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The α/β Interfaces of α1β1, α3β3, and F1: Domain Motions and Elastic Energy Stored during γ Rotation

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Abstract

ATP synthase (FoF1) consists of F1 (ATP-driven motor) and Fo (H+-driven motor). F1 is a complex of α3β3γδε subunits, and γ is the rotating cam in α3β3. Thermophilic F1 (TF1) is exceptional in that it can be crystallized as a β monomer and an α3β3 oligomer, and it is sufficiently stable to allow αβ refolding and reassembly of hybrid complexes containing 1, 2, and 3 modified α or β. The nucleotide-dependent open–close conversion of conformation is an inherent property of an isolated β and energy and signals are transferred through α/β interfaces. The catalytic and noncatalytic interfaces of both mitochondrial F1 (MF1) and TF1 were analyzed by an atom search within the limits of 0.40 nm across the αβ interfaces. Seven (plus thermophilic loop in TF1) contact areas are located at both the catalytic and noncatalytic interfaces on the open β form. The number of contact areas on closed β increased to 11 and 9, respectively, in the catalytic and noncatalytic interfaces. The interfaces in the barrel domain are immobile. The torsional elastic strain applied through the mobile areas is concentrated in hinge residues and the P-loop in β. The notion of elastic energy in FoF1 has been revised. X-ray crystallography of F1 is a static snap shot of one state and the elastic hypotheses are still inconsistent with the structure, dyamics, and kinetics of FoF1. The domain motion and elastic energy in FoF1 will be elucidated by time-resolved crystallography.

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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 

  • Aloise, P., Kagawa, Y., and Coleman, P. S. (1991). J. Biol. Chem. 266, 10368-10376.

    Google Scholar 

  • Amano, T., Hisabori, T., Muneyuki, E., and Yoshida, M. (1996). J. Biol. Chem. 271, 18127-18133.

    Google Scholar 

  • Amano, T., Matsui, T., Muneyuki, E., Noji, H., Hara, K., Yoshida, M., and Hisabori, T. (1999). Biochem. J. 343, 135-138.

    Google Scholar 

  • Arai, M., and Kuwajima, K. (2000). Advan. Protein Chem. 53, 209-282.

    Google Scholar 

  • Argos, P., Rossmann, M. G., Grqu, U. M., Zuber, H., Frank, G., and Tratschin, J. D. (1979). Biochemistry 18, 5698-5703.

    Google Scholar 

  • Bald, D., Amano, T., Muneyuki, E., Pitard, B., Rigaud, J-L., Kruip, J., Hisabori, T., Yoshida, M., and Shibata, M. (1998). J. Biol. Chem. 273, 865-870.

    Google Scholar 

  • Bianchet, M. A., Hullihen, J., Pedersen, P. L., and Amzel, L. M. (1998). Proc. Natl. Acad. Sci. USA 95, 11065-11070.

    Google Scholar 

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

    Google Scholar 

  • Burgard, S., Nett, J. H., Sauer, H. E., Kagawa, Y., Schäfer, H-J., Wise, J. G., Vogel, P. D., and Trommer, W. E. (1994). J. Biol. Chem. 269, 17815-17819.

    Google Scholar 

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

    Google Scholar 

  • Collinson, I. R., Skehel, J. M., Fearnley, I. M., Runswick, J. M., and Walker, J. E. (1996). Biochemistry 35, 12640-12646.

    Google Scholar 

  • Futai, M., and Omote, H. (1996). J. Bioenerg. Biomembr. 28, 409-414.

    Google Scholar 

  • Futai, M., Noumi, T., and Maeda, M. (1989). Annu. Rev. Biochem. 58, 111-136.

    Google Scholar 

  • Garcia, J. J., and Capaldi, R. A. (1998). J. Biol. Chem. 273, 15940-15945.

    Google Scholar 

  • Hall, D., and Pravitt, N. (1984). Compt. Chem. 5, 441-450.

    Google Scholar 

  • Hayward, S. (1999). Proteins 36, 425-435.

    Google Scholar 

  • Hirata, H., Ohno, K., Sone, N., Kagawa, Y., and Hamamoto, T. (1986). J. Biol.Chem. 261, 8939-8943.

    Google Scholar 

  • Hofmann, H., Voss, T., Kuhn, K., and Engel, J. (1984). J. Mol. Biol. 172, 325-343.

    Google Scholar 

  • Ichida, M., Hakamata, Y., Hayakawa, H., Ueno, E., Ikeda, U., Shimada, K., Hamamoto, T., Kagawa, Y., and Endo, H. (2000). J. Biol. Chem. 275, 15992-16001.

    Google Scholar 

  • Jaenicke, R., and Boehm, G. (1998). Curr. Opinion Struct. Biol. 8, 738-748.

