subunit. J. Biol. Chem. 258 (1983) 14599-14609
45. Dunn S.D., and Chandler J. Characterization of a b(2)delta complex from Escherichia coli ATP synthase. J. Biol. Chem. 273 (1998) 8646-8651
46. 0-ATPase. J. Biol. Chem. 272 (1997) 30047-30053
47. Mendelhartvig J., and Capaldi R.A. Structure-function-relationships of the delta-subunit in Escherichia coli adenosine-triphosphatase. Biochim. Biophys. Acta 1060 (1991) 115-124
48. McLachlin D.T., Bestard J.A., and Dunn S.D. The b and delta subunits of the Escherichia coli ATP synthase interact via residues in their C-terminal regions. J. Biol. Chem. 273 (1998) 15162-15168
49. McLachlin D.T., Coveny A.M., Clark S.M., and Dunn S.D. Site-directed cross-linking of b to the alpha, beta, and a subunits of the Escherichia coli ATP synthase J. Biol. Chem. 275 (2000) 17571-17577
50. Herrmann R.G., Steppuhn J., Herrmann G.S., and Nelson N. The nuclear-encoded polypeptide Cfo-II from spinach is a real, ninth subunit of chloroplast ATP synthase. FEBS Lett. 326 (1993) 192-198
51. Cozens A.L., and Walker J.E. The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Syechococcus 6301. Support for an endosymbiotic origin of chloroplasts. J. Mol. Biol. 194 (1987) 359-383
52. 0 sectors. Biochem. J. 254 (1988) 109-122