Journal of Bioenergetics and Biomembranes

, Volume 32, Issue 4, pp 325–332

ATP Synthases in the Year 2000: Evolving Views about the Structures of These Remarkable Enzyme Complexes

  • Peter L. Pedersen
  • Young Hee Ko
  • Sangjin Hong
Article

Abstract

This introductory article briefly summarizes how our views about the structural features ofATP synthases (F0F1) have evolved over the past 30 years and also reviews some of our currentviews in the year 2000 about the structures of these remarkably unique enzyme complexes.Suffice it to say that as we approach the end of the first year of this new millinium, we canbe conservatively confident that we have a reasonably good grasp of the overall “low-resolution”structural features of ATP synthases. Electron microscopy techniques, combined with the toolsof biochemistry, molecular biology, and immunology, have played the leading role here byidentifying the headpiece, basepiece, central stalk, side stalk, cap, and in the mitochondrialenzyme, the collar around the central stalk. We can be reasonably confident also that we havea fairly good grasp of much of the “high-resolution” structural features of both the F1 moietycomprised of fives subunit types (α, β, γ, δ, and ∈) and parts of the F0 moiety comprised ofeither three (E. coli) or at least ten (mitochondria) subunit types. This information acquiredin several different laboratories, either by X-ray crystallography or NMR spectroscopy, includesdetails about the active site and subunit relationships. Moreover, it is consistent with recentlyreported data that the F1 moiety may be an ATP driven motor, which, during ATP synthesis,is driven in reverse by the electrochemical proton gradient generated by the electron transportchain. The real structural challenges of the future are to acquire at high resolution “complete”ATP synthase complexes representative of different stages of the catalytic cycle during ATPsynthesis and representative also of key regulatory states.

ATP synthase FOF1-ATP synthase/ATPase F1-ATPase ATP synthesis oxidative phosphorylation molecular motors 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Abrahams, J. B., Leslie, A. G. W., Lutter, R., and Walker, J. E. (1994). Nature (London) 370, 621–628.Google Scholar
  2. Abrahams, J. G., Buchanan, S. K., van Raaij, M. J., Fearnley, I. M., Leslie, A. G., and Walker, J. E. (1996). Proc. Natl. Acad. Sci. USA 93, 9420–9424.Google Scholar
  3. Amzel, L. M. and Pedersen, P. L. (1978). J. Biol. Chem. 253, 2067–2069.Google Scholar
  4. Amzel, L. M., McKinney, M., Narayanan, P., and Pedersen, P. L. (1982). Proc. Natl. Acad. Sci. USA 79, 5852–5856.Google Scholar
  5. Bianchet, M. A., Ysern, S., Hullihen, J., Pedersen, P. L., and Amzel, L. M. (1991). J. Biol. Chem. 266, 21197–21201.Google Scholar
  6. Bianchet, M. A., Hullihen, J., Pedersen, P. L., and Amzel, L. M. (1998). Proc. Natl. Acad. Sci. USA 95, 11065–11070.Google Scholar
  7. Boekema, E. J., Berden, J. A., and Van Heel, M. G. (1986). Biochem. Biophys. Acta 851, 353–360.Google Scholar
  8. Bottcher, B., Schwarz, L., and Graber, P. (1998). J. Mol. Biol. 281, 757–762.Google Scholar
  9. Braig, K., Menz, R. I., Montgomery, M. G., Leslie, A. G., and Walker, J. E. (2000). Structure Fold Des. 8, 567–573.Google Scholar
  10. Capaldi, R. A., Schulenberg, B., Murray, J., and Aggeler, R. (2000). J. Exp. Biol. 203, 29–33.Google Scholar
  11. Catterall, W. A. and Pedersen, P. L. (1974). Biochem. Soc. Spec. Publ. 4, 63–88.Google Scholar
  12. Catterall, W. A., Coty, W. A., and Pedersen, P. L. (1973). J. Biol. Chem. 248, 7427–7431.Google Scholar
  13. Dmitriev, O., Jones, P. C., Jiang, W., and Fillingame, R. H. (1999). J. Biol.Chem. 274, 15598–15604.Google Scholar
  14. Ferandez-Moran, H. (1962). Circulation 26, 1039–1065.Google Scholar
  15. Gibbons, C., Montgomery, M. G., Leslie, A. G. W., and Walker, J. E. (2000). Biochem. Biophys. Acta, EBEC Short Reports, 11, 212, Nature Struc. Biol. 7, 1055–1061.Google Scholar
  16. Girvin, M. E. and Fillingame, R. H. (1995). Biochemistry 34, 1635–1645.Google Scholar
  17. Girvin, M. E., Rastogi, V. V., Abildgaard, F., Markley, J. L., and Fillingame, R. H. (1998). Biochemistry 37, 8817–8824.Google Scholar
  18. Gogel, E. P., Lucken, U., and Capaldi, R. A. (1987). FEBS Lett. 219, 274–278.Google Scholar
  19. Gogel, E. P., Johnson, E., Aggeler, R., and Capaldi, R. A. (1990). Proc. Natl. Acad. Sci. USA 87, 9585–9589.Google Scholar
  20. Graber, P., Bottcher, B., and Boekema, E. J. (1990). Bioelectro-chemistry III (Milazzo, G. and Blank, M., eds.), Plenum Press, New York, pp 247–276.Google Scholar
  21. Hausrath, A. C., Gruber, G., Matthews, B. W., and Capaldi, R. A. (1999). Proc. Natl. Acad. Sci. USA 96, 13697–13702.Google Scholar
  22. Junge, W., Lill, H., and Engelbrecht, S. (1997). Trends Biochem. Sci. 22, 420–423.Google Scholar
  23. Kagawa, Y. (1972). Biochem. Biophys. Acta 265, 297–338.Google Scholar
  24. Karrash, S. and Walker, J. E. (1999). J. Mol. Biol. 290, 379–384.Google Scholar
  25. Ko, Y. H., Hullihen, J., Hong, S., and Pedersen, P. L. (2000). J. Biol. Chem., 276, 32931–32939.Google Scholar
  26. Lutter, R., Abrahams, J. B., van Raaij, M. J., Todd, R. J., Lundquist, T., Buchanan, S. K., Leslie, A. G.W., and Walker, J. E. (1993). J. Mol. Biol. 229, 787–790.Google Scholar
  27. Mitchell, P. (1979). Science 206, 1148–1159.Google Scholar
  28. Orriss, G. L., Leslie, A. G., Braig, K., and Walker, J. E. (1998). Structure 6, 831–837.Google Scholar
  29. Oschida, W. J. and Bowman, B. J. (1992). J. Biol. Chem. 267, 18783–18789.Google Scholar
  30. Pedersen, P. L. (1996). J. Bioenerg. Biomembr. 38, 389–395.Google Scholar
  31. Pedersen, P. L., Hullihen, J., Bianchet, M., Amzel, L. M., and Lebowitz, M. S. (1995). J. Biol. Chem. 270, 1775–1784.Google Scholar
  32. Rastogi, V. K. and Girvin, M. E. (1999). Nature (London) 402, 263–268.Google Scholar
  33. Seelert, H., Poetsch, A., Dencher, N. A., Engel, A., Stahlberg, H., and Muller, D. J. (2000). Nature (London) 405, 418–419.Google Scholar
  34. Shirakihara, Y., Leslie, A. G. W., Abrahams, J. P., Walker, J. E., Udea, T., Sekimato, Y., Kambara, M., Saika, K., Kagawa, Y., and Yoshida, M. (1997). Structure 5, 825–836.Google Scholar
  35. Soper, J. W., Decker, G. L., and Pedersen, P. L. (1979). J. Biol. Chem. 254, 11170–11176.Google Scholar
  36. Stock, D., Leslie, A. G. W., and Walker, J. E. (1999). Science 286, 1700–1705.Google Scholar
  37. Tsuprun, L., Orlova, E. V., and Mesyanzhinova, J. V. (1989). FEBS Lett. 244, 279–282.Google Scholar
  38. Uhlin, U., Cox, G. B., and Guss, J. M. (1998). Structure 5, 1219–1230.Google Scholar
  39. van Raaij, M. J., Abrahams, J. P., Leslie, A. G. W., and Walker, J. E. (1996). Proc. Natl. Acad. Sci. USA 93, 6913–6917.Google Scholar
  40. Velours, J. and Arselin, G. (2000). J. Bioenerg. Biomemb. 32, 383–390.Google Scholar
  41. Wilkens, S. and Capaldi, R. A. (1998a). Nature (London) 393, 29.Google Scholar
  42. Wilkens, S. and Capaldi, R. A. (1998b). Biochim. Biophys. Acta 1365, 93–97.Google Scholar
  43. Wilkens, S. and Capaldi, R. A. (1998c). J. Biol. Chem. 273, 26645–26651.Google Scholar
  44. Wilkens, S. Dunn, S. D., Chandler, J., Dahlquist, F.W., and Capaldi, R. A. (1997). Natur. Struct. Biol. 4, 198–201.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Peter L. Pedersen
    • 1
  • Young Hee Ko
    • 2
  • Sangjin Hong
    • 2
  1. 1.Department of Biological ChemistryJohns Hopkins University, School of MedicineBaltimore
  2. 2.Department of Biological ChemistryJohns Hopkins University, School of MedicineBaltimore

Personalised recommendations