    Google Scholar 

  • Jault, J. M., Matsui, T., Jault, F. M., Kaibara, C., Muneyuki, E., Yoshida, M., Kagawa, Y., and Allison, W. S. (1995). Biochemistry 34, 16412-16418.

    Google Scholar 

  • Jones, P. C., Jiang, W., and Fillingame, R. H. (1998). J. Biol. Chem. 273, 17178-17185.

    Google Scholar 

  • Kagawa, Y. (1999). Advan. Biophys. 36, 1-25.

    Google Scholar 

  • Kagawa, Y., and Hamamoto, T. (1996). J. Bioenerg. Biomembr. 28, 421-431.

    Google Scholar 

  • Kagawa, Y., and Hamamoto, T. (1997). Biochem. Biophys. Res. Commun. 240, 247-256.

    Google Scholar 

  • Kagawa, Y., and Racker, E. (1966a). J. Biol. Chem. 241, 2467-2474.

    Google Scholar 

  • Kagawa, Y., and Racker, E. (1966b). J. Biol. Chem. 241, 2475-2482.

    Google Scholar 

  • Kagawa, Y., and Racker, E. (1971). J. Biol. Chem. 246, 5477-5487.

    Google Scholar 

  • Kagawa, Y., Ishizuka, M., Saishu, T., and Nakao, S. (1986). J. Biochem. 100, 923-934.

    Google Scholar 

  • Kagawa, Y., Ohta, S., Harada, M., Sato, M., and Ito, Y. (1992). Ann. N.Y. Acad. Sci. 671, 366-376.

    Google Scholar 

  • Kagawa, Y., Hamamoto, T., Endo, H., Ichida, M., Shibui, H., and Hayakawa, M. (1997). Biosci. Rept. 17, 115-146.

    Google Scholar 

  • Kagawa, Y., Cha, S-H., Hasegawa, K., Hamamoto, T., and Endo, H. (1999). Biochem. Biophys. Res. Commun. 266, 662-667.

    Google Scholar 

  • Kaibara, C., Matsui, T., Hisabori, T., and Yoshida, M. (1996). J. Biol. Chem. 271, 2433-2438.

    Google Scholar 

  • Kamiyama, T., and Gekko, K. (2000). Biochim. Biophys. Acta 1478, 257-266.

    Google Scholar 

  • Kinoshita, K. Jr. (1999). FASEB J. Suppl. 2, S201-S208.

    Google Scholar 

  • Masaike, T., Mitome, N., Noji, H., Muneyuki, E., Yasuda, R., Kinoshita, K., Jr., and Yoshida, M. (2000). J. Exp. Biol. 203, 1-8.

    Google Scholar 

  • Le, N. P., Omote, H., Wada, Y., Al-Shawi, M. K., Nakamoto, R. K., and Futai, M. (2000). Biochemistry 39, 2778-2783.

    Google Scholar 

  • Leslie, A. G. W., and Walker, J. E. (2000). Phil. Trans. R. Soc. Lond. B 355, 465-472.

    Google Scholar 

  • Mitchell, P. (1979) Science 206, 1148-1159.

    Google Scholar 

  • Moffat, K. (1998). Acta Crystallogr. A. 54, 833-841.

    Google Scholar 

  • Noji, H., Amano, T., and Yoshida, M. (1996). J. Bioenerg. Biomembr. 28, 451-457.

    Google Scholar 

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

    Google Scholar 

  • Ohta, S., and Kagawa, Y. (1986). J. Biochem. 99, 135-141.

    Google Scholar 

  • Ohta, S., Tsuboi, M., Yoshida, M., and Kagawa, Y. (1980). Biochemistry 19, 2160-2168.

    Google Scholar 

  • Omote, H., Nga, P. L., Park, M-Y., Maeda, M., and Futai, M. (1995). J. Biol. Chem. 270, 25656-25660.

    Google Scholar 

  • Omote, H., Tainaka, K., Fujie, K., Iwamoto-Kihara, A., Wada, Y., and Futai, M. (1998). Arch. Biochem. Biophys. 358, 277-282.

    Google Scholar 

  • Oster, G., and Wang, H. (2000). Biochim. Biophys. Acta 1458, 482-510.

    Google Scholar 

  • Paik, S. R., Yokoyama, K., Yoshida, M., Ohta, T., Kagawa, Y., and Allison, W. S. (1993). J. Bioenerg. Biomembr. 25, 679-684.

    Google Scholar 

  • Pedersen, P. L. (1996). J. Bioenerg. Biomembr. 28, 389-395.

    Google Scholar 

  • Ren, H., and Allison, W. S. (2000). J. Biol. Chem. 275, 10057-10063.

    Google Scholar 

  • Ren, H., Dou, C., Stelzer, M. S., and Allison, W. S. (1999). J. Biol. Chem. 274, 31366-31372.

