Skip to main content
SpringerLink
Log in

Transmembrane topology, genes, and biogenesis of the mitochondrial phosphate and oxoglutarate carriers

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Phosphate and oxoglutarate carriers transport phosphate and oxoglutarate across the inner membranes of mitochondria in exchange for OH− and malate, respectively. Both carriers belong to the mitochondrial carrier protein family, characterized by a tripartite structure made up of related sequences about 100 amino acids in length. The results obtained on the topology of the phosphate and oxoglutarate carriers are consistent with the six α-helix model proposed by Saraste and Walker. In both carriers the N- and C-terminal regions are exposed toward the cytosol. In addition, the oxoglutarate carrier has been shown to be a dimer by means of cross-linking studies. The bovine and human genes coding for the oxoglutarate carrier are split into eight and six exons, respectively, and five introns are found in the same position in both genes. The bovine and human phosphate carrier genes have the same organization with nine exons separated by eight introns at exactly the same positions. The phosphate carrier of mammalian mitochondria is synthesized with a cleavable presequence, in contrast to the oxoglutarate carrier and the other members of the mitochondrial carrier family. The precursor of the phosphate carrier is efficiently imported, proteolytically processed, and correctly assembled in isolated mitochondria. The presequence-deficient phosphate carrier is imported with an efficiency of about 50% as compared with the precursor of the phosphate carrier and is correctly assembled, demonstrating that the mature portion of the phosphate carrier contains sufficient information for import and assembly into mitochondria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adrian, G. S., McCammon, M. T., Montgomery, D. L., and Douglas, M. G. (1986).Mol Cell. Biol. 6 626–634.

    PubMed  Google Scholar 

  • Aquila, H., Link, T. A., and Klingenberg, M. (1987).FEBS Lett. 212 1–9.

    PubMed  Google Scholar 

  • Arends, H., and Sebald, W. (1984).EMBO J. 3 377–382.

    PubMed  Google Scholar 

  • Battini, R., Ferrari, S., Kaczmarek, L., Calabretta, B., Chen, S. T., and Baserga, R. (1987).J. Biol. Chem. 262 4355–4359.

    PubMed  Google Scholar 

  • Bisaccia, F., Indiveri, C., and Palmieri, F. (1985).Biochim. Biophys. Acta 810 362–369.

    PubMed  Google Scholar 

  • Bisaccia, F., Capobianco, L., Brandolin, G., and Palmieri, F. (1993),In preparation.

  • Bouillaud, F., Weissenbach, J., Ricquier, D. (1986).J. Biol. Chem. 261 1487–1490.

    PubMed  Google Scholar 

  • Capobianco, L., Brandolin, G., and Palmieri, F. (1991).Biochemistry 30 4963–4969.

    PubMed  Google Scholar 

  • Cozens, A. L., Runswick, M. J., and Walker, J. E. (1989).J. Mol. Biol. 206 261–280.

    Google Scholar 

  • Dietmeier, K., Zara, V., Palmisano, A., Palmieri, F., Voos, W., Moczko, M., Kispal, G., and Pfanner, N. (1993), submitted.

  • Dolce, V., Fiermonte, G., Messina, A., and Palmieri, F. (1991).DNA Seq. 2 131–134.

    Google Scholar 

  • Ferreira, G. C., Pratt, R. D., and Pedersen, P. L. (1989).J. Biol. Chem. 264 15628–15633.

    PubMed  Google Scholar 

  • Ferreira, G. C., Pratt, R. D., and Pedersen, P. L. (1990).J. Biol. Chem. 265 21202–21206.

    PubMed  Google Scholar 

  • Fiermonte, G., Runswick, M. J., Walker, J. E., and Palmieri, F. (1992).DNA Seq. 3 71–78.

    Google Scholar 

  • Fiermonte, G., Walker, J. E., and Palmieri, F. (1993).Biochem. J. 294 293–299.

    PubMed  Google Scholar 

  • Guérin, B., Bukusoglu, C., Rakotomanana, F., and Wohlrab, H. (1990).J. Biol. Chem. 265 19736–19741.

    PubMed  Google Scholar 

  • Houldsworth, J., and Attardi, G. (1988).Proc. Natl. Acad. Sci. USA 85 377–381.

    PubMed  Google Scholar 

  • Iacobazzi, V., Palmieri, F., Runswick, M. J., and Walker, J. E. (1992).DNA Seq. 3 79–88.

    PubMed  Google Scholar 

  • Indiveri, C., Palmieri, F., Bisaccia, F., and Krämer, R. (1987).Biochim. Biophys. Acta 890 310–318.

    PubMed  Google Scholar 

  • Indiveri, C., Dierks, T., Krämer, R., and Palmieri, F. (1991).Eur. J. Biochem. 198 339–347.

    PubMed  Google Scholar 

  • Klaus, S., Casteilla, L., Bouillaud, F., and Ricquier, D. (1991).Int. J. Biochem. 23 791–801.

    PubMed  Google Scholar 

  • Klingenberg, M. (1981).Nature (London) 290 449–454.

    PubMed  Google Scholar 

  • Klingenberg, M., Gawaz, M., Douglas, M. G., and Lawson, J. E. (1992). InMolecular Mechanisms of Transport (Quagliariello, E., and Palmieri, F., eds.), Elsevier, Amsterdam, pp. 187–195.

    Google Scholar 

  • Kozak, L. P., Britton, J. H., Kozak, U. C., and Wells, J. M. (1988).J. Biol. Chem. 263 12274–12277.

    PubMed  Google Scholar 

  • Krämer, R., and Palmieri, F. (1989).Biochim, Biophys. Acta 974 1–23.

    Google Scholar 

  • Krämer, R., and Palmieri, F. (1992). InMolecular Mechanisms in Bioenergetics (Ernster, L., ed.), Elsevier, Amsterdam, 359–384.

    Google Scholar 

  • Martin, J., Mahlke, K., and Pfanner, N. (1991).J. Biol. Chem. 266 18051–18057.

    PubMed  Google Scholar 

  • Murakami, H., Blobel, G., and Pain, D. (1990).Nature (London) 347 488–491.

    PubMed  Google Scholar 

  • Murdza-Inglis, D. L., Patel, H. V., Freeman, K. B., Jezek, P., Orosz, D. E., and Garlid, K. D. (1991).J. Biol. Chem. 266 11871–11875.

    PubMed  Google Scholar 

  • Neckelmann, N., Li, K., Wade, R. P., Shuster, R., and Wallace, D. C. (1987).Proc. Natl. Acad. Sci. USA 84 7580–7584.

    PubMed  Google Scholar 

  • Pain, D., Murakami, H., and Blobed, G. (1990).Nature (London) 347 444–449.

    PubMed  Google Scholar 

  • Palmieri, F., Basaccia, F., Capobianco, L., Dolce, V., Iacobazzi, V., Indiveri, C., and Zara, V. (1992a). InMolecular Mechanisms of Transport (Quagliariello, E., and Palmieri, F. eds.), Elsevier, Amsterdam, pp. 151–158.

    Google Scholar 

  • Palmieri, F., Bisaccia, F., Iacobazzi, V., Indiveri, C., and Zara, V. (1992b).Biochim. Biophys. Acta 1101 223–227.

    PubMed  Google Scholar 

  • Palmieri, F., Indiveri, C., Bisaccia, F., and Krämer, R. (1993).J. Bionerg. Biomembr. 25 525–535.

    Google Scholar 

  • Phelps, A., Schobert, C., and Wohlrab, H. (1991).Biochemistry 30 248–252.

    PubMed  Google Scholar 

  • Pratt, R. D., Ferreira, G. C., and Pedersen, P. L. (1991).J. Biol. Chem 266 1276–1280.

    PubMed  Google Scholar 

  • Runswick, M. J., Powell, S. J., Nyren, P., and Walker, J. E. (1987).EMBO J. 6 1367–1373.

    PubMed  Google Scholar 

  • Runswick, M. J., Walker, J. E., Bisaccia, F., Iacobazzi, V., and Palmieri, F. (1990).Biochemistry 29 11033–11040.

    PubMed  Google Scholar 

  • Runswick, M. J., Philippedes, A., Lauria, G., and Walker, J. E. (1993).Biochem. J., in press.

  • Saraste, M., and Walker, J. E. (1982).FEBS Lett. 144 250–254.

    PubMed  Google Scholar 

  • Steger, H. F., Söllner, T., Kiebler, M., Dietmeier, K. A., Pfaller, R., Trülzsch, K. S., Tropschug, M., Neupert, W., and Pfanner, N. (1990).J. Cell. Biol. 111 2353–2363.

    PubMed  Google Scholar 

  • Walker, J. E., Cozens, A. L., Dyer, M. R., Fearnley, I. M., Powell, S. J., and Runswick, M. J. (1987).Chem. Scr. 27B 97–105.

    Google Scholar 

  • Walker, J. E., (1992).Curr. Opinion Struct. Biol. 2 519–526.

    Google Scholar 

  • Weisenberger, G., Link, T. A., von Ahsen, U., Waldherr, M., and Schweyen, R. J. (1991).J. Mol. Biol. 217 23–37.

    PubMed  Google Scholar 

  • Williams, K. R., and Herrick, G. (1991).Nucleic Acids Res. 19 4717–4724.

    PubMed  Google Scholar 

  • Zara, V., Rassow, J., Wachter, E., Tropschug, M., Palmieri, F., Neupert, W., and Pfanner, N. (1991).Eur. J. Biochem. 198 405–410.

    PubMed  Google Scholar 

  • Zara, V., Palmieri, F., Mahlke, K., and Pfanner, N. (1992).J. Biol. Chem. 267 12077–12081.

    PubMed  Google Scholar 

  • Zarrilli, R., Oates, E. L., McBride, O. W., Lerman, M. I., Chan, J. Y., Santisteban, P., Ursini, M. V., Notkins, A. L., and Kohn, L. D. (1989).Mol. Endocrinol. 3 1498–1508.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmaco-Biology, Laboratory of Biochemistry and Molecular Biology, University of Bari, Via E. Orabona 4, Bari, Italy

    F. Palmieri, F. Bisaccia, L. Capobianco, V. Dolce, G. Fiermonte, V. Iacobazzi & V. Zara

Authors
  1. F. Palmieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Bisaccia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. Capobianco
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. Dolce
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Fiermonte
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Iacobazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. V. Zara
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palmieri, F., Bisaccia, F., Capobianco, L. et al. Transmembrane topology, genes, and biogenesis of the mitochondrial phosphate and oxoglutarate carriers. J Bioenerg Biomembr 25, 493–501 (1993). https://doi.org/10.1007/BF01108406

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01108406

Key words

Search

Navigation