Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Apr 29;355(1396):465–471. doi: 10.1098/rstb.2000.0588

Structural model of F1-ATPase and the implications for rotary catalysis.

A G Leslie 1, J E Walker 1
PMCID: PMC1692760  PMID: 10836500

Abstract

The crystal structure of bovine mitochondrial F1-ATPase is described. Several features of the structure are consistent with the binding change mechanism of catalysis, in which binding of substrates induces conformational changes that result in a high degree of cooperativity between the three catalytic sites. Furthermore, the structure also suggests that catalysis is accompanied by a physical rotation of the centrally placed gamma-subunit relative to the approximately spherical alpha3beta3 subassembly.

Full Text

The Full Text of this article is available as a PDF (572.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abrahams J. P., Buchanan S. K., Van Raaij M. J., Fearnley I. M., Leslie A. G., Walker J. E. The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9420–9424. doi: 10.1073/pnas.93.18.9420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Abrahams J. P., Leslie A. G., Lutter R., Walker J. E. Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature. 1994 Aug 25;370(6491):621–628. doi: 10.1038/370621a0. [DOI] [PubMed] [Google Scholar]
  3. Aggeler R., Cai S. X., Keana J. F., Koike T., Capaldi R. A. The gamma subunit of the Escherichia coli F1-ATPase can be cross-linked near the glycine-rich loop region of a beta subunit when ADP + Mg2+ occupies catalytic sites but not when ATP + Mg2+ is bound. J Biol Chem. 1993 Oct 5;268(28):20831–20837. [PubMed] [Google Scholar]
  4. Amano T., Tozawa K., Yoshida M., Murakami H. Spatial precision of a catalytic carboxylate of F1-ATPase beta subunit probed by introducing different carboxylate-containing side chains. FEBS Lett. 1994 Jul 4;348(1):93–98. doi: 10.1016/0014-5793(94)00588-5. [DOI] [PubMed] [Google Scholar]
  5. Bianchet M. A., Hullihen J., Pedersen P. L., Amzel L. M. The 2.8-A structure of rat liver F1-ATPase: configuration of a critical intermediate in ATP synthesis/hydrolysis. Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11065–11070. doi: 10.1073/pnas.95.19.11065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boyer P. D. The binding change mechanism for ATP synthase--some probabilities and possibilities. Biochim Biophys Acta. 1993 Jan 8;1140(3):215–250. doi: 10.1016/0005-2728(93)90063-l. [DOI] [PubMed] [Google Scholar]
  7. Cross R. L. The mechanism and regulation of ATP synthesis by F1-ATPases. Annu Rev Biochem. 1981;50:681–714. doi: 10.1146/annurev.bi.50.070181.003341. [DOI] [PubMed] [Google Scholar]
  8. Elston T., Wang H., Oster G. Energy transduction in ATP synthase. Nature. 1998 Jan 29;391(6666):510–513. doi: 10.1038/35185. [DOI] [PubMed] [Google Scholar]
  9. Futai M., Noumi T., Maeda M. ATP synthase (H+-ATPase): results by combined biochemical and molecular biological approaches. Annu Rev Biochem. 1989;58:111–136. doi: 10.1146/annurev.bi.58.070189.000551. [DOI] [PubMed] [Google Scholar]
  10. Gogol E. P., Lücken U., Capaldi R. A. The stalk connecting the F1 and F0 domains of ATP synthase visualized by electron microscopy of unstained specimens. FEBS Lett. 1987 Jul 27;219(2):274–278. doi: 10.1016/0014-5793(87)80234-x. [DOI] [PubMed] [Google Scholar]
  11. Junge W., Lill H., Engelbrecht S. ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem Sci. 1997 Nov;22(11):420–423. doi: 10.1016/s0968-0004(97)01129-8. [DOI] [PubMed] [Google Scholar]
