Molecular identification of three Arabidopsis thaliana mitochondrial dicarboxylate carrier isoforms: Organ distribution, bacterial expression, reconstitution into liposomes and functional characterization

Biochemical Journal

Volumn 410, Issue 3, 2008, Pages 621-629

  Palmieri, Luigi ^a,b   Picault, Nathalie ^c   Arrigoni, Roberto ^a,b   Besin, Evelyne ^c   Palmieri, Ferdinando ^a,b,d   Hodges, Michael ^c  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^d UNIVERSITÉ DE PERPIGNAN   (France)

Author keywords

Arabidopsis thaliana; Dicarboxylate carrier; Functional reconstitution; Mitochondria; Mitochondrial carrier family; Transport

Indexed keywords

CELL MEMBRANES; GENE EXPRESSION; LIPOSOMES; MITOCHONDRIA; PROTEINS;

ARABIDOPSIS THALIANA; DICARBOXYLATE CARRIERS; FUNCTIONAL RECONSTITUTION; MITOCHONDRIAL CARRIER FAMILY;

YEAST;

2 OXOGLUTARIC ACID; DICARBOXYLIC ACID; ISOPROTEIN; MALIC ACID; OXALOACETIC ACID; PHOSPHATE; SUCCINIC ACID; SULFATE; THIOSULFATE;

ARABIDOPSIS; ARTICLE; CYTOSOL; ENZYME SPECIFICITY; GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN DISTRIBUTION; OXIDATION REDUCTION REACTION; PLANT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; SEQUENCE HOMOLOGY; YEAST;

AMINO ACID SEQUENCE; ARABIDOPSIS; BASE SEQUENCE; DICARBOXYLIC ACID TRANSPORTERS; DNA PRIMERS; DNA, COMPLEMENTARY; ESCHERICHIA COLI; KINETICS; LIPOSOMES; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROTEIN ISOFORMS; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 41149086750     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070867     Document Type: Article

References (49)

