A bi-site mechanism for Escherichia coli F1-ATPase accounts for the observed positive catalytic cooperativity

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1787, Issue 8, 2009, Pages 1016-1023

  Bulygin, Vladimir V ^a   Milgrom, Yakov M ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

ATP synthase; Bi site catalysis; Catalytic cooperativity; Centrifugal filtration; Nucleotide binding; Tri site catalysis

Indexed keywords

ADENOSINE TRIPHOSPHATASE (MAGNESIUM); ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; EPSILON SUBUNIT; NUCLEOTIDE; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CATALYSIS; CENTRIFUGATION; CONTROLLED STUDY; ENZYME SUBSTRATE; ESCHERICHIA COLI; FILTRATION; HYDROLYSIS; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN BINDING; STEADY STATE;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTON-TRANSLOCATING ATPASES; CATALYSIS; DIPHOSPHATES; ESCHERICHIA COLI; HYDROLYSIS; KINETICS; SODIUM SELENITE;

ESCHERICHIA COLI;

EID: 67649414406     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2009.02.025     Document Type: Article

References (83)

1. 1-ATPase from bovine heart mitochondria. Nature 370 (1994) 621-628
2. 1-ATPase. Evidence for three exchangeable sites that are distinct from three noncatalytic sites. J. Biol. Chem. 257 (1982) 2874-2881
3. Boyer P.D., Cross R.L., and Momsen W. A new concept for energy coupling in oxidative phosphorylation based on a molecular explanation of the oxygen exchange reactions. Proc. Natl. Acad. Sci. U. S. A. 70 (1973) 2837-2839
4. Kayalar C., Rosing J., and Boyer P.D. An alternating site sequence for oxidative phosphorylation suggested by measurement of substrate binding patterns and exchange reaction inhibitions. J. Biol. Chem. 252 (1977) 2486-2491
5. Boyer P.D., and Kohlbrenner W.E. The present status of the binding-change mechanism and its relation to ATP formation by chloroplasts. In: Selman B.R., and Selman-Reiner S. (Eds). Energy Coupling in Photosynthesis (1981), Elsevier North Holland, New York 231-240
6. Boyer P.D. The binding change mechanism for ATP synthase - some probabilities and possibilities. Biochim. Biophys. Acta 1140 (1993) 215-250
7. 1-ATPase. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 10964-10968
8. Sabbert D., Engelbrecht S., and Junge W. Intersubunit rotation in active F-ATPase. Nature 381 (1996) 623-625
9. 1-ATPase. Nature 386 (1997) 299-302
10. 1-ATPase. J. Biol. Chem. 273 (1998) 19375-19377
11. 1 ATP synthase from cross-linking of subunits b and c in the Escherichia coli enzyme. J. Biol. Chem. 275 (2000) 31340-31346
12. o ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 898-902
13. O sector of Escherichia coli ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 8519-8524
14. 1 enzyme complexes during ATP synthesis or hydrolysis. FEBS Lett. 525 (2002) 156-163
15. Nishio K., Iwamoto-Kihara A., Yamamoto A., Wada Y., and Futai M. Subunit rotation of ATP synthase embedded in membranes: a or β subunit rotation relative to the c subunit ring. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 13448-13452
16. 1-ATP synthase. Nat. Struct. Mol. Biol. 11 (2004) 135-141
17. 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
18. 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
19. 1-ATPase. Evidence for alternating high affinity sites during steady-state turnover. J. Biol. Chem. 263 (1988) 18850-18856
20. Zhou J.-M., and Boyer P.D. Evidence that energization of the chloroplast ATP synthase favors ATP formation at the tight binding catalytic site and increases the affinity for ADP at another catalytic site. J. Biol. Chem. 265 (1993) 1531-1538
