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Subunit composition, biosynthesis, and assembly of the yeast vacuolar proton-translocating ATPase

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Abstract

The yeast vacuole is acidified by a vacuolar proton-translocating ATPase (H+-ATPase) that closely resembles the vacuolar H+-ATPases of other fungi, animals, and plants. The yeast enzyme is purified as a complex of eight subunits, which include both integral and peripheral membrane proteins. The genes for seven of these subunits have been cloned, and mutant strains lacking each of the subunits (vma mutants) have been constructed. Disruption of any of the subunit genes appears to abolish the function of the vacuolar H+-ATPase, supporting the subunit composition derived from biochemical studies. Genetic studies of vacuolar acidification have also revealed an additional set of gene products that are required for vacuolar H+-ATPase activity, but may not be part of the final enzyme complex. The biosynthesis, assembly, and targeting of the enzyme is being elucidated by biochemical and cell biological studies of thevma mutants. Initial results suggest that the peripheral and integral membrane subunits may be independently assembled.

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References

  • Adachi, I., Puopolo, K., Marquez-Sterling, N., Arai, H., and Forgac, M. (1990).J. Biol. Chem. 265, 967–973.

    Google Scholar 

  • Anraku, Y., Hirata, R., Umemoto, N., and Ohya, Y. (1991). InNew Era of Bioenergetics (Mukohata, Y., ed.), Academic Press, pp. 131–168.

  • Arai, H., Berne, M., and Forgac, M. (1987a).J. Biol. Chem. 262, 11006–11011.

    Google Scholar 

  • Arai, H., Berne, M., Terres, G., Terres, H., Puopolo, K., and Forgac, M. (1987b).Biochemistry 26, 6632–6638.

    Google Scholar 

  • Arai, H., Terres, G., Pink, S., and Forgac, M. (1988).J. Biol. Chem. 263, 8796–8802.

    Google Scholar 

  • Aris, J. P., Klionsky, D. J., and Simoni, R. D. (1985).J. Biol. Chem. 260, 11207–11215.

    Google Scholar 

  • Banta, L. M., Robinson, J. S., Klionsky, D. J., and Emr, S. D. (1988).J. Cell. Biol. 107, 1369–1383.

    Google Scholar 

  • Bonifacino, J. S., Lippincott-Schwartz, J., Chen, C., Antusch, D., Samelson, L. E., and Klausner, R. D. (1988).J. Biol. Chem. 263, 8965–8971.

    Google Scholar 

  • Bowman, B. J., Dschida, W. J., Harris, T., and Bowman, E. J. (1989).J. Biol. Chem. 264, 15606–15612.

    Google Scholar 

  • Bowman, E. J. (1983).J. Biol. Chem. 258, 15238–15244.

    Google Scholar 

  • Bowman, E. J., Tenney, K., and Bowman, B. J. (1988).J. Biol. Chem. 263, 13994–14001.

    Google Scholar 

  • Forgac, M. (1989).Physiol. Rev. 69, 765–796.

    Google Scholar 

  • Foury, F. (1990).J. Biol. Chem. 265, 18554–18560.

    Google Scholar 

  • Franzusoff, A., and Schekman, R. (1989).EMBO J. 8, 2695–2702.

    Google Scholar 

  • Gluck, S., and Caldwell, J. (1987).J. Biol. Chem. 262, 15780–15789.

    Google Scholar 

  • Hirata, R., Ohsumi, Y., Nakano, A., Kawasaki, H., Suzuki, K., and Anraku, Y. (1990).J. Biol. Chem. 265, 6726–6733.

    Google Scholar 

  • Hirsch, S., Strauss, A., Masood, K., Lee, S., Sukhatme, V., and Gluck, S. (1988).Proc. Natl. Acad. Sci. USA 85, 3004–3008.

    Google Scholar 

  • Hurtley, S. M., and Helenius, A. (1989).Annu. Rev. Cell Biol. 5, 277–307.

    Google Scholar 

  • Johnson, L. M., Bankaitis, V. A., and Emr, S. D. (1987).Cell 48, 875–885.

    Google Scholar 

  • Jones, E. W. (1984).Annu. Rev. Genet. 18, 233–270.

    Google Scholar 

  • Kaestner, K. H., Randall, S. K., and Sze, H. (1988).J. Biol. Chem. 263, 1282–1287.

    Google Scholar 

  • Kane, P. M., Yamashiro, C. T., Rothman, J. H., and Stevens, T. H. (1989a).J. Cell. Sci. Suppl. 11, 161–178.

    Google Scholar 

  • Kane, P. M., Yamashiro, C. T., and Stevens, T. H. (1989b).J. Biol. Chem. 264, 19236–19244.

    Google Scholar 

  • Kane, P. M., Yamashiro, C. T., Wolczyk, D. F., Neff, N., Goebl, M., and Stevens, T. H. (1990).Science 250, 651–657.

    Google Scholar 

  • Kane, P. M., Kuehn, M. C., Howald, I., and Stevens, T. H. (1992).J. Biol. Chem. 267, 447–454.

    Google Scholar 

  • Klionsky, D. J., and Emr, S. D. (1989).EMBO J. 8, 2241–2250.

    Google Scholar 

  • Klionsky, D. J., and Simoni, R. D. (1985).J. Biol. Chem. 260, 11200–11206.

    Google Scholar 

  • Klionsky, D. J., Banta, L. M., and Emr, S. D. (1988).Mol. Cell. Biol. 8, 2105–2116.

    Google Scholar 

  • Klionsky, D. J., Herman, P. K., and Emr, S. D. (1990).Microbiol. Rev.54, 266–292.

    Google Scholar 

  • Manolson, M. F., Rea, P. A., and Poole, R. J. (1985).J. Biol. Chem. 260, 12273–12279.

    Google Scholar 

  • Matile, P. (1978).Annu. Rev. Plant Physiol. 29, 193–213.

    Google Scholar 

  • Moriyama, Y., and Nelson, N. (1987).J. Biol. Chem. 262, 9175–9180.

    Google Scholar 

  • Moriyama, Y., and Nelson, N. (1989).J. Biol. Chem. 264, 3577–3582.

    Google Scholar 

  • Nelson, H., and Nelson, N. (1989).FEBS Lett. 247, 147–153.

    Google Scholar 

  • Nelson, H., and Nelson, N. (1990).Proc. Natl. Acad. Sci. USA 87, 3503–3507.

    Google Scholar 

  • Nelson, H., Mandiyan, S., and Nelson, N. (1989).J. Biol. Chem. 264, 1775–1778.

    Google Scholar 

  • Nelson, H., Mandiyan, S., Noumi, T., Moriyama, Y., Miedel, M. C., and Nelson, N. (1990).J. Biol. Chem. 265, 20390–20393.

    Google Scholar 

  • Nelson, N., and Taiz, L. (1989).Trends Biochem. Sci. 14, 113–116.

    Google Scholar 

  • Nobrega, M. P., Nobrega, F. G., and Tzagoloff, A. (1990).J. Biol. Chem. 265, 14220–14226.

    Google Scholar 

  • Noumi, T., Beltran, C., Nelson, H., and Nelson, N. (1991).Proc. Natl. Acad. Sci. USA 88, 1938–1942.

    Google Scholar 

  • Novick, P., Ferro, S., and Schekman, R. (1981).Cell 25, 461–469.

    Google Scholar 

  • Ohsumi, Y., and Anraku, Y. (1981).J. Biol. Chem. 256, 2079–2082.

    Google Scholar 

  • Ohsumi, Y., and Anraku, Y. (1983).J. Biol. Chem. 258, 5614–5617.

    Google Scholar 

  • Ohya, Y., Umemoto, N., Tanida, I., Ohta, A., Iida, H., and Anraku, Y. (1991).J. Biol. Chem. 266, 13971–13977.

    Google Scholar 

  • Parry, R. V., Turner, J. C., and Rea, P. A. (1989).J. Biol. Chem. 264, 20025–20032.

    Google Scholar 

  • Pedersen, P. L., and Carafoli, E. (1987).Trends Biochem. Sci. 12, 146–150.

    Google Scholar 

  • Perin, M. S., Fried, V. A., Stone, D. K., Xie, X.-S., and Sudhof, T. C. (1991).J. Biol. Chem. 266, 3877–3881.

    Google Scholar 

  • Puopolo, K., and Forgac, M. (1990).J. Biol. Chem. 265, 14836–14841.

    Google Scholar 

  • Preston, R. A., Murphy, R. F., and Jones, E. W. (1989).Proc. Natl. Acad. Sci. USA 86, 7027–7031.

    Google Scholar 

  • Raymond, C. K., O'Hara, P. J., Eichinger, G., Rothman, J. H., and Stevens, T. H. (1990).J. Cell. Biol. 111, 877–892.

    Google Scholar 

  • Raymond, C. K., Roberts, C. J., Moore, K. E., Howald-Stevenson, I., and Stevens, T. H. (1992).Int. Rev. Cytol., in press.

  • Rea, P. A., Griffith, C. J., and Sanders, D. (1987).J. Biol. Chem. 262, 14745–14752.

    Google Scholar 

  • Roberts, C. J., Pohlig, G., Rothman, J. H., and Stevens, T. H. (1989).J. Cell. Biol. 108, 1363–1373.

    Google Scholar 

  • Shih, C.-K., Wagner, R., Feinstein, S., Kanik-Ennulat, C., and Neff, N. (1988).Mol. Cell. Biol. 8, 3094–3103.

    Google Scholar 

  • Shih, C.-K., Kwong, J., Montalvo, E., and Neff, N. (1990).Mol. Cell. Biol. 10, 3397–3404.

    Google Scholar 

  • Stevens, T. H., Esmon, B., and Schekman, R. (1982).Cell 30, 439–448.

    Google Scholar 

  • Sun, S.-Z., Xie, X.-S., and Stone, D. K. (1987).J. Biol. Chem. 262, 14790–14794.

    Google Scholar 

  • Uchida, E., Ohsumi, Y., and Anraku, Y. (1985).J. Biol. Chem. 260, 1090–1095.

    Google Scholar 

  • Uchida, E., Ohsumi, Y., and Anraku, Y. (1988).J. Biol. Chem. 263, 45–51.

    Google Scholar 

  • Umemoto, N., Yoshihisa, T., Hirata, R., and Anraku, Y. (1990).J. Biol. Chem. 265, 18447–18453.

    Google Scholar 

  • Umemoto, N., Ohya, Y., and Anraku, Y. (1991).J. Biol. Chem. 266, 24526–24532.

    Google Scholar 

  • Valls, L., Hunter, C. P., Rothman, J. H., and Stevens, T. H. (1987).Cell 48, 887–897.

    Google Scholar 

  • Wang, S.-Y., Moriyama, Y., Mandel, M., Hulmes, J. D., Pan, Y.-C. E., Danho, W., Nelson, H., and Nelson N. (1988).J. Biol. Chem. 263, 17638–17642.

    Google Scholar 

  • Winther, J. R., Stevens, T. H., and Kielland-Brandt, M. C. (1991).Eur. J. Biochem. 197, 681–689.

    Google Scholar 

  • Xie, X.-S., and Stone, D. K. (1986).J. Biol. Chem. 261, 2492–2495.

    Google Scholar 

  • Yamashiro, C. T., Kane, P. M., Wolczyk, D. F., Preston, R. A., and Stevens, T. H. (1990).Mol. Cell. Biol. 10, 3737–3749.

    Google Scholar 

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Authors and Affiliations

  1. Department of Chemistry, College of William and Mary, 23187, Williamsburg, Virginia

    Patricia M. Kane

  2. Institute of Molecular Biology, University of Oregon, 97403, Eugene, Oregon

    Tom H. Stevens

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  1. Patricia M. Kane
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Kane, P.M., Stevens, T.H. Subunit composition, biosynthesis, and assembly of the yeast vacuolar proton-translocating ATPase. J Bioenerg Biomembr 24, 383–393 (1992). https://doi.org/10.1007/BF00762531

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  • DOI: https://doi.org/10.1007/BF00762531

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