1. Laloi, M. (1999) Plant mitochondrial carriers: an overview. Cell. Mol. Life Sci. 56, 918-944
2. Palmieri, F. (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Eur. J. Physiol. Pflugers Arch. 447, 689-709
3. Palmieri, F., Picault, N., Palmieri, L. and Hodges, M. (2004) Plant mitochondrial carriers. In Plant Mitochondria: From Genome to Function (Day, D. A., Millar, A. H. and Whelan, J., eds.), pp. 247-276, Kluwer Academic Press, New York
4. Picault, N., Hodges, M., Palmieri, L. and Palmieri, F. (2004) The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci. 9, 138-146
5. Palmieri, F., Agrimi, G., Blanco, E., Castegna, A., Di Noia, M. A., Iacobazzi, V., Lasorsa, F. M., Marobbio, C. M., Palmieri, L., Scarcia, P. et al. (2006) Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim. Biophys. Acta 1757, 1249-1262
6. 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
7. 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
8. Baker, A. and Leaver, C. J. (1985) Isolation and sequence analysis of a cDNA encoding the ATP/ADP translocator of Zea mays L. Nucleic Acids Res. 13, 5857-5867
9. Laloi, M., Klein, M., Riesmeier, J., Muller-Rober, B., Fleury, C., Bouillaud, F. and Ricquier, D. (1997) A plant cold-induced uncoupling protein. Nature 389, 135-136
10. Kiiskinen, M., Korhonen, M. and Kangasjärvi, J. (1997) Isolation and characterization of cDNA for a plant mitochondrial phosphate translocator (Mpt1): ozone stress induces Mpt1 mRNA accumulation in birch (Betula pendula Roth). Plant Mol. Biol. 35, 271-279
11. Takabatake, R., Hata, S., Taniguchi, M., Kouchi, H., Sugiyama, T. and Izui, K. (1999) Isolation and characterisation of cDNAs encoding mitochondrial phosphate transporters in soybean, maize, rice and Arabidopsis. Plant Mol. Biol. 40, 479-486
12. Picault, N., Palmieri, L., Pisano, I., Hodges, M. and Palmieri, F. (2002) Identification of a novel transporter for dicarboxylates and tricarboxylates in plant mitochondria. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J. Biol. Chem. 277, 24204-24211
13. Hoyos, M. E., Palmieri, L., Wertin, T., Arrigoni, R., Polacco, J. C. and Palmieri, F. (2003) Identification of a mitochondrial transporter for basic amino acids in Arabidopsis thaliana by functional reconstitution into liposomes and complementation in yeast. Plant J. 33, 1027-1035
14. Palmieri, L., Arrigoni, R., Blanco, E., Carrari, F., Zanor, M. I., Studart-Guimaraes, C., Fernie, A. R. and Palmieri, F. (2006) Molecular identification of an Arabidopsis S-adenosylmethionine transporter. Analysis of organ distribution, bacterial expression, reconstitution into liposomes, and functional characterization. Plant Physiol. 142, 855-865
15. Bouvier, F., Linka, N., Isner, J.-C., Mutterer, J., Weber, A. P. M. and Camara, B. (2006) Arabidopsis SAMT1 defines a plastid transporter regulating plastid biogenesis and plant development. Plant Cell 18, 3088-3105
16. Catoni, E., Desimone, M., Hilpert, M., Wipf, D., Kunze, R., Schneider, A., Flügge, U.-I., Schumacher, K. and Frommer, W. B. (2003) Expression pattern of a nuclear encoded mitochondrial arginine-ornithine translocator gene from Arabidopsis. BMC Plant Biol. 3, 1-10
17. Catoni, E., Schwab, R., Hilpert, M., Desimone, M., Schwacke, R., Flugge, U.-I., Schumacher, K. and Frommer, W. B. (2003) Identification of an Arabidopsis mitochondrial succinate-fumarate translocator. FEBS Lett. 534, 87-92
18. De Santis, A., Arrigoni, O. and Palmieri, F. (1976) Carrier-mediated transport of metabolites in purified bean mitochondria. Plant Cell Physiol. 17, 1221-1233
19. Krämer, R. and Palmieri, F. (1992) Metabolite carriers in mitochondria. In Molecular Mechanisms in Bioenergetics (Ernster, L., ed.), pp. 359-384, Elsevier Science Publishers, Amsterdam
20. Palmieri, L., Vozza, A., Hönlinger, A., Dietmeier, K., Palmisano, A., Zara, V. and Palmieri, F. (1999) The mitochondrial dicarboxylate carrier is essential for the growth of Saccharomyces cerevisiae on ethanol or acetate as the sole carbon source. Mol. Microbiol. 31, 569-577
21. Hanning, I., Baumgarten, K., Schott, K. and Heldt, H. W. (1999) Oxaloacetate transport into plant mitochondria. Plant Physiol. 119, 1025-1031
22. Sellars, M. J., Vuocolo, T., Leeton, L. A., Coman, G. J., Degnan, B. M. and Preston, N. P. (2007) Real-time RT-PCR quantification of Kuruma shrimp transcripts: a comparison of relative and absolute quantification procedures. J. Biotechnol. 129, 391-399
23. 2+-stimulated aspartate/glutamate transporters in mitochondria. EMBO J. 20, 5060-5069
24. Palmieri, F., Indiveri, C., Bisaccia, F. and Iacobazzi, V. (1995) Mitochondrial metabolite carrier proteins: purification, reconstitution, and transport studies. Methods Enzymol. 260, 349-369
25. Fiermonte, G., Dolce, V. and Palmieri, F. (1998) Expression in Escherichia coli, functional characterization, and tissue distribution of isoforms A and B of the phosphate carrier from bovine mitochondria. J. Biol. Chem. 273, 22782-22787
26. Fiermonte, G., Dolce, V., Arrigoni, R., Runswick, M. J., Walker, J. E. and Palmieri, F. (1999) Organization and sequence of the gene for the human mitochondrial dicarboxylate carrier: evolution of the carrier family. Biochem. J. 344, 953-960
27. 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
28. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L. and Gruissem, W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632
29. Palmieri, L., De Marco, V., Iacobazzi, V., Palmieri, F., Runswick, M. J. and Walker, J. E. (1997) Identification of the yeast ARG-11 gene as a mitochondrial ornithine carrier involved in arginine biosynthesis. FEBS Lett. 410, 447-451
30. Vozza, A., Blanco, E., Palmieri, L. and Palmieri, F. (2004) Identification of the mitochondrial GTP/GDP transporter in Saccharomyces cerevisiae. J. Biol. Chem. 279, 20850-20857
31. Marobbio, C. M. T., Agrimi, G., Lasorsa, F. M. and Palmieri, F. (2003) Identification and functional reconstitution of yeast mitochondrial carrier for S-adenosylmethionine. EMBO J. 22, 5975-5982
32. Runswick, M. J., Walker, J. E., Bisaccia, F., Iacobazzi, V. and Palmieri, F. (1990) Sequence of the bovine 2-oxoglutarate/malate carrier protein: structural relationship to other mitochondrial transport proteins. Biochemistry 29, 11033-11040
33. Palmieri, L., Lasorsa, F. M., De Palma, A., Palmieri, F., Bunswick, M. J. and Walker, J. E. (1997) Identification of the yeast ACR1 gene product as a succinate-fumarate transporter essential for growth on ethanol or acetate. FEBS Lett. 417, 114-118
34. 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
35. Fiermonte, G., Dolce, V., Palmieri, L., Ventura, M., Runswick, M. J., Palmieri, F. and Walker, J. E. (2001) Identification of the human mitochondrial oxodicarboxylate carrier: bacterial expression, reconstitution, functional characterization, tissue distribution, and chromosomal location. J. Biol. Chem. 276, 8225-8230
36. Nogueira, F. T. S., Borecky, J., Vercesi, A. E. and Arruda, P. (2005) Genomic structure and regulation of mitochondrial uncoupling protein genes in mammals and plants. Biosci. Rep. 25, 209-226
37. Borecky, J., Nogueira, F. T. S., de Oliveira, K. A. P., Maia, I. G., Vercesi, A. E. and Arruda, P. (2006) The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. J. Exp. Bot. 57, 849-864
38. Vercesi, A. E., Borecky, J., Maia, I. G., Arruda, P., Cuccovia, I. M. and Chaimovich, H. (2006) Plant uncoupling mitochondrial proteins. Annu. Rev. Plant Biol. 57, 383-404
39. Wieckowski, M. R. and Wojtczak, L. (1997) Involvement of the dicarboxylate carrier in the protonophoric action of long-chain fatty acids in mitochondria. Biochem. Biophys. Res. Commun. 232, 414-417
40. + transport by free fatty acids, which is further stimulated by mersalyl. J. Biol. Chem. 269, 27329-27336
41. Samartsev, V. N., Mokhova, E. N. and Skulachev, V. P. (1997) The pH-dependent reciprocal changes in contributions of ADP/ATP anfiporter and aspartate/glutamate antiporter to the fatty acid-induced uncoupling. FEBS Lett. 412, 179-182
42. Samartsev, V. N., Smirnov, A. V., Zeldi, I. P., Markova, O. V., Mokhova, E. N. and Skulachev, V. P. (1997) Involvement of aspartate/glutamate antiport in fatty acid-induced uncoupling of liver mitochondria. Biochim. Biophys. Acta 1319, 251-257
43. Wiskich, J. T. (1975) Phosphate dependent substrate transport into mitochondria. Oxidative studies. Plant Physiol. 56, 121-125
44. Day, D. A. and Hanson, J. B. (1997) Effect of phosphate and uncouplers on substrate transport and oxidation by isolated corn mitochondria. Plant Physiol. 59, 139-144
45. Scheibe, R. (2004) Malate valves to balance cellular energy supply. Physiol. Plant. 120, 21-26
46. Hanning, I. and Heldt, H. W. (1993) On the function of mitochondrial metabolism during photosynthesis in spinach (Spinacia oleracea L.) leaves. Partitioning between respiration and export of redox equivalents and precursors for nitrate assimilation products. Plant Physiol. 103, 1147-1154
47. Raghavendra, A. S., Reumann, S. and Heldt, H. W. (1998) Participation of mitochondrial metabolism in photorespiration. Reconstituted system of peroxisomes and mitochondria from spinach leaves. Plant Physiol. 116, 1333-1337
48. Zoglowek, C., Krömer, S. and Heldt, H. W. (1988) Oxaloacetate and malate transport by plant mitochondria. Plant Physiol. 87, 109-115
49. Pastore, D., Di Pede, S. and Passarella, S. (2003) Isolated durum wheat and potato cell mitochondria oxidize externally added NADH mostly via the malate/oxaloacetate shuttle with a rate that depends on the carrier-mediated transport. Plant Physiol. 133, 2029-2039