Robustness of the rotary catalysis mechanism of F1-ATPase

Journal of Biological Chemistry

Volumn 289, Issue 28, 2014, Pages 19331-19340

  Watanabe, Rikiya ^a,b   Matsukage, Yuki ^c   Yukawa, Ayako ^a   Tabata, Kazuhito V ^a,b   Noji, Hiroyuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE;

CATALYSIS MECHANISMS; CHARGED RESIDUES; ENERGY COUPLINGS; NUCLEOPHILIC ATTACK; ROTARY MOTIONS; ROTATIONAL VELOCITY; SINGLE-MOLECULE; TORQUE GENERATION;

CATALYSIS;

ARGININE; GLUTAMIC ACID; LYSINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CATALYSIS; CHEMICAL REACTION; CHEMO MECHANICAL ENERGY COUPLING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME MECHANISM; HYDROGEN BOND; HYDROLYSIS; MICHAELIS CONSTANT; MICHAELIS MENTEN KINETICS; PRIORITY JOURNAL; PROTEIN FUNCTION; TORQUE; VELOCITY; WILD TYPE;

ATP SYNTHASE; BIOENERGETICS; F1FO-ATPASE; MOLECULAR MOTOR; SINGLE-MOLECULE BIOPHYSICS;

ADENOSINE TRIPHOSPHATE; CATALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTON-TRANSLOCATING ATPASES;

EID: 84904197168     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.569905     Document Type: Article

References (49)

1. Vale, R. D., and Milligan, R. A. (2000) The way things move: looking under the hood of molecular motor proteins. Science 288, 88-95
2. + proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6, 519-529
3. Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982) Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1, 945-951
4. 1-ATP synthase: general structural features of 'ATP-engine' and a problem on free energy transduction. Biochim. Biophys. Acta 1458, 467-481
5. 1-ATPase revealed by molecular simulations and single-molecule observations. J. Am. Chem. Soc. 134, 8447-8454
6. McGrath, M. J., Kuo, I. F., Hayashi, S., and Takada, S. (2013) Adenosine triphosphate hydrolysis mechanism in kinesin studied by combined quantum-mechanical/molecular-mechanical metadynamics simulations. J. Am. Chem. Soc. 135, 8908-8919
7. Scheffzek, K., Ahmadian, M. R., Kabsch, W., Wiesmüller, L., Lautwein, A., Schmitz, F., and Wittinghofer, A. (1997) The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277, 333-338 (Pubitemid 27450699)
8. 1-ATPase from bovine heart mitochondria. Nature 370, 621-628
9. Chen, Z., Yang, H., and Pavletich, N. P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489-494 (Pubitemid 351733325)
10. 1-ATPase β subunit revealed by NMR. J. Biol. Chem. 284, 2374-2382
11. 1-ATPase β-subunit. J. Biol. Chem. 267, 21471-21478
12. Li, X. D., Rhodes, T. E., Ikebe, R., Kambara, T., White, H. D., and Ikebe, M. (1998) Effects of mutations in the γ-phosphate binding site of myosin on its motor function. J. Biol. Chem. 273, 27404-27411 (Pubitemid 28500458)
13. Yoshida, M., Muneyuki, E., and Hisabori, T. (2001) ATP synthase-a marvelous rotary engine of the cell. Nat. Rev. Mol. Cell Biol. 2, 669-677 (Pubitemid 33674070)
14. 1-ATPase. Nature 459, 364-370
15. 1-ATPase reveal an interdependence between the power stroke and the dwell duration. Biochemistry 48, 7979-7985
16. 1 sector rotation. Defective torque generation in the β subunit Ser-174 to Phe mutant and its suppression by second mutations. J. Biol. Chem. 276, 47508-47511
17. Cherepanov, D. A., and Junge, W. (2001) Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: curvature as an indicator of the torque. Biophys. J. 81, 1234-1244 (Pubitemid 32783568)
18. 1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 93, 1117-1124
19. 1-ATPase. Phys. Rev. Lett. 104, 218103
20. 1-ATPase. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120023
21. 1-ATPase single molecules. Nature 433, 773-777
22. 1-ATPase. Nature 427, 465-468
23. Weber, J. (2010) Structural biology: Toward the ATP synthase mechanism. Nat. Chem. Biol. 6, 794-795
24. Yasuda, R., Noji, H., Yoshida, M., Kinosita, K., Jr., and Itoh, H. (2001) Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410, 898-904 (Pubitemid 32335828)
25. 1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40 degree substep rotation. Proc. Natl. Acad. Sci. U.S.A. 100, 14731-14736
26. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321
27. 1-ATPase catalytic cycle follows ADP release. Nat. Chem. Biol. 6, 814-820
28. 1-ATPase. Residues involved in catalysis and coupling. Ann. N.Y. Acad. Sci. 671, 335-343
29. 1-ATPase inhibited by ADP and beryllium fluoride. EMBO J. 23, 2734-2744
30. Kabaleeswaran, V., Puri, N., Walker, J. E., Leslie, A. G., and Mueller, D. M. (2006) Novel features of the rotary catalytic mechanism revealed in the structure of yeast F1 ATPase. EMBO J. 25, 5433-5442 (Pubitemid 44764152)
31. 1) from Escherichia coli in an autoinhibited conformation. Nat. Struct. Mol. Biol. 18, 701-707
32. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 100, 874-879
33. 1-ATPase. Biophys. J. 87, 2954-2967
34. 1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 108, 20550-20555
35. 1-ATPase β subunit probed by introducing different carboxylate-containing side chains. FEBS Lett. 348, 93-98
36. Le, N. P., Omote, H., Wada, Y., Al-Shawi, M. K., Nakamoto, R. K., and Futai, M. (2000) Escherichia coli ATP synthase α subunit Arg-376: the catalytic site arginine does not participate in the hydrolysis/synthesis reaction but is required for promotion to the steady state. Biochemistry 39, 2778-2783 (Pubitemid 30148933)
37. 1-ATPase, roles of three catalytic site residues. J. Biol. Chem. 272, 3648-3656
38. 1-ATPase. Eur. Biophys. J. 39, 1589-1596
39. 1-ATPase. J. Biol. Chem. 287, 15134-15142
40. 1 motor by external force. Proc. Natl. Acad. Sci. U.S.A. 102, 4288-4293
41. Yildiz, A., Forkey, J. N., McKinney, S. A., Ha, T., Goldman, Y. E., and Selvin, P. R. (2003) Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300, 2061-2065 (Pubitemid 36760126)
42. Sun, Y., Sato, O., Ruhnow, F., Arsenault, M. E., Ikebe, M., and Goldman, Y. E. (2010) Single-molecule stepping and structural dynamics of myosin X. Nat. Struct. Mol. Biol. 17, 485-491
43. Cho, C., Reck-Peterson, S. L., and Vale, R. D. (2008) Regulatory ATPase sites of cytoplasmic dynein affect processivity and force generation. J. Biol. Chem. 283, 25839-25845
44. 1-ATPase. Biophys. J. 103, 970-978
45. 1-ATPase. J. Biol. Chem. 276, 25480-25486
46. 1-ATPase powered rotation. Proc. Natl. Acad. Sci. U.S.A. 111, 3715-3720
47. 1. J. Biol. Chem. 287, 1884-1891
48. 1-ATPase devoid of the entire amino-terminal helix of the rotor that fills half of the stator orifice. Biophys. J. 101, 188-195
49. Watanabe, R., and Noji, H. (2014) Timing of inorganic phosphate release modulates the catalytic activity of ATP-driven rotary motor protein. Nat. Commun. 5, 3486