Advertisement

Biochemistry (Moscow)

, Volume 83, Issue 10, pp 1141–1160 | Cite as

ADP-Inhibition of H+-FOF1-ATP Synthase

  • A. S. Lapashina
  • B. A. FenioukEmail author
Review

Abstract

H+-FOF1-ATP synthase (F-ATPase, F-type ATPase, FOF1 complex) catalyzes ATP synthesis from ADP and inorganic phosphate in eubacteria, mitochondria, chloroplasts, and some archaea. ATP synthesis is powered by the transmembrane proton transport driven by the proton motive force (PMF) generated by the respiratory or photosynthetic electron transport chains. When the PMF is decreased or absent, ATP synthase catalyzes the reverse reaction, working as an ATP-dependent proton pump. The ATPase activity of the enzyme is regulated by several mechanisms, of which the most conserved is the non-competitive inhibition by the MgADP complex (ADP-inhibition). When ADP binds to the catalytic site without phosphate, the enzyme may undergo conformational changes that lock bound ADP, resulting in enzyme inactivation. PMF can induce release of inhibitory ADP and reactivate ATP synthase; the threshold PMF value required for enzyme reactivation might exceed the PMF for ATP synthesis. Moreover, membrane energization increases the catalytic site affinity to phosphate, thereby reducing the probability of ADP binding without phosphate and preventing enzyme transition to the ADP-inhibited state. Besides phosphate, oxyanions (e.g., sulfite and bicarbonate), alcohols, lauryldimethylamine oxide, and a number of other detergents can weaken ADP-inhibition and increase ATPase activity of the enzyme. In this paper, we review the data on ADP-inhibition of ATP synthases from different organisms and discuss the in vivo role of this phenomenon and its relationship with other regulatory mechanisms, such as ATPase activity inhibition by subunit ε and nucleotide binding in the noncatalytic sites of the enzyme. It should be noted that in Escherichia coli enzyme, ADP-inhibition is relatively weak and rather enhanced than prevented by phosphate.

Keywords

ATP synthase F-ATPase ADP-inhibition regulation LDAO sulfite bioenergetics FOF1 proton-motive force phosphate ATP hydrolysis 

