Cooperative three-step motions in catalytic subunits of F 1-ATPase correlate with 80° and 40° substep rotations

Nature Structural and Molecular Biology

Volumn 15, Issue 12, 2008, Pages 1326-1333

  Masaike, Tomoko ^a   Koyama Horibe, Fumie ^a   Oiwa, Kazuhiro ^b   Yoshida, Masasuke ^c,d   Nishizaka, Takayuki ^a,e  

^a GAKUSHUIN UNIVERSITY   (Japan)

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

^c TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DICYCLOHEXYLCARBODIIMIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SUBUNIT; FLUORESCENCE MICROSCOPY; MOLECULAR DYNAMICS; MOLECULE; MOTION; PRIORITY JOURNAL; ROTATION;

CATALYTIC DOMAIN; MICROSCOPY, FLUORESCENCE; PROTEIN CONFORMATION; PROTON-TRANSLOCATING ATPASES; ROTATION; STAINING AND LABELING;

EID: 57149107555     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1510     Document Type: Article

References (51)

1. 1-ATPase. Nature 386, 299-302 (1997).
2. 1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps. Cell 93, 1117-1124 (1998).
3. 1-ATPase. Nature 410, 898-904 (2001).
4. 1 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).
5. 1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321 (2007).
6. 1-ATPase. EMBO Rep. 9, 84-90 (2008).
7. 1-ATPase. Biophys. J. 95, 761-770 (2008).
8. 1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits. Nat. Struct. Mol. Biol. 14, 841-846 (2007).
9. 1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation. Nat. Struct. Mol. Biol. 11, 142-148 (2004).
10. Weber, J. & Senior, A.E. ATP synthase: what we know about ATP hydrolysis and what we do not know about ATP synthesis. Biochim. Biophys. Acta 1458, 300-309 (2000).
11. 1-ATPase. Biochim. Biophys. Acta 1607, 35-44 (2003).
12. 1-ATPase does not hydolyze ATP at a significant rate until the substrate binds to the catalytic site of the lowest affinity. Biochemistry 45, 6222-6230 (2006).
13. Kayalar, C., Rosing, J. & Boyer, P.D. An alternating site sequence for oxidative phosphorylation suggested by measurement of substrate binding patterns and exchange reaction inhibitions. J. Biol. Chem. 252, 2486-2491 (1977).
14. 1-ATPase from bovine heart mitochondria. Nature 370, 621-628 (1994).
15. 1-ATPase indicates that only two β subunits can exist in the closed conformation simultaneously. J. Biol. Chem. 274, 31366-31372 (1999).
16. 1-ATPase. J. Biol. Chem. 274, 5701-5706 (1999).
17. 1-ATPase β subunit. J. Biochem. 130, 527-533 (2001).
18. +-ATPase β monomer revealed on segmental isotope labeling NMR spectroscopy. J. Am. Chem. Soc. 126, 16632-16638 (2004).
19. 1-ATPase changes its conformations upon phosphate release. J. Biol. Chem. 277, 21643-21649 (2002).
20. 1-ATP synthase in catalysis. Biochem. Biophys. Res. Commun. 342, 800-807 (2006).
21. 1 motor of ATP synthase. Nature 396, 279-282 (1998).
22. 1-ATPase and its implications for the rotational cycle. Biophys. J. 86, 1373-1384 (2004).
23. Forkey, J.N., Quinlan, M.E., Shaw, M.A., Corrie, J.E. & Goldman, Y.E. Three-dimensional structural dynamics of myosin V by single-molecule fluorescence polarization. Nature 422, 399-404 (2003).
24. Tomishige, M., Stuurman, N. & Vale, R.D. Single-molecule observations of neck linker conformational changes in the kinesin motor protein. Nat. Struct. Mol. Biol. 13, 887-894 (2006).
25. Yildiz, A. et al. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science 300, 2061-2065 (2003).
26. Mori, T., Vale, R.D. & Tomishige, M. How kinesin waits between steps. Nature 450, 750-754 (2007).
27. Iino, R., Rondelez, Y., Yoshida, M. & Noji, H. Chemomechanical coupling in single-molecule F-type ATP synthase. J. Bioenerg. Biomembr. 37, 451-454 (2005).
28. +-ATP synthase. EMBO J. 24, 2053-2063 (2005).
29. 3 oligomer fixed by OSCP-b stator via the β DELSEED sequence. J. Bioenerg. Biomembr. 28, 421-431 (1996).
30. 1-ATPase. J. Biol. Chem. 275, 14260-14263 (2000).
31. Corrie, J.E. et al. Dynamic measurement of myosin light-chain-domain tilt and twist in muscle contraction. Nature 400, 425-430 (1999).
32. Ha, T., Enderle, T., Chemla, D.S., Selvin, P.R. & Weiss, S. Single molecule dynamics studied by polarization modulation. Phys. Rev. Lett. 77, 3979-3982 (1996).
33. 1-ATPase β subunit probed by introducing different carboxylate-containing side chains. FEBS Lett. 348, 93-98 (1994).
34. 1-ATPase with one, two, or three altered catalytic sites that bind ATP only slowly. J. Biol. Chem. 277, 24870-24874 (2002).
35. 1-ATPase at 2.4 Å resolution. Nat. Struct. Biol. 7, 1055-1061 (2000).
36. 1-ATPase complexed with the peptide antibiotic efrapeptin. Proc. Natl. Acad. Sci. USA 93, 9420-9424 (1996).
37. 1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc. Natl. Acad. Sci. USA 93, 6913-6917 (1996).
38. 1-ATPase covalently inhibited with 4-chloro-7-nitrobenzofurazan: the structure provides further support for a rotary catalytic mechanism. Structure 6, 831-837 (1998).
39. 2+ ADP and aluminium fluoride. Structure 8, 567-573 (2000).
40. 1-ATPase inhibited by ADP and beryllium fluoride. EMBO J. 23, 2734-2744 (2004).
41. Bowler, M.W., Montgomery, M.G., Leslie, A.G. & Walker, J.E. How azide inhibits ATP hydrolysis by the F-ATPases. Proc. Natl. Acad. Sci. USA 103, 8646-8649 (2006).
42. 1-ATPase from bovine heart mitochondria at 1.9 Å resolution. J. Biol. Chem. 282, 14238-14242 (2007).
43. 1-ATPase. Biochim. Biophys. Acta 1319, 19-58 (1997).
44. Nakamoto, R.K., Baylis Scanlon, J.A. & Al-Shawi, M.K. The rotary mechanism of the ATP synthase. Arch. Biochem. Biophys. 476, 43-50 (2008).
45. 1-ATPase revealed by single-pair fluorescence resonance energy transfer. Proc. Natl. Acad. Sci. USA 100, 9314-9318 (2003).
46. 1-ATPase with nucleotide bound to all three catalytic sites: implications for the mechanism of rotary catalysis. Cell 106, 331-341 (2001).
47. 1-ATPase rotates in the correct direction. Science 319, 955-958 (2008).
48. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T. & Yamaguchi, A. Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature 443, 173-179 (2006).
49. Suno, R. et al. Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol. Cell 22, 575-585 (2006).
50. 1-ATPase during catalysis. Proc. Natl. Acad. Sci. USA 98, 13649-13654 (2001).
51. 1-ATPase. EMBO J. 25, 5433-5442 (2006).