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The Structural and Functional Connection between the Catalytic and Proton Translocating Sectors of the Mitochondrial F 1 F 0 -ATP Synthase

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Abstract

The structural and functional connection between the peripheral catalytic F1 sector and theproton-translocating membrane sector F0 of the mitochondrial ATP synthase is reviewed. Theobservations examined show that the N-terminus of subunit γ, the carboxy-terminal and centralregion of F0I-PVP(b), OSCP, and part of subunit d constitute a continuous structure, the lateralstalk, which connects the peripheries of F1 to F0 and surrounds the central element of thestalk, constituted by subunits γ and δ. The ATPase inhibitor protein (IF1) binds at one sideof the F1F0 connection. The carboxy-terminal segment of IF1 apparently binds to OSCP. The42L-58K segment of IF1, which is per se the most active domain of the protein, binds at thesurface of one of the three α/β pairs of F1, thus preventing the cyclic interconversion of thecatalytic sites required for ATP hydrolysis.

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REFERENCES

  • Abrahams, J. P., Leslie, A. G. W., Lutter, R., and Walker, J. E. (1994). Nature (London) 370, 621–628.

    Google Scholar 

  • Aggeler, R., Ogilvie, I., and Capaldi, R. A. (1997). J. Biol. Chem. 272, 19621–19624.

    Google Scholar 

  • Arnold, I., Pfeiffer, K., Neupert, W., Stuart, R. A., and Shagger, H. (1998). EMBO J. 17, 7170–7178.

    Google Scholar 

  • Baracca, A., Barogi, S., Carelli, V., Lenaz, G., and Solaini, G. (2000). J. Biol. Chem. 275, 4177–4182.

    Google Scholar 

  • Belogrudov, G. I., Tomich, J. M., and Hatefi, Y. (1996). J. Biol. Chem. 271, 20340–20345.

    Google Scholar 

  • Birkenhager, R., Hoppert, M., Deckers-Hebestreit, G., Mayer, F., and Altendorf, K. (1995). Eur. J. Biochem. 230, 58–67.

    Google Scholar 

  • Boekema, E. J., Van Breemen, J. F. L., Brisson, A., Ubbink-Kok, T., Konings, W. N., and Lolkema, J. S. (1999). Nature (London) 401, 37–38.

    Google Scholar 

  • Bottcher, B., Schwarz, L., and Graber, P. (1998). J. Mol. Biol. 281, 757–762.

    Google Scholar 

  • Boyer, P. D. (1997). Annu. Rev. Biochem. 66, 717–749.

    Google Scholar 

  • Cabezon, E., Butler, P. J. G., Runswick, M. J., and Walker, J. E. (2000). J. Biol. Chem., 275, 25460–25464.

    Google Scholar 

  • Capaldi, R. A., Aggeler, R., Turina, P., and Wilkens, S. (1994). Trends Biochem. Sci. 19, 284–289.

    Google Scholar 

  • Capaldi, R. A., Schulenberg, B., Murray, J., and Aggeler, R. (2000). J. Exp. Biol. 203, 29–33.

    Google Scholar 

  • Cherepanov, D. A., Mulkidjanian, A. Y., and Junge, W. (1999). FEBS Lett. 449, 1–6.

    Google Scholar 

  • Collinson, I. R., van Raaij, M. J., Runswick, M. J., Fearnley, I. M., Skehel, J. M., Orris, G. L., Miroux, B., and Walker, J. E. (1994a). J. Mol. Biol. 242, 408–421.

    Google Scholar 

  • Collinson, I. R., Fearnley, I. M., Skehel, J. M., Runswick, M. J., and Walker, J. E. (1994b). Biochem. J. 303, 639–645.

    Google Scholar 

  • Collinson, I. R., Runswick, M. J., Buchanan, S. K., Fearnley, I. M., Skehel, J. M., van Raaij, M. J., Griffiths, D. E., and Walker, J. E. (1994c). Biochemistry 33, 7971–7978.

