Structural comparison of F1-ATPase: Interplay among enzyme structures, catalysis, and rotations

Structure

Volumn 19, Issue 4, 2011, Pages 588-598

  Okazaki, Kei Ichi ^a,b,c   Takada, Shoji ^a  

^a KYOTO UNIVERSITY   (Japan)

^b WASEDA UNIVERSITY   (Japan)

^c KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ADENOSINE TRIPHOSPHATE; PROTEIN SUBUNIT; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; BETA CHAIN; CATALYSIS; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME STRUCTURE; HINGE REGION; PRIORITY JOURNAL; PROTEIN BINDING; ROTATION; X RAY CRYSTALLOGRAPHY; ANIMAL; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ENZYME ACTIVE SITE; HUMAN; METABOLISM; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN DATABASE; PROTEIN SECONDARY STRUCTURE;

ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DATABASES, PROTEIN; HUMANS; MODELS, MOLECULAR; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; PROTON-TRANSLOCATING ATPASES;

EID: 79953855777     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.01.013     Document Type: Article

References (53)

1. J.P. Abrahams, S.K. Buchanan, M.J. Van Raaij, I.M. Fearnley, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin Proc. Natl. Acad. Sci. USA 93 1996 9420 9424 (Pubitemid 26296623)
2. J.P. Abrahams, A.G. Leslie, R. Lutter, and J.E. Walker Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria Nature 370 1994 621 628
3. K. Adachi, K. Oiwa, T. Nishizaka, S. Furuike, H. Noji, H. Itoh, M. Yoshida, and K. Kinosita Jr. Coupling of rotation and catalysis in F(1)-ATPase revealed by single-molecule imaging and manipulation Cell 130 2007 309 321 (Pubitemid 47086326)
4. R.A. Bockmann, and H. Grubmuller Nanoseconds molecular dynamics simulation of primary mechanical energy transfer steps in F1-ATP synthase Nat. Struct. Biol. 9 2002 198 202 (Pubitemid 34171312)
5. M.W. Bowler, M.G. Montgomery, A.G. Leslie, and J.E. Walker How azide inhibits ATP hydrolysis by the F-ATPases Proc. Natl. Acad. Sci. USA 103 2006 8646 8649 (Pubitemid 43878074)
6. M.W. Bowler, M.G. Montgomery, A.G. Leslie, and J.E. Walker Ground state structure of F1-ATPase from bovine heart mitochondria at 1.9 A resolution J. Biol. Chem. 282 2007 14238 14242 (Pubitemid 47100445)
7. P.D. Boyer The ATP synthase - a splendid molecular machine Annu. Rev. Biochem. 66 1997 717 749 (Pubitemid 27274672)
8. K. Braig, R.I. Menz, M.G. Montgomery, A.G. Leslie, and J.E. Walker Structure of bovine mitochondrial F(1)-ATPase inhibited by Mg(2+) ADP and aluminium fluoride Structure 8 2000 567 573 (Pubitemid 30409309)
9. E. Cabezon, M.G. Montgomery, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase in complex with its regulatory protein IF1 Nat. Struct. Biol. 10 2003 744 750 (Pubitemid 37052414)
10. Q. Cui, G. Li, J. Ma, and M. Karplus A normal mode analysis of structural plasticity in the biomolecular motor F(1)-ATPase J. Mol. Biol. 340 2004 345 372 (Pubitemid 38759915)
11. M. Dittrich, S. Hayashi, and K. Schulten On the mechanism of ATP hydrolysis in F1-ATPase Biophys. J. 85 2003 2253 2266
12. M. Dittrich, S. Hayashi, and K. Schulten ATP hydrolysis in the betaTP and betaDP catalytic sites of F1-ATPase Biophys. J. 87 2004 2954 2967
13. Y.Q. Gao, W. Yang, and M. Karplus A structure-based model for the synthesis and hydrolysis of ATP by F-1-ATPase Cell 123 2005 195 205 (Pubitemid 41457211)
14. C. Gibbons, M.G. Montgomery, A.G. Leslie, and J.E. Walker The structure of the central stalk in bovine F(1)-ATPase at 2.4 A resolution Nat. Struct. Biol. 7 2000 1055 1061
15. J.R. Gledhill, M.G. Montgomery, A.G. Leslie, and J.E. Walker How the regulatory protein, IF(1), inhibits F(1)-ATPase from bovine mitochondria Proc. Natl. Acad. Sci. USA 104 2007 15671 15676 (Pubitemid 350035358)
16. J.R. Gledhill, M.G. Montgomery, A.G. Leslie, and J.E. Walker Mechanism of inhibition of bovine F1-ATPase by resveratrol and related polyphenols Proc. Natl. Acad. Sci. USA 104 2007 13632 13637 (Pubitemid 350003372)
17. A.A. Gorfe, B.J. Grant, and J.A. McCammon Mapping the nucleotide and isoform-dependent structural and dynamical features of Ras proteins Structure 16 2008 885 896 (Pubitemid 351778381)
18. B.J. Grant, J.A. McCammon, L.S. Caves, and R.A. Cross Multivariate analysis of conserved sequence-structure relationships in kinesins: coupling of the active site and a tubulin-binding sub-domain J. Mol. Biol. 368 2007 1231 1248 (Pubitemid 46617587)
19. M.J. Gresser, J.A. Myers, and P.D. Boyer Catalytic site 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
20. S. Hayward, and H.J. Berendsen Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme Proteins 30 1998 144 154 (Pubitemid 28080149)
21. Y. Hirono-Hara, K. Ishizuka, K. Kinosita Jr., M. Yoshida, and H. Noji Activation of pausing F1 motor by external force Proc. Natl. Acad. Sci. USA 102 2005 4288 4293 (Pubitemid 40397104)
22. Y. Ito, and M. Ikeguchi Molecular dynamics simulations of the isolated beta subunit of F-1-ATPase Chem. Phys. Lett. 490 2010 80 83
23. H. Itoh, A. Takahashi, K. Adachi, H. Noji, R. Yasuda, M. Yoshida, and K. Kinosita Mechanically driven ATP synthesis by F1-ATPase Nature 427 2004 465 468 (Pubitemid 38168502)
24. I.T. Jolliffe Principal Component Analysis 2002 Springer New York
25. W. Junge, H. Sielaff, and S. Engelbrecht Torque generation and elastic power transmission in the rotary F(O)F(1)-ATPase Nature 459 2009 364 370
26. V. Kabaleeswaran, N. Puri, J.E. Walker, A.G. Leslie, and D.M. Mueller Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase EMBO J. 25 2006 5433 5442 (Pubitemid 44764152)
27. V. Kabaleeswaran, H. Shen, J. Symersky, J.E. Walker, A.G. Leslie, and D.M. Mueller Asymmetric structure of the yeast F1 ATPase in the absence of bound nucleotides J. Biol. Chem. 284 2009 10546 10551
28. R. Kagawa, M.G. Montgomery, K. Braig, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase inhibited by ADP and beryllium fluoride EMBO J. 23 2004 2734 2744 (Pubitemid 39013546)
29. K. Kinosita Jr., K. Adachi, and H. Itoh Rotation of F1-ATPase: how an ATP-driven molecular machine may work Annu. Rev. Biophys. Biomol. Struct. 33 2004 245 268 (Pubitemid 38829960)
30. N. Koga, and S. Takada Folding-based molecular simulations reveal mechanisms of the rotary motor F1-ATPase Proc. Natl. Acad. Sci. USA 103 2006 5367 5372
31. T. Masaike, F. Koyama-Horibe, K. Oiwa, M. Yoshida, and T. Nishizaka Cooperative three-step motions in catalytic subunits of F(1)-ATPase correlate with 80 degrees and 40 degrees substep rotations Nat. Struct. Mol. Biol. 15 2008 1326 1333
32. R.I. Menz, A.G. Leslie, and J.E. Walker The structure and nucleotide occupancy of bovine mitochondrial F(1)-ATPase are not influenced by crystallization at high concentrations of nucleotide FEBS Lett. 494 2001 11 14 (Pubitemid 32289362)
33. R.I. Menz, J.E. Walker, and A.G. Leslie Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis Cell 106 2001 331 341 (Pubitemid 32772617)
