Skip to main content
SpringerLink
Log in

Adenine nucleotide transporters in organelles: novel genes and functions

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

In eukaryotes, cellular energy in the form of ATP is produced in the cytosol via glycolysis or in the mitochondria via oxidative phosphorylation and, in photosynthetic organisms, in the chloroplast via photophosphorylation. Transport of adenine nucleotides among cell compartments is essential and is performed mainly by members of the mitochondrial carrier family, among which the ADP/ATP carriers are the best known. This work reviews the carriers that transport adenine nucleotides into the organelles of eukaryotic cells together with their possible functions. We focus on novel mechanisms of adenine nucleotide transport, including mitochondrial carriers found in organelles such as peroxisomes, plastids, or endoplasmic reticulum and also mitochondrial carriers found in the mitochondrial remnants of many eukaryotic parasites of interest. The extensive repertoire of adenine nucleotide carriers highlights an amazing variety of new possible functions of adenine nucleotide transport across eukaryotic organelles.

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

Fig. 1a–d
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7a, b
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

MCF:

Mitochondrial carrier family

CAT:

Carboxyatractyloside

BKA:

Bongkrekic acid

AAC:

ADP/ATP carrier

SCaMC:

Short calcium-binding mitochondrial carrier

CoA:

Coenzyme A

ORF:

Open-reading frame

References

  1. Winkler HH, Neuhaus HE (1999) Non-mitochondrial ATP transport. Trends Biochem Sci 24:64–68

    Article  PubMed  CAS  Google Scholar 

  2. del Arco A, Satrústegui J (2005) New mitochondrial carriers: an overview. Cell Mol Life Sci 62:2204–2227

    Article  PubMed  Google Scholar 

  3. Picault N, Hodges M, Palmieri L, Palmieri F (2004) The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci 9:138–146

    Article  PubMed  CAS  Google Scholar 

  4. Palmieri F, Pierri CL (2010) Mitochondrial metabolite transport. Essays Biochem 47:37–52

    Article  PubMed  CAS  Google Scholar 

  5. Palmieri F, Agrimi G, Blanco E, Castegna A, Di Noia MA, Iacobazzi V, Lasorsa FM, Marobbio CM, Palmieri L, Scarcia P, Todisco S, Vozza A, Walker J (2006) Identification of mitochondrial carriers in Saccharomyces cerevisiae by transport assay of reconstituted recombinant proteins. Biochim Biophys Acta 1757:1249–1262

    Article  PubMed  CAS  Google Scholar 

  6. Kunji ER, Robinson AJ (2006) The conserved substrate binding site of mitochondrial carriers. Biochim Biophys Acta 1757:1237–1248

    Article  PubMed  CAS  Google Scholar 

  7. Robinson AJ, Kunji ER (2006) Mitochondrial carriers in the cytoplasmic state have a common substrate binding site. Proc Natl Acad Sci USA 103:2617–2622

    Article  PubMed  CAS  Google Scholar 

  8. Robinson AJ, Overy C, Kunji ER (2008) The mechanism of transport by mitochondrial carriers based on analysis of symmetry. Proc Natl Acad Sci USA 105:17766–17771

    Article  PubMed  CAS  Google Scholar 

  9. Rial E, Zardoya R (2009) Oxidative stress, thermogenesis and evolution of uncoupling proteins. J Biol 8:58

    Article  PubMed  Google Scholar 

  10. Klingenberg M (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778:1978–2021

    Article  PubMed  CAS  Google Scholar 

  11. Traba J, Satrústegui J, del Arco A (2009) Transport of adenine nucleotides in the mitochondria of Saccharomyces cerevisiae: interactions between the ADP/ATP carriers and the ATP-Mg/Pi carrier. Mitochondrion 9:79–85

    Article  PubMed  CAS  Google Scholar 

  12. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, Shu S, Neupane R, Cipriano M, Mancuso J, Tu H, Salamov A, Lindquist E, Shapiro H, Lucas S, Grigoriev IV, Cande WZ, Fulton C, Rokhsar DS, Dawson SC (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631–642

    Article  PubMed  CAS  Google Scholar 

  13. Adl SM, Leander BS, Simpson AG, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, Kolisko M, Lane CE, Lodge DJ, Mann DG, Meisterfeld R, Mendoza L, Moestrup Ø, Mozley-Standridge SE, Smirnov AV, Spiegel F (2007) Diversity, nomenclature, and taxonomy of protists. Syst Biol 56:684–689

    Article  PubMed  Google Scholar 

  14. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trézéguet V, Lauquin GJ, Brandolin G (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426:39–44

    Article  PubMed  CAS  Google Scholar 

  15. Hatanaka T, Hashimoto M, Majima E, Shinohara Y, Terada H (1999) Functional expression of the tandem-repeated homodimer of the mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae. Biochem Biophys Res Commun 262:726–730

    Article  PubMed  CAS  Google Scholar 

  16. Huang SG, Odoy S, Klingenberg M (2001) Chimers of two fused ADP/ATP carrier monomers indicate a single channel for ADP/ATP transport. Arch Biochem Biophys 394:67–75

    Article  PubMed  CAS  Google Scholar 

  17. Phelps A, Wohlrab H (2004) Homodimeric mitochondrial phosphate transport protein. Transient subunit/subunit contact site between the transport relevant transmembrane helices A. Biochemistry 43:6200–6207

    Article  PubMed  CAS  Google Scholar 

  18. Kunji ER, Crichton PG (2010) Mitochondrial carriers function as monomers. Biochim Biophys Acta 1797:817–831

    Article  PubMed  CAS  Google Scholar 

  19. Palmieri F, Pierri CL (2010) Structure and function of mitochondrial carriers—role of the transmembrane helix P and G residues in the gating and transport mechanism. FEBS Lett 584:1931–1939

    Article  PubMed  CAS  Google Scholar 

  20. Vozza A, Blanco E, Palmieri L, Palmieri F (2004) Identification of the mitochondrial GTP/GDP transporter in Saccharomyces cerevisiae. J Biol Chem 279:20850–20857

    Article  PubMed  CAS  Google Scholar 

  21. De Marcos Lousa C, Trézéguet V, Dianoux AC, Brandolin G, Lauquin GJ (2002) The human mitochondrial ADP/ATP carriers: kinetic properties and biogenesis of wild-type and mutant proteins in the yeast S. cerevisiae. Biochemistry 41:14412–14420

    Article  PubMed  Google Scholar 

  22. Murcha MW, Millar AH, Whelan J (2005) The N-terminal cleavable extension of plant carrier proteins is responsible for efficient insertion into the inner mitochondrial membrane. J Mol Biol 351:16–25

    Article  PubMed  CAS  Google Scholar 

  23. Satre M, Mattei S, Aubry L, Gaudet P, Pelosi L, Brandolin G, Klein G (2007) Mitochondrial carrier family: repertoire and peculiarities of the cellular slime mould Dictyostelium discoideum. Biochimie 89:1058–1069

    Article  PubMed  CAS  Google Scholar 

  24. Colasante C, Peña Diaz P, Clayton C, Voncken F (2009) Mitochondrial carrier family inventory of Trypanosoma brucei brucei: identification, expression and subcellular localisation. Mol Biochem Parasitol 167:104–117

    Article  PubMed  CAS  Google Scholar 

  25. Schnaufer A, Clark-Walker GD, Steinberg AG, Stuart K (2005) The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24:4029–4040

    Article  PubMed  CAS  Google Scholar 

  26. Vaidya AB, Mather MW (2009) Mitochondrial evolution and functions in malaria parasites. Annu Rev Microbiol 63:249–267

    Article  PubMed  CAS  Google Scholar 

  27. Painter HJ, Morrisey JM, Mather MW, Vaidya AB (2007) Specific role of mitochondrial electron transport in blood-stage Plasmodium falciparum. Nature 446:88–91

    Article  PubMed  CAS  Google Scholar 

  28. Uyemura SA, Luo S, Moreno SN, Docampo R (2000) Oxidative phosphorylation, Ca(2+) transport, and fatty acid-induced uncoupling in malaria parasites mitochondria. J Biol Chem 275:9709–9815

    Article  PubMed  CAS  Google Scholar 

  29. Aprille JR (1988) Regulation of the mitochondrial adenine nucleotide pool size in liver: mechanism and metabolic role. FASEB J 2:2547–2556

    PubMed  CAS  Google Scholar 

  30. Aprille JR (1993) Mechanism and regulation of the mitochondrial ATP-Mg/P(i) carrier. J Bioenerg Biomembr 25:473–481

    Article  PubMed  CAS  Google Scholar 

  31. del Arco A, Satrústegui J (2004) Identification of a novel human subfamily of mitochondrial carriers with calcium-binding domains. J Biol Chem 279:24701–24713

    Article  PubMed  Google Scholar 

  32. Fiermonte G, De Leonardis F, Todisco S, Palmieri L, Lasorsa FM, Palmieri F (2004) Identification of the mitochondrial ATP-Mg/Pi transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J Biol Chem 279:30722–30730

    Article  PubMed  CAS  Google Scholar 

  33. Traba J, Froschauer EM, Wiesenberger G, Satrústegui J, del Arco A (2008) Yeast mitochondria import ATP through the calcium-dependent ATP-Mg/Pi carrier Sal1p, and are ATP consumers during aerobic growth in glucose. Mol Microbiol 69:570–585

    Article  PubMed  CAS  Google Scholar 

  34. Traba J, Satrústegui J, del Arco A (2009) Characterization of SCaMC-3-like/slc25a41, a novel calcium-independent mitochondrial ATP-Mg/Pi carrier. Biochem J 418:125–133

    Article  PubMed  CAS  Google Scholar 

  35. Satrústegui J, Pardo B, del Arco A (2007) Mitochondrial transporters as novel targets for intracellular calcium signaling. Physiol Rev 87:29–67

    Article  PubMed  Google Scholar 

  36. Cavero S, Traba J, del Arco A, Satrústegui J (2005) The calcium-dependent ATP-Mg/Pi mitochondrial carrier is a target of glucose-induced calcium signalling in Saccharomyces cerevisiae. Biochem J 392:537–544

    Article  PubMed  CAS  Google Scholar 

  37. Laco J, Zeman I, Pevala V, Polčic P, Kolarov J (2010) Adenine nucleotide transport via Sal1 carrier compensates for the essential function of the mitochondrial ADP/ATP carrier. FEMS Yeast Res 10:290–306

    Article  PubMed  CAS  Google Scholar 

  38. Rehling P, Brandner K, Pfanner N (2004) Mitochondrial import and the twin-pore translocase. Nat Rev Mol Cell Biol 5:519–530

    Article  PubMed  CAS  Google Scholar 

  39. Lill R, Mühlenhoff U (2008) Maturation of iron-sulfur proteins in eukaryotes: mechanisms, connected processes, and diseases. Annu Rev Biochem 77:669–700

    Article  PubMed  CAS  Google Scholar 

  40. Drgon T, Sabova L, Nelson N, Kolarov J (1991) ADP/ATP translocator is essential only for anaerobic growth of yeast Saccharomyces cerevisiae. FEBS Lett 289:159–162

    Article  PubMed  CAS  Google Scholar 

  41. Chen XJ (2004) Sal1p, a calcium-dependent carrier protein that suppresses an essential cellular function associated with the Aac2 isoform of ADP/ATP translocase in Saccharomyces cerevisiae. Genetics 167:607–617

    Article  PubMed  CAS  Google Scholar 

  42. Smith CP, Thorsness PE (2008) The molecular basis for relative physiological functionality of the ADP/ATP carrier isoforms in Saccharomyces cerevisiae. Genetics 179:1285–1299

    Article  PubMed  CAS  Google Scholar 

  43. Dimitrov LN, Brem RB, Kruglyak L, Gottschling DE (2009) Polymorphisms in multiple genes contribute to the spontaneous mitochondrial genome instability of Saccharomyces cerevisiae S288C strains. Genetics 183:365–383

    Article  PubMed  CAS  Google Scholar 

  44. Kucejova B, Li L, Wang X, Giannattasio S, Chen XJ (2008) Pleiotropic effects of the yeast Sal1 and Aac2 carriers on mitochondrial function via an activity distinct from adenine nucleotide transport. Mol Genet Genomics 280:25–39

    Article  PubMed  CAS  Google Scholar 

  45. Chen XJ, Clark-Walker GD (1999) The petite mutation in yeasts: 50 years on. Int Rev Cytol 194:197–238

    Article  CAS  Google Scholar 

  46. Haitina T, Lindblom J, Renstrom T, Fredriksson R (2006) Fourteen novel human members of mitochondrial solute carrier family 25 (SLC25) widely expressed in the central nervous system. Genomics 88:779–790

    Article  PubMed  CAS  Google Scholar 

  47. del Arco A (2005) Novel variants of human SCaMC-3, an isoform of the ATP-Mg/P(i) mitochondrial carrier, generated by alternative splicing from 3′-flanking transposable elements. Biochem J 389:647–655

    Article  PubMed  Google Scholar 

  48. Colasante C, Alibu VP, Kirchberger S, Tjaden J, Clayton C, Voncken F (2006) Characterization and developmentally regulated localization of the mitochondrial carrier protein homologue MCP6 from Trypanosoma brucei. Eukaryot Cell 5:1194–1205

    Article  PubMed  CAS  Google Scholar 

  49. Prohl C, Pelzer W, Diekert K, Kmita H, Bedekovics T, Kispal G, Lill R (2001) The yeast mitochondrial carrier Leu5p and its human homologue Graves’ disease protein are required for accumulation of coenzyme A in the matrix. Mol Cell Biol 21:1089–1097

    Article  PubMed  CAS  Google Scholar 

  50. Fiermonte G, Paradies E, Todisco S, Marobbio CM, Palmieri F (2009) 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 284:18152–18159

    Article  PubMed  CAS  Google Scholar 

  51. Palmieri L, Santoro A, Carrari F, Blanco E, Nunes-Nesi A, Arrigoni R, Genchi F, Fernie AR, Palmieri F (2008) Identification and characterization of ADNT1, a novel mitochondrial adenine nucleotide transporter from Arabidopsis. Plant Physiol 148:1797–1808

    Article  PubMed  CAS  Google Scholar 

  52. Roberts J, Aubert S, Gout E, Bligny R, Douce R (1997) Cooperation and competition between adenylate kinase, nucleoside diphosphokinase, electron transport and ATP synthase in plant mitochondria studied by 31P-nuclear magnetic resonance. Plant Physiol 113:191–199

    PubMed  CAS  Google Scholar 

  53. Monné M, Robinson AJ, Boes C, Harbour ME, Fearnley IM, Kunji ER (2007) The mimivirus genome encodes a mitochondrial carrier that transports dATP and dTTP. J Virol 81:3181–3186

    Article  PubMed  Google Scholar 

  54. Tzagoloff A, Jang J, Glerum DM, 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

    Article  PubMed  CAS  Google Scholar 

  55. Spaan AN, Ijlst L, van Roermund CW, Wijburg FA, Wanders RJ, Waterham HR (2005) Identification of the human mitochondrial FAD transporter and its potential role in multiple acyl-CoA dehydrogenase deficiency. Mol Genet Metab 86:441–447

    Article  PubMed  CAS  Google Scholar 

  56. Bedhomme M, Hoffmann M, McCarthy EA, Gambonnet B, Moran RG, Rébeillé F, Ravanel S (2005) Folate metabolism in plants: an Arabidopsis homolog of the mammalian mitochondrial folate transporter mediates folate import into chloroplasts. J Biol Chem 280:34823–34831

    Article  PubMed  CAS  Google Scholar 

  57. Todisco S, Agrimi G, Castegna A, Palmieri F (2006) Identification of the mitochondrial NAD+ transporter in Saccharomyces cerevisiae. J Biol Chem 281:1524–1531

    Article  PubMed  CAS  Google Scholar 

  58. Palmieri F, Rieder B, Ventrella A, Blanco E, Do PT, Nunes-Nesi A, Trauth AU, Fiermonte G, Tjaden J, Agrimi G, Kirchberger S, Paradies E, Fernie AR, Neuhaus HE (2009) Molecular identification and functional characterization of Arabidopsis thaliana mitochondrial and chloroplastic NAD+ carrier proteins. J Biol Chem 284:31249–31259

    Article  PubMed  CAS  Google Scholar 

  59. Marobbio CM, Di Noia MA, Palmieri F (2006) Identification of a mitochondrial transporter for pyrimidine nucