Abstract
One of the central energy-coupling reactions in living systems is the intraconversion of ATP with a transmembrane proton gradient, carried out by proton-translocating F- and V-type ATPases/synthases. These reversible enzymes can hydrolyze ATP and pump protons, or can use the energy of a transmembrane proton gradient to synthesize ATP from ADP and inorganic phosphate. The stoichiometry of these processes (H+/ATP, or coupling ratio) has been studied in many systems for many years, with no universally agreed upon solution. Recent discoveries concerning the structure of the ATPases, their assembly and the stoichiometry of their numerous subunits, particularly the proton-carrying proteolipid (subunit c) of the FO and V0 sectors, have shed new light on this question and raise the possibility of variable coupling ratios modulated by variable proteolipid stoichiometries.
Similar content being viewed by others
REFERENCES
Abrahams, J. P., Leslie, A. G., Lutter, R., and Walker, J. E. (1994). Nature (London) 370, 621-8.
Alexandre, A., Reynafarje, B., and Lehninger, A. L. (1978). Proc. Natl. Acad. Sci. USA 75, 5296-5300.
Arai, H., Terres, G., Pink, S., and Forgac, M. (1988). J. Biol. Chem. 263, 8796-8802.
Azzone, G. F., Pozzan, T., Massari, S., and Bragadin, M. (1978a). Biochim. Biophys. Acta 501, 296-306.
Azzone, G. F., Pozzan, T., and Massari, S. (1978b). Biochim. Biophys. Acta 501, 307-316.
Azzone, G. F., Pozzan, T., Viola, E., and Arslan, P. (1978c). Biochim. Biophys. Acta 501, 317-329.
Baccarini-Melandri, A., Casadio, R., and Melandri, B. A. (1977). Eur. J. Biochem. 78, 389-402.
Bennett, A. B., and Spanswick, R. M. (1984). Plant Physiol. 74, 545-548.
Berry, E. A., and Hinkle, P. C. (1983). J. Biol. Chem. 258, 1474-1468.
Booth, I. R. (1985). Microbiol. Rev. 49, 359-378.
Boyer, P. D. (1989). Faseb J. 3, 2164-2178.
Boyer, P. D. (1997). Annu. Rev. Biochem. 66, 717-749.
Brand, M. D. (1977). Biochem. Soc. Trans. 5, 1615-1620.
Brusilow, W. S. A. (1987). J. Bacteriol. 169, 4984-4990.
Capaldi, R. A., Aggeler, R., Turina, P., and Wilkens, S. (1994). TIBS 19, 284-289.
Clark, A. J., Cotton, N. P. J., and Jackson, J. M. (1983). Biochim. Biophys. Acta 723, 440-453.
Cross, R. L., and Taiz, L. (1990). FEBS Lett. 259, 227-229.
Davenport, J. W., and McCarty, R. E. (1981). J. Biol. Chem. 256, 8947-8954.
Davenport, J. W., and McCarty, R. E. (1984). Biochim. Biophys. Acta 851, 136-145.
Davies, J. M., Hunt, I., and Sanders, D. (1994). Proc. Natl. Acad. Sci. USA 91, 8547-8551.
Davies, J. M., Sanders, J., and Gradmann, D. (1996). J. Membr. Biol. 150, 231-241.
Deckers-Hebestreit, G., and Altendorf, K. (1996). Annu. Rev. Microbiol. 50, 791-824.
Dewey, T. G., and Hammes, G. G. (1981). J. Biol. Chem. 256, 8941-8946.
Ferguson, S. J., and Sorgato, M. C. (1982). Annu. Rev. Biochem. 51, 185-217.
Forgac, M. (1999). J. Bioenerg. Biomembr. 31, 57-66.
Foster, D. L., and Fillingame, R. H. (1979). J. Biol. Chem. 254, 8230-8236.
Foster, D. L., and Fillingame, R. H. (1982). J. Biol. Chem. 257, 2009-2015.
Gogarten, J. P., Starke, T., Kibak, H., Fishman, J., and Taiz, L. (1992). J. Exp. Biol. 172, 137-147.
Grabe, M., Wang, H., and Oster, G. (2000). Biophys. J. 78, 2798-2813.
Gräber, P., and Witt, H. T. (1976). Biochim. Biophys. Acta 423, 141-163.
Hirata, R., Graham, L. A., Takatsuki, A., Stevens, T. H., and Anraku, Y. (1997). J. Biol.Chem. 272, 4795-4803.
Hirata, T., Nakamura, N., Omote, H., Wada, Y., and Futai, M. (2000). J. Biol. Chem. 275, 386-389.
Holian, A., and Wilson, D. F. (1980). Biochemistry 19, 4213-4221.
Izawa, S. (1970). Biochim. Biophys. Acta 223, 165-173.
Jensen, B. D., Gunter, K. K., and Gunter, T. E. (1986). Arch. Biochem. Biophys. 248, 79-83.
Jensen, P. R., Michelsen, O., and Westerhoff, H. V. (1995). J. Bioenerg. Biomembr. 27, 543-554.
Johnson, R. G., Beers, M. F., and Scarpa, A. (1982). J. Biol. Chem. 257, 10701-10707.
Jones, P. C., and Fillingame, R. H. (1998). J. Biol. Chem. 273, 29701-29705.
Kakinuma, Y., Yamato, I., and Murata, T. (1999). J. Bioenerg. Biomembr. 31, 7-14.
Kane, P. M. (1999). J. Bioenerg. Biomembr. 31, 3-6.
Kashket, E. R. (1982). Biochemistry 21, 5534-5538.
Kashket, E. R. (1983). FEBS Lett. 154, 343-346.
Kashket, E. R. (1985). Annu. Rev. Micro. 39, 219-242.
Kasho, V. N., and Boyer, P. D. (1989). Proc. Natl. Acad. Sci. USA 86, 8708-8711.
Ketcham, S. R., Davenport, J. W., Warncke, K., and McCarty, R. E. (1984). J. Biol. Chem. 259, 7286-7293.
Krenn, B. E., van Walraven, H. S., Scholts, M. J. C., and Kraayenhof, R. (1993). Biochem. J. 294, 705-709.
Lüger, P. (1991). Electrogenic Ion Pumps, Sinauer Associates: Sunderland, MA, U.S.A.
Lemaire, C., Girault, G., and Galmiche, J. M. (1985). Biochim. Biophys. Acta 807, 285-292.
Lemasters, J. J. (1984). J. Biol. Chem. 259, 13123-13130.
Low, R., Rockel, B., Kirsch, M., Ratajczak, R., Hortensteiner, S., Martinoia E., Luttge, U., and Rausch, T. (1996). Plant Physiol. 110, 259-265.
Luvisetto, S., Pietrobon, D., and Azzone, G. F. (1987). Biochemistry 26, 7332-7338.
Maloney, P. C., and Hansen, F. C. 3rd. (1982). J. Membr. Biol. 66, 63-75.
Maloney, P. C. (1983). J. Bacteriol. 153, 1461-1470.
McCarty, R. E., and Portis, A. R. Jr. (1976). Biochemistry 15, 5110-5114.
Mitchell, P. (1966). Chemiosmotic Coupling in Oxidative and Photosynthetic Phosphorylation, Glynn Research, Bodmin.
Mitchell, P., and Moyle, J. (1969). Eur. J. Biochem. 7, 471-484.
Moriyama Y., and Nelson, N. (1988). The Ion Pumps: Structure, Function, and Regulation, pp. 387-394.
Moyle, J., and Mitchell, P. (1973). FEBS Lett. 30, 317-320.
Müller, V., Ruppert, C., and Lemker, T. (1999). J. Bioenerg. Biomembr. 31, 15-28.
Müller, D. J., Stahlberg, H., Engel, A., Seelert, H., and Dencher, N. (2000). Biophys. J. 78, 280A.
Nalin, C. M., and McCarty, R. E. (1984). J. Biol. Chem. 259, 7275-7280.
Nelson, H., and Nelson, N. (1989). FEBS Lett. 247, 147-153.
Nelson, N. (1992). Biochim. Biophys. Acta 1100, 109-124.
Nicholls, D. G., and Bernson, V. S. M. (1977). Eur. J. Biochem. 75, 601-612.
Noji, H., Yasuda, R., Yoshida, M., and Kinosita, K. Jr. (1997). Nature (London) 386, 299-302.
Ogawa, S., and Lee, T. M. (1984). J. Biol. Chem. 259, 10004-10011.
Oster, G., Wang H., and Grabe, M. (2000). Phil. Trans. R. Soc. Lond. B Biol. Sci. 355, 523-528.
Patlak, C. S. (1957). Bull. Math. Biophys. 19, 209-235.
Pedersen, P. L., and Amzel, L. M. (1993). J. Biol. Chem. 268, 9937-9940.
Pedersen, P. L., Schwerzmann, K, and Cintron, N. (1981). Curr. Top. Bioenerg. 11, 149-199.
Perlin, D. S., San Fransisco, M. J. D., Slayman, C. W., and Rosen, B. P. (1986). Arch. Biochem. Biophys. 248, 53-61.
Petty, K. M., and Jackson, J. B. (1979a). Biochim. Biophys. Acta 547, 463-473.
Petty, K. M., and Jackson, J. B. (1979b). Biochim. Biophys. Acta 547, 474-483.
Pietrobon, D., and Caplan, S. R. (1985). Biochemistry 24, 5764-5776.
Pietrobon, D., Zoratti, M., and Azzone, G. F. (1983). Biochim. Biophys. Acta 723, 317-321.
Pietrobon, D., Zoratti, M., Azzone, G. F., and Caplan, S. R. (1986). Biochemistry 25, 767-775.
Pietrobon, D., Luvisetto, S., and Azzone, G. F. (1987). Biochemistry 26, 7339-7347.
Pitard, B., Richard, P., Dunach, M., Rigaud, J. L. (1996). Eur. J. Biochem. 235, 779-788.