34. T. Nishizaka, K. Oiwa, H. Noji, S. Kimura, E. Muneyuki, M. Yoshida, and K. Kinosita Jr. Chemomechanical coupling in F1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation Nat. Struct. Mol. Biol. 11 2004 142 148 (Pubitemid 38146517)
35. H. Noji, R. Yasuda, M. Yoshida, and K. Kinosita Jr. Direct observation of the rotation of F1-ATPase Nature 386 1997 299 302
36. D. Okuno, R. Fujisawa, R. Iino, Y. Hirono-Hara, H. Imamura, and H. Noji Correlation between the conformational states of F1-ATPase as determined from its crystal structure and single-molecule rotation Proc. Natl. Acad. Sci. USA 105 2008 20722 20727
37. G.L. Orriss, A.G. Leslie, K. Braig, and J.E. Walker Bovine F1-ATPase covalently inhibited with 4-chloro-7-nitrobenzofurazan: the structure provides further support for a rotary catalytic mechanism Structure 6 1998 831 837 (Pubitemid 28348646)
38. J. Pu, and M. Karplus How subunit coupling produces the gamma-subunit rotary motion in F1-ATPase Proc. Natl. Acad. Sci. USA 105 2008 1192 1197 (Pubitemid 351397029)
39. D.M. Rees, A.G. Leslie, and J.E. Walker The structure of the membrane extrinsic region of bovine ATP synthase Proc. Natl. Acad. Sci. USA 106 2009 21597 21601
40. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680 (Pubitemid 24354800)
41. M.J. van Raaij, J.P. Abrahams, A.G. Leslie, and J.E. Walker The structure of bovine F1-ATPase complexed with the antibiotic inhibitor aurovertin B Proc. Natl. Acad. Sci. USA 93 1996 6913 6917 (Pubitemid 26243474)
42. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT - a program to generate schematic diagrams of protein ligand interactions Protein Eng. 8 1995 127 134
43. H. Wang, and G. Oster Energy transduction in the F1 motor of ATP synthase Nature 396 1998 279 282 (Pubitemid 28541394)
44. R. Watanabe, R. Iino, and H. Noji Phosphate release in F-1-ATPase catalytic cycle follows ADP release Nat. Chem. Biol. 6 2010 814 820
45. J. Weber, and A.E. Senior ATP synthase: what we know about ATP hydrolysis and what we do not know about ATP synthesis Biochim. Biophys. Acta 1458 2000 300 309 (Pubitemid 30320713)
46. S. Wilkens, F.W. Dahlquist, L.P. McIntosh, L.W. Donaldson, and R.A. Capaldi Structural features of the epsilon subunit of the Escherichia coli ATP synthase determined by NMR spectroscopy Nat. Struct. Biol. 2 1995 961 967
47. H. Yagi, T. Tsujimoto, T. Yamazaki, M. Yoshida, and H. Akutsu Conformational change of H+-ATPase beta monomer revealed on segmental isotope labeling NMR spectroscopy J. Am. Chem. Soc. 126 2004 16632 16638 (Pubitemid 40081965)
48. W. Yang, Y.Q. Gao, Q. Cui, J. Ma, and M. Karplus The missing link between thermodynamics and structure in F1-ATPase Proc. Natl. Acad. Sci. USA 100 2003 874 879 (Pubitemid 36183923)
49. L. Yang, G. Song, A. Carriquiry, and R.L. Jernigan Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes Structure 16 2008 321 330 (Pubitemid 351215213)
50. Y. Yang, H. Yu, and Q. Cui Extensive conformational transitions are required to turn on ATP hydrolysis in myosin J. Mol. Biol. 381 2008 1407 1420
51. R. Yasuda, H. Noji, M. Yoshida, K. Kinosita Jr., and H. Itoh Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase Nature 410 2001 898 904 (Pubitemid 32335828)
52. W. Zheng Normal-mode-based modeling of allosteric couplings that underlie cyclic conformational transition in F(1) ATPase Proteins 76 2009 747 762
53. W. Zheng, and B.R. Brooks Probing the local dynamics of nucleotide-binding pocket coupled to the global dynamics: myosin versus kinesin Biophys. J. 89 2005 167 178 (Pubitemid 41098273)