Abstract
Mitochondrial ATP synthase (F1F0-ATPase) is regulated by an intrinsic ATPase inhibitor protein. In this study, we overexpressed and purified human and bovine ATPase inhibitors and their properties were compared with those of a yeast inhibitor. The human and bovine inhibitors inhibited bovine ATPase in a similar way. The yeast inhibitor also inhibited bovine F1F0-ATPase, although the activity was about three times lower than the mammalian inhibitors. All three inhibitors inhibited yeast F1F0-ATPase in a similar way. The activities of all inhibitors decreased at higher pH, but the magnitude of the decrease was different for each combination of inhibitor and ATPase. The results obtained in this study show that the inhibitory mechanism of the inhibitors was basically shared in yeast and mammals, but that mammalian inhibitors require unique residues, which are lacking in the yeast inhibitor, for their maximum inhibitory activity. Common inhibitory sites of mammalian and yeast inhibitors are suggested.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrahams, J. P., Leslie, A. G. W., Lutter, R., and Walker, J. E. (1994). Nature 370, 621–628.
Boyer, P. D. (1997). Annu. Rev. Biochem. 66, 717–749.
Cabezón, E., Butler, P. J. G., Runswick, M. J., Carbajo, R. J., and Walker, J. E. (2002). J. Biol. Chem. 277, 41334–41341.
Cabezón, E., Runswick, M. J., Leslie, A. G. W., and Walker, J. E. (2001). EMBO J. 20, 6990–6996.
Dianoux, A. C., and Hoppe, J. (1987). Eur. J. Biochem. 163, 155–160.
Frangione, B., Rosenwasser, E., Penefsky, H. S., and Pullman, M. E. (1981). Proc. Natl. Acad. Sci. U.S.A. 78, 7403–7407.
Gordon-Smith, D. J., Carbajo, R. J., Yang, J.-C., Videler, H., Runswick, M. J., Walker, J. E., and Neuhaus, D. (2001). J. Mol. Biol. 308, 325–339.
Hara, K. Y., Kato-Yamada, Y., Kikuchi Y., Hisabori, T., and Yoshida, M. (2001). J. Biol. Chem. 276, 23969–23973.
Hashimoto, T., Yoshida, Y., and Tagawa, K. (1984). J. Biochem. 95, 131–136.
Higuti, T., Kuroiwa, K., Kawamura, Y., Morimoto, K., and Tsujita, H. (1993). Biochim. Biophys. Acta 1172, 311–314.
Horstman, L. L., and Racker, E. (1970). J. Biol. Chem. 245, 1336–1344.
Ichikawa, N., Fujisaka, R., and Kuribayashi, R. (2000). Biosci. Biotechnol. Biochem. 64, 89–95.
Ichikawa, N., Fukuda, M., Hashimoto, T., and Tagawa, K. (1998). J. Biochem. 124, 886–891.
Ichikawa, N., Karaki, A., Kawabata, M., Ushida, S., Mizushima, M., and Hashimoto, T. (2001). J. Biochem. 130, 687–693.
Ichikawa, N., Nakabayashi, K., and Hashimoto, T. (2002). J. Biochem. 132, 649–654.
Ichikawa, N., Ushida, S., Kawabata, M., and Masazumi, Y. (1999). Biosci. Biotechnol. Biochem. 63, 2225–2227.
Ichikawa, N., Yoshida, Y., Hashimoto, T., Ogasawara, N., Yoshikawa, H., Imamoto, F., and Tagawa, K. (1990). J. Biol. Chem. 265, 6274–6278.
Kato-Yamada, Y., Bald, D., Koike, M., Motohashi, K., Hisabori, T., and Yoshida, M. (1999). J. Biol. Chem. 274, 33991–33994.
Kitamura, M., Kojima, S., Ogasawara, K., Nakaya, T., Sagara, T., Niki, K., Miura, K., Akutsu, H., and Kumagai, I. (1994). J. Biol. Chem. 269, 5566–5573.
Kuki, M., Noumi, T., Maeda, M., Amemura, A., and Futai, M. (1988). J. Biol. Chem. 263, 17437–17442.
Lebowitz, M. S., and Pedersen, P. L. (1993). Arch. Biochem. Biophys. 301, 64–70.
Lebowitz, M. S., and Pedersen, P. L. (1996). Arch. Biochem. Biophys. 330, 342–354.
Lopez-Mediavilla, C., Vigny, H., and Godinot, C. (1993). Eur. J. Biochem. 215, 487–496.
Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951). J. Biol. Chem. 193, 265–275.
Matsubara, H., Hase, T., Hashimoto, T., and Tagawa, K. (1981). J. Biochem. 90, 1159–1165.
Moriyama, Y., Iwamoto, A., Hanada, H., Maeda, M., and Futai, M. (1991). J. Biol. Chem. 266, 22141–22146.
Noji, H., Yasuda, R., Yoshida, M., and Kinosita, K., Jr. (1997). Nature 386, 299–302.
Omote, H., Tainaka, K., Fujie, K., Iwamoto-Kihara, A., Wada, Y., and Futai, M. (1998). Arch. Biochem. Biophys. 358, 277–282.
Pullman, M. E., and Monroy, G. C. (1963). J. Biol. Chem. 238, 3762–3769.
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.
Schnizer, R., Van Heeke, G., Amaturo, D., and Schuster, S. M. (1996). Biochim. Biophys. Acta 1292, 241–248.
Schwerzmann, K., and Pedersen, P. L. (1986). Arch. Biochem. Biophys. 250, 1–18.
Sternweis, P. C., and Smith, J. B. (1980). Biochemistry 19, 526–531.
Takeshige, K., Hess, B., Böhm, M., and Zimmermann-Telschow, H. (1976). Hoppe-Seyler's Z. Physiol. Chem. 357, 1605–1622.
van Raaij, M. J., Orriss, G. L., Montgomery, M. G., Runswick, M. J., Fearnley, I. M., Skehel, J. M., and Walker, J. E. (1996). Biochemistry 35, 15618–15625.
Yamada, E., Ishiguro, N., Miyaishi, O., Takeuchi, A., Nakashima, I., Iwata, H., and Isobe, K. (1997). Immunology 92, 571–576.
Zanotti, F., Raho, G., Vuolo, R., Gaballo, A., Papa, F., and Papa, S. (2000). FEBS Lett. 482, 163–166.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ichikawa, N., Ogura, C. Overexpression, Purification, and Characterization of Human and Bovine Mitochondrial ATPase Inhibitors: Comparison of the Properties of Mammalian and Yeast ATPase Inhibitors. J Bioenerg Biomembr 35, 399–407 (2003). https://doi.org/10.1023/A:1027383629565
Issue Date:
DOI: https://doi.org/10.1023/A:1027383629565