Abbreviations

LDAO

lauryldimethylamine oxide

PMF

proton-motive force

SBP

subbacterial inverted membrane particles

SMP

submitochondrial inverted membrane particles

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Gruber, G., Manimekalai, M. S. S., Mayer, F., and Muller, V. (2014) ATP synthases from archaea: the beauty of a molecular motor, Biochim. Biophys. Acta, 1837, 940–952.PubMedCrossRefGoogle Scholar
  2. 2.
    Mulkidjanian, A. Y., Makarova, K. S., Galperin, M. Y., and Koonin, E. V. (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases, Nat. Rev. Microbiol., 5, 892–899.PubMedCrossRefGoogle Scholar
  3. 3.
    Sumi, M., Yohda, M., Koga, Y., and Yoshida, M. (1997) FOF1-ATPase genes from an archaebacterium, Methanosarcina barkeri, Biochem. Biophys. Res. Commun., 241, 427–433.PubMedCrossRefGoogle Scholar
  4. 4.
    Foster, D. L., and Fillingame, R. H. (1982) Stoichiometry of subunits in the H+-ATPase complex of Escherichia coli, J. Biol. Chem., 257, 2009–2015.PubMedGoogle Scholar
  5. 5.
    Sobti, M., Smits, C., Wong, A. S., Ishmukhametov, R., Stock, D., Sandin, S., and Stewart, A. G. (2016) Cryo-EM structures of the autoinhibited E. coli ATP synthase in three rotational states, Elife, 5, e21598.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Cozens, A. L., and Walker, J. E. (1987) The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301, J. Mol. Biol., 194, 359–383.PubMedCrossRefGoogle Scholar
  7. 7.
    Borghese, R., Turina, P., Lambertini, L., and Melandri, B. A. (1998) The atpIBEXF operon coding for the F0 sector of the ATP synthase from the purple nonsulfur photosynthetic bac-terium Rhodobacter capsulatus, Arch. Microbiol., 170, 385–388.PubMedCrossRefGoogle Scholar
  8. 8.
    Hotra, A., Suter, M., Biukovic, G., Ragunathan, P., Kundu, S., Dick, T., and Gruber, G. (2016) Deletion of a unique loop in the mycobacterial F-ATP synthase γ subunit sheds light on its inhibitory role in ATP hydrolysis-driven H(+) pumping, FEBS J., 283, 1947–1961.PubMedCrossRefGoogle Scholar
  9. 9.
    Liu, S., Charlesworth, T. J., Bason, J. V., Montgomery, M. G., Harbour, M. E., Fearnley, I. M., and Walker, J. E. (2015) The purification and characterization of ATP synthase complexes from the mitochondria of four fungal species, Biochem. J., 468, 167–175.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Stewart, A. G., Laming, E. M., Sobti, M., and Stock, D. (2014) Rotary ATPases-dynamic molecular machines, Curr. Opin. Struct. Biol., 25, 40–48.PubMedCrossRefGoogle Scholar
  11. 11.
    Watanabe, R. (2013) Rotary catalysis of FoF1-ATP syn-thase, Biophysics, 9, 51–56.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Junge, W., and Nelson, N. (2015) ATP synthase, Annu. Rev. Biochem., 84, 631–657.PubMedCrossRefGoogle Scholar
  13. 13.
    Slooten, L., and Vandenbranden, S. (1989) ATP-synthesis by proteoliposomes incorporating Rhodospirillum rubrum FOF1 as measured with firefly luciferase: dependence on Δpsi and ΔpH, Biochim. Biophys. Acta, 976, 150–160.PubMedCrossRefGoogle Scholar
  14. 14.
    Etzold, C., Deckers-Hebestreit, G., and Altendorf, K. (1997) Turnover number of Escherichia coli FOF1 ATP syn-thase for ATP synthesis in membrane vesicles, Eur. J. Biochem., 243, 336–343.PubMedCrossRefGoogle Scholar
  15. 15.
    Junesch, U., and Graber, P. (1987) Influence of the redox state and the activation of the chloroplast ATP synthase on proton-transport-coupled ATP synthesis/hydrolysis, Biochim. Biophys. Acta, 893, 275–288.CrossRefGoogle Scholar
  16. 16.
    Matsuno-Yagi, A., and Hatefi, Y. (1988) Estimation of the turnover number of bovine heart FOF1 complexes for ATP synthesis, Biochemistry, 27, 335–340.PubMedCrossRefGoogle Scholar
  17. 17.
    Mueller, D. M. (1988) Arginine 328 of the beta-subunit of the mitochondrial ATPase in yeast is essential for protein stability, J. Biol. Chem., 263, 5634–5639.PubMedGoogle Scholar
  18. 18.
    Dunn, S. D., Tozer, R. G., and Zadorozny, V. D. (1990) Activation of Escherichia coli F1-ATPase by lauryldimethylamine oxide and ethylene glycol: relationship of ATPase activity to the interaction of the epsilon and beta subunits, Biochemistry, 29, 4335–4340.PubMedCrossRefGoogle Scholar
  19. 19.
    Sekiya, M., Nakamoto, R. K., Al-Shawi, M. K., Nakanishi-Matsui, M., and Futai, M. (2009) Temperature dependence of single molecule rotation of the Escherichia coli ATP synthase F1 sector reveals the importance of γ-β subunit interactions in the catalytic dwell, J. Biol. Chem., 284, 22401–22410.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Ishmukhametov, R. R., Galkin, M. A., and Vik, S. B. (2005) Ultrafast purification and reconstitution of His-tagged cysteine-less Escherichia coli F1Fo ATP synthase, Biochim. Biophys. Acta, 1706, 110–116.PubMedCrossRefGoogle Scholar
  21. 21.
    Suzuki, T., Tanaka, K., Wakabayashi, C., Saita, E.-I., and Yoshida, M. (2014) Chemomechanical coupling of human mitochondrial F1-ATPase motor, Nat. Chem. Biol., 10, 930–936.PubMedCrossRefGoogle Scholar
  22. 22.
    Penin, F., Deleage, G., Godinot, C., and Gautheron, D. C. (1986) Efficient reconstitution of mitochondrial energy-transfer reactions from depleted membranes and F1-ATPase as a function of the amount of bound oligomycin sensitivity-conferring protein (OSCP), Biochim. Biophys. Acta, 852, 55–67.PubMedCrossRefGoogle Scholar
  23. 23.
    Munoz, E., Salton, M. R. J., Ng, M. H., and Schor, M. T. (1969) Membrane adenosine triphosphatase of Micrococcus lysodeikticus: purification, properties of the “soluble” enzyme and properties of the membrane-bound enzyme, Eur. J. Biochem., 7, 490–501.PubMedCrossRefGoogle Scholar
  24. 24.
    Gonzales-Siles, L., Karlsson, R., Kenny, D., Karlsson, A., and Sjoling, A. (2017) Proteomic analysis of enterotoxi-genic Escherichia coli (ETEC) in neutral and alkaline con-ditions, BMC Microbiol., 17, 11.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Ruhle, T., and Leister, D. (2015) Assembly of F1F0-ATP synthases, Biochim. Biophys. Acta, 1847, 849–860.PubMedCrossRefGoogle Scholar
  26. 26.
    Grover, G. J., Atwal, K. S., Sleph, P. G., Wang, F.-L., Monshizadegan, H., Monticello, T., and Green, D. W. (2004) Excessive ATP hydrolysis in ischemic myocardium by mitochondrial F1F0-ATPase: effect of selective pharma-cological inhibition of mitochondrial ATPase hydrolase activity, Am. J. Physiol. Heart Circ. Physiol., 287, H1747–H1755.PubMedCrossRefGoogle Scholar
  27. 27.
    Rouslin, W., Erickson, J. L., and Solaro, R. J. (1986) Effects of oligomycin and acidosis on rates of ATP depletion in ischemic heart muscle, Am. J. Physiol., 250, H503–H508.PubMedGoogle Scholar
  28. 28.
    Jennings, R. B., Reimer, K. A., and Steenbergen, C. (1991) Effect of inhibition of the mitochondrial ATPase on net myocardial ATP in total ischemia, J. Mol. Cell. Cardiol., 23, 1383–1395.PubMedCrossRefGoogle Scholar
  29. 29.
    Hensel, M., Deckers-Hebestreit, G., and Altendorf, K. (1991) Purification and characterization of the F1 portion of the ATP synthase (F1Fo) of Streptomyces lividans, Eur. J. Biochem., 202, 1313–1319.PubMedCrossRefGoogle Scholar
  30. 30.
    Lynn, W. S., and Straub, K. D. (1969) ADP kinase and ATPase in chloroplasts, Proc. Natl. Acad. Sci. USA, 63, 540–547.PubMedCrossRefGoogle Scholar
  31. 31.
    Bakels, R. H. A., van Walraven, H. S., van Wielink, J. E., van der Zwetdegraaff, I., Krenn, B. E., Krab, K., Berden, J. A., and Kraayenhof, R. (1994) The effect of sulfite on the ATP hydrolysis and synthesis activity of membrane-bound H+-ATP synthase from various species, Biochem. Biophys. Res. Commun., 201, 487–492.PubMedCrossRefGoogle Scholar
  32. 32.
    Pacheco-Moises, F., Minauro-Sanmiguel, F., Bravo, C., and Garcia, J. J. (2002) Sulfite inhibits the F1F0-ATP syn-thase and activates the F1F0-ATPase of Paracoccus denitrificans, J. Bioenerg. Biomembr., 34, 269–278.PubMedCrossRefGoogle Scholar
  33. 33.
    Keis, S., Stocker, A., Dimroth, P., and Cook, G. M. (2006) Inhibition of ATP hydrolysis by thermoalkaliphilic F1Fo-ATP synthase is controlled by the C-terminus of the epsilon subunit, J. Bacteriol., 188, 3796–3804.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Du, Z. Y., and Boyer, P. D. (1990) On the mechanism of sulfite activation of chloroplast thylakoid ATPase and the relation of ADP tightly bound at a catalytic site to the binding change mechanism, Biochemistry, 29, 402–407.PubMedCrossRefGoogle Scholar
  35. 35.
    Larson, E. M., and Jagendorf, A. T. (1989) Sulfite stimula-tion of chloroplast coupling factor ATPase, Biochim. Biophys. Acta, 973, 67–77.CrossRefGoogle Scholar
  36. 36.
    Avron, M. (1962) Light-dependent adenosine triphos-phatase in chloroplasts, J. Biol. Chem., 237, 2011–2017.PubMedGoogle Scholar
  37. 37.
    Yu, F., and McCarty, R. E. (1985) Detergent activation of the ATPase activity of chloroplast coupling factor 1, Arch. Biochem. Biophys., 238, 61–68.PubMedCrossRefGoogle Scholar
  38. 38.
    Farron, F., and Racker, E. (1970) Mechanism of the con-version of coupling factor 1 from chloroplasts to an active ATPase, Biochemistry, 9, 3829–3836.PubMedCrossRefGoogle Scholar
  39. 39.
    Mal’yan, A. N. (1981) Chloroplasts ATPase (CF1): allosteric regulation by ADP and Mg2+ ions, Photosynthetica, 15, 474–483.Google Scholar
  40. 40.
    Ren, H. M., and Allison, W. S. (1997) Photoinactivation of the F1-ATPase from spinach chloroplasts by dequalinium is accompanied by derivatization of methionine beta183, J. Biol. Chem., 272, 32294–32300.PubMedCrossRefGoogle Scholar
  41. 41.
    Ebel, R. E., and Lardy, H. A. (1975) Stimulation of rat liver mitochondrial adenosine triphosphatase by anions, J. Biol. Chem., 250, 191–196.PubMedGoogle Scholar
  42. 42.
    Vazquez-Laslop, N., and Dreyfus, G. (1986) Mitochondrial H+-ATPase activation by an amine oxide detergent, J. Biol. Chem., 261, 7807–7810.PubMedGoogle Scholar
  43. 43.
    Mueller, D. M. (1989) A mutation altering the kinetic responses of the yeast mitochondrial F1-ATPase, J. Biol. Chem., 264, 16552–16556.PubMedGoogle Scholar
  44. 44.
    Vasilyeva, E. A., Minkov, I. B., Fitin, A. F., and Vinogradov, A. D. (1982) Kinetic mechanism of mitochondrial adenosine triphosphatase. Inhibition by azide and activation by sulfite, Biochem. J., 202, 15–23.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Mitchell, P., and Moyle, J. (1971) Activation and inhibition of mitochondrial adenosine triphosphatase by various anions and other agents, J. Bioenerg., 2, 1–11.PubMedCrossRefGoogle Scholar
  46. 46.
    Feniouk, B. A., and Yoshida, M. (2008) Regulatory mech-anisms of proton-translocating F(O)F(1)-ATP synthase, Results Probl. Cell Differ., 45, 279–308.PubMedCrossRefGoogle Scholar
  47. 47.
    Pullman, M. E., and Monroy, G. C. (1963) A naturally occurring inhibitor of mitochondrial adenosine triphos-phatase, J. Biol. Chem., 238, 3762–3769.PubMedGoogle Scholar
  48. 48.
    Cabezon, E., Butler, P. J., Runswick, M. J., and Walker, J. E. (2000) Modulation of the oligomerization state of the bovine F1-ATPase inhibitor protein, IF1, by pH, J. Biol. Chem., 275, 25460–25464.PubMedCrossRefGoogle Scholar
  49. 49.
    Panchenko, M. V., and Vinogradov, A. D. (1985) Interaction between the mitochondrial ATP synthetase and ATPase inhibitor protein. Active/inactive slow pH-depend-ent transitions of the inhibitor protein, FEBS Lett., 184, 226–230.PubMedCrossRefGoogle Scholar
  50. 50.
    Rouslin, W., and Broge, C. W. (1989) Regulation of mito-chondrial matrix pH and adenosine 5′-triphosphatase activity during ischemia in slow heart-rate hearts. Role of Pi/H+ symport, J. Biol. Chem., 264, 15224–15229.PubMedGoogle Scholar
  51. 51.
    Garcia-Bermudez, J., and Cuezva, J. M. (2016) The ATPase inhibitory factor 1 (IF1): a master regulator of energy metabolism and of cell survival, Biochim. Biophys. Acta, 1857, 1167–1182.PubMedCrossRefGoogle Scholar
  52. 52.
    Campanella, M., Parker, N., Tan, C. H., Hall, A. M., and Duchen, M. R. (2009) IF(1): setting the pace of the F(1)F(o)-ATP synthase, Trends Biochem. Sci., 34, 343–350.PubMedCrossRefGoogle Scholar
  53. 53.
    Feniouk, B. A., Suzuki, T., and Yoshida, M. (2006) The role of subunit epsilon in the catalysis and regulation of FoF1-ATP synthase, Biochim. Biophys. Acta, 1757, 326–338.PubMedCrossRefGoogle Scholar
  54. 54.
    Suzuki, T., Murakami, T., Iino, R., Suzuki, J., Ono, S., Shirakihara, Y., and Yoshida, M. (2003) FOF1-ATPase/syn-thase is geared to the synthesis mode by conformational rearrangement of epsilon subunit in response to proton motive force and ADP/ATP balance, J. Biol. Chem., 278, 46840–46846.PubMedCrossRefGoogle Scholar
  55. 55.
    Feniouk, B. A., Kato-Yamada, Y., Yoshida, M., and Suzuki, T. (2010) Conformational transitions of subunit epsilon in ATP synthase from thermophilic Bacillus PS3, Biophys. J., 98, 434–442.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Tsunoda, S. P., Rodgers, A. J., Aggeler, R., Wilce, M. C., Yoshida, M., and Capaldi, R. A. (2001) Large conforma-tional changes of the epsilon subunit in the bacterial F1F0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme, Proc. Natl. Acad. Sci. USA, 98, 6560–6564.PubMedCrossRefGoogle Scholar
  57. 57.
    Nowak, K. F., and McCarty, R. E. (2004) Regulatory role of the C-terminus of the epsilon subunit from the chloroplast ATP synthase, Biochemistry, 43, 3273–3279.PubMedCrossRefGoogle Scholar
  58. 58.
    Kato-Yamada, Y., and Yoshida, M. (2003) Isolated epsilon subunit of thermophilic F1-ATPase binds ATP, J. Biol. Chem., 278, 36013–36016.PubMedCrossRefGoogle Scholar
  59. 59.
    Kato-Yamada, Y. (2005) Isolated epsilon subunit of Bacillus subtilis F1-ATPase binds ATP, FEBS Lett., 579, 6875–6878.PubMedCrossRefGoogle Scholar
  60. 60.
    Kato, S., Yoshida, M., and Kato-Yamada, Y. (2007) Role of the epsilon subunit of thermophilic F1-ATPase as a sensor for ATP, J. Biol. Chem., 282, 37618–37623.PubMedCrossRefGoogle Scholar
  61. 61.
    Nakanishi-Matsui, M., Sekiya, M., and Futai, M. (2016) ATP synthase from Escherichia coli: mechanism of rotational catalysis, and inhibition with the ε subunit and phy-topolyphenols, Biochim. Biophys. Acta, 1857, 129–140.PubMedCrossRefGoogle Scholar
  62. 62.
    Hisabori, T., Sunamura, E.-I., Kim, Y., and Konno, H. (2013) The chloroplast ATP synthase features the characteristic redox regulation machinery, Antioxid. Redox Signal., 19, 1846–1854.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Ort, D. R., and Oxborough, K. (1992) In situ regulation of chloroplast coupling factor activity, Annu. Rev. Plant Physiol. Plant Mol. Biol., 43, 269–291.CrossRefGoogle Scholar
  64. 64.
    Kramer, D. M., and Crofts, A. R. (1989) Activation of the chloroplast ATPase measured by the electrochromic change in leaves of intact plants, Biochim. Biophys. Acta, 976, 28–41.CrossRefGoogle Scholar
  65. 65.
    McKinney, D. W., Buchanan, B. B., and Wolosiuk, R. A. (1978) Activation of chloroplast ATPase by reduced thioredoxin, Phytochemistry, 17, 794–795.CrossRefGoogle Scholar
  66. 66.
    Dann, M. S., and McCarty, R. E. (1992) Characterization of the activation of membrane-bound and soluble CF1 by thioredoxin, Plant Physiol., 99, 153–160.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Kramer, D. M., Wise, R. R., Frederick, J. R., Alm, D. M., Hesketh, J. D., Ort, D. R., and Crofts, A. R. (1990) Regulation of coupling factor in field-grown sunflower: a redox model relating coupling factor activity to the activi-ties of other thioredoxin-dependent chloroplast enzymes, Photosynth. Res., 26, 213–222.PubMedCrossRefGoogle Scholar
  68. 68.
    Kohzuma, K., Froehlich, J. E., Davis, G. A., Temple, J. A., Minhas, D., Dhingra, A., Cruz, J. A., and Kramer, D. M. (2017) The role of light-dark regulation of the chloroplast ATP synthase, Front. Plant Sci., 8, 1248.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Gruber, G., Godovac-Zimmermann, J., and Nawroth, T. (1994) ATP synthesis and hydrolysis of the ATP-synthase from Micrococcus luteus regulated by an inhibitor subunit and membrane energization, Biochim. Biophys. Acta, 1186, 43–51.PubMedCrossRefGoogle Scholar
  70. 70.
    Morales-Rios, E., de la Rosa-Morales, F., Mendoza-Hernandez, G., Rodriguez-Zavala, J. S., Celis, H., Zarco-Zavala, M., and Garcia-Trejo, J. J. (2010) A novel 11-kDa inhibitory subunit in the F1Fo ATP synthase of Paracoccus denitrificans and related alpha-proteobacteria, FASEB J., 24, 599–608.PubMedCrossRefGoogle Scholar
  71. 71.
    Zarco-Zavala, M., Morales-Rios, E., Mendoza-Hernandez, G., Ramirez-Silva, L., Perez-Hernandez, G., and Garcia-Trejo, J. J. (2014) The ζ subunit of the F1Fo-ATP synthase of α-proteobacteria controls rotation of the nanomotor with a different structure, FASEB J., 28, 2146–2157.PubMedCrossRefGoogle Scholar
  72. 72.
    Garcia-Trejo, J. J., Zarco-Zavala, M., Mendoza-Hoffmann, F., Hernandez-Luna, E., Ortega, R., and Mendoza-Hernandez, G. (2016) The inhibitory mechanism of the ζ subunit of the F1Fo-ATPase nanomotor of Paracoccus den-itrificans and related α-proteobacteria, J. Biol. Chem., 291, 538–546.PubMedCrossRefGoogle Scholar
  73. 73.
    Morales-Rios, E., Montgomery, M. G., Leslie, A. G. W., and Walker, J. E. (2015) Structure of ATP synthase from Paracoccus denitrificans determined by X-ray crystallogra-phy at 4.0 Е resolution, Proc. Natl. Acad. Sci. USA, 112, 13231–13236.PubMedCrossRefGoogle Scholar
  74. 74.
    Ragunathan, P., Sielaff, H., Sundararaman, L., Biukovic, G., Subramanian Manimekalai, M. S., Singh, D., Kundu, S., Wohland, T., Frasch, W., Dick, T., and Gruber, G. (2017) The uniqueness of subunit α of mycobacterial F-ATP synthases: an evolutionary variant for niche adapta-tion, J. Biol. Chem., 292, 11262–11279.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Petrack, B., Craston, A., Sheppy, F., and Farron, F. (1965) Studies on the hydrolysis of adenosine triphosphate by spinach chloroplasts, J. Biol. Chem., 240, 906–914.PubMedGoogle Scholar
  76. 76.
    Carmeli, C., and Lifshitz, Y. (1972) Effects of Pi and ADP on ATPase activity in chloroplasts, Biochim. Biophys. Acta, 267, 86–95.PubMedCrossRefGoogle Scholar
  77. 77.
    Strotmann, H., and Bickel-Sandkotter, S. (1977) Energy-dependent exchange of adenine nucleotides on chloroplast coupling factor (CF1), Biochim. Biophys. Acta, 460, 126–135.PubMedCrossRefGoogle Scholar
  78. 78.
    Shoshan, V., and Selman, B. R. (1979) The relationship between light-induced adenine nucleotide exchange and ATPase activity in chloroplast thylakoid membranes, J. Biol. Chem., 254, 8801–8807.PubMedGoogle Scholar
  79. 79.
    Mal’yan, A. N., and Vitseva, O. I. (1990) Kinetic analysis of ADP-and Mg2+-dependent inactivation of CF1-ATPase, Photosynthetica, 24, 613–622.Google Scholar
  80. 80.
    Dunham, K. R., and Selman, B. R. (1981) Interactions of inorganic phosphate with spinach coupling factor 1. Effects on ATPase and ADP binding activities, J. Biol. Chem., 256, 10044–10049.PubMedGoogle Scholar
  81. 81.
    Czarnecki, J. J., Dunham, K. R., and Selman, B. R. (1985) Photoaffinity labeling of the tight ADP binding site of the chloroplast coupling factor one (CF1): the effect on the CF1-ATPase activity, Biochim. Biophys. Acta, 809, 51–56.PubMedCrossRefGoogle Scholar
  82. 82.
    Zhou, J. M., Xue, Z. X., Du, Z. Y., Melese, T., and Boyer, P. D. (1988) Relationship of tightly bound ADP and ATP to control and catalysis by chloroplast ATP synthase, Biochemistry, 27, 5129–5135.PubMedCrossRefGoogle Scholar
  83. 83.
    Drobinskaya, I. Y., Kozlov, I. A., Murataliev, M. B., and Vulfson, E. N. (1985) Tightly bound adenosine diphosphate, which inhibits the activity of mitochondrial F1-ATPase, is located at the catalytic site of the enzyme, FEBS Lett., 182, 419–424.PubMedCrossRefGoogle Scholar
  84. 84.
    Wei, J., Howlett, B., and Jagendorf, A. T. (1988) Azide inhibition of chloroplast ATPase is prevented by a high pro-tonmotive force, Biochim. Biophys. Acta, 934, 72–79.CrossRefGoogle Scholar
  85. 85.
    Larson, E. M., Umbach, A., and Jagendorf, A. T. (1989) Sulfite-stimulated release of [3H]ADP bound to chloroplast thylakoid ATPase, Biochim. Biophys. Acta, 973, 78–85.CrossRefGoogle Scholar
  86. 86.
    Minkov, I. B., and Strotmann, H. (1989) The effect of azide on regulation of the chloroplast H+-ATPase by ADP and phosphate, Biochim. Biophys. Acta, 973, 7–12.CrossRefGoogle Scholar
  87. 87.
    Melandri, B. A., Baccarini-Melandri, A., and Fabbri, E. (1972) Energy transduction in photosynthetic bacteria. IV: Light-dependent ATPase in photosynthetic membranes from Rhodopseudomonas capsulata, Biochim. Biophys. Acta, 275, 383–394.PubMedCrossRefGoogle Scholar
  88. 88.
    Edwards, P. A., and Jackson, J. B. (1976) The control of the adenosine triphosphatase of Rhodospirillum rubrum chromatophores by divalent cations and the membrane high energy state, Eur. J. Biochem., 62, 7–14.PubMedCrossRefGoogle Scholar
  89. 89.
    Slooten, L., and Nuyten, A. (1981) Activation-deactivation reactions in the ATPase enzyme in Rhodospirillum rubrum chromatophores, Biochim. Biophys. Acta, 638, 305–312.CrossRefGoogle Scholar
  90. 90.
    Turina, P., Rumberg, B., Melandri, B. A., and Graber, P. (1992) Activation of the H(+)-ATP synthase in the photo-synthetic bacterium Rhodobacter capsulatus, J. Biol. Chem., 267, 11057–11063.PubMedGoogle Scholar
  91. 91.
    Cappellini, P., Turina, P., Fregni, V., and Melandri, B. A. (1997) Sulfite stimulates the ATP hydrolysis activity of but not proton translocation by the ATP synthase of Rhodobacter capsulatus and interferes with its activation by delta muH+, Eur. J. Biochem., 248, 496–506.PubMedCrossRefGoogle Scholar
  92. 92.
    Bakels, R., Walraven, H. S., and Krab, K. (1993) On the activation mechanism of the H+-ATP synthase and unusual thermodynamic properties in the alkalophilic cyanobac-terium Spirulina platensis, Eur. J. Biochem., 213, 957–964.PubMedCrossRefGoogle Scholar
  93. 93.
    Krab, K., Bakels, R., and Scholts, M. (1993) Activation of the H+-ATP synthase in thylakoid vesicles from the cyanobacterium Synechococcus 6716 by \(\Delta {\tilde \mu _{{H^ + }}}\). Including a comparison with chloroplasts and introducing a new method to calibrate light-induced \(\Delta {\tilde \mu _{{H^ + }}}\), Biochim. Biophys. Acta, 1141, 197–205.CrossRefGoogle Scholar
  94. 94.
    Bakels, R., van Wielink, J. E., Krab, K., and van Walraven, H. S. (1996) The effect of sulfite on the ATP hydrolysis and synthesis activities in chloroplasts and cyanobacterial membrane vesicles can be explained by competition with phosphate, Arch. Biochem. Biophys., 332, 170–174.PubMedCrossRefGoogle Scholar
  95. 95.
    Hockel, M., Hulla, F. W., Risi, S., and Dose, K. (1978) Kinetic studies on bacterial plasma membrane ATPase (F1). Nucleotide-induced long-term inactivation of ATP hydrolyzing activity is linked to the formation of multiple “tight” enzyme nucleotide complexes, J. Biol. Chem., 253, 4292–4296.PubMedGoogle Scholar
  96. 96.
    Yoshida, M., and Allison, W. S. (1986) Characterization of the catalytic and noncatalytic ADP binding sites of the F1-ATPase from the thermophilic bacterium, PS3, J. Biol. Chem., 261, 5714–5721.PubMedGoogle Scholar
  97. 97.
    Paik, S. R., Jault, J.-M., and Allison, W. S. (1994) Inhibition and inactivation of the F1 adenosine triphos-phatase from Bacillus PS3 by dequalinum and activation of the enzyme by lauryl dimethylamine oxide, Biochemistry, 33, 126–133.PubMedCrossRefGoogle Scholar
  98. 98.
    Jault, J. M., Matsui, T., Jault, F. M., Kaibara, C., Muneyuki, E., Yoshida, M., Kagawa, Y., and Allison, W. S. (1995) The alpha3beta3 gamma complex of the F1-ATPase from thermophilic Bacillus PS3 containing the alpha D261N substitution fails to dissociate inhibitory MgADP from a catalytic site when ATP binds to noncat-alytic sites, Biochemistry, 34, 16412–16418.PubMedCrossRefGoogle Scholar
  99. 99.
    Mitome, N., Ono, S., Suzuki, T., Shimabukuro, K., Muneyuki, E., and Yoshida, M. (2002) The presence of phosphate at a catalytic site suppresses the formation of the MgADP-inhibited form of F(1)-ATPase, Eur. J. Biochem., 269, 53–60.PubMedCrossRefGoogle Scholar
  100. 100.
    Hirono-Hara, Y., Noji, H., Nishiura, M., Muneyuki, E., Hara, K. Y., Yasuda, R., Kinosita, K., Jr., and Yoshida, M. (2001) Pause and rotation of F(1)-ATPase during catalysis, Proc. Natl. Acad. Sci. USA, 98, 13649–13654.PubMedCrossRefGoogle Scholar
  101. 101.
    Hirono-Hara, Y., Ishizuka, K., Kinosita, K., Jr., Yoshida, M., and Noji, H. (2005) Activation of pausing F1 motor by external force, Proc. Natl. Acad. Sci. USA, 102, 4288–4293.PubMedCrossRefGoogle Scholar
  102. 102.
    Saita, E.-I., Iino, R., Suzuki, T., Feniouk, B. A., Kinosita, K., Jr., and Yoshida, M. (2010) Activation and stiffness of the inhibited states of F1-ATPase probed by single-mole-cule manipulation, J. Biol. Chem., 285, 11411–11417.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Pacheco-Moises, F., Garcia, J. J., Rodriguez-Zavala, J. S., and Moreno-Sanchez, R. (2000) Sulfite and membrane energization induce two different active states of the Paracoccus denitrificans FOF1-ATPase, Eur. J. Biochem., 267, 993–1000.PubMedCrossRefGoogle Scholar
  104. 104.
    Zharova, T. V., and Vinogradov, A. D. (2004) Energy-dependent transformation of FOF1-ATPase in Paracoccus denitrificans plasma membranes, J. Biol. Chem., 279, 12319–12324.PubMedCrossRefGoogle Scholar
  105. 105.
    Moyle, J., and Mitchell, P. (1975) Active/inactive state transitions of mitochondrial ATPase molecules influenced by Mg2+, anions and aurovertin, FEBS Lett., 56, 55–61.PubMedGoogle Scholar
  106. 106.
    Fitin, A. F., Vasilyeva, E. A., and Vinogradov, A. D. (1979) An inhibitory high affinity binding site for ADP in the oligomycin-sensitive ATPase of beef heart submitochondrial particles, Biochem. Biophys. Res. Commun., 86, 434–439.PubMedCrossRefGoogle Scholar
  107. 107.
    Minkov, I. B., Fitin, A. F., Vasilyeva, E. A., and Vinogradov, A. D. (1979) Mg2+-induced ADP-dependent inhibition of the ATPase activity of beef heart mitochondr-ial coupling factor F1, Biochem. Biophys. Res. Commun., 89, 1300–1306.PubMedCrossRefGoogle Scholar
  108. 108.
    Roveri, O. A., Muller, J. L., Wilms, J., and Slater, E. C. (1980) The pre-steady state and steady-state kinetics of the ATPase activity of mitochondrial F1, Biochim. Biophys. Acta, 589, 241–255.PubMedCrossRefGoogle Scholar
  109. 109.
    Vasilyeva, E. A., Fitin, A. F., Minkov, I. B., and Vinogradov, A. D. (1980) Kinetics of interaction of adenosine diphosphate and adenosine triphosphate with adenosine triphosphatase of bovine heart submitochondrial par-ticles, Biochem. J., 188, 807–815.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Vasilyeva, E. A., Minkov, I. B., Fitin, A. F., and Vinogradov, A. D. (1982) Kinetic mechanism of mitochondrial adeno-sine triphosphatase. ADP-specific inhibition as revealed by the steady-state kinetics, Biochem. J., 202, 9–14.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Martins, O. B., Tuena de Gomez-Puyou, M., and Gomez-Puyou, A. (1988) Pre-steady-state studies of the adenosine triphosphatase activity of coupled submitochondrial particles. Regulation by ADP, Biochemistry, 27, 7552–7558.PubMedCrossRefGoogle Scholar
  112. 112.
    Galkin, M. A., and Vinogradov, A. D. (1999) Energy-dependent transformation of the catalytic activities of the mitochondrial FOF1-ATP synthase, FEBS Lett., 448, 123–126.PubMedCrossRefGoogle Scholar
  113. 113.
    Jault, J.-M., Dou, C., Grodsky, N. B., Matsui, T., Yoshida, M., and Allison, W. S. (1996) The α3β3γ sub-complex of the F1-ATPase from the thermophilic Bacillus PS3 with the βT165S substitution does not entrap inhibitory MgADP in a catalytic site during turnover, J. Biol. Chem., 271, 28818–28824.PubMedCrossRefGoogle Scholar
  114. 114.
    Omote, H., Maeda, M., and Futai, M. (1992) Effects of mutations of conserved Lys-155 and Thr-156 residues in the phosphate-binding glycine-rich sequence of the F1-ATPase beta subunit of Escherichia coli, J. Biol. Chem., 267, 20571–20576.PubMedGoogle Scholar
  115. 115.
    Hu, D., Strotmann, H., Shavit, N., and Leu, S. (1998) The C. reinhardtii CF1 with the mutation betaT168S has high ATPase activity, FEBS Lett., 421, 65–68.PubMedCrossRefGoogle Scholar
  116. 116.
    Feniouk, B. A., Wakabayashi, C., Suzuki, T., and Yoshida, M. (2012) A point mutation, betaGln259Leu, relieves MgADP inhibition in Bacillus PS3 ATP synthase, Biochim. Biophys. Acta, 1817, S13.CrossRefGoogle Scholar
  117. 117.
    Al-Shawi, M. K., and Nakamoto, K. R. (1998) Intergenic suppression of the γM23K uncoupling mutation in FOF1 ATP synthase by βGlu-381 substitutions: the role of the β380DELSEED386 segment in energy coupling, Biochem. J., 330, 707–712.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Feniouk, B. A., Rebecchi, A., Giovannini, D., Anefors, S., Mulkidjanian, A. Y., Junge, W., Turina, P., and Melandri, B. A. (2007) Met23Lys mutation in subunit gamma of F(o)F(1)-ATP synthase from Rhodobacter capsulatus impairs the activation of ATP hydrolysis by proton-motive force, Biochim. Biophys. Acta, 1767, 1319–1330.PubMedCrossRefGoogle Scholar
  119. 119.
    Cross, R. L., and Nalin, C. M. (1982) Adenine nucleotide binding sites on beef heart F1-ATPase. Evidence for three exchangeable sites that are distinct from three noncatalyt-ic sites, J. Biol. Chem., 257, 2874–2881.PubMedGoogle Scholar
  120. 120.
    Abrahams, J. P., Leslie, A. G. W., Lutter, R., and Walker, J. E. (1994) Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria, Nature, 370, 621–628.PubMedCrossRefGoogle Scholar
  121. 121.
    Milgrom, Y. M., Ehler, L. L., and Boyer, P. D. (1991) The characteristics and effect on catalysis of nucleotide binding to noncatalytic sites of chloroplast F1-ATPase, J. Biol. Chem., 266, 11551–11558.PubMedGoogle Scholar
  122. 122.
    Malyan, A. N. (2013) Noncatalytic nucleotide binding sites: properties and mechanism of involvement in ATP synthase activity regulation, Biochemistry, 78, 1512–1523.PubMedGoogle Scholar
  123. 123.
    Milgrom, Y. M., Ehler, L. L., and Boyer, P. D. (1990) ATP binding at noncatalytic sites of soluble chloroplast F1-ATPase is required for expression of the enzyme activity, J. Biol. Chem., 265, 18725–18728.PubMedGoogle Scholar
  124. 124.
    Murataliev, M. B., and Boyer, P. D. (1992) The mecha-nism of stimulation of Mg-ATPase activity of chloroplast F1-ATPase by non-catalytic adenine-nucleotide binding. Acceleration of the ATP-dependent release of inhibitory ADP from a catalytic site, Eur. J. Biochem., 209, 681–687.PubMedCrossRefGoogle Scholar
  125. 125.
    Jault, J. M., and Allison, W. S. (1993) Slow binding of ATP to noncatalytic nucleotide binding sites which accelerates catalysis is responsible for apparent negative cooperativity exhibited by the bovine mitochondrial F1-ATPase, J. Biol. Chem., 268, 1558–1566.PubMedGoogle Scholar
  126. 126.
    Malyan, A. N. (2003) Interaction of oxyanions with thioredoxin-activated chloroplast coupling factor 1, Biochim. Biophys. Acta, 1607, 161–166.PubMedCrossRefGoogle Scholar
  127. 127.
    Malyan, A. N. (2013) Activation of MgADP-inactivated chloroplast F1-ATPase depends on oxyanion binding to noncatalytic sites, Dokl. Biochem. Biophys., 450, 123–125.PubMedCrossRefGoogle Scholar
  128. 128.
    Matsui, T., Muneyuki, E., Honda, M., Allison, W. S., Dou, C., and Yoshida, M. (1997) Catalytic activity of the alpha3beta3gamma complex of F1-ATPase without non-catalytic nucleotide binding site, J. Biol. Chem., 272, 8215–8221.PubMedCrossRefGoogle Scholar
  129. 129.
    Bald, D., Muneyuki, E., Amano, T., Kruip, J., Hisabori, T., and Yoshida, M. (1999) The noncatalytic site-deficient alpha3beta3gamma subcomplex and FoF1-ATP synthase can continuously catalyze ATP hydrolysis when Pi is pres-ent, Eur. J. Biochem., 262, 563–568.PubMedCrossRefGoogle Scholar
  130. 130.
    Amano, T., Matsui, T., Muneyuki, E., Noji, H., Hara, K., Yoshida, M., and Hisabori, T. (1999) alpha3beta3gamma complex of F1-ATPase from thermophilic Bacillus PS3 can maintain steady-state ATP hydrolysis activity depending on the number of non-catalytic sites, Biochem. J., 343, 135–138.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Ishikawa, T., and Kato-Yamada, Y. (2014) Severe MgADP inhibition of Bacillus subtilis F1-ATPase is not due to the absence of nucleotide binding to the noncatalytic nucleotide binding sites, PLoS One, 9, 1–5.Google Scholar
  132. 132.
    Hyndman, D. J., Milgrom, Y. M., Bramhall, E. A., and Cross, R. L. (1994) Nucleotide-binding sites on Escherichia coli F1-ATPase. Specificity of noncatalytic sites and inhibition at catalytic sites by MgADP, J. Biol. Chem., 269, 28871–28877.PubMedGoogle Scholar
  133. 133.
    Weber, J., Wilke-Mounts, S., Grell, E., and Senior, A. E. (1994) Tryptophan fluorescence provides a direct probe of nucleotide binding in the noncatalytic sites of Escherichia coli F1-ATPase, J. Biol. Chem., 269, 11261–11268.PubMedGoogle Scholar
  134. 134.
    Bennett, B. D., Kimball, E. H., Gao, M., Osterhout, R., Van Dien, S. J., and Rabinowitz, J. D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli, Nat. Chem. Biol., 5, 593–599.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Lotscher, H. R., de Jong, C., and Capaldi, R. A. (1984) Interconversion of high and low adenosine triphosphatase activity forms of Escherichia coli F1 by the detergent lau-ryldimethylamine oxide, Biochemistry, 23, 4140–4143.PubMedCrossRefGoogle Scholar
  136. 136.
    Bragg, P. D., and Hou, C. (1986) Effect of disulfide cross-linking between alpha and delta subunits on the properties of the F1 adenosine triphosphatase of Escherichia coli, Biochim. Biophys. Acta, 851, 385–394.PubMedCrossRefGoogle Scholar
  137. 137.
    Peskova, Y. B., and Nakamoto, R. K. (2000) Catalytic con-trol and coupling efficiency of the Escherichia coli FoF1 ATP synthase: influence of the Fo sector and epsilon subunit on the catalytic transition state, Biochemistry, 39, 11830–11836.PubMedCrossRefGoogle Scholar
  138. 138.
    Montero-Lomeli, M., and Dreyfus, G. (1987) Activation of Mg-ATP hydrolysis in isolated Rhodospirillum rubrum H+-ATPase, Arch. Biochem. Biophys., 257, 345–351.PubMedCrossRefGoogle Scholar
  139. 139.
    Glaser, E., Hamasur, B., Norling, B., and Andersson, B. (1987) Activation of F1-ATPase isolated from potato tuber mitochondria, FEBS Lett., 223, 304–308.CrossRefGoogle Scholar
  140. 140.
    Sherman, P. A., and Wimmer, M. J. (1984) Activation of ATPase of spinach coupling factor 1. Release of tightly bound ADP from the soluble enzyme, Eur. J. Biochem., 139, 367–371.PubMedCrossRefGoogle Scholar
  141. 141.
    Du, Z., and Boyer, P. D. (1989) Control of ATP hydrolysis by ADP bound at the catalytic site of chloroplast ATP syn-thase as related to proton-motive force and magnesium, Biochemistry, 28, 873–879.CrossRefGoogle Scholar
  142. 142.
    Junge, W. (1970) The critical electric potential difference for photophosphorylation. Its relation to the chemiosmotic hypothesis and to the triggering requirements of the ATPase system, Eur. J. Biochem., 14, 582–592.PubMedCrossRefGoogle Scholar
  143. 143.
    Feniouk, B. A., and Junge, W. (2005) Regulation of the FOF1-ATP synthase: the conformation of subunit ε might be determined by directionality of subunit γ rotation, FEBS Lett., 579, 5114–5118.PubMedCrossRefGoogle Scholar
  144. 144.
    Bakker-Grunwald, T., and Van Dam, K. (1974) On the mechanism of activation of the ATPase in chloroplasts, Biochim. Biophys. Acta, 347, 290–298.PubMedCrossRefGoogle Scholar
  145. 145.
    Rosing, J., Kayalar, C., and Boyer, P. D. (1977) Evidence for energy-dependent change in phosphate binding for mitochondrial oxidative phosphorylation based on measurements of medium and intermediate phosphate-water exchanges, J. Biol. Chem., 252, 2478–2485.PubMedGoogle Scholar
  146. 146.
    Kayalar, C., Rosing, J., and Boyer, P. D. (1976) 2,4-Dinitrophenol causes a marked increase in the apparent Km of Pi and of ADP for oxidative phosphorylation, Biochem. Biophys. Res. Commun., 72, 1153–1159.PubMedCrossRefGoogle Scholar
  147. 147.
    Mccarthy, J., and Ferguson, S. J. (1983) Characterization of membrane vesicles from Paracoccus denitrificans and measurements of the effect of partial uncoupling on their thermodynamics of oxidative phosphorylation, Eur. J. Biochem., 132, 417–424.PubMedCrossRefGoogle Scholar
  148. 148.
    Al-Shawi, M. K., Parsonage, D., and Senior, A. E. (1990) Thermodynamic analyses of the catalytic pathway of F1-ATPase from Escherichia coli. Implications regarding the nature of energy coupling by F1-ATPases, J. Biol. Chem., 265, 4402–4410.PubMedGoogle Scholar
  149. 149.
    Feniouk, B. A., Suzuki, T., and Yoshida, M. (2007) Regulatory interplay between proton motive force, ADP, phosphate, and subunit ε in bacterial ATP synthase, J. Biol. Chem., 282, 764–772.PubMedCrossRefGoogle Scholar
  150. 150.
    Zharova, T. V., and Vinogradov, A. D. (2006) Energy-linked binding of Pi is required for continuous steady-state proton-translocating ATP hydrolysis catalyzed by FoF1 ATP synthase, Biochemistry, 45, 14552–14558.PubMedCrossRefGoogle Scholar
  151. 151.
    Senior, A. E., Lee, R. S., Al-Shawi, M. K., and Weber, J. (1992) Catalytic properties of Escherichia coli F1-ATPase depleted of endogenous nucleotides, Arch. Biochem. Biophys., 297, 340–344.PubMedCrossRefGoogle Scholar
  152. 152.
    Dunn, S. D., Zadorozny, V. D., Tozer, R. G., and Orr, L. E. (1987) Epsilon subunit of Escherichia coli F1-ATPase: effects on affinity for aurovertin and inhibition of product release in unisite ATP hydrolysis, Biochemistry, 26, 4488–4493.PubMedCrossRefGoogle Scholar
  153. 153.
    Kato, Y., Sasayama, T., Muneyuki, E., and Yoshida, M. (1995) Analysis of time-dependent change of Escherichia coli F1-ATPase activity and its relationship with apparent nega-tive cooperativity, Biochim. Biophys. Acta, 1231, 275–281.PubMedCrossRefGoogle Scholar
  154. 154.
    Fischer, S., Graber, P., and Turina, P. (2000) The activity of the ATP synthase from Escherichia coli is regulated by the transmembrane proton motive force, J. Biol. Chem., 275, 30157–30162.PubMedCrossRefGoogle Scholar
  155. 155.
    Sekiya, M., Hosokawa, H., Nakanishi-Matsui, M., Al-Shawi, M. K., Nakamoto, R. K., and Futai, M. (2010) Single molecule behavior of inhibited and active states of Escherichia coli ATP synthase F1 rotation, J. Biol. Chem., 285, 42058–42067.PubMedPubMedCentralCrossRefGoogle Scholar
  156. 156.
    D’Alessandro, M., Turina, P., and Melandri, B. A. (2008) Intrinsic uncoupling in the ATP synthase of Escherichia coli, Biochim. Biophys. Acta, 1777, 1518–1527.PubMedCrossRefGoogle Scholar
  157. 157.
    Konno, H., Murakami-Fuse, T., Fuji, F., Koyama, F., Ueoka-Nakanishi, H., Pack, C.-G., Kinjo, M., and Hisabori, T. (2006) The regulator of the F1 motor: inhibi-tion of rotation of cyanobacterial F1-ATPase by the epsilon subunit, EMBO J., 25, 4596–4604.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Tsumuraya, M., Furuike, S., Adachi, K., Kinosita, K., Jr., and Yoshida, M. (2009) Effect of epsilon subunit on the rotation of thermophilic Bacillus F1-ATPase, FEBS Lett., 583, 1121–1126.PubMedCrossRefGoogle Scholar
  159. 159.
    Sugawa, M., Okazaki, K.-I., Kobayashi, M., Matsui, T., Hummer, G., Masaike, T., and Nishizaka, T. (2016) F1-ATPase conformational cycle from simultaneous single-molecule FRET and rotation measurements, Proc. Natl. Acad. Sci. USA, 113, 2916–2924.CrossRefGoogle Scholar
  160. 160.
    Hara, K. Y., Kato-Yamada, Y., Kikuchi, Y., Hisabori, T., and Yoshida, M. (2001) The role of the betaDELSEED motif of F1-ATPase: propagation of the inhibitory effect of the epsilon subunit, J. Biol. Chem., 276, 23969–23973.PubMedCrossRefGoogle Scholar
  161. 161.
    Ferguson, S. A., Cook, G. M., Montgomery, M. G., Leslie, A. G. W., and Walker, J. E. (2016) Regulation of the thermoalkaliphilic F1-ATPase from Caldalkalibacillus thermarum, Proc. Natl. Acad. Sci. USA, 113, 10860–10865.PubMedCrossRefGoogle Scholar
  162. 162.
    Haruyama, T., Hirono-Hara, Y., and Kato-Yamada, Y. (2010) Inhibition of thermophilic F1-ATPase by the ε sub-unit takes different path from the ADP-Mg inhibition, Biophysics, 6, 59–65.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Mizumoto, J., Kikuchi, Y., Nakanishi, Y.-H., Mouri, N., Cai, A., Ohta, T., Haruyama, T., and Kato-Yamada, Y. (2013) ε subunit of Bacillus subtilis F1-ATPase relieves MgADP inhibition, PLoS One, 8, e73888.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Kato-Yamada, Y., Bald, D., Koike, M., Motohashi, K., Hisabori, T., and Yoshida, M. (1999) Epsilon subunit, an endogenous inhibitor of bacterial F(1)-ATPase, also inhibits F(0)F(1)-ATPase, J. Biol. Chem., 274, 33991–33994.PubMedCrossRefGoogle Scholar
  165. 165.
    Iino, R., Murakami, T., Iizuka, S., Kato-Yamada, Y., Suzuki, T., and Yoshida, M. (2005) Real-time monitoring of conformational dynamics of the epsilon subunit in F1-ATPase, J. Biol. Chem., 280, 40130–40134.PubMedCrossRefGoogle Scholar
  166. 166.
    Cingolani, G., and Duncan, T. M. (2011) Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation, Nat. Struct. Mol. Biol., 18, 701–707.PubMedPubMedCentralCrossRefGoogle Scholar
  167. 167.
    Shirakihara, Y., Leslie, A. G., Abrahams, J. P., Walker, J. E., Ueda, T., Sekimoto, Y., Kambara, M., Saika, K., Kagawa, Y., and Yoshida, M. (1997) The crystal structure of the nucleotide-free alpha3beta3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer, Structure, 5, 825–836.PubMedCrossRefGoogle Scholar
  168. 168.
    Menz, R. I., Leslie, A. G., and Walker, J. E. (2001) The structure and nucleotide occupancy of bovine mitochon-drial F(1)-ATPase are not influenced by crystallization at high concentrations of nucleotide, FEBS Lett., 494, 11–14.PubMedCrossRefGoogle Scholar
  169. 169.
    Lodeyro, A. F., Castelli, M. V., and Roveri, O. A. (2008) ATP hydrolysis-driven H+ translocation is stimulated by sulfate, a strong inhibitor of mitochondrial ATP synthesis, J. Bioenerg. Biomembr., 40, 269–279.PubMedCrossRefGoogle Scholar
  170. 170.
    Shah, N. B., Hutcheon, M. L., Haarer, B. K., and Duncan, T. M. (2013) F1-ATPase of Escherichia coli: the ε-inhibited state forms after ATP hydrolysis, is distinct from the ADP-inhibited state, and responds dynamical-ly to catalytic site ligands, J. Biol. Chem., 288, 9383–9395.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  1. 1.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia
  2. 2.A. N. Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations