F1-ATPase of Escherichia coli: The ε-inhibited state forms after ATP hydrolysis, is distinct from the ADP-inhibited state, and responds dynamically to catalytic site ligands

Journal of Biological Chemistry

Volumn 288, Issue 13, 2013, Pages 9383-9395

  Shah, Naman B ^a   Hutcheon, Marcus L ^a   Haarer, Brian K ^a   Duncan, Thomas M ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; CATALYTIC COMPLEXES; COMPETING PROCESS; CONFORMATIONAL CHANGE; N-TERMINAL DOMAINS; ROTARY NANOMOTOR; ROTATIONAL MOBILITY; SUBUNIT ROTATION;

BINDING ENERGY; ESCHERICHIA COLI; HYDROLYSIS; PLANTS (BOTANY);

LIGANDS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ANTIINFECTIVE AGENT; CROSS LINKING REAGENT; LIGAND; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ADENOSINE TRIPHOSPHATE HYDROLYSIS; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME INHIBITION; ESCHERICHIA COLI; HYDROLYSIS; INHIBITION KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DOSE RESPONSE; DRUG DESIGN; KINETICS; METABOLISM; PLASMID; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; TIME; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANTI-BACTERIAL AGENTS; BIOLOGICAL TRANSPORT; CROSS-LINKING REAGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DESIGN; ESCHERICHIA COLI; HYDROLYSIS; KINETICS; LIGANDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PLASMIDS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTON-TRANSLOCATING ATPASES; TIME FACTORS;

MLCS; MLOWN;

EID: 84875967309     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451583     Document Type: Article

References (81)