Portis, A. R., Jr., and McCarty, R. E. (1974). J. Biol. Chem. 249, 6250-6254.
Portis, A. R., Jr., and McCarty, R. E. (1976). J. Biol. Chem. 251, 1610-1617.
Possmayer, F. E., and Gräber, P. (1994). J. Biol. Chem. 269, 1896-1904.
Pullman, M. E., and Monroy, G. C. (1963). J. Biol. Chem. 238, 3762-3769.
Rahlfs, S., Aufurth, S., and Müller, V. (1999). J. Biol. Chem. 274, 33999-34004.
Rastogi, V. K., and Girvin, M. E. (1999). Nature (London) 402, 263-268.
Rottenberg, H., and Gutman, M. (1977). Biochemistry 16, 3220-3227.
Ruppert, C., Kavermann, H., Wimmers, S., Schmid, R., Kellermann, J., Lottspeich, F., Huber, H., Stetter, K. O., and Müller, V. (1999). J. Biol. Chem. 274, 25281-25284.
Sambongi, Y., Iko, Y., Tanabe, M., Omote, H., Iwamoto-Kihara, A., Ueda, I., Yanagida, T., Wada, Y., and Futai, M. (1999). Science 286, 1722-1724.
Schaefer, E. M., Hartz, D., Gold, L., and Simoni, R. D. (1989). J. Bacteriol. 171, 3901-3908.
Schemidt, R. A., Hsu, D. K. W., Deckers-Hebestreit, G., Altendorf, K., and Brusilow, W. S. A. (1995). Arch. Biochem. Biophys. 323, 423-428.
Schemidt, R. A., Qu, J., Williams, J. R., and Brusilow, W. S. A. (1998). J. Bacteriol. 180, 3205-3208.
Schmidt, A. L., and Briskin, D. P. (1993a). Arch. Biochem. Biophys. 301, 165-173.
Schmidt, A. L., and Briskin, D. P. (1993b). Arch. Biochem. Biophys. 306, 407-414.
Scholes, T. A., and Hinkle, P. C. (1984). Biochemistry 23, 3341-3345.
Senior, A. E. (1988). Physiol. Rev. 68, 177-231.
Solomon, K. A., and Brusilow, W. S. A. (1988). J. Biol. Chem. 263, 5402-5407.
Sorgato, M. C., Galiazzo, F., Panato, L., and Ferguson, S. J. (1982). Biochim. Biophys. Acta 682, 184-188.
Stevens, T. H., and Forgac, M. (1997). Annu. Rev. Cell Develop. Biol. 13, 779-808.
Stock, D., Leslie, A. G. W., and Walker, J. E. (1999). Science 286, 1700-1704.
Thayer, W. S., and Hinkle, P. C. (1973). J. Biol. Chem. 248, 5395-5402.
Tomashek, J. J. (1997). Dissertation. University of California, Davis.
Van Dam, K., Westerhoff, H. V., Krab, K., Van der Meer, R., and Arents, J. C. (1980). Biochim. Biophys. Acta 591, 240-250.
Van der Bend, R. L., Cornelissen, J. B. W. J., Berden, J. A., and Van Dam, K. (1984). Biochim. Biophys. Acta 767, 87-101.
van Walraven, H. S., Haak, N. P., Krab, K., and Kraayenhof, R. (1986). FEBS Lett. 208, 138-142.
van Walraven, H. S., Strotmann, H., Schwarz, O., and Rumberg, B. (1996). FEBS Lett. 379, 309-313.
Vik, S. B., and Antonio, B. J. (1994). J. Biol. Chem. 269, 30364-30369.
Vink, R., Bendall, M. R., Simpson, S. J., and Rogers, P. J. (1984). Biochemistry 23, 3667-3675.
Westerhoff, H. V., Colen, A. M., and Van Dam, K. (1983a). Biochem. Soc. Trans. 11, 81-85.
Westerhoff, H. V., Hellingwerf, K. J., and Van Dam, K. (1983b) 80, 305-309.
Westerhoff, H. V., Melandri, B. A., Venturoli, G., Azzone, G. F., and Kell, D. B. (1984a). FEBS Lett. 165, 1-5.
Westerhoff, H. V., Melandri, B. A., Venturoli, G., Azzone, G. F., and Kell, D. B. (1984b). Biochem. Biophys. Acta 768, 257-292.
Yokoyama, K., Ohkuma, S., Taguchi, H., Yasunaga, T., Wakabayashi, T., and Yoshida, M. (2000). J. Biol. Chem. 275, 13955-13961.
Zoratti, M., Favaron, M., Pietrobon, D., and Azzone, G. F. (1986). Biochemistry 25, 760-767.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Tomashek, J.J., Brusilow, W.S.A. Stoichiometry of Energy Coupling by Proton-Translocating ATPases: A History of Variability. J Bioenerg Biomembr 32, 493–500 (2000). https://doi.org/10.1023/A:1005617024904
Issue Date:
DOI: https://doi.org/10.1023/A:1005617024904