Biogenesis of yeast dicarboxylate carrier: The carrier signature facilities translocation across the mitochondrial outer membrane

Journal of Cell Science

Volumn 120, Issue 23, 2007, Pages 4099-4106

  Zara, Vincenzo ^a   Ferramosca, Alessandra ^a   Capoblanco, Loredana ^a,b   Baltz, Katrin M ^c,d   Randel, Olga ^c   Rassow, Joachim ^c   Palmieri, Ferdinando ^b   Papatheodorou, Panagiotis ^c  

^a UNIVERSITY OF SALENTO   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Carrier signature; Metabolite carrier proteins; Mitochondria

Indexed keywords

ALANINE; AMINO ACID; CARRIER PROTEIN; DICARBOXYLIC ACID; PHOSPHATE; PROTEIN TOM70; RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONTROLLED STUDY; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE;

ALANINE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CONSERVED SEQUENCE; DICARBOXYLIC ACID TRANSPORTERS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PHOSPHATES; PHOSPHORUS RADIOISOTOPES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SULFUR RADIOISOTOPES; TIME FACTORS;

EID: 38349014361     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.018929     Document Type: Article

References (50)

1. Aquila, U., Misra, D., Eulitz, M. and Klingenberg, M. (1982). Complete amino acid sequence of the ADP/ATP carrier from beef heart mitochondria. Hoppe Seylers Z. Physiol. Chem. 363, 345-349.
2. Arends, H. and Sebald, W. (1984). Nucleotide sequence of the cloned mRNA and gene of the ADP/ATP carrier from Neurospora crassa. EMBO J. 3, 377-382.
3. Bauer, M. F., Hofmann, S., Neupert, W. and Brunner, M. (2000), Protein translocation into mitochondria: the role of TIM complexes. Trends Cell Biol. 10, 25-31.
4. Brandner, K., Rehling, P. and Truscott, K. N. (2005). The carboxyl-terminal third of the dicarboxylate carrier is crucial for productive association with the inner membrane twin-pore translocase. J. Biol. Chem. 280, 6215-6221.
5. Brix, J., Ziegler, G. A., Dietmeier, K., Schneider-Mergener, J., Schutz, G. E. and Pfanner, N. (2000). The mitochondrial import receptor Tom70: identification of a 25 kDa core domain with a specific binding site for preproteins. J. Mol. Biol. 303, 479-488.
6. Capobianco, L., Bisaccia, F., Mazzeo, M. and Palmieri, F. (1996), The mitochondrial oxoglutarate carrier: sulfhydryl reagents bind to cysteine-184, and this interaction is enhanced by substrate binding. Biochemistry 35, 8974-8980.
7. Cappello, A. R., Miniero, D. V., Curcio, R., Ludovico, A., Daddabbo, L., Stipani, I., Robinson, A. J., Kunji, E. R. and Palmieri, F. (2007). Functional and structural role of amino acid residues in the odd-numbered transmembrane alpha-helices of the bovine mitochondrial oxoglutarate carrier. J. Mol. Biol. 369, 400-412.
8. Curran, S. P., Leuenberger, D., Oppliger, W. and Koehler, C. M. (2002). The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP/ATP carrier. EMBO J. 21, 942-953.
9. Davis, A. J., Sepuri, N. B., Holder, J., Johnson, A. E. and Jensen, R. E. (2000). Two intermembrane space TIM complexes interact with different domains of Tim23p during its import into mitochondria. J. Cell Biol. 150, 1271-1282.
10. de Marcos-Lousa, C., Sideris, D. P. and Tokatlidis, K. (2006). Translocation of mitochondrial inner-membrane proteins: conformation matters. Trends Biochem. Sci. 31, 259-267.
11. Endres, M., Neupert, W. and Brunner, M. (1999). Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J. 18, 3214-3221.
12. Fiermonte, G., Palmieri, L., Dolce, V., Lasorsa, F. M., Palmieri, F., Runswick, M. J. and Walker, J. E. (1998). The sequence, bacterial expression, and functional reconstitution of the rat mitochondrial dicarboxylate transporter cloned via distant homologs in yeast and Caenorhabditis elegans. J. Biol. Chem. 273, 24754-24759.