21. 2+ in enzyme inactivation. J. Biol. Chem. 269 (1994) 15431-15439
22. 1-ATPase. Biochem. J. 330 (1998) 1037-1043
23. 0 ATP synthase displays biphasic synthesis kinetics. J. Biol. Chem. 279 (2004) 4465-4470
24. 1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps. Cell 93 (1998) 1117-1124
25. 1-ATPase. Nature 410 (2001) 898-904
26. 1-ATPase over ATP concentrations from millimolar down to nanomolar. Biophys. J. 88 (2005) 2047-2056
27. 1-ATP synthase. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1333-1338
28. Matsuno-Yagi A., and Hatefi Y. Studies on the mechanism of oxidative phosphorylation. Positive cooperativity in ATP synthesis. J. Biol. Chem. 265 (1990) 82-88
29. 1-ATPase provides a direct probe of nucleotide binding: maximal ATP hydrolysis occurs with three sites occupied. J. Biol. Chem. 268 (1993) 20126-20133
30. 1). Biochim. Biophys. Acta 1184 (1994) 54-64
31. 1-ATPases based on kinetic and structural considerations. Biochem. Soc. Trans. 24 (1995) 752-756
32. 1 ATP synthase. Annu. Rev. Biophys. Biomol. Struct. 28 (1999) 205-234
33. 1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106 (2001) 331-341
34. 1-ATPase. Biochim. Biophys. Acta 1607 (2003) 35-44
35. 1-ATPase inhibitory peptide. Role of catalytic intermediates and enzyme turnover. J. Biol. Chem. 280 (2005) 9927-9936
36. 1-ATPase: does it exist?. J. Biol. Chem. 276 (2001) 35422-35428
37. 1-ATPase does not hydrolyze ATP at a significant rate until the substrate binds to the catalytic site of the lowest affinity. Biochemistry 45 (2006) 6222-6230
38. 1-ATP synthase. Nat. Struct. Mol. Biol. 11 (2004) 142-148
39. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130 (2007) 309-321
40. 1-ATPase correlates with the filling of the second of three catalytic sites. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 13831-13836
41. Lee R.S.-F., Pagan J., Wilke-Mounts S., and Senior A.E. Characterization of Escherichia coli ATP synthase β-subunit mutations using a chromosomal deletion strain. Biochemistry 30 (1991) 6842-6847
42. Wise J.G. Site-directed mutagenesis of the conserved β subunit tyrosine 331 of Escherichia coli ATP synthase yields catalytically active enzymes. J. Biol. Chem. 265 (1990) 10403-10409
43. Senior A.E., Downie J.A., Cox G.B., Gibson F., Langman L., and Fayle D.R.H. The uncA gene codes for the α-subunit of the adenosine triphosphatase of Escherichia coli. Electrophoretic analysis of uncA mutant strains. Biochem. J. 180 (1979) 103-109
44. 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
45. 1-ATPase. Specificity of noncatalytic sites and inhibition at catalytic sites by MgADP. J. Biol. Chem. 269 (1994) 28871-28877
46. 1-ATPase complex by site-directed spin labeling. Biochemistry 40 (2001) 10664-10670
47. i by beef heart mitochondrial adenosine triphosphatase. J. Biol. Chem. 252 (1977) 2891-2899
48. Pullman M.E., Penefsky H.S., Datta A., and Racker E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. I. Purification and properties of soluble, dinitrophenol-stimulated adenosine triphosphatase. J. Biol. Chem. 235 (1960) 3322-3329
49. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83 (1977) 346-356
50. 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
51. 1 ATPase. Arch. Biochem. Biophys. 197 (1979) 83-89
52. Sternweis P.C., and Smith J.B. Characterization of the inhibitory (e{open}) subunit of the proton-translocating adenosine triphosphatase from Escherichia coli. Biochemistry 19 (1980) 526-531
53. Wise J.G., Latchney L.R., Ferguson A.M., and Senior A.E. Defective proton ATPase of uncA mutants of Escherichia coli. 5′-Adenylyl imidodiphosphate binding and ATP hydrolysis. Biochemistry 23 (1984) 1426-1432
54. l8O exchanges. J. Biol. Chem. 262 (1987) 2180-2186
55. l-ATPase activity and its relationship with apparent negative cooperativity. Biochim. Biophys. Acta 1231 (1995) 275-281
56. 1 ATP synthase are dependent on the energy of interaction between γ and β subunits. J. Biol. Chem. 272 (1997) 2300-2306
57. 1 ATPase binds the e{open} subunit. J. Biol. Chem. 257 (1982) 7354-7359
58. 1-ATPase using monoclonal anti-e{open} antibody affinity chromatography. Anal. Biochem. 159 (1986) 35-42
59. Tuttas-Dorshug R., and Hanstein W.G. Coupling factor 1 from Escherichia coli lacking subunits δ and e{open}: preparation and specific binding to depleted membranes, mediated by subunits δ or e{open}. Biochemistry 28 (1989) 5107-5113
60. 1-ATPase catalytic sites. J. Biol. Chem. 274 (1999) 19124-19128
61. Ebel R.E., and Lardy H.A. Stimulation of rat liver mitochondrial adenosine triphosphatase by anions. J. Biol. Chem. 250 (1975) 191-196
62. 1-ATPase: effects on affinity for aurovertin and inhibition of product release in unisite ATP hydrolysis. Biochemistry 26 (1987) 4488-4493
63. Vasilyeva E.A., Minkov I.B., Fitin A.F., and Vinogradov A.D. Kinetic mechanism of mitochondrial adenosine triphosphatase. Inhibition by azide and activation by sulphite. Biochem. J. 202 (1982) 15-23
64. 1-ATPase functioning. V. A steady state kinetics study. Biol. Membr. (USSR) 3 (1986) 339-351
65. 1-ATPase. Eur. J. Biochem. 177 (1988) 213-218
66. 1-ATPase. Cooperative interactions between sites and specificity of noncatalytic sites. J. Biol. Chem. 268 (1993) 23179-23185
67. Vasilyeva E.A., Fitin A.F., Minkov I.B., and Vinogradov A.D. Kinetics of interaction of adenosine diphosphate and adenosine triphosphate with adenosine triphosphatase of bovine heart submitochondrial particles. Biochem. J. 188 (1980) 807-815
68. 1 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
69. 2+- and ADP-dependent inactivation during ATP hydrolysis. Biochemistry 31 (1992) 12885-12892
70. 1-ATPase. J. Biol. Chem. 268 (1993) 1558-1566
71. 1-ATPase. J. Biol. Chem. 270 (1995) 12653-12658
72. Perlin D.S., Latchney L.R., Wise J.G., and Senior A.E. Specificity of the proton adenosine triphosphatase of Escherichia coli for adenine, guanine, and inosine nucleotides in catalysts and binding. Biochemistry 23 (1984) 4998-5003
73. 1-ATPase from the uncD412 mutant of Escherichia coli. Biochem. J. 215 (1983) 343-350
74. 1-ATPase exhibits strong positive catalytic cooperativity. J. Biol. Chem. 272 (1997) 32211-32214
75. 1-ATPase. J. Bioenerg. Biomembr. 24 (1992) 479-484
76. 1-ATPase from the thermophilic Bacillus PS3 fails to dissociate ADP when MgATP is hydrolyzed at a single catalytic site and attains maximal velocity when three catalytic sites are saturated with MgATP. Biochemistry 37 (1998) 16757-16764
77. Corvest V., Sigalat C., and Haraux F. Insight into the bind-lock mechanism of the yeast mitochondrial ATP synthase inhibitory peptide. Biochemistry 46 (2007) 8680-8688
78. Boyer P.D. The ATP synthase-a splendid molecular machine. Annu. Rev. Biochem. 66 (1997) 717-749
79. 1-ATPase using fluorescence quenching. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 4327-4331
80. 1-ATPase from the thermophilic bacterium, PS3. J. Biol. Chem. 261 (1986) 5714-5721
81. 1-ATPase caused by the γ subunit generates a high affinity nucleotide binding site. J. Biol. Chem. 271 (1996) 2433-2438
82. 1-ATPase without noncatalytic nucleotide binding site. J. Biol. Chem. 272 (1997) 8215-8221
83. Boyer P.D. Catalytic site occupancy during ATP synthase catalysis. FEBS Lett. 512 (2002) 29-32