    Google Scholar 

  • Saika, K., and Yoshida, M. (1995). FEBS Lett. 368, 207-210.

    Google Scholar 

  • Saika, K., Inaka, K., Matsui, T., Yoshida, M., and Miki, K. (1994). J. Mol. Biol. 242, 709-711.

    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, 1687-1688.

    Google Scholar 

  • Sasaki, N., Shimada, T., and Sutoh, K. (1998). J. Biol. Chem. 273, 20334-20340.

    Google Scholar 

  • Sato, M., Ito, Y., Harada, M., Kihara, H., Tsuruta, H. S., Ohta, S.,and Kagawa, Y. (1995). J. Biochem. 117, 113-119.

    Google Scholar 

  • Schäfer, H-J., Rathgeber, G., and Kagawa, Y. (1995). FEBS Lett. 377, 408-412.

    Google Scholar 

  • Senter, P., Eckstein, F., and Kagawa, Y. (1983). Biochemistry 22, 5514-5518.

    Google Scholar 

  • Shibui, H., Hamamoto, T., Yohda, M., and Kagawa, Y. (1997). Biochem. Biophys. Res. Commun. 234, 341-345.

    Google Scholar 

  • Shirakihara, Y., Leslie, A. G.W., Abrahams, J. P., Walker, J. E., Ueda, T., Sekimoto, Y., Kambara, M., Saika, K., Kagawa, Y., and Yoshida, M. (1997). Structure. 5, 825-836.

    Google Scholar 

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

    Google Scholar 

  • Tozawa, K., Sekino, N., Soga, M., Yagi, H., Yoshida, M., and Akutsu, H. (1995). FEBS Lett. 376, 190-194.

    Google Scholar 

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

    Google Scholar 

  • Tsunoda, S. P., Muneyuki, E., Amano, T., Yoshida, M., and Noji, H. (1999). J. Biol. Chem. 274, 5701-5706.

    Google Scholar 

  • Wang, Z. G., and Ackerman, S. H. (2000). J. Biol. Chem. 275, 5767-5772.

    Google Scholar 

  • Weber, J., and Senior, A. E. (2000). Biochim. Biophys. Acta 1458, 300-309.

    Google Scholar 

  • Wilkens, S., and Capaldi, R. A. (1998). Biochim. Biophys. Acta 1365, 93-97.

    Google Scholar 

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

    Google Scholar 

  • Yagi, H., Tozawa, K., Sekino, N., Iwabuchi, T., Yoshida, M., and Akutsu, H. (1999). Biophys. J. 77, 2175-2183.

    Google Scholar 

  • Yan, B., Zhang, W., Ding, J., and Arnold, E. (1999). J. Protein Chem. 18, 807-811.

    Google Scholar 

  • Yanagida, T., Kinanuma, K., Tanaka, H., Hikikoshi-Iwane, A., and Esaki, S. (2000). Curr. Opinion Cell Biol. 12, 20-25.

    Google Scholar 

  • Yasuda, R., Noji, H., Kinoshita, K. Jr., and Yoshida, M. (1998). Cell 93, 1117-1124.

    Google Scholar 

  • Yohda, M., Kagawa, Y., and Yoshida, M. (1986). Biochim. Biophys. Acta 850, 429-435.

    Google Scholar 

  • Yohda, M., Ohta, S., Hisabori, T., and Kagawa, Y. (1988). Biochim. Biophys. Acta 933, 156-164.

    Google Scholar 

  • Yoshida, M., Sone, N., Hirata, H., and Kagawa, Y. (1975). J. Biol. Chem. 250, 7910-7915.

    Google Scholar 

  • Yoshida, M., Sone, N., Hirata, H., Kagawa, Y., and Ui, N. (1979). J. Biol. Chem. 254, 9525-9533.

    Google Scholar 

  • Yoshida, T., Yohda, M., Iida, T., Maruyama, T., Taguchi, H., Yazaki, K., Ohta, T., Okada, M., Endo, I., and Kagawa, Y. (1997). J. Mol. Biol. 273, 635-645.

    Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Jichi Medical School, Minamikawachi, Tochigi, 329-0498

    Yasuo Kagawa, Toshiro Hamamoto & Hitoshi Endo

  2. Graduate School, Women's University of Nutrition, Sakado, Saitama, 350-0288, Japan

    Yasuo Kagawa

  3. Graduate School, Women's University of Nutrition, Sakado, Saitama, 350-0288, Japan

    Toshiro Hamamoto & Hitoshi Endo

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Kagawa, Y., Hamamoto, T. & Endo, H. The α/β Interfaces of α1β1, α3β3, and F1: Domain Motions and Elastic Energy Stored during γ Rotation. J Bioenerg Biomembr 32, 471–484 (2000). https://doi.org/10.1023/A:1005612923995

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