Principal role of the arginine finger in rotary catalysis of F 1-ATPase

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 15134-15142

  Komoriya, Yoshihito ^a   Ariga, Takayuki ^b   Iino, Ryota ^b   Imamura, Hiromi ^a   Okuno, Daichi ^a   Noji, Hiroyuki ^b  

^a OSAKA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ATP ANALOGS; ATP HYDROLYSIS; ATP-BINDING; CATALYTIC RESIDUE; CATALYTIC SITES; COOPERATIVITY; COUPLING RATIOS; REACTION STEPS; ROTARY MOTOR; STATOR RINGS; TORQUE GENERATION; TRANSITION STATE; UNIDIRECTIONAL ROTATION; WILD TYPES;

HYDROLYSIS;

ARGININE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ARGININE; LYSINE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

AMINO ACID ANALYSIS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BETA CHAIN; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; HYDROLYSIS; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN STABILITY; WILD TYPE;

ADENOSINE TRIPHOSPHATE; AMINO ACID SUBSTITUTION; BACILLUS; BACTERIAL PROTEINS; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; PROTON-TRANSLOCATING ATPASES;

EID: 84860359572     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.328153     Document Type: Article

References (44)

1. Kinosita, K., Jr., Yasuda, R., and Noji, H. (2000) F1-ATPase: a highly efficient rotary ATP machine. Essays Biochem. 35, 3-18 (Pubitemid 33203771)
2. Nakamoto, R. K., Baylis Scanlon, J. A., and Al-Shawi, M. K. (2008) The rotary mechanism of the ATP synthase. Arch Biochem. Biophys 476, 43-50
3. 0-ATP synthase. Biochim Biophys Acta 1553, 188-211
4. 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)
5. 1-ATP synthase. EMBO J. 28, 2689-2696
6. Noji, H., Yasuda, R., Yoshida, M., and Kinosita, K., Jr. (1997) Direct observation of the rotation of F1-ATPase. Nature 386, 299-302
7. Spetzler, D., York, J., Daniel, D., Fromme, R., Lowry, D., and Frasch, W. (2006) Microsecond time scale rotation measurements of single F1-ATPase molecules. Biochemistry 45, 3117-3124 (Pubitemid 43376330)
8. 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)
9. Omote, H., Sambonmatsu, N., Saito, K., Sambongi, Y., Iwamoto-Kihara, A., Yanagida, T., Wada, Y., and Futai, M. (1999) The γ-subunit rotation and torque generation in F1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 96, 7780-7784 (Pubitemid 29328358)
10. Uchihashi, T., Iino, R., Ando, T., and Noji, H. (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755-758
11. Watanabe, R., Iino, R., and Noji, H. (2010) Phosphate release in F1-ATPase catalytic cycle follows ADP release. Nat. Chem. Biol. 6, 814-820
12. Weber, J. (2010) Structural biology: Toward the ATP synthase mechanism. Nat. Chem. Biol. 6, 794-795
13. Ariga, T., Muneyuki, E., and Yoshida, M. (2007) F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat Struct Mol Biol 14, 841-846 (Pubitemid 47373838)
14. Adachi, K., Oiwa, K., Nishizaka, T., Furuike, S., Noji, H., Itoh, H., Yoshida, M., and Kinosita, K., Jr. (2007) Coupling of rotation and catalysis in F(1)-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321 (Pubitemid 47086326)
15. Abrahams, J. P., Leslie, A. G., Lutter, R., and Walker, J. E. (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621-628
16. 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 (Pubitemid 43878074)
17. Sielaff, H., Rennekamp, H., Engelbrecht, S., and Junge, W. (2008) Functional halt positions of rotary FOF1-ATPase correlated with crystal structures. Biophys. J. 95, 4979-4987
18. Okuno, D., Fujisawa, R., Iino, R., Hirono-Hara, Y., Imamura, H., and Noji, H. (2008) Correlation between the conformational states of F1-ATPase as determined from its crystal structure and single-molecule rotation. Proc. Natl. Acad. Sci. U.S.A. 105, 20722-20727
19. Masaike, T., Koyama-Horibe, F., Oiwa, K., Yoshida, M., and Nishizaka, T. (2008) 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, 1326-1333
20. Oster, G., and Wang, H. (2000) Reverse engineering a protein: the mechanochemistry of ATP synthase. Biochim Biophys Acta 1458, 482-510 (Pubitemid 30320727)
21. Kagawa, R., Montgomery, M. G., Braig, K., Leslie, A. G., and Walker, J. E. (2004) The structure of bovine F1-ATPase inhibited by ADP and beryllium fluoride. EMBO J. 23, 2734-2744 (Pubitemid 39013546)
22. Menz, R. I., Walker, J. E., and Leslie, A. G. (2001) Structure of bovine mitochondrial F(1)-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106, 331-341 (Pubitemid 32772617)
23. Mao, H. Z., and Weber, J. (2007) Identification of the βTP site in the x-ray structure of F1-ATPase as the high-affinity catalytic site. Proc. Natl. Acad. Sci. U.S.A. 104, 18478-18483 (Pubitemid 350210722)
24. Noel, J. P., Hamm, H. E., and Sigler, P. B. (1993) The 2.2 A crystal structure of transducin-α complexed with GTPγS. Nature 366, 654-663
25. 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)
26. Soga, S., Noumi, T., Takeyama, M., Maeda, M., and Futai, M. (1989) Mutational replacements of conserved amino acid residues in the α subunit change the catalytic properties of Escherichia coli F1-ATPase. Arch. Biochem. Biophys. 268, 643-648 (Pubitemid 19049743)
27. 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)
28. Nadanaciva, S., Weber, J., Wilke-Mounts, S., and Senior, A. E. (1999) Importance of F1-ATPase residue α-Arg-376 for catalytic transition state stabilization. Biochemistry 38, 15493-15499 (Pubitemid 129503589)
29. Turina, P., Aggeler, R., Lee, R. S., Senior, A. E., and Capaldi, R. A. (1993) The cysteine introduced into the α subunit of the Escherichia coli F1-ATPase by the mutation α R376C is near the αβ subunit interface and close to a noncatalytic nucleotide binding site. J. Biol. Chem. 268, 6978-6984 (Pubitemid 23105581)
30. Dittrich, M., Hayashi, S., and Schulten, K. (2003) On the mechanism of ATP hydrolysis in F1-ATPase. Biophys. J. 85, 2253-2266
31. Yang, W., Gao, Y. Q., Cui, Q., Ma, J., and Karplus, M. (2003) The missing link between thermodynamics and structure in F1-ATPase. Proc. Natl. Acad. Sci. U.S.A. 100, 874-879 (Pubitemid 36183923)
32. Enoki, S., Watanabe, R., Iino, R., and Noji, H. (2009) Single-molecule study on the temperature-sensitive reaction of F1-ATPase with a hybrid F1 carrying a single β(E190D). J. Biol. Chem. 284, 23169-23176
33. Digel, J. G., Kishinevsky, A., Ong, A. M., and McCarty, R. E. (1996) Differences between two tight ADP binding sites of the chloroplast coupling factor 1 and their effects on ATPase activity. J. Biol. Chem. 271, 19976-19982 (Pubitemid 26281745)
34. 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. U.S.A. 102, 4288-4293 (Pubitemid 40397104)
35. Toyabe, S., Okamoto, T., Watanabe-Nakayama, T., Taketani, H., Kudo, S., and Muneyuki, E. Nonequilibrium energetics of a single F1-ATPase molecule. Phys. Rev. Lett. 104:198103, 2010
36. Noji, H., Bald, D., Yasuda, R., Itoh, H., Yoshida, M., and Kinosita, K., Jr. (2001) Purine but not pyrimidine nucleotides support rotation of F(1)-ATPase. J. Biol. Chem. 276, 25480-25486
37. 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. U.S.A. 98, 13649-13654
38. Watanabe, R., Okuno, D., Sakakihara, S., Shimabukuro, K., Iino, R., Yoshida, M., and Noji, H. (2012) Mechanical modulation of catalytic power on F(1)-ATPase. Nat. Chem. Biol. 8, 86-92
39. Iko, Y., Tabata, K. V., Sakakihara, S., Nakashima, T., and Noji, H. (2009) Acceleration of the ATP-binding rate of F1-ATPase by forcible forward rotation. FEBS Lett. 583, 3187-3191
40. Shimabukuro, K., Yasuda, R., Muneyuki, E., Hara, K. Y., Kinosita, K., Jr.,and Yoshida, M. (2003) Catalysis and rotation of F1 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 (Pubitemid 37517959)
41. Ahmad, Z., and Senior, A. E. (2005) Identification of phosphate binding residues of Escherichia coli ATP synthase. J. Bioenerg. Biomembr. 37, 437-440 (Pubitemid 43725172)
42. 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)
43. Kabaleeswaran, V., Shen, H., Symersky, J., Walker, J. E., Leslie, A. G., and Mueller, D. M. (2009) Asymmetric structure of the yeast F1 ATPase in the absence of bound nucleotides. J. Biol. Chem. 284, 10546 -10551
44. Shimo-Kon, R., Muneyuki, E., Sakai, H., Adachi, K., Yoshida, M., and Kinosita, K., Jr. (2010) Chemo-mechanical coupling in F(1)-ATPase revealed by catalytic site occupancy during catalysis. Biophys. J. 98, 1227-1236