1. Boyer, P. D. (1997) The ATP synthase. A splendid molecular machine. Annu. Rev. Biochem. 66, 717-749
2. Duncan, T. M. (2004) The ATP Synthase. Parts and Properties of a Rotary Motor. in The Enzymes, Vol. XXIII, 3rd Ed. (Hackney, D. D., and Tamanoi, F., eds) pp. 203-275, Elsevier Academic Press, New York
3. 1 ATP Synthase (Eaton-Rye, J. J., Tripathy, B. C., and Sharkey, T. D., eds) pp. 561-590, Springer, Dordrecht, Netherlands
4. Cox, G. B., Devenish, R. J., Gibson, F., Howitt, S. M., and Nagley, P. (1992) The structure and assembly of ATP synthase. in Molecular Mechanisms in Bioenergetics (Ernster, L., ed) pp. 283-315, Elsevier Science, New York
5. Andries, K., Verhasselt, P., Guillemont, J., Göhlmann, H. W., Neefs, J. M., Winkler, H., Van Gestel, J., Timmerman, P., Zhu, M., Lee, E., Williams, P., de Chaffoy, D., Huitric, E., Hoffner, S., Cambau, E., Truffot-Pernot, C., Lounis, N., and Jarlier, V. (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307, 223-227
6. Koul, A., Vranckx, L., Dendouga, N., Balemans, W., Van den Wyngaert, I., Vergauwen, K., Göhlmann, H. W., Willebrords, R., Poncelet, A., Guillemont, J., Bald, D., and Andries, K. (2008) Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J. Biol. Chem. 283, 25273-25280
7. Diacon, A. H., Pym, A., Grobusch, M., Patientia, R., Rustomjee, R., Page-Shipp, L., Pistorius, C., Krause, R., Bogoshi, M., Churchyard, G., Venter, A., Allen, J., Palomino, J. C., De Marez, T., van Heeswijk, R. P., Lounis, N., Meyvisch, P., Verbeeck, J., Parys, W., de Beule, K., Andries, K., and Mc Neeley, D. F. (2009) The diarylquinoline TMC207 for multidrug-resistant tuberculosis. N. Engl. J. Med. 360, 2397-2405
8. 1) from Escherichia coli in an autoinhibited conformation. Nat. Struct. Mol. Biol. 18, 701-707
9. 1-ATP synthase. Biochim. Biophys. Acta 1757, 326-338
10. Richter, M. L. (2004) γ-ε interactions regulate the chloroplast ATP synthase. Photosynth. Res. 79, 319-329
11. 1. Cell Metab. 8, 13-25
12. 1-ATP synthase. J. Biol. Chem. 284, 17457-17464
13. 1-ATP synthase in catalysis. Biochem. Biophys. Res. Commun. 342, 800-807
14. 1- ATPase. Structure 15, 904-914
15. 1-ATPase at 2.4 Å resolution. Nat. Struct. Biol. 7, 1055-1061
16. 1 ATPase. EMBO J. 25, 5433-5442
17. Uhlin, U., Cox, G. B., and Guss, J. M. (1997) Crystal structure of the ε subunit of the proton-translocating ATP synthase from Escherichia coli. Structure 5, 1219-1230
18. 1-ATPase from Escherichia coli and interactions of this subunit with β subunits in the complex. J. Biol. Chem. 273, 26645-26651
19. 1-ATPase ε subunit suggesting ATP-regulated arm motion of its C-terminal domain in F1. Proc. Natl. Acad. Sci. U.S.A. 104, 11233-11238
20. Watt, I. N., Montgomery, M. G., Runswick, M. J., Leslie, A. G., and Walker, J. E. (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc. Natl. Acad. Sci. U.S.A. 107, 16823-16827
21. O complex of Escherichia coli. Cross-linking studies show the same structure in situ as when isolated. J. Biol. Chem. 274, 28351-28355
22. 1 rotation. J. Biol. Chem. 285, 42058-42067
23. 1-ATPase by the ε subunit. EMBO J. 25, 4596-4604
24. 1-ATPase. FEBS Lett. 583, 1121-1126
25. 1-ATPase. J. Biol. Chem. 286, 13423-13429
26. 1-ATPase probed by single-molecule manipulation. J. Biol. Chem. 285, 11411-11417
27. 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
28. 1-ATPase. Effects on affinity for aurovertin and inhibition of product release in unisite ATP hydrolysis. Biochemistry 26, 4488-4493
29. 1-ATPase catalytic sites. J. Biol. Chem. 274, 19124-19128
30. 1-ATPase complex by site-directed spin labeling. Biochemistry 40, 10664-10770
31. Cipriano, D. J., and Dunn, S. D. (2006) The role of the ε subunit in the Escherichia coli ATP synthase. The C-terminal domain is required for efficient energy coupling. J. Biol. Chem. 281, 501-507
32. Tsao, K.-L., DeBarbieri, B., Michel, H., and Waugh, D. S. (1996)Aversatile plasmid expression vector for the production of biotinylated proteins by site-specific, enzymatic modification in Escherichia coli. Gene 169, 59-64
33. Bhardwaj, A., Walker-Kopp, N., Wilkens, S., and Cingolani, G. (2008) Foldon-guided self-assembly of ultra-stable protein fibers. Protein Sci. 17, 1475-1485
34. 1 ATP synthase β and γ subunits with disulphide cross-links. Biochem. Soc. Trans. 23, 736-741
35. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
36. Peterson, G. L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83, 346-356
37. 1- ATPase using monoclonal anti-ε antibody affinity chromatography. Anal. Biochem. 159, 35-42
38. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 92, 10964-10968
39. Penefsky, H. S. (1977) Reversible binding of Pi by beef heart mitochondrial adenosine triphosphatase. J. Biol. Chem. 252, 2891-2899
40. Pullman, M. E., Penefsky, H. S., Datta, A., and Racker, E. (1960) Partial resolution of the enzymes catalysing oxidative phosphorylation. I. Purification and properties of soluble dinitrophenyl-stimulated adonosine triphophatase. J. Biol. Chem. 235, 3322-3329
41. Abdiche, Y., Malashock, D., Pinkerton, A., and Pons, J. (2008) Determining kinetics and affinities of protein interactions using a parallel real-time label-free biosensor, the Octet. Anal. Biochem. 377, 209-217
42. 1-ATPase. Eur. J. Biochem. 161, 513-518
43. 1 ATPase binds the γ subunit. J. Biol. Chem. 257, 7354-7359
44. Sternweis, P. C., and Smith, J. B. (1980) Characterization of the inhibitory ε subunit of the proton-translocating adenosine triphosphatase from Escherichia coli. Biochemistry 19, 526-531
45. 1-ATPase. Specificity of noncatalytic sites and inhibition at catalytic sites by MgADP. J. Biol. Chem. 269, 28871-28877
46. 1-ATPase activity and its relationship with apparent negative cooperativity. Biochim. Biophys. Acta 1231, 275-281
47. 1- ATPase from thermophilic Bacillus PS3 containing the α D261N substitution fails to dissociate inhibitoryMgADPfrom a catalytic site when ATP binds to noncatalytic sites. Biochemistry 34, 16412-16418
48. 1-ATPase, is located at the catalytic site of the enzyme. FEBS Lett. 182, 419-424
49. 1-ATPase and inhibits catalysis is bound at a catalytic site. Biochim. Biophys. Acta 1020, 43-48
50. 1 ATPase from chloroplasts. Biochemistry 30, 8305-8310
51. 1 ATPases. J. Biol. Chem. 265, 16280-16287
52. 1 β-subunit increases catalytic site interaction with GDP and IDP and produces negative cooperativity of GTP and ITP hydrolysis. J. Biol. Chem. 268, 20762-20767
53. Xiong, H., Zhang, D., and Vik, S. B. (1998) Subunit ε of the Escherichia coli ATP synthase. Novel insights into structure and function by analysis of thirteen mutant forms. Biochemistry 37, 16423-16429
54. Mendel-Hartvig, J., and Capaldi, R. A. (1991) Nucleotide-dependent and dicyclohexylcarbodiimide-sensitive conformational changes in the ε subunit of Escherichia coli ATP synthase. Biochemistry 30, 10987-10991
55. Mendel-Hartvig, J., and Capaldi, R. A. (1991) Catalytic site nucleotide and inorganic phosphate dependence of the conformation of the ε subunit in Escherichia coli adenosinetriphosphatase. Biochemistry 30, 1278-1284
56. 1-ATPase. J. Biol. Chem. 267, 18953-18960
57. 1- ATPase during catalysis. Proc. Natl. Acad. Sci. U.S.A. 98, 13649-13654
58. 1 sector. Stochastic fluctuation and a key domain of the β subunit. J. Biol. Chem. 282, 20698-20704
59. 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 sulphite. Biochem. J. 202, 15-23
60. 1-ATPase by non-catalytic adeninenucleotide binding. Acceleration of the ATP-dependent release of inhibitory ADP from a catalytic site. Eur. J. Biochem. 209, 681-687
61. Bowler, M. W., Montgomery, M. G., Leslie, A. G., and Walker, J. E. (2006) How azide inhibits ATP hydrolysis by the F-ATPases. Proc. Natl. Acad. Sci. U.S.A. 103, 8646-8649
62. 1 motor protein. Chem. Sci. 2, 2086-2093
63. 1-ATPase. A prototypical rotary molecular motor. Adv. Exp. Med. Biol. 726, 5-16
64. 1-ATPase from bovine heart mitochondria. Proc. Natl. Acad. Sci. U.S.A. 109, 11139-11143
65. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 105, 17760-17765
66. 1-ATPase as determined from its crystal structure and single-molecule rotation. Proc. Natl. Acad. Sci. U.S.A. 105, 20722-20727
67. 1-ATPase correlated with crystal structures. Biophys. J. 95, 4979-4987
68. 1-ATPase with nucleotide bound to all three catalytic sites. Implications for the mechanism of rotary catalysis. Cell 106, 331-341
69. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 105, 1192-1197
70. 1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Mol. Biol. 11, 142-148
71. 1- ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321
72. 1-ATPase revealed by catalytic site occupancy during catalysis. Biophys. J. 98, 1227-1236
73. 1 examined by cryoelectronmicroscopy. Biol. Chem. Hoppe-Seyler 375, 43-51
74. +-ATP synthase. EMBO J. 24, 2053-2063
75. 1-ATPase from bovine mitochondria. Proc. Natl. Acad. Sci. U.S.A. 104, 15671-15676
76. 1 motor by external force. Proc. Natl. Acad. Sci. U.S.A. 102, 4288-4293
77. 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
78. 1-ATPase. Cooperative interactions between sites and specificity of noncatalytic sites. J. Biol. Chem. 268, 23179-23185
79. 1-ATPase accounts for the observed positive catalytic cooperativity. Biochim. Biophys. Acta 1787, 1016-1023
80. Haagsma, A. C., Driessen, N. N., Hahn, M. M., Lill, H., and Bald, D. (2010) ATP synthase in slow- and fast-growing mycobacteria is active in ATP synthesis and blocked in ATP hydrolysis direction. FEMS Microbiol. Lett. 313, 68-74
81. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera.Avisualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612