Skip to main content
SpringerLink
Log in

The ATP synthase (F0−F1) complex in oxidative phosphorylation

  • Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

The transmembrane electrochemical proton gradient generated by the redox systems of the respiratory chain in mitochondria and aerobic bacteria is utilized by proton translocating ATP synthases to catalyze the synthesis of ATP from ADP and Pi. The bacterial and mitochondrial H+-ATP synthases both consist of a membranous sector, F0, which forms a H+-channel, and an extramembranous sector, F1, which is responsible for catalysis. When detached from the membrane, the purified F1 sector functions mainly as an ATPase. In chloroplasts, the synthesis of ATP is also driven by a proton motive force, and the enzyme complex responsible for this synthesis is similar to the mitochondrial and bacterial ATP synthases. The synthesis of ATP by H+-ATP synthases proceeds without the formation of a phosphorylated enzyme intermediate, and involves co-operative interactions between the catalytic subunits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Al-Shawi, M., and Senior, A. E., Complete kinetic and thermodynamic characterization of the unisite catalytic pathway ofEscherichia coli F1-ATPase. Comparison with mitochondrial F1-ATPase and application to the study of mutant enzymes. J. biol. Chem.263 (1988) 19640–19648.

    PubMed  Google Scholar 

  2. Andrews, W. W., Hill, F. C., and Allison, W. S., Identification of the essential tyrosine residue in the β subunit of bovine heart mitochondrial F1-ATPase that is modified by 7-chloro-4-nitro-[14C]benzofurazan. J. biol. Chem.259 (1984) 8219–8225.

    PubMed  Google Scholar 

  3. Andrews, W. W., Hill, F. C., and Allison, W. S., Identification of the lysine residue to which the 4-nitrobenzofurazan group migrates after the bovine mitochondrial F1-ATPase is inactivated with 7-chloro-4-nitro[14C]benzofurazan. J. biol. Chem.259 (1984) 14378–14382.

    PubMed  Google Scholar 

  4. Azzi, A., Bragadin, M. A., Tamburro, A. M., and Santato, M., Sitedirected spin labeling of the mitochondrial membrane. Synthesis and utilization of the adenosine triphosphatase inhibitor (N-(2,2,6,6-tetramethyl-piperidyl-1-oxyl)-N′-(cyclohexyl)-carbodiimide). J. biol. Chem.248 (1973) 5520–5526.

    PubMed  Google Scholar 

  5. Baubichon, H., Godinot, C., Di Pietro, A., and Gautheron, D. C., Competition between ADP and nucleotide analogues to occupy regulatory site(s) related to hysteretic inhibition of mitochondrial F1-ATPase. Biochem. biophys. Res. Commun.100 (1981) 1032–1038.

    PubMed  Google Scholar 

  6. Baubichon, H., Di Pietro, A., Godinot, C., and Gautheron, D. C., Abolition of anion-activation of mitochondrial F1-ATPase by the partial ADP-induced hysteretic inhibition. FEBS Lett.137 (1982) 261–264.

    PubMed  Google Scholar 

  7. Beechey, R. B., Linnett, P. E., and Fillingame, R. H., Isolation of carbodiimide-binding proteins from mitochondria andEscherichia coli. Meth. Enzymol.55 (1979) 426–434.

    PubMed  Google Scholar 

  8. Bianchet, M., Ysern, X., Hullihen, J., Pedersen, P. L., and Amzel, L. M., Mitochondrial ATP synthase. Quaternary structure of the F1 moiety at 3.6 Å determined by X-ray diffraction analysis. J. biol. Chem.266 (1991) 21 197–21 201.

    Google Scholar 

  9. Boekema, E. J., Berden, J. A., and Van Heel, M. G., Structure of the mitochondrial F1-ATPase studied by electron microscopy and image processing. Biochim. biophys. Acta851 (1986) 353–360.

    PubMed  Google Scholar 

  10. Bossard, M. J., Vik, T. A., and Schuster, S. M., Beef heart mitochondrial adenosine triphosphatase-catalyzed formation of a transition state analog in ATP synthesis. J. biol. Chem.255 (1980) 5342–5346.

    PubMed  Google Scholar 

  11. Boyer, P. D., A perspective of the binding change mechanism for ATP synthesis. FASEB J.3 (1989) 2164–2178.

    PubMed  Google Scholar 

  12. Bragg, P. D., and Hou, C., Chemical crosslinking of a subunits in the F1 adenosine triphosphatase ofEscherichia coli. Archs biochem. Biophys.244 (1986) 361–372.

    Google Scholar 

  13. Bragg, P. D., and Hou, C. Role of minor subunits in the structural asymmetry of theEscherichia coli F1-ATPase. Biochem. biophys. Res. Commun.166 (1990) 431–435.

    PubMed  Google Scholar 

  14. Bullough, D. A., and Allison, W. S., Three copies of the β subunit must be modified to achieve complete inactivation of the bovine mitochondrial F1-ATPase by 5′-p-fluorosulfonylbenzoyladenosine. J. biol. Chem.261 (1986) 5722–5730.

    PubMed  Google Scholar 

  15. Bullough, D. A., and Allison, W. S., Inactivation of the bovine heart mitochondrial F1-ATPase by 5′-p-fluorosulfonylbenzoyl-[3H]-inosine is accompanied by modification of tyrosine 345 in a single β subunit. J. biol. Chem.261 (1986) 14171–14177.

    PubMed  Google Scholar 

  16. Bullough, D. A., Verburg, J. G., Yoshida, M., and Allison, W. S., Evidence for a functional heterogeneity among the catalytic sites of the bovine heart mitochondrial F1-ATPase. J. biol. Chem.262 (1987) 11675–11683.

    PubMed  Google Scholar 

  17. Choate, G. L., Hutton, R. L., and Boyer, P. D., Occurrence and significance of oxygen exchange reactions catalyzed by mitochondrial adenosine triphosphatase preparations. J. biol. Chem.254 (1979) 286–290.

    PubMed  Google Scholar 

  18. Chuan, H., and Wang, J. H., 3′-O-(5-fluoro-2,4-dinitrophenyl)ADP ether and ATP ether. Affinity reagents for labeling ATPase. J. biol. Chem.163 (1988) 13003–13006.

    Google Scholar 

  19. Cox, G. B., Jans, D. A., Fimmel, A. L., Gibson, F., and Hatch, L., The mechanism of ATP synthase. Conformational change by rotation of the β-subunit. Biochim. biophys. Acta768 (1984) 201–208.

    PubMed  Google Scholar 

  20. Cross, R. L., The number of functional catalytic sites of F1-ATPases and the effects of quaternary structural asymmetry on their properties. J. Bioenerg. Biomemb.20 (1988) 395–405.

    Google Scholar 

  21. Cross, R. L., and Nalin, C. M., Adenine nucleotide binding sites on beef heart F1-ATPase. Evidence for three exchangeable sites that are distinct from three noncatalytic sites. J. biol. Chem.257 (1982) 2874–2881.

    PubMed  Google Scholar 

  22. Cross, R. L., Grubmeyer, C., and Penefsky, H. S., Mechanism of ATP hydrolysis by beef heart mitochondrial ATPase. Rate enhancements resulting from cooperative interactions between multiple catalytic sites. J. biol. Chem.257 (1982) 12101–12105.

    PubMed  Google Scholar 

  23. Cross, R. L., Cunningham, D., Miller, C. G., Xue, Z., Zhou, J.-M., and Boyer, P. D., Adenine nucleotide binding sites on beef heart F1-ATPase: photoaffinity labeling of β-sunbunit Tyr-368 at a noncatalytic site and β Tyr-345 at a catalytic site. Proc. natl Acad. Sci.84 (1987) 5715–5719.

    PubMed  Google Scholar 

  24. Di Pietro, A., Penin, F., Godinot, C., and Gautheron, D. C., “Hysteretic” behavior and nucleotide binding sites of pig heart mitochondrial F1 adenosine 5′-triphosphatase. Biochemistry19 (1980) 5671–5678.

    PubMed  Google Scholar 

  25. Dunn, S. D., ATP causes a large change in the conformation of the isolated α subunit ofEscherichia coli F1-ATPase. J. biol. Chem.255 (1980) 11857–11860.

    PubMed  Google Scholar 

  26. Dunn, S. D., The isolated γ subunit ofEscherichia coli F1-ATPase binds the ε subunit. J. biol. Chem.257 (1982) 7354–7359.

    PubMed  Google Scholar 

  27. Dunn, S. D., and Futai, M., Reconstitution of the functional coupling factor from the isolated subunits ofEscherichia coli F1-ATPase. J. biol. Chem.255 (1980) 113–118.

    PubMed  Google Scholar 

  28. Dunn, S. D., Heppel, L. A., and Fullmer, C. S., The NH2-terminal portion of the α subunit ofEscherichia coli F1-ATPase is required for binding the δ subunit. J. biol. Chem.255 (1980) 6891–6896.

    PubMed  Google Scholar 

  29. Dupuis, A., Issartel, J.-P., Lunardi, J., Satre, M., and Vignais, P. V., Interactions between the oligomycin sensitivity conferring protein (OSCP) and beef heart mitochondrial F1-ATPase. 1. Study of the binding parameters with a chemically radiolabeled OSCP. Biochemistry24 (1985) 728–733.

    PubMed  Google Scholar 

  30. Dupuis, A., Lunardi, J., Issartel, J.-P., and Vignais, P. V., Interactions between the oligomycin sensitivity conferring protein (OSCP) and beef heart mitochondrial F1-ATPase. 2. Identification of the interacting F1 subunits by cross-linking. Biochemistry24 (1985) 734–739.

    PubMed  Google Scholar 

  31. Dupuis, A., Issartel, J.-P., and Vignais, P. V., Direct identification of the fluoroaluminate and fluoroberyllate species responsible for inhibition of the mitochondrial F1-ATPase. FEBS Lett.255 (1989) 47–52.

    Google Scholar 

  32. Engelbrecht, S., Lill, H., and Junge, W., Reconstitution of CF1-depleted thylakoid membranes with complete and fragmented chloroplast ATPase. The role of the δ subunit for proton conduction through CF0. Eur. J. Biochem.160 (1986) 635–643.

    PubMed  Google Scholar 

  33. Esch, F. S., Böhlen, P., Otsuka, A. S., Yoshida, M., and Allison, W. S., Inactivation of the bovine mitochondrial F1-ATPase with Dicyclohexyl[14C]carbodiimide leads to the modification of a specific glutamic acid residue in the β subunit. J. biol. Chem.256 (1981) 9084–9089.

    PubMed  Google Scholar 

  34. Feldman, R. I., and Sigman, D. S., The synthesis of enzyme bound ATP by soluble chloroplast coupling factor 1. J. biol. Chem.257 (1982) 1676–1683

    PubMed  Google Scholar 

  35. Fellous, G., Godinot, C., Baubichon, H., Di Pietro, A., and Gautheron, D. C., Photolabeling on β-subunit of the nucleotide site related to hysteretic inhibition of mitochondrial F1-ATPase. Biochemistry23 (1984) 5294–5299.

    Google Scholar 

  36. Fleury B., Di Pietro, A., Godinot, C., and Gautheron, D. C., Role of magnesium of kinetic parameters of soluble F1-ATPase from pig heart mitochondria. Biochimie62 (1980) 733–737.

    PubMed  Google Scholar 

  37. Foster, D. L., and Fillingame, R. H., Stoichiometry of subunits in the H+-ATPase complex ofEscherichia coli. J. biol. Chem.257 (1982) 2009–2015.

    PubMed  Google Scholar 

  38. Fraga, D., and Fillingame, R. H., Essential residues in the polar loop region of subunit c ofEscherichia coli F1-F0 ATP synthase defined by random oligonucleotide-primed mutagenesis. J. Bact.173 (1991) 2639–2643.

    PubMed  Google Scholar 

  39. Fry, D. C., Kuby, S. A., and Mildvan, A. S., ATP-binding site of adenylate kinase: Mechanistic implications of its homology withras-encoded p21, F1-ATPase, and other nucleotide-binding proteins. Proc. natl Acad. Sci.83 (1986) 907–911.

    PubMed  Google Scholar 

  40. Futai, M., Noumi, T., and Maeda, M., Molecular genetics of F1-ATPase fromEscherichia coli. J. Bioenerg. Biomemb.20 (1988) 41–58.

    Google Scholar 

  41. Garboczi, D. N., Shenbagamurthi, P., Kirk, W., Hullihen, J., and Pedersen, P. L., Mitochondrial ATP synthase. Interaction of a synthetic 50-amino acid, β subunit peptide with ATP. J. biol. Chem.263 (1988) 812–816.

    PubMed  Google Scholar 

  42. Garboczi, D. N., Thomas, P. J., and Pedersen, P. L., Rat liver mitochondrial ATP synthase. Effects of mutations in the glycine-rich region of a β subumit peptide on its interaction with adenine nucleotides. J. biol. Chem.265 (1990) 14632–14637.

    PubMed  Google Scholar 

  43. Garin, J., Boulay, F., Issartel, J.-P., Lunardi, J., and Vignais, P. V., Identification of amino acid residues photolabeled with 2-azido(α-32P)adenosine diphosphate in the β subunit of beef heart mitochondrial F1-ATPase. Biochemistry25 (1986) 4431–4437.

    PubMed  Google Scholar 

  44. Garin, J., Michel, L., Dupuis, A., Issartel, J.-P., Lunardi, J., Hoppe, J., and Vignais, P., Photolabeling of the phosphate binding site of mitochondrial F1-ATPase by (32P)azidonitrophenyl phosphate. Identification of the photolabeled amino acid residues. Biochemistry28 (1989) 1442–1448.

    PubMed  Google Scholar 

  45. Garrett, N. E., and Penefsky, H. S., Interaction of adenine nucleotides with multiple binding sites on beef heart mitochondrial adenosine triphosphatase. J. biol. Chem.250 (1975) 6640–6647.

    PubMed  Google Scholar 

  46. Girault, G., Berger, G., Galmiche, J.-M., and André, F., Characterization of six nucleotide-binding sites on chloroplast coupling factor 1 and one site on its purified β subunit. J. biol. Chem.263 (1988) 14690–14695.

    PubMed  Google Scholar 

  47. Gogol, E. P., Lücken, U., and Capalid, R. A., The stalk connecting the F1 and F0 domains of ATP synthase visualized by electron microscopy of unstained specimens. FEBS Lett.219 (1987) 274–278.

    PubMed  Google Scholar 

  48. Gogol, E. P., Lücken, U., Bork, T.,and Capaldi, R. A., Molecular architecture ofEscherichia coli F1 adenosine triphosphatase. Biochemistry28 (1989) 4709–4716.

    PubMed  Google Scholar 

  49. Gresser, M. J., Myers, J. A., and Boyer, P. D., Catalytic cooperativity of beef heart mitochondrial F1 adenosine triphosphatase. Correlations of initial velocity, bound intermediate and oxygen exchange measurements with an alternating three-site model. J. biol. Chem.257 (1982) 12030–12038.

    PubMed  Google Scholar 

  50. Grubmeyer, C., and Penefsky, H. S., Cooperativity between catalytic sites in the mechanism of action of beef heart mitochondrial adenosine triphosphatase. J. biol. Chem.256 (1981) 3728–3734.

    PubMed  Google Scholar 

  51. Grubmeyer, C., Cross, R. L. and Penefsky, H. S., Mechanism of ATP hydrolysis by beef heart mitochondrial ATPase. Rate constants for elementary steps in catalysis at a single site. J. biol. Chem.257 (1982) 12092–12100.

    PubMed  Google Scholar 

  52. Harris, D. A., The interactions of coupling ATPases with nucleotides. Biochim. biophys. Acta463 (1978) 245–273.

    PubMed  Google Scholar 

  53. Harris, D. A., Azide as a probe of co-operative interactions in the mitochondrial F1-ATPase. Biochim. biophys. Acta974 (1989) 156–162.

    PubMed  Google Scholar 

  54. Harris, D. A., Rosing, J., Van de Stadt, R. J. and Slater, E. C., Tight binding of adenine nucleotides of beef heart mitochondrial ATPase. Biochim. biophys. Acta314 (1973) 149–153.

    PubMed  Google Scholar 

  55. Hayashi, S., and Oosawa, F., A rotary model of F1-F0 ATPase based on a loose coupling mechanism. Proc. Jap. Acad.60 (1984) 161–164.

    Google Scholar 

  56. Higuti, T., Negama, T., Takigawa, M., Uchida, J., Yamane, T., Asai, T., Tani, I., Oeda, K., Shimizu, M., Nakamura, K., and Ohkawa, H., A hydrophobic protein, Chargerin II, purified from rat liver mitochondria is encoded in the unidentified reading frame A6L of mitochondrial DNA. J. biol. Chem.263 (1988) 6772–6776.

    PubMed  Google Scholar 

  57. Hollemans, M., Runswick, M. J., Fearnley, I. M., and Walker, J. E., The sites of labeling of the β-subunit of bovine mitochondrial F1-ATPase with 8-azido-ATP. J. biol. Chem.258 (1983) 9307–9313.

    PubMed  Google Scholar 

  58. Hoppe, J., Friedl, P., Schairer, H. U., Sebald, W., Von Meyenburg, K., and Jorgensen, B. B., The topology of the proton translocating F0 component of the ATP synthase fromE. coli K12: studies with proteases. EMBO J.2 (1983) 105–110.

    PubMed  Google Scholar 

  59. Ida, K., Noumi, T., Maeda, M., Fukui, T., and Futai, M., Catalytic site of F1-ATPase ofEscherichia coli. Lys-155 and Lys-201 of the β subunit are located near the γ-phosphate group of ATP in the presence of Mg2+. J. biol. Chem.266 (1991) 5424–5429.

    PubMed  Google Scholar 

  60. Issartel, J.-P. and Vignais, P. V., Evidence for a nucleotide binding site on the isolated β subunit fromEscherichia coli F1-ATPase. Interaction between nucleotide and aurovertin D binding sites. Biochemistry23 (1984) 6591–6595.

    PubMed  Google Scholar 

  61. Issartel, J.-P., Lunardi, J., and Vignais, P. V., Characterization of exchangeable and non exchangeable bound adenine nucleotides in F1-ATPase fromEscherichia coli. J. biol. Chem.261 (1986) 895–901.

    PubMed  Google Scholar 

  62. Issartel, J.-P., Favre-Bulle, O., Lunardi, J., and Vignais, P. V., Is pyrophosphate an analog of adenosine diphosphate for beef heart mitochondrial F1-ATPase. J. biol. Chem.262 (1987) 13538–13544.

    PubMed  Google Scholar 

  63. Issartel, J.-P., Dupuis, A., Lunardi, J., and Vignais, P. V., Fluoroaluminum and fluoroberyllium nucleoside disphosphate complexes are probes of the enzymatic mechanism of the mitochondrial F1-ATPase. Biochemistry30 (1991) 4726–4733.

    PubMed  Google Scholar 

  64. Iwamoto, A., Omote, H., Hanada, H., Tomioka, N., Itai, A., Maeda, M., and Futai, M., Mutations in Ser 174 and the glycine-rich sequence (Gly 149, Gly 150, and Thr 156) in the β subunit ofEscherichia coli H+-ATPase. J. biol. Chem.266 (1991) 16350–16355.

    PubMed  Google Scholar 

  65. Jackson, P. J., and Harris, D. A., Binding of mitochondrial ATPase from ox heart to its naturally occurring inhibitor protein: Localization by antibody binding. Biosci. Rep.3 (1983) 921–926.

    PubMed  Google Scholar 

  66. Kasahara, M., and Penefsky, H. S., High affinity binding of monovalent Pi by beef heart mitochondrial adenosine triphosphosphatase. J. biol. Chem.253 (1978) 4180–4187.

    PubMed  Google Scholar 

  67. Khananshvili, D., and Gromet-Elhanan, Z., Characterization of an inorganic phosphate binding site on the isolated, reconstitutively active β subunit of F0-F1 ATP synthase. Biochemistry24 (1985) 2482–2487.

    Google Scholar 

  68. Kironde, F. A. S., and Cross, R. L., Adenine nucleotide-binding sites on beef heart F1-ATPase. Conditions that affect occupancy of catalytic and noncatalytic sites. J. biol. Chem.261 (1986) 12544–12549.

    PubMed  Google Scholar 

  69. Klein, G., Satre, M., Dianoux, A.-C., and Vignais, P. V., Radiolabeling of natural adenosine triphosphatase inhibitor with phenyl(14C) isothiocyanate and study of its interaction with mitochondrial adenosine triphosphatase. Localization of inhibitor binding sites and stoichiometry of binding. Biochemistry19 (1980) 2919–2925.

    PubMed  Google Scholar 

  70. Klein, G., Satre, M., Dianoux, A.-C., and Vignais, P. V., Photoaffinity labeling of mitochondrial adenosine triphosphatase by an azido derivative of the natural adenosine triphosphatase inhibitor. Biochemistry20 (1981) 1339–1344.

    PubMed  Google Scholar 

  71. Kozlov, I. A., and Vulfson, E. N., Tightly bound nucleotides affect phosphate binding to mitochondrial F1-ATPase. FEBS Lett.182 (1985) 425–428.

    PubMed  Google Scholar 

  72. Laikind, P. K., Hill, F. C., and Allison, W. S., The use of (3H)aniline to identify the essential carboxyl group in the bovine mitochondrial F1-ATPase that reacts with 1-(Ethoxycarbonyl)-2-ethoxy-1,2-dihydroquinoline. Archs Biochem. Biophys.240 (1985) 904–920.

    Google Scholar 

  73. Lauquin, G., Pougeois, R., and Vignais, P. V., 4-azido-2-nitrophenyl phosphate, a new photoaffinity derivative of inorganic phosphate. Study of its interaction with the inorganic phosphate binding site of beef heart mitochondrial adenosine triphosphatase. Biochemistry19 (1980) 4620–4626.

    PubMed  Google Scholar 

  74. Lee, R. S.-F., Pagan, J., Satre, M., Vignais, P. V., and Senior, A. E., Identification of a mutation inEscherichia coli F1-ATPase β-subunit conferring resistance to aurovertin. FEBS Lett.253 (1989) 269–272.

    PubMed  Google Scholar 

  75. Lee, R. S.-F., Pagan, J., Wilke-Mounts S., Senior, A. E., Characterization ofEscherichia coli ATP synthase β-subunit mutations using a chromosomal deletion strain. Biochemistry30 (1991) 6842–6847.

    PubMed  Google Scholar 

  76. Lightowlers, R. N., Howitt, S. M., Hatch, L., Gibson, F., and Cox, G., The proton pore in theEscherichia coli F0-F1-ATPase: substitution of glutamate by glutamine at position 219 of the α-subunit prevents F0-mediated proton permeability. Biochim. biophys. Acta933 (1988) 241–248.

    PubMed  Google Scholar 

  77. Lippe, G., Sorgato, M. C., and Harris D. A., Kinetics of the release of the mitochondrial inhibitor protein. Correlation with synthesis and hydrolysis of ATP. BBA933 (1988) 1–11.

    PubMed  Google Scholar 

  78. Lötscher, H.-R., de Jong, C., and Capaldi, R. A., Inhibition of the adenosine triphosphatase activity ofEscherichia coliF1 by the water-soluble carbodiimide 1-ethyl-3-(3-(dimethylamino)propyl)-carbodiimide is due to modification of several carboxyls in the β subunit. Biochemistry23 (1984), 4134–4140.

    PubMed  Google Scholar 

  79. Lübben, M., Lücken, U., Weber, J. and Schäfer, G., Azidonaphthoyl-ADP: a specific photolabel for the high-affinity nucleotide-binding sites of F1-ATPase. Eur. J. Biochem.143 (1984) 483–490.

    PubMed  Google Scholar 

  80. Lunardi, J., and Vignais, P. V., Studies of the nucleotide-binding sites on the mitochondrial F1-ATPase through the use of a photoactivable derivative of adenylyl imidodiphosphate. Biochim. biophys. Acta682 (1982) 124–134.

    PubMed  Google Scholar 

  81. Lunardi, J., Dupuis, A., Garin, J., Issartel, J.-P., Michel, L., Chabre, M. and Vignais, P. V., Inhibition of H+-transporting ATPase by formation of a tight nucleotide diphosphate-fluoroaluminate complex at the catalytic site.Proc. natl Acad. Sci.85 (1988) 8958–8962.

    PubMed  Google Scholar 

  82. Lünsdorf, H., Ehrig, K., Friedl, P., and Schairer, H. U., Use of monoclonal antibodies in immuno-electron microscopy for the determination of subunit stoichiometry in oligomeric enzymes. There are three α-subunits in the F1-ATPase ofEscherichia coli. J. molec. Biol.173 (1984) 131–136.

    PubMed  Google Scholar 

  83. Matsuno-Yagi, A., Yagi, T., and Hatefi, Y., Studies on the mechanism of oxidative phosphorylation: Effects of specific F0 modifiers on ligand-induced conformation changes of F1. Proc. natl Acad. Sci.82 (1985) 7550–7554.

    PubMed  Google Scholar 

  84. Milgrom, Y. M., and Murataliev, M. B., Characterization of the nucleotide tight-binding sites of the isolated mitochondrial F1-ATPase. FEBS Lett.219 (1987) 156–160.

    PubMed  Google Scholar 

  85. Mitchell, P., Coupling of phosphorylation to electron and hydrogen transfer by a chemiosmotic type of mechanism. Nature191 (1961) 144–148.

    PubMed  Google Scholar 

  86. Mitchell, P., A chemiosmotic molecular mechanism for protontranslocating adenosine triphosphatases. FEBS Lett.43 (1974) 189–194.

    PubMed  Google Scholar 

  87. Mitchell, P., Molecular mechanics of protonmotive F0-F1 ATPases. Rolling well and turnstile hypothesis. FEBS Lett.182 (1985) 1–7.

    PubMed  Google Scholar 

  88. Miwa, K., and Yoshida, M., and α3β3 complex, the catalytic core of F1-ATPase. Proc. natl. Acad. Sci.86 (1989) 6484–6487.

    PubMed  Google Scholar 

  89. Miwa, K., Ohtsubo, M., Denda, K., Hisabori, T., Data, T., and Yoshida, M., Reconstituted F1-ATPase complexes containing one impaired β subunit are ATPase-active. J. Biochem.106 (1989) 679–683.

    PubMed  Google Scholar 

  90. Mueller, D. M., A mutation altering the kinetic responses of the yeast mitochondrial F1-ATPase. J. biol. Chem.264 (1989) 16552–16556.

    PubMed  Google Scholar 

  91. Nagley, P., Eukaryote membrane genetics: the F0 sector of mitochondrial ATP synthase. Trends Gen.4 (1988) 46–52.

    Google Scholar 

  92. Noumi, T., Taniai, M., Kanazawa, H., and Futai, M., Replacement of arginine 246 by histidine in the β subunit ofEscherichia coli H+-ATPase resulted in loss of multi-site ATPase activity. J. biol. Chem.261 (1986) 9196–9201.

    PubMed  Google Scholar 

  93. Odaka, M., Kobayashi, H., Muneyuki, E., and Yoshida, M., Aromatic rings of tyrosine residues at adenine nucleotide binding sites of the β subunits of F1-ATPase are not necessary for ATPase activity. Biochem. biophys. Res. Commun.168 (1990) 372–378.

    PubMed  Google Scholar 

  94. Ohta, S., Tsuboi, M., Oshima, T., Yoshida, M., and Kagawa, Y., Nucleotide binding to isolated alpha and beta subunits of proton translocating adenosine triphosphatase studied with circular dichroism. J. Biochem.87 (1980) 1609–1617.

    PubMed  Google Scholar 

  95. Pagan, J., and Senior, A. E., Tight ATP and ADP binding in the noncatalytic sites ofEscherichia coli F1-ATPase is not affected by mutation of bulky residues in the “glycine-rich loop”. FEBS Lett.273 (1990) 147–149.

    PubMed  Google Scholar 

  96. Paradies, H. H., Effect of ATP on the translation diffusion coefficient of the α-subunit ofEscherichia coli F1-ATPase. FEBS Lett.120 (1980) 289–292.

    PubMed  Google Scholar 

  97. Parsonage, D., Wilke-Mounts, S., and Senior, A. E., Directed mutagenesis of the β-subunit of F1-ATPase fromEscherichia coli. J. biol. Chem.262 (1987) 8022–8026.

    PubMed  Google Scholar 

  98. Parsonage, D., Wilke-Mounts, S., and Senior, A. E., Directed mutagenesis of the dicyclohexylcarbodiimide-reactive carboxyl residues in β-subunit of F1-ATPase ofEscherichia coli. Archs Biochem. Biophys.261 (1988) 222–225.

    Google Scholar 

  99. Penefsky, H. S., Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase. J. biol. Chem.252 (1977) 2891–2899.

    PubMed  Google Scholar 

  100. Penefsky, H. S., Mechanism of inhibition of mitochondrial adenosine triphosphatase by dicyclohexylcarbodiimide and oligomycin: Relationship to ATP synthesis.Proc. natl Acad. Sci.82 (1985) 1589–1593.

    PubMed  Google Scholar 

  101. Penefsky, H. S., Molecular mechanism of ATP synthesis in oxidative phosphorylation. Biochem. Soc. Trans.15 (1987) 97–99.

    PubMed  Google Scholar 

  102. Penefsky, H. S., Rate of chase-promoted hydrolysis of ATP in the high affinity catalytic site of beef heart mitochondrial ATPase. J. biol. Chem.263 (1988) 6020–6022.

    PubMed  Google Scholar 

  103. Penefsky, H. S., and Cross, R. L., Structure and mechanism of F0-F1-type ATP synthases and ATPase. Advances Enzymol.64 (1991) 173–214.

    Google Scholar 

  104. Perlin, D. S., Latchney, L. R., Wise, J. G., and Senior, A. E., Specificity of the proton adenosine triphosphatase ofEscherichia coli for adenine, guanine, and inosine nucleotides in catalysis and binding. Biochemistry23 (1984) 4998–5003.

    PubMed  Google Scholar 

  105. Perlin, D. S., Latchney, L. R. and Senior, A. E., Inhibition ofEscherichia coli H+-ATPase by venturicidin, oligomycin and ossamycin. Biochim. biophys. Acta807 (1985) 238–244.

    PubMed  Google Scholar 

  106. Pullman, M. E., and Monroy, G. C., A naturally occurring inhibitor of mitochondrial adenosine triphosphatase. J. biol. Chem.238 (1963) 3762–3769.

    PubMed  Google Scholar 

  107. Pullman, M. E., Penefsky, H. S., Datta, A., and Racker, E., Partial resolution of the enzymes catalying oxidative phosphorylation. I. Purification and properties of soluble, dinitrophenol-stimulated adenosine triphosphatase. J. biol. Chem.235 (1960) 3322–3329.

    PubMed  Google Scholar 

  108. Rao, R., and Senior, A. E., The properties of hybrid F1-ATPase enzymes suggest that a cyclical catalytic mechanism involving three catalytic sites occurs. J. biol. Chem.262 (1987) 17450–17454.

    PubMed  Google Scholar 

  109. Rao, R., Cunningham, D., Cross, R. L., and Senior, A. E., Pyridoxal 5′-diphospho-5′ adenosine binds at a single site on isolated α-subunit fromEscherichia coli F1-ATPase and specifically reacts with lysine 201. J. biol. Chem.263 (1988) 5640–5645.

    PubMed  Google Scholar 

  110. Rögner, M., Gröber, P., Lücken, U., Tiedge, H., Weber, J., and Schäfer, G., Subunit-subuni: interactions in TF1 as revealed by ligand binding to isolated and integrated α and β subunits. Biochim. biophys. Acta849 (1986) 121–130.

    Google Scholar 

  111. Roveri, O. A., and Calcaterra, N. B., Steady-state kinetics of F1-ATPase. Mechanism of anion activation. FEBS Lett.192 (1985) 123–127.

    PubMed  Google Scholar 

  112. Sakamoto, J., and Tonomura, Y., Synthesis of enzyme-bound ATP by mitochondrial soluble F1-ATPase in the presence of dimethylsufoxide. J. Biochem.93 (1983) 1601–1614.

    PubMed  Google Scholar 

  113. Satre, M., Klein, G., and Vignais, P. V., Structure of beef heart mitochondrial F1-ATPase. Arrangement of subunits as disclosed by cross-linking reagents and selective labeling by radioactive ligands. Biochim. biophys. Acta453 (1976) 111–120.

    PubMed  Google Scholar 

  114. Satre, M., Klein, G., and Vignais, P. V., Isolation ofEscherichia coli mutants with an adenosine triphosphatase insensitive to aurovertin. J. Bact.134 (1978) 17–23.

    PubMed  Google Scholar 

  115. Satre, M., Bof, M., and Vignais, P. V., Interaction ofEscherichia coli adenosine triphosphatase with aurovertin and citreovirdin: inhibition and fluorescence studies. J. Bact.142 (1980) 768–776.

    PubMed  Google Scholar 

  116. Schäfer, H.-J., Mainka, L., and Rathgeber, G., Photoaffinity crosslinking of oligomycin-sensitive ATPase from beef heart mitochondria by 3′-arylazido-8-azido ATP. Biochem. biophys. Res. Commun.111 (1983) 732–739.

    PubMed  Google Scholar 

  117. Schneider, E., and Altendorf, K., The proton-translocating portion (F0) of theE. coli ATP synthase. Trends Biochem. Sci.9 (1984) 51–53.

    Google Scholar 

  118. Sebald, W., and Wachter, E., Amino acid sequence of the putative protonophore of the energy-transducing ATPase complex, in: Energy Conservation in Biological Membranes, pp. 228–236. Eds G. Schäfer and M. Klingenberg, Springer-Verlag, Berlin 1978.

    Google Scholar 

  119. Senda, M., Kanazawa, H., Tsuchiya, T., and Futai, M., Conformational change of the α subunit ofEscherichia coli F1 ATPase: ATP changes the trypsin sensitivity of the subunit. Archs Biochem. Biophys.220 (1983) 398–404.

    Google Scholar 

  120. Senior, A. E., ATP synthesis by oxidative phosphorylation. Physiol. Rev.68 (1988) 177–231.

    PubMed  Google Scholar 

  121. Tamura, J. K., and Wang, J. H., Changes in chemical properties of mitochondrial adenosine triphosphatase upon removal of tightly bound nucleotides. Biochemistry22 (1983) 1947–1954.

    PubMed  Google Scholar 

  122. Tiedge, H., and Schäfer, G., Symmetry in F1-type ATPases. Biochim. biophys. Acta977 (1989) 1–9.

    PubMed  Google Scholar 

  123. Tiedge, H., Schäfer, G., and Mayer, F., An electron microscopic approach to the quaternary structure of mitochondrial F1-ATPase. Eur. J. Biochem.132 (1983) 37–45.

    PubMed  Google Scholar 

  124. Tsuprun, V. L., Mesyanzhinova, I. V., Kozlov, I. A., and Orlova, E. V., Electron microscopy of beef heart mitochondrial F1-ATPase. FEBS Lett.167 (1984) 285–290.

    PubMed  Google Scholar 

  125. Velours, J., Esparza, M., Hoppe, J., Sebald, W., and Guerin, B., Amino acid sequence of a new mitochondrially synthesized proteolipid of the ATP synthase ofSaccharomyces cerevisiae. EMBO J.3 (1984) 207–212.

    PubMed  Google Scholar 

  126. Verburg, J. G., and Allison, W. S., Tyrosine α244 is derivatized when the bovine heart mitochondrial F1-ATPase is inactivated with 5′-pfluorosulfonylbenzoylethenoadenosine. J. biol. Chem.265 (1990) 8065–8074.

    PubMed  Google Scholar 

  127. Vignais, P. V., and Lunardi, J., Chemical probes of the mitochondrial ATP synthesis and translocation. A. Rev. Biochem.54 (1985) 977–1014.

    Google Scholar 

  128. Vogel, P. D., and Cross, R. L., Adenine nucleotide-binding sites on mitochondrial F1-ATPase. Evidence for an adenylate kinase-like orientation of catalytic and noncatalytic sites. J. biol. Chem.266 (1991) 6101–6105.

    PubMed  Google Scholar 

  129. Von Meyenburg, K., Jorgensen, B. B., Nierlsen, J., Hausen, F. G., and Michelson, O., The membrane-bound ATP synthase ofEscherichia coli: a review of structural and functional analysis of theatp operon. Tokai exp. clin. Med.7 (1982) 23–31.

    Google Scholar 

  130. Wagner, R., Ponse, G., and Strotmann, H., Binding of 2′(3′)-O-(2,4,6-trinitrophenyl)-adenosine-5′-diphosphate opens the pathway for protons through the chloroplast ATPase complex. Eur. J. Biochem.161 (1986) 205–209.

    PubMed  Google Scholar 

  131. Walker, J. E., Saraste, M., and Gay, N. J., Theunc operon. Nucleotide sequence, regulation and structure of ATP-synthase. Biochim. biophys. Acta768 (1984) 164–200.

    PubMed  Google Scholar 

  132. Walker, J. E., Lutter, R., Dupuis, A., and Runswick, M. J., Identification of the subunits of F1-F0-ATPase from bovine heart mitochondria. Biochemistry30 (1991) 5369–5378.

    PubMed  Google Scholar 

  133. Wang, J. H., Functionally distinct β subunits in F1-adenosine triphosphatase. J. biol. Chem.260 (1985) 1374–1377.

    PubMed  Google Scholar 

  134. Webb, M. R., Grubmeyer, C., Penefsky, H. S., and Trentham, D. R., The stereochemical course of phosphoric residue transfer catalyzed by beef heart mitochondrial ATPase. J. biol. Chem.255 (1980) 11637–11639.

    PubMed  Google Scholar 

  135. Weber, J., Lücken, U., and Schäfer, G., Total number and differentiation of nucleotide binding sites on mitochondrial F1-ATPase. An approach by photolabeling and equilibrium binding studies. Eur. J. Biochem.148 (1985) 41–47.

    PubMed  Google Scholar 

  136. Weber, J., Schmitt, S., Grell, E., and Schäfer, G., Differentiation of the nucleotide-binding sites on nucleotide-depleted mitochondrial F1-ATPase by means of a fluorescent ADP analogue. J. biol. Chem.265 (1990) 10884–10892.

    PubMed  Google Scholar 

  137. Williams, N., Hullihen, J. M., and Pedersen, P. L., The proton adenosine triphosphatase complex of rat liver mitochondria. Temperature-dependent dissociation-reassociation of the F1-ATPase subunits. Biochemistry23 (1984) 780–785.

    PubMed  Google Scholar 

  138. Wise, J. G., Site-directed mutagenesis of the conserved β subunit tyrosine 331 ofEscherichia coli ATP synthase yields catalytically active enzymes. J. biol. Chem.265 (1990) 10403–10409.

    PubMed  Google Scholar 

  139. Wise, J. G., and Senior, A. E., Catalytic properties of theEscherichia coli proton adenosine triphosphatase: evidence that nucleotide bound at noncatalytic sites is not involved in regulation of oxidative phosphorylation. Biochemistry24 (1985) 6949–6954.

    PubMed  Google Scholar 

  140. Wong, S.-Y., Matsuno-Yagi, A., and Hatefi, Y., Kinetics of ATP hydrolysis by F1-ATPase and the effects of anion activation, removal of tightly bound nucleotides, and partial inhibition of the ATPase by covalent modification. Biochemistry23 (1984) 5004–5009.

    PubMed  Google Scholar 

  141. Xue, Z., and Boyer, P. D., Modulation of the GTPase activity of the chloroplast F1-ATPase by ATP binding at non-catalytic sites. Eur. J. Biochem.179 (1989) 677–681.

    PubMed  Google Scholar 

  142. Yoshida, M., The synthesis of enzyme-bound ATP by the F1-ATPase from the thermophilic bacterium PS3 in 50% dimethyl sulfoxide. Biochem. biophys. Res. Commun.114 (1983) 907–912.

    PubMed  Google Scholar 

  143. Yoshida, M., and Allison, W. S., Characterization of the catalytic and noncatalytic ADP binding sites of the F1-ATPase from the thermophilic bacterium PS3. J. biol. Chem.261 (1986) 5714–5721.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biochimie (URA 1130 du CNRS), Département de Biologie Moléculaire et Structurale, Centre d'Etudes Nucléaires 85X, F-38041, Grenoble cedex, (France)

    J. P. Issartel, A. Dupuis, J. Garin, J. Lunardi, L. Michel & P. V. Vignais

Authors
  1. J. P. Issartel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Dupuis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Garin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Lunardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. V. Vignais
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Issartel, J.P., Dupuis, A., Garin, J. et al. The ATP synthase (F0−F1) complex in oxidative phosphorylation. Experientia 48, 351–362 (1992). https://doi.org/10.1007/BF01923429

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01923429

Key words

Search

Navigation