    Google Scholar 

  • Cox, G. B., Devenish, R. J., Gibson, F., Howitt, S. M., and Nagley, P. (1992). In Molecular Mechanism in Bioenergetics (Ernster, L., ed.). Elsevier, Amsterdam, The Netherlands, pp. 283–315.

    Google Scholar 

  • Duncan, T. M., Bulygin, V.V., Zhou, Y., Hutcheon, M. L., and Cross, R. L. (1995). Proc. Natl. Acad. Sci. USA 92, 10964–10968.

    Google Scholar 

  • Dunn, S. D., Heppel, L. A., and Fullmer, C. S. (1980). J. Biol. Chem. 255, 6891–6896.

    Google Scholar 

  • Elston, T., Wang, H., and Oster, G. (1998). Nature (London) 391, 510–513.

    Google Scholar 

  • Engelbrecht, S. and Junge, W. (1997). FEBS Lett. 414, 485–491.

    Google Scholar 

  • Fernandez-Moran, H. (1962). Circulation 26, 1039–1065.

    Google Scholar 

  • Fillingame, R. H. (1996). Curr. Opin. Struct. Biol. 6, 491–498.

    Google Scholar 

  • Fillingame, R. H. (1997). J. Exp. Biol. 200, 217–224.

    Google Scholar 

  • Fillingame, R. H., Jones, P. C., Jiang, W., Valiyaveetil, F. I., and Dmitriev, O.Y. (1998). Biochim. Biophys. Acta 1365, 135–142.

    Google Scholar 

  • Gaballo, A., Zanotti, F., Raho, G., and Papa, S. (1999). FEBS Lett. 463, 7–11.

    Google Scholar 

  • Gaballo, A., Zanotti, F., Solimeo, A., and Papa S., (1998). Biochemistry 37, 17519–17526.

    Google Scholar 

  • Garnier J., Gibrat, J. F., and Robson, B. (1996). Methods Enzymol. 266, 540–553.

    Google Scholar 

  • Gogol, E. P., Lucken, U., and Capaldi, R. A. (1987). FEBS Lett. 219, 274–278.

    Google Scholar 

  • Green, D. W. and Grover, G. J. (2000). Biochim. Biophys. Acta 1458, 343–355.

    Google Scholar 

  • Guerrieri, F., Zanotti, F., Capozza, G., Colaianni, G., Ronchi, S., and Papa, S., (1991). Biochim. Biophys. Acta 1059, 348–354.

    Google Scholar 

  • Harris, D. A. and Das, A. M. (1991). Biochem. J. 280, 561–573.

    Google Scholar 

  • Hausrath, A. C., Gruber, G., Matthews, B. W., and Capaldi, R. A. (1999). Proc. Natl. Acad. Sci. USA 96, 13697–13702.

    Google Scholar 

  • Heckman, C., Tomich, J. M., and Hatefi, Y. (1991). J. Biol. Chem. 266, 13564–13571.

    Google Scholar 

  • Houstek, J., Kopecky, J., Zanotti, F., Guerrieri, F., Jirillo, E., Capozza, G., and Papa, S. (1988). Eur. J. Biochem. 173, 1–8.

    Google Scholar 

  • Hundal, T., Norling, B., and Ernster, L. (1983). FEBS Lett. 162, 5–10.

    Google Scholar 

  • Jackson, P. J. and Harris, D. A. (1988). FEBS Lett. 229, 224–228.

    Google Scholar 

  • Joshi, S. and Burrows, R. (1990). J. Biol. Chem. 265, 14518–14525.

    Google Scholar 

  • Junge, W., Lill, H., and Engelbrecht, S. (1997). Trends Biochem. Sci. 22, 123–126.

    Google Scholar 

  • Karrasch, S. and Walker, J. E. (1999). J. Mol. Biol. 290, 379–384.

    Google Scholar 

  • Kato-Yamada, Y., Noji, H., Yasuda, R., Kinosita, K., and Yoshida, M. (1998). J. Biol. Chem. 273, 19375–19377.

    Google Scholar 

  • Lebowitz, M. S. and Pedersen, P. L. (1996). Azch. Biochem. Biophys. 330, 342–354.

    Google Scholar 

  • Mendel-Hartvig, J. and Capaldi, R. A. (1991). Biochim. Biophys. Acta 1060, 115–124.

    Google Scholar 

  • Mimura, H., Hashimoto, T., Yoshida, Y., Ichikawa, N., and Tagawa, K. (1993). J. Biochem. 113, 350–354.

    Google Scholar 

  • Noji, H., Yasuda, R., Yoshida, M., and Kinosita, K. (1997). Nature (London) 386, 299–302.

    Google Scholar 

  • Oda, T., Futaky, S., Kitagawa, K., Yoshihara, Y., Tani I., and Higuti, T. (1989). Biochem. Biophys. Res. Commun. 165, 449–456.

    Google Scholar 

  • Ogilvie, I., Aggeler, R., and Capaldi, R. A. (1997). J. Biol. Chem. 272, 16652–16656.

    Google Scholar 

  • Oster, G. and Wang, H. (1999). Structure 7, R 67-R72.

    Google Scholar 

  • Ovchinnikov, Y. A., Modyanov, N. N., Grinkevich, V. A., Aldanova, N. A., Trubetskaya, O. E., Nazimov, I. V., Hundal, T., and Ernster, L. (1984). FEBS Lett. 166, 19–22.

    Google Scholar 

  • Packer, L., Tristram, S., Herz, J. M., Russel, C., and Borders, C. L. (1979). FEBS Lett. 108, 243–248.

    Google Scholar 

  • Panke, O., Gumbiowski, K., Junge, W., and Engelbrecht (2000). FEBS Lett. 472, 34–38.

    Google Scholar 

  • Papa, S., Guerrieri, F., Zanotti, F., Houstek, J., Capozza, G., and Ronchi, S. (1989). FEBS Lett. 249, 62–66.

    Google Scholar 

  • Papa, S., Zanotti, F., Cocco, T., Perrucci, C., Candita, C., and Minuto, M. (1996). Eur. J. Biochem. 240, 461–467.

    Google Scholar 

  • Papa, S., Xu, T., Gaballo, A., and Zanotti, F. (1999). In Frontiers of Cellular Bioenergetics: Molecular Biology, Biochemistry and Physiopathology (Papa, S., Guerrieri, F., Tager, J. M., eds.), Plenum Press, London, New York, pp. 459–487.

    Google Scholar 

  • Paul, M. F., Guerin, B., and Velours, J. (1992). Eur. J. Biochem. 205, 163–172.

    Google Scholar 

  • Pedersen, P. L., Schwerzmann, K., and Cintron, N. M. (1981). Curr. Top. Bioenerge. 11, 149–199.

    Google Scholar 

  • Raho, G., Zanotti, F., Gaballo, A., Vuolo, R., and Papa, S. (2000). In preparation.

  • Sabbert, D., Engelbrecht, S., and Junge, W. (1996). Nature (London) 381, 623–625.

    Google Scholar 

  • 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.

    Google Scholar 

  • Schneider, E. and Altendorf, K. (1984). Proc. Natl. Acad. Sci. USA 81, 7279–7283.

    Google Scholar 

  • Schneider, E. and Altendorf, K. (1985). Eur. J. Biochem. 153, 105–109.

    Google Scholar 

  • Schneider, E. and Altendorf, K. (1987). Microbiol. Rev. 51, 477–497.

    Google Scholar 

  • Senior, A. E. (1990). Annu. Rev. Biophys. Biophys. Chem. 19, 7–41.

    Google Scholar 

  • Singh, S., Turina, P., Bustamante, C. J., Keller, D. J., and Capaldi, R. A. (1996). FEBS Lett. 397, 30–34.

    Google Scholar 

  • Stock, D., Leslie, A. G. W., and Walker, J. E. (1999). Science 286, 1700–1705.

    Google Scholar 

  • Stout, J. S., Partridge, B. E., Dibbern, D. A., and Schuster, S. M. (1993). Biochemistry 32, 7496–7502.

    Google Scholar 

  • Takeyasu, K., Omote, H., Nettikadan, S., Tokumasu, F., Iwamoto-Kihara, A., and Futai, M.(1996). FEBS Lett. 392, 110–113.

    Google Scholar 

  • Tsunoda, S. P., Aggeler, R., Noji, H., Kinosita, K., Yoshida, M., and Capaldi, R. A. (2000). FEBS Lett. 470, 244–248.

    Google Scholar 

  • Ubbink-Kok, T., Boekema, E. J., van Breemen, J. F., Brisson, A., Konings, W. N., and Lolkema, J. S. (2000). J. Mol. Biol. 296, 311–321.

    Google Scholar 

  • van Raaij, M. J., Orris, G. L., Montgomery, M. G., Runswick, M. J., Fearnley, I. M., Skehel, J. M., and Walker, J. E. (1996). Biochemistry 35, 15618–15625.

    Google Scholar 

  • Walker, J. E. and Collinson, I. R. (1994). FEBS Lett. 346, 39–43.

    Google Scholar 

  • Walker, J. E., Fearnley, I. M., Gay, N. J., Gibson, B. W., Northrop, F. D., Powell, S. J., Runswick, M. J., Saraste, M., and Tybulewicz, W. L. J. (1985). J. Mol. Biol. 184, 677–701.

    Google Scholar 

  • Walker, J. E., Runswick, M. J. and Poulter, L., (1987) J. Mol. Biol. 197, 89–100.

    Google Scholar 

  • Watts, S. D., Zhang, Y., Fillingame, R. H., and Capaldi, R. A. (1995). FEBS Lett. 368, 235–238.

    Google Scholar 

  • Watts, S. D., Tang, C., and Capaldi, R. A. (1996). J. Biol. Chem. 271, 28341–28347.

    Google Scholar 

  • Wilkens, S. and Capaldi, R. A. (1998). Nature (London) 393, 29.

    Google Scholar 

  • Wilkens, S., Dunn, S. D., Chandler, J., Dahlquist, F.W., and Capaldi, R. A. (1997). Nature Struct. Biol. 4, 198–201.

    Google Scholar 

  • Wilkens, S., Zhou, J., Nakayama, J., Dunn, S. D., and Capaldi, R. (2000). J. Mol. Biol. 295, 387–391.

    Google Scholar 

  • Xu, T., Candita, C., Amoruso, G., and Papa, S. (1998). Eur. J. Biochem. 252, 155–161.

    Google Scholar 

  • Xu, T., Zanotti, F., Gaballo, A., Raho, G., and Papa, S. (2000). Eur. J. Biochem. 267, 4445–4455.

    Google Scholar 

  • Zanotti, F., Guerrieri, F., Scarfó, R., Berden, J., and Papa, S. (1985). Biochem. Biophys. Res. Commun. 132, 985–990.

    Google Scholar 

  • Zanotti, F., Guerrieri, F., Capozza, G., Houstek, J., Ronchi, S., and Papa, S. (1988). FEBS Lett. 237, 9–14.

    Google Scholar 

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Authors and Affiliations

  1. Department of Medical Biochemistry and Biology, University of Bari, 70124, Bari, Italy

    Sergio Papa

  2. Department of Medical Biochemistry and Biology, University of Bari, 70124, Bari, Italy

    Fzaneo Zanotti & Antonio Gaballo

  3. Centre for the Study of Mitochondria and Energy Metabolism, Consiglio Nazionale delle Ricerche, University of Bari, Italy

    Fzaneo Zanotti

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  1. Sergio Papa
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  2. Fzaneo Zanotti
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  3. Antonio Gaballo
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Papa, S., Zanotti, F. & Gaballo, A. The Structural and Functional Connection between the Catalytic and Proton Translocating Sectors of the Mitochondrial F 1 F 0 -ATP Synthase . J Bioenerg Biomembr 32, 401–411 (2000). https://doi.org/10.1023/A:1005584221456

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