The mitochondrial transporter family SLC25: Identification, properties and physiopathology

Molecular Aspects of Medicine

Volumn 34, Issue 2-3, 2013, Pages 465-484

  Palmieri, Ferdinando ^a  

^a UNIVERSITY OF BARI   (Italy)

Author keywords

Membrane transport; Mitochondrial carrier; Mitochondrial carrier disease; Mitochondrial carrier family; Mitochondrial transporter; SLC25

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE DEFICIENCY; ASPARTATE GLUTAMATE CARRIER ISOFORM 2 DEFICIENCY; ASPARTATE GLUTAMATE DEFICIENCY; CARNITINE DEFICIENCY; CONGENITAL AMISH MICROCEPHALY; EPILEPTIC ENCEPHALOPATHY; GENE; GENE ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE MUTATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC DISORDER; HEREDITARY SIDEROBLASTIC ANEMIA; HUMAN; HYPERORNITHINEMIA HYPERAMMONEMIA HOMOCITRULLINURIA SYNDROME; MFRN1 GENE; MFRN2 GENE; MULTIGENE FAMILY; NEUROPATHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHOSPHATE DEFICIENCY; PHYLOGENY; REVIEW; SEQUENCE ANALYSIS; SLC25 GENE; SLC25A17 GENE; SLC25A26 GENE; SLC25A29 GENE; SLC25A31 GENE; SLC25A32 GENE; SLC25A33 GENE; SLC25A36 GENE; SLC25A38 GENE; SLC25A42 GENE; STRUCTURE ACTIVITY RELATION;

ANION TRANSPORT PROTEINS; HUMANS; MEMBRANE TRANSPORT PROTEINS; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIGENE FAMILY; PHYLOGENY; PROTEIN CONFORMATION; SPECIES SPECIFICITY;

EUKARYOTA;

EID: 84875218644     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2012.05.005     Document Type: Review

References (65)

1. G. Agrimi, M.A. Di Noia, C.M.T. Marobbio, G. Fiermonte, F.M. Lasorsa, and F. Palmieri Identification of the human mitochondrial S-adenosylmethionine transporter: bacterial expression, reconstitution, functional characterization and tissue distribution Biochem. J. 379 2004 183 190
2. + Biochem. J. 443 2012 241 247
3. H. Aquila, D. Misra, M. Eulitz, and M. Klingenberg Complete amino acid sequence of the ADP/ATP carrier from beef heart mitochondria Hoppe-Seyler's Z. Physiol. Chem. 363 1982 345 349
4. M.J. Berardi, W.M. Shih, S.C. Harrison, and J.J. Chou Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching Nature 476 2011 109 113
5. J.V. Brower, C.H. Lim, M. Jorgensen, S.P. Oh, and N. Terada Adenine nucleotide translocase 4 deficiency leads to early meiotic arrest of murine male germ cells Reproduction 138 2009 463 470
6. J.V. Brower, N. Rodic, T. Seki, M. Jorgensen, N. Fliess, A.T. Yachnis, J.R. McCarrey, S.P. Oh, and N. Terada Evolutionarily conserved mammalian adenine nucleotide translocase 4 is essential for spermatogenesis J. Biol. Chem. 282 2007 29658 29666
7. J.A. Camacho, C. Obie, B. Biery, B.K. Goodman, C.A. Hu, S. Almashanu, G. Steel, R. Casey, M. Lambert, G.A. Mitchell, and D. Valle Hyperornithinaemia- hyperammonaemia-homocitrullinuria syndrome is caused by mutations in a gene encoding a mitochondrial ornithine transporter Nat. Genet. 22 1999 151 158
8. J.A. Camacho, and N. Rioseco-Camacho The human and mouse SLC25A29 mitochondrial transporters rescue the deficient ornithine metabolism in fibroblasts of patients with the hyperornithinemia-hyperammonemia- homocitrullinuria (HHH) syndrome Pediatr. Res. 66 2009 35 41
9. V. Dolce, F. Fiermonte, M.J. Runswick, F. Palmieri, and J.E. Walker The human mitochondrial deoxynucleotide carrier and its role in toxicity of nucleoside antivirals Proc. Nat. Acad. Sci. USA 98 2001 2284 2288
10. V. Dolce, P. Scarcia, D. Iacopetta, and F. Palmieri A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution FEBS Lett. 579 2005 633 637
11. A. Echaniz-Laguna, M. Chassagne, J. Ceresuela, I. Rouvet, S. Padet, C. Acquaviva, S. Nataf, S. Vinzio, D. Bozon, and B. Mousson de Camaret Complete loss of expression of the ANT1 gene causing cardiomyopathy and myopathy J. Med. Genet. 49 2012 146 150
12. G. Fiermonte, F. De Leonardis, S. Todisco, L. Palmieri, F.M. Lasorsa, and F. Palmieri Identification of the mitochondrial ATP-Mg/Pi transporter: bacterial expression, reconstitution, functional characterization and tissue distribution J. Biol. Chem. 279 2004 30722 30730
13. G. Fiermonte, V. Dolce, and F. Palmieri 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 1998 22782 22787
14. G. Fiermonte, V. Dolce, R. Arrigoni, M.J. Runswick, J.E. Walker, and F. Palmieri Organization and sequence of the gene for the human mitochondrial dicarboxylate carrier: evolution of the carrier family Biochem. J. 344 1999 953 960
15. G. Fiermonte, V. Dolce, L. David, F.M. Santorelli, C. Dionisi-Vici, F. Palmieri, and J.E. Walker The mitochondrial ornithine transporter: bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms J. Biol. Chem. 278 2003 32778 32783
16. G. Fiermonte, L. Palmieri, S. Todisco, G. Agrimi, F. Palmieri, and J.E. Walker Identification of the mitochondrial glutamate transporter: bacterial expression, reconstitution, functional characterization, and tissue distribution of two human isoforms J. Biol. Chem. 277 2002 19289 19294
17. G. Fiermonte, E. Paradies, S. Todisco, C.M.T. Marobbio, and F. Palmieri A novel member of solute carrier family 25 (SLC25A42) is a transporter of coenzyme a and adenosine 3′,5′-diphosphate in human mitochondria J. Biol. Chem. 284 2009 18152 18159
18. S. Floyd, C. Favre, F.M. Lasorsa, M. Leahy, G. Trigiante, P. Stroebel, A. Marx, G. Loughran, K. O'Callaghan, C.M.T. Marobbio, D.J. Slotboom, E.R.S. Kunji, F. Palmieri, and R. O'Connor The IGF-I-mTOR signaling pathway induces the mitochondrial pyrimidine nucleotide carrier to promote cell growth Mol. Biol. Cell 18 2007 3545 3555
19. D.L. Guernsey, H. Jiang, D.R. Campagna, S.C. Evans, M. Ferguson, M.D. Kellogg, M. Lachance, M. Matsuoka, M. Nightingale, A. Rideout, L. Saint-Amant, P.J. Schmidt, A. Orr, S.S. Bottomley, M.D. Fleming, M. Ludman, S. Dyack, C.V. Fernandez, and M.E. Samuels Mutations in mitochondrial carrier family gene SLC25A38 cause nonsyndromic autosomal recessive congenital sideroblastic anemia Nat. Genet. 41 2009 651 653
20. M. Huizing, V. Iacobazzi, L. Ijlst, P. Savelkoul, W. Ruitenbeek, L.P. van den Heuvel, C. Indiveri, J. Smeitink, F.J.M. Trijbels, R.J.A. Wanders, and F. Palmieri Cloning of the human carnitine-acylcarnitine carrier cDNA, and identification of the molecular defect in a patient Am. J. Hum. Genet. 61 1997 1239 1245
21. V. Iacobazzi, P. Convertini, V. Infantino, P. Scarcia, S. Todisco, and F. Palmieri Statins, fibrates and retinoic acid upregulate mitochondrial acylcarnitine carrier gene expression Biochem. Biophys. Res. Commun. 388 2009 643 647
22. C. Indiveri, V. Iacobazzi, N. Giangregorio, and F. Palmieri The mitochondrial carnitine carrier protein: cDNA cloning, primary structure, and comparison with other mitochondrial transport proteins Biochem. J. 321 1997 713 719
23. C. Indiveri, V. Iacobazzi, A. Tonazzi, N. Giangregorio, V. Infantino, P. Convertini, L. Console, and F. Palmieri The mitochondrial carnitine/ acylcarnitine carrier: function, structure and physiopathology Mol. Aspects Med. 32 2011 223 233
24. + translocation Biochem. J. 327 1997 349 356
25. M. Klingenberg The ADP, ATP shuttle of the mitochondrion Trends Biochem. Sci. 4 1979 249 252
26. M. Klingenberg The ADP and ATP transport in mitochondria and its carrier Biochim. Biophys. Acta 1778 2008 1978 2021
27. K. Kobayashi, D.S. Sinasac, M. Iijima, A.P. Boright, L. Begum, J.R. Lee, T. Yasuda, S. Ikeda, R. Hirano, H. Terazono, M.A. Crackower, I. Kondo, L.C. Tsui, S.W. Scherer, and T. Saheki The gene mutated in adult-onset type II citrullinaemia encodes a putative mitochondrial carrier protein Nat. Genet. 22 1999 159 163
28. E.R.S. Kunji, and M. Harding Projection structure of the atractyloside-inhibited mitochondrial ADP/ATP carrier of Saccharomyces cerevisiae J. Biol. Chem. 278 2003 36985 36988
29. E.R.S. Kunji, and A.J. Robinson Coupling of proton and substrate translocation in the transport cycle of mitochondrial carriers Curr. Opin. Struct. Biol. 20 2010 440 447
30. W. Lewis, C.P. Haase, Y.K. Miller, B. Ferguson, T. Stuart, T. Ludaway, J. McNaught, R. Russ, J. Steltzer, R. Santoianni, R. Long, G. Fiermonte, and F. Palmieri Transgenic expression of the deoxynucleotide carrier causes mitochondrial damage that is enhanced by NRTIs for AIDS Lab. Invest. 85 2005 972 981
31. M.J. Lindhurst, G. Fiermonte, S. Song, E. Struys, F. De Leonardis, P.L. Schwartzberg, A. Chen, A. Castegna, N. Verhoeven, C.K. Mathews, F. Palmieri, and L.G. Biesecker Knockout of Slc25a19 causes mitochondrial thiamine pyrophosphate depletion, embryonic lethality, CNS malformations, and anemia Proc. Natl. Acad. Sci. USA 103 2006 15927 15932
32. J.A. Mayr, O. Merkel, S.D. Kohlwein, B.R. Gebhardt, H. Böhles, U. Fötschl, J. Koch, M. Jaksch, H. Lochmüller, R. Horváth, P. Freisinger, and W. Sperl Mitochondrial phosphate-carrier deficiency: a novel disorder of oxidative phosphorylation Am. J. Hum. Genet. 80 2007 478 484
33. J.A. Mayr, F.A. Zimmermann, R. Horváth, H.-C. Schneider, B. Schoser, E. Holinski-Feder, B. Czermin, P. Freisinger, and W. Sperl Deficiency of the mitochondrial phosphate carrier presenting as myopathy and cardiomyopathy in a family with three affected children Neuromuscul. Disord. 21 2011 803 808
34. C.M.T. Marobbio, G. Agrimi, F.M. Lasorsa, and F. Palmieri Identification and functional reconstitution of yeast mitochondrial carrier for S-adenosylmethionine EMBO J. 22 2003 5975 5982
35. C.M.T. Marobbio, G. Giannuzzi, E. Paradies, C.L. Pierri, and F. Palmieri α-isopropylmalate, a leucine biosynthesis intermediate in yeast, is transported by the mitochondrial oxaloacetate carrier J. Biol. Chem. 283 2008 28445 28453
36. F. Molinari, A. Kaminska, G. Fiermonte, N. Boddaert, A. Raas-Rothschild, P. Plouin, L. Palmieri, F. Brunelle, F. Palmieri, O. Dulac, A. Munnich, and L. Colleaux Mutations in the mitochondrial glutamate carrier SLC25A22 in neonatal epileptic encephalopathy with suppression bursts Clin. Genet. 76 2009 188 194
37. F. Molinari, A. Raas-Rothschild, M. Rio, G. Fiermonte, F. Encha-Razavi, L. Palmieri, F. Palmieri, Ziva-Ben-Neriah, N. Khadom, M. Vekemans, T. Attié-Bitach, A. Munnich, P. Rustin, and L. Colleaux Impaired mitochondrial glutamate transport in autosomal recessive neonatal myoclonic epilepsy Am. J. Hum. Genet. 76 2005 334 339
38. M. Monné, V. Miniero, L. Daddabbo, A.J. Robinson, E.R.S. Kunji, and F. Palmieri The substrate specificity of the two mitochondrial ornithine carriers can be swapped by a single mutation in the substrate binding site J. Biol. Chem. 287 2012 7925 7934
39. D.R. Nelson, C.M. Felix, and J.M. Swanson Highly conserved charge-pair networks in the mitochondrial carrier family J. Mol. Biol. 277 1998 285 308
40. Palmieri, F.; 2004. The mitochondrial transporter family (SLC25): physiological and pathological implications. In: Hediger, M.A. (Ed.), "The ABC of solute carriers", Pflugers Arch. Eur. J. Physiol. 447, 689-709.
41. F. Palmieri Diseases caused by defects of mitochondrial carriers: a review Biochim. Biophys. Acta 1777 2008 564 578
42. F. Palmieri, G. Agrimi, E. Blanco, A. Castegna, M.A. Di Noia, V. Iacobazzi, F.M. Lasorsa, C.M.T. Marobbio, L. Palmieri, P. Scarcia, S. Todisco, A. Vozza, and J. Walker Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins Biochim. Biophys. Acta 1757 2006 1249 1262
43. F. Palmieri, F. Bisaccia, L. Capobianco, V. Dolce, G. Fiermonte, V. Iacobazzi, and V. Zara Transmembrane topology, genes and biogenesis of the mitochondrial phosphate and oxoglutarate carriers J. Bioenerg. Biomembr. 25 1993 493-505
44. F. Palmieri, C. Indiveri, F. Bisaccia, and R. Krämer Functional properties of purified and reconstituted mitochondrial metabolite carriers J. Bioenerg. Biomembr. 25 1993 525 535
45. F. Palmieri, and C.L. Pierri Structure and function of mitochondrial carriers - Role of the transmembrane helix P and G residues in the gating and transport mechanism FEBS Lett. 584 2010 1931 1939
46. F. Palmieri, and C.L. Pierri Mitochondrial metabolite transport Essays Biochem. 47 2010 37 52
47. F. Palmieri, C.L. Pierri, A. De Grassi, A. Nunes-Nesi, and A.R. Fernie Evolution, structure and function of mitochondrial carriers: a review with new insights Plant J. 66 2011 161 181
48. Palmieri, L.; Alberio, S.; Pisano, I.; Lodi, T.; Meznaric Petrusa, M.; Zidar, J.; Santoro, A.; Scarcia, P.; Fontanesi, F.; Lamantea, E.; Ferrero, I.; Zeviani, M.; 2005. Complete loss-of-function of the heart-/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy. Hum. Mol. Genet. 14, 3079-3088.
49. 2+-stimulated aspartate/glutamate transporters in mitochondria EMBO J. 20 2001 5060 5069
50. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trézé guet, G. Lauquin, and G. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
51. N. Picault, M. Hodges, L. Palmieri, and F. Palmieri The growing family of mitochondrial carriers in Arabidopsis Trends Plant Sci. 9 2004 138 146
52. N. Ramoz, J.G. Reichert, C.J. Smith, J.M. Silverman, I.N. Bespalova, K.L. Davis, and J.D. Buxbaum Linkage and association of the mitochondrial aspartate/glutamate carrier SLC25A12 gene with autism Am. J. Psychiatry 161 2004 662 669
53. A. Robinson, and E. Kunji Mitochondrial carriers in the cytoplasmic state have a common substrate binding site Proc. Natl. Acad. Sci. USA 103 2006 2617 2622
54. A. Robinson, C. Overy, and E. Kunji The mechanism of transport by mitochondrial carriers based on analysis of symmetry Proc. Natl. Acad. Sci. USA 105 2008 17766 17771
55. M.J. Rosenberg, R. Agarwala, G. Bouffard, J. Davis, G. Fiermonte, M.S. Hilliard, T. Koch, L.M. Kalikin, I. Makalowska, D.H. Morton, E.M. Petty, J.L. Weber, F. Palmieri, R.I. Kelley, A.A. Schaffer, and L.G. Biesecker Mutant deoxynucleotide carrier is associated with congenital microcephaly Nat. Genet. 32 2002 175 179
56. T. Saheki, K. Inoue, A. Tushima, K. Mutoh, and K. Kobayashi Citrin deficiency and current treatment concepts Mol. Genet. Metab. 100 Suppl 1 2010 S59 S64
57. M. Saraste, and J. Walker Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase FEBS Lett. 144 1982 250 254
58. E. Sekoguchi, N. Sato, A. Yasui, S. Fukada, Y. Nimura, H. Aburatani, K. Ikeda, and A. Matsuura A novel mitochondrial carnitine-acylcarnitine translocase induced by partial hepatectomy and fasting J. Biol. Chem. 278 2003 38796 38802
59. G.C. Shaw, J.J. Cope, L. Li, K. Corson, C. Hersey, G.E. Ackermann, B. Gwynn, A.J. Lambert, R.A. Wingert, D. Traver, N.S. Trede, B.A. Barut, Y. Zhou, E. Minet, A. Donovan, A. Brownlie, R. Balzan, M.J. Weiss, L.L. Peters, J. Kaplan, L.I. Zon, and B.H. Paw Mitoferrin is essential for erythroid iron assimilation Nature 440 2006 96 100
60. A.N. Spaan, L. Ijlst, C.W. van Roermund, F.A. Wijburg, R.J. Wanders, and H.R. Waterham Identification of the human mitochondrial FAD transporter and its potential role in multiple acyl-CoA dehydrogenase deficiency Mol. Genet. Metab. 86 2005 441 447
61. R. Spiegel, A. Shaag, S. Edvardson, H. Mandel, P. Stepensky, S.A. Shalev, Y. Horovitz, O. Pines, and O. Elpeleg SLC25A19 mutation as a cause of neuropathy and bilateral striatal necrosis Annual Neurol. 66 2009 419 424
62. S.A. Titus, and R.G. Moran Retrovirally mediated complementation of the glyB phenotype. Cloning of a human gene encoding the carrier for entry of folates into mitochondria J. Biol. Chem. 275 2000 36811 36817
63. 2+ buffering Cell Death Diff. 19 2011 650 660
64. J. Traba, J. Satrustegui, and A. del Arco Characterization of SCaMC-3-like/slc25a41, a novel calcium-independent mitochondrial ATP-Mg/Pi carrier Biochem. J. 418 2009 125 133
65. R. Wibom, F.M. Lasorsa, V. Töhönen, M. Barbaro, F.H. Sterky, T. Kucinski, K. Naess, M. Jonsson, C.L. Pierri, F. Palmieri, and A. Wedell AGC1 deficiency associated with global cerebral hypomyelination New Engl. J. Med. 361 2009 489 495