  12. Kinosita K., Jr, Yasuda R., Noji H., Ishiwata S., Yoshida M. F1-ATPase: a rotary motor made of a single molecule. Cell. 1998 Apr 3;93(1):21–24. doi: 10.1016/s0092-8674(00)81142-3. [DOI] [PubMed] [Google Scholar]
  13. Noji H., Yasuda R., Yoshida M., Kinosita K., Jr Direct observation of the rotation of F1-ATPase. Nature. 1997 Mar 20;386(6622):299–302. doi: 10.1038/386299a0. [DOI] [PubMed] [Google Scholar]
  14. Orriss G. L., Leslie A. G., Braig K., Walker J. E. Bovine F1-ATPase covalently inhibited with 4-chloro-7-nitrobenzofurazan: the structure provides further support for a rotary catalytic mechanism. Structure. 1998 Jul 15;6(7):831–837. doi: 10.1016/s0969-2126(98)00085-9. [DOI] [PubMed] [Google Scholar]
  15. Park M. Y., Omote H., Maeda M., Futai M. Conserved Glu-181 and Arg-182 residues of Escherichia coli H(+)-ATPase (ATP synthase) beta subunit are essential for catalysis: properties of 33 mutants between beta Glu-161 and beta Lys-201 residues. J Biochem. 1994 Nov;116(5):1139–1145. doi: 10.1093/oxfordjournals.jbchem.a124640. [DOI] [PubMed] [Google Scholar]
  16. Sabbert D., Engelbrecht S., Junge W. Intersubunit rotation in active F-ATPase. Nature. 1996 Jun 13;381(6583):623–625. doi: 10.1038/381623a0. [DOI] [PubMed] [Google Scholar]
  17. Sabbert D., Junge W. Stepped versus continuous rotatory motors at the molecular scale. Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2312–2317. doi: 10.1073/pnas.94.6.2312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Senior A. E. ATP synthesis by oxidative phosphorylation. Physiol Rev. 1988 Jan;68(1):177–231. doi: 10.1152/physrev.1988.68.1.177. [DOI] [PubMed] [Google Scholar]
  19. Senior A. E., al-Shawi M. K. Further examination of seventeen mutations in Escherichia coli F1-ATPase beta-subunit. J Biol Chem. 1992 Oct 25;267(30):21471–21478. [PubMed] [Google Scholar]
  20. Shirakihara Y., Leslie A. G., Abrahams J. P., Walker J. E., Ueda T., Sekimoto Y., Kambara M., Saika K., Kagawa Y., Yoshida M. The crystal structure of the nucleotide-free alpha 3 beta 3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer. Structure. 1997 Jun 15;5(6):825–836. doi: 10.1016/s0969-2126(97)00236-0. [DOI] [PubMed] [Google Scholar]
  21. Walker J. E., Fearnley I. M., Gay N. J., Gibson B. W., Northrop F. D., Powell S. J., Runswick M. J., Saraste M., Tybulewicz V. L. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol. 1985 Aug 20;184(4):677–701. doi: 10.1016/0022-2836(85)90313-4. [DOI] [PubMed] [Google Scholar]
  22. Walker J. E., Lutter R., Dupuis A., Runswick M. J. Identification of the subunits of F1F0-ATPase from bovine heart mitochondria. Biochemistry. 1991 Jun 4;30(22):5369–5378. doi: 10.1021/bi00236a007. [DOI] [PubMed] [Google Scholar]
  23. Weber J., Bowman C., Senior A. E. Specific tryptophan substitution in catalytic sites of Escherichia coli F1-ATPase allows differentiation between bound substrate ATP and product ADP in steady-state catalysis. J Biol Chem. 1996 Aug 2;271(31):18711–18718. doi: 10.1074/jbc.271.31.18711. [DOI] [PubMed] [Google Scholar]
  24. Yasuda R., Noji H., Kinosita K., Jr, Yoshida M. F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell. 1998 Jun 26;93(7):1117–1124. doi: 10.1016/s0092-8674(00)81456-7. [DOI] [PubMed] [Google Scholar]
  25. van Raaij M. J., Abrahams J. P., Leslie A. G., Walker J. E. The structure of bovine F1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):6913–6917. doi: 10.1073/pnas.93.14.6913. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES