Transmembrane topology, genes, and biogenesis of the mitochondrial phosphate and oxoglutarate carriers
- 60 Downloads
- 29 Citations
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.
Key words
Mitochondria carriers sequences transmembrane topology genes biogenesisPreview
Unable to display preview. Download preview PDF.
References
- Adrian, G. S., McCammon, M. T., Montgomery, D. L., and Douglas, M. G. (1986).Mol Cell. Biol. 6 626–634.PubMedGoogle Scholar
- Aquila, H., Link, T. A., and Klingenberg, M. (1987).FEBS Lett. 212 1–9.PubMedGoogle Scholar
- Arends, H., and Sebald, W. (1984).EMBO J. 3 377–382.PubMedGoogle Scholar
- Battini, R., Ferrari, S., Kaczmarek, L., Calabretta, B., Chen, S. T., and Baserga, R. (1987).J. Biol. Chem. 262 4355–4359.PubMedGoogle Scholar
- Bisaccia, F., Indiveri, C., and Palmieri, F. (1985).Biochim. Biophys. Acta 810 362–369.PubMedGoogle Scholar
- Bisaccia, F., Capobianco, L., Brandolin, G., and Palmieri, F. (1993),In preparation.Google Scholar
- Bouillaud, F., Weissenbach, J., Ricquier, D. (1986).J. Biol. Chem. 261 1487–1490.PubMedGoogle Scholar
- Capobianco, L., Brandolin, G., and Palmieri, F. (1991).Biochemistry 30 4963–4969.PubMedGoogle 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.Google Scholar
- 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.PubMedGoogle Scholar
- Ferreira, G. C., Pratt, R. D., and Pedersen, P. L. (1990).J. Biol. Chem. 265 21202–21206.PubMedGoogle 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.PubMedGoogle Scholar
- Guérin, B., Bukusoglu, C., Rakotomanana, F., and Wohlrab, H. (1990).J. Biol. Chem. 265 19736–19741.PubMedGoogle Scholar
- Houldsworth, J., and Attardi, G. (1988).Proc. Natl. Acad. Sci. USA 85 377–381.PubMedGoogle Scholar
- Iacobazzi, V., Palmieri, F., Runswick, M. J., and Walker, J. E. (1992).DNA Seq. 3 79–88.PubMedGoogle Scholar
- Indiveri, C., Palmieri, F., Bisaccia, F., and Krämer, R. (1987).Biochim. Biophys. Acta 890 310–318.PubMedGoogle Scholar
- Indiveri, C., Dierks, T., Krämer, R., and Palmieri, F. (1991).Eur. J. Biochem. 198 339–347.PubMedGoogle Scholar
- Klaus, S., Casteilla, L., Bouillaud, F., and Ricquier, D. (1991).Int. J. Biochem. 23 791–801.PubMedGoogle Scholar
- Klingenberg, M. (1981).Nature (London) 290 449–454.PubMedGoogle 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.PubMedGoogle 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.PubMedGoogle Scholar
- Murakami, H., Blobel, G., and Pain, D. (1990).Nature (London) 347 488–491.PubMedGoogle 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.PubMedGoogle Scholar
- Neckelmann, N., Li, K., Wade, R. P., Shuster, R., and Wallace, D. C. (1987).Proc. Natl. Acad. Sci. USA 84 7580–7584.PubMedGoogle Scholar
- Pain, D., Murakami, H., and Blobed, G. (1990).Nature (London) 347 444–449.PubMedGoogle 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.PubMedGoogle 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.PubMedGoogle Scholar
- Pratt, R. D., Ferreira, G. C., and Pedersen, P. L. (1991).J. Biol. Chem 266 1276–1280.PubMedGoogle Scholar
- Runswick, M. J., Powell, S. J., Nyren, P., and Walker, J. E. (1987).EMBO J. 6 1367–1373.PubMedGoogle Scholar
- Runswick, M. J., Walker, J. E., Bisaccia, F., Iacobazzi, V., and Palmieri, F. (1990).Biochemistry 29 11033–11040.PubMedGoogle Scholar
- Runswick, M. J., Philippedes, A., Lauria, G., and Walker, J. E. (1993).Biochem. J., in press.Google Scholar
- Saraste, M., and Walker, J. E. (1982).FEBS Lett. 144 250–254.PubMedGoogle 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.PubMedGoogle 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.PubMedGoogle Scholar
- Williams, K. R., and Herrick, G. (1991).Nucleic Acids Res. 19 4717–4724.PubMedGoogle Scholar
- Zara, V., Rassow, J., Wachter, E., Tropschug, M., Palmieri, F., Neupert, W., and Pfanner, N. (1991).Eur. J. Biochem. 198 405–410.PubMedGoogle Scholar
- Zara, V., Palmieri, F., Mahlke, K., and Pfanner, N. (1992).J. Biol. Chem. 267 12077–12081.PubMedGoogle 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.PubMedGoogle Scholar