13. Huang, S., Ratliff, K. S., Schwartz, M. P., Spenner, J. M. and Matouschek, A. (1999). Mitochondria unfold precursor proteins by unraveling them from their N-termini. Nat. Struct. Biol. 6, 1132-1138.
14. Kakhniashvili, D., Mayor, J. A., Gremse, D. A., Xu, Y. and Kaplan, R. S. (1997). Identification of a novel gene encoding the yeast mitochondrial dicarboxylate transport protein via overexpression, purification, and characterization of its protein product. J. Biol. Chem. 272, 4516-4521.
15. Kaplan, R. S., Mayor, J. A., Gremse, D. A. and Wood, D. O. (1995). High level expression and characterization of the mitochondrial citrate transport protein from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 270, 4108-4114.
16. Klingenberg, M., Winkler, E. and Huang, S. (1995). ADP/ATP carrier and uncoupling protein. Meth. Enzymol. 260, 369-389.
17. Koehler, C. M., Jarosch, E., Tokatlidis, K., Schmid, K., Schweyen, R. J. and Schatz, G. (1998). Import of mitochondrial carriers mediated by essential proteins of the intermembrane space. Science 279, 369-373.
18. Kunji, E. R. (2004). The role and structure of mitochondrial carriers. FEBS Lett. 564, 239-244.
19. Lancar-Benba, J., Foucher, B. and Saint-Macary, M. (1996). Characterization, purification and properties of the yeast mitochondrial dicarboxylate carrier (Saccharomyces cerevisiae). Biochimie 78, 195-200.
20. Leuenberger, D., Bally, N. A., Schatz, G. and Koehler, C. M. (1999). Different import pathways through the mitochondrial intermembrane space for inner membrane proteins. EMBO J. 18, 4816-4822.
21. Luciano, P., Vial, S., Vergnolle, M. A., Dyall, S. D., Robinson, D. R. and Tokatlidis, K. (2001). Functional reconstitution of the import of the yeast ADP/ATP carrier mediated by the TIM10 complex. EMBO J. 20, 4099-4106.
22. Moczko, M., Ehmann, B., Gärtner, F., Hönlinger, A., Schäfer, E. and Pfanner, N. (1994). Deletion of the receptor MOM19 strongly impairs import of cleavable preproteins into Saccharomyces cerevisiae mitochondria. J. Biol. Chem. 269, 9045-9051.
23. Nelson, D. R., Felix, C. M. and Swanson, J. M. (1998). Highly conserved charge-pair networks in the mitochondrial carrier family. J. Mol. Biol. 277, 285-308.
24. Neupert, W. and Herrmann, J. M. (2007). Trarslocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749.
25. Nury, H., Dahout-Gonzalez, C., Trezeguet, V., Lauquin, G. J., Brandolin, G. and Pebay-Peyroula, E. (2006). Relations between structure and function of the mitochondrial ADP/ATP carrier. Annu. Rev. Biochem. 75, 713-741.
26. Palmieri, F. (1994). Mitochondrial carrier proteins. FEBS Lett. 346, 48-54.
27. Palmieri, F., Indiveri, C., Bisaccia, F. and Iacobazzi, V. (1995). Mitochondrial metabolite carrier proteins: purification, reconstitution, and transport studies. Meth. Enzymol. 260, 349-369.
28. Palmieri, L., Palmieri, F., Runswick, M. J. and Walker, J. E. (1996). Identification by bacterial expression and functional reconstitution of the yeast genomic sequence encoding the mitochondrial dicarboxylate carrier protein. FEBS Lett. 399, 299-302.
29. Palmieri, L., Vozza, A., Agrimi, G., De Marco, V., Runswick, M. J., Palmieri, F. and Walker, J. E. (1999). Identification of the yeast mitochondrial transporter for oxaloacetate and sulfate. J. Biol. Chem. 274, 22184-22190.
30. Papatheodorou, P., Domanska, G. and Rassow, J. (2007). Protein targeting to mitochondria of Saccharomyces cerevisiae and Neurospora crassa. In Methods in Molecular Biology: Protein Targeting Protocols. 2nd edn (ed. M. van der Giezen), pp. 151-166. Totowa, NJ: Humana Press.
31. Papworth, C., Bauer, J. C., Braman, J. and Wright, D. A. (1996). QuikChange site-directed mutagenesis. Strategies 9, 3-4.
32. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trezeguet, V., Lauquin, G. J. and Brandolin, G. (2003). Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44.
33. Pfanner, N. and Geissler, A. (2001). Versatility of the mitochondrial protein import machinery. Nat. Rev. Mol. Cell Biol. 2, 339-349.
34. Pfanner, N. and Neupert, W. (1987). Distinct steps in the import of ADP/ATP carrier into mitochondria. J. Biol. Chem. 262, 7528-7536.
35. Rassow, J., Hartl, F. U., Guiard, B., Pfanner, N. and Neupert, W. (1990). Polypeptides traverse the mitochondrial envelope in ail extended state. FEBS Lett. 275, 190-194.
36. Rehling, P., Brandner, K. and Pfanner, N. (2004). Mitochondrial import and the twinpore translocase. Nat. Rev. Mol. Cell Biol. 5, 519-530.
37. Ryan, M. T., Müller, H. and Pfanner, N. (1999). Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane. J. Biol. Chem. 274, 20619-20627.
38. Sikorski, R. S. and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
39. Sirrenberg, C., Endres, M., Fölsch, H., Stuart, R. A., Neupert, W. and Brunner, M. (1998). Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391, 912-915.
40. + transporter in Saccharomyces cerevisiae. J. Biol. Chem. 281, 1524-1531.
41. Truscott, K. N., Wiedemann, N., Rehling, P., Müller, H., Meisinger, C., Pfanner, N. and Guiard, B. (2002). Mitochondrial import of the ADP/ATP carrier: the essential TIM complex of the intermembrane space is required for precursor release from the TOM complex. Mol. Cell. Biol. 22, 7780-7789.
42. Tzagoloff, A., Jang, J., Glerum, D. M. and Wu, M. (1996). FLX1 codes for a carrier protein involved in maintaining a proper balance of flavin nucleotides in yeast mitochondria. J. Biol. Chem. 271, 7392-7397.
43. Vasiljev, A., Ahting, U., Nargang, F. E., Go, N. E., Habib, S. J., Kozany, C., Panneels, V., Sinning, I., Prokisch, H., Neupert, W. et al. (2004). Reconstituted TOM core complex and Tim9/Tim10 complex of mitochondria are sufficient for translocation of the ADP/ATP carrier across membranes. Mol. Biol. Cell 15, 1445-1458.
44. Vial, S., Lu, H., Allen, S., Savory, P., Thornton, D., Sheehan, J. and Tokatlidis, K. (2002). Assembly of Tim9 and Tim10 into a functional chaperone. J. Biol. Chem. 277, 36100-36108.
45. Wiedemann, N., Pfanner, N. and Ryan, M. T. (2001). The three modules of ADP/ATP carrier cooperate in receptor recruitment and translocation into mitochondria. EMBO J. 20, 951-960.
46. Zara, V., Palmisano, I., Rassow, J. and Palmieri, F. (2001). Biogenesis of the dicarboxylate carrier (DIC): Translocation across the mitochondrial outer membrane and subsequent release from the TOM channel are membrane potential-independent. J. Mol. Biol. 310, 965-971.
47. Zara, V., Ferramosca, A. and Rassow, J. (2003a). Import of metabolite carrier proteins into mitochondria. In Recent Research Developments in Molecular and Cellular Biology. Vol. 4 (ed. S. G. Pandalai),pp. 101-114. Kerala, India: Research Signpost.
48. Zara, V., Ferramosca, A., Palmisano, I., Palmieri, F. and Rassow, J. (2003b). Biogenesis of rat mitochondrial citrate carrier (CIC): The N-terminal presequence facilitates the solubility of the preprotein but does not act as a targeting signal. J. Mol. Biol. 325, 399-408.
49. Zara, V., Ferramosca, A., Papatheodorou, P., Palmieri, F. and Rassow, J. (2005). Import of rat mitochondrial citrate carrier (CIC) at increasing salt concentrations promotes presequence binding to import receptor Tom20 and inhibits membrane translocation. J. Cell Sci. 118, 3985-3995.
50. Zara, V., Dolce, V., Capobianco, L., Ferramosca, A., Papatheodorou, P., Rassow, J. and Palmieri, F. (2007). Biogenesis of eel liver citrate carrier (CIC): negative charges can substitute for positive charges in the presequence. J. Mol. Biol. 365, 958-967.