Controlled rotation of the F 1 -ATPase reveals differential and continuous binding changes for ATP synthesis

Nature Communications

Volumn 3, Issue , 2012, Pages

  Adachi, Kengo ^a,e   Oiwa, Kazuhiro ^b   Yoshida, Masasuke ^c,d   Nishizaka, Takayuki ^a   Kinosita, Kazuhiko ^e  

^a GAKUSHUIN UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFORMATION AND COMMUNICATIONS TECHNOLOGY   (Japan)

^c KYOTO SANGYO UNIVERSITY   (Japan)

^d ATP synthesis Regulation Project   (Japan)

^e WASEDA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; BINDING KINETICS; CONTROLLED STUDY; HYDROLYSIS; MAGNET; NONHUMAN; PROTEIN BINDING; ROTATION;

EID: 84866110008     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2026     Document Type: Article

References (39)

1. Boyer, P. D. The binding change mechanism for ATP synthase-some probabilities and possibilities. Biochim. Biophys. Acta. 1140, 215-250 (1993). (Pubitemid 23015689)
2. Yoshida, M., Muneyuki, E. & Hisabori, T. Nat. Rev. Mol. Cell Biol. 2, 669-677 (2001).
3. Senior, A. E., Nadanaciva, S. & Weber, J. The molecular mechanism of ATP synthesis by F1F0-ATP synthase. Biochim. Biophys. Acta. 1553, 188-211 (2002). (Pubitemid 34460564)
4. Kinosita, K. Jr., Adachi, K. & Itoh, H. Rotation of F1-ATPase: how an ATP-driven molecular machine may work. Annu. Rev. Biophys. Biomol. Struct. 33, 245-268 (2004). (Pubitemid 38829960)
5. Junge, W., Sielaff, H. & Engelbrecht, S. Torque generation and elastic power transmission in the rotary FOF1-ATPase. Nature 459, 364-370 (2009).
6. Adachi, K. et al. Chemo-mechanical coupling in the rotary molecular motor F1-ATPase. In Single Molecule Spectroscopy in Chemistry, Physics and Biology, Vol 96 (eds Gräslund, A., Rigler, R. & Widengren, J.) 271-285 (Springer, Berlin, Heidelberg, 2010).
7. Noji, H., Yasuda, R., Yoshida, M. & Kinosita, K. Jr. Direct observation of the rotation of F1-ATPase. Nature 386, 299-302 (1997).
8. Boyer, P. D. & Kohlbrenner, W. E. The present status of the binding-change mechanism and its relation to ATP formation by chloroplasts. In Energy Coupling in Photosynthesis (eds Selman, B.R. & Selman-Reimer, S.) 231-240 (Elsevier, 1981).
9. Oosawa, F. & Hayashi, S. The loose coupling mechanism in molecular machines of living cells. Adv. Biophys. 22, 151-183 (1986).
10. Abrahams, J. P., Leslie, A. G. W., Lutter, R. & Walker, J. E. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621-628 (1994).
11. Itoh, H. et al. Mechanically driven ATP synthesis by F1-ATPase. Nature 427, 465-468 (2004). (Pubitemid 38168502)
12. Rondelez, Y. et al. Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433, 773-777 (2005). (Pubitemid 40292989)
13. Yasuda, R., Noji, H., Kinosita, K. Jr. & Yoshida, M. F1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps. Cell 93, 1117-1124 (1998). (Pubitemid 28307417)
14. Yasuda, R., Noji, H., Yoshida, M., Kinosita, K. Jr. & Itoh, H. Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410, 898-904 (2001). (Pubitemid 32335828)
15. Adachi, K. et al. Coupling of rotation and catalysis in F1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321 (2007). (Pubitemid 47086326)
16. Furuike, S. et al. Axle-less F1-ATPase rotates in the correct direction. Science 319, 955-958 (2008). (Pubitemid 351263766)
17. Uchihashi, T., Iino, R., Ando, T. & Noji, H. High-speed atomic force microscopy reveals rotary catalysis of rotorless F1-ATPase. Science 333, 755-758 (2011).
18. Shimo-Kon, R. et al. Chemo-mechanical coupling in F1-ATPase revealed by catalytic site occupancy during catalysis. Biophys. J. 98, 1227-1236 (2010).
19. Watanabe, R., Iino, R. & Noji, H. Phosphate release in F1-ATPase catalytic cycle follows ADP release. Nat. Chem. Biol. 6, 814-820 (2010).
20. Oiwa, K. et al. Comparative single-molecule and ensemble myosin enzymology: sulfoindocyanine ATP and ADP derivatives. Biophys. J. 78, 3048-3071 (2000). (Pubitemid 30396935)
21. Oiwa, K. et al. The 2′-O- and 3′-O-Cy3-EDA-ATP(ADP) complexes with myosin subfragment-1 are spectroscopically distinct. Biophys. J. 84, 634-642 (2003). (Pubitemid 36026431)
22. Funatsu, T., Harada, Y., Tokunaga, M., Saito, K. & Yanagida, T. Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature 374, 555-559 (1995).
23. Watanabe-Nakayama, T. et al. Effect of external torque on the ATP-driven rotation of F1-ATPase. Biochem. Biophys. Res. Commun. 366, 951-957 (2008).
24. Iko, Y., Tabata, K. V., Sakakihara, S., Nakashima, T. & Noji, H. Acceleration of the ATP-binding rate of F1-ATPase by forcible forward rotation. FEBS Lett. 583, 3187-3191 (2009).
25. Watanabe, R. et al. Mechanical modulation of catalytic power on F1-ATPase. Nat. Chem. Biol. 8, 86-92 (2012).
26. Koshland, D. E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl Acad. Sci. USA 44, 98-104 (1958).
27. Yasuda, R. et al. The ATP-waiting conformation of rotating F1-ATPase revealed by single-pair fluorescence resonance energy transfer. Proc. Natl Acad. Sci. USA 100, 9314-9318 (2003). (Pubitemid 37033925)
28. Masaike, T., Koyama-Horibe, F., Oiwa, K., Yoshida, M. & Nishizaka, T. Cooperative three-step motions in catalytic subunits of F1-ATPase correlate with 80° and 40° substep rotations. Nat. Struct. Mol. Biol. 15, 1326-1333 (2008).
29. Sielaff, H., Rennekamp, H., Engelbrecht, S. & Junge, W. Functional halt positions of rotary FOF1-ATPase correlated with crystal structures. Biophys. J. 95, 4979-4987 (2008).
30. Okuno, D. et al. Correlation between the conformational states of F1-ATPase as determined from its crystal structure and single-molecule rotation. Proc. Natl Acad. Sci. USA 105, 20722-20727 (2008).
31. Shimabukuro, K. et al. Catalysis and rotation of F1 motor: cleavage of ATP at the catalytic site occurs in 1 ms before 40° substep rotation. Proc. Natl Acad. Sci. USA 100, 14731-14736 (2003). (Pubitemid 37517959)
32. Nishizaka, T. et al. Chemomechanical coupling in F1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Mol. Biol. 11, 142-148 (2004). (Pubitemid 38146517)
33. Ariga, T., Muneyuki, E. & Yoshida, M. F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat. Struct. Mol. Biol. 14, 841-846 (2007). (Pubitemid 47373838)
34. Shimabukuro, K., Muneyuki, E. & Yoshida, M. An alternative reaction pathway of F1-ATPase suggested by rotation without 80°/40° substeps of a sluggish mutant at low ATP. Biophys. J. 90, 1028-1032 (2006).
35. Adachi, K. et al. Stepping rotation of F1-ATPase visualized through angle-resolved single-fluorophore imaging. Proc. Natl Acad. Sci. USA 97, 7243-7247 (2000). (Pubitemid 30431448)
36. Sakaki, N. et al. One rotary mechanism for F1-ATPase over ATP concentrations from millimolar down to nanomolar. Biophys. J. 88, 2047-2056 (2005). (Pubitemid 40976214)
37. Soga, N., Kinosita, K. Jr., Yoshida, M. & Suzuki, T. Efficient ATP synthesis by thermophilic Bacillus FoF1-ATP synthase. FEBS J. 278, 2647-2654 (2011).
38. Zimmermann, B., Diez, M., Zarrabi, N., Gr?ber, P. & B?rsch, M. Movements of the ?-subunit during catalysis and activation in single membrane-bound H+-ATP synthase. EMBO J. 24, 2053-2063 (2005). (Pubitemid 40961790)
39. Noji, H. et al. Purine but not pyrimidine nucleotides support rotation of F1-ATPase. J. Biol. Chem. 276, 25480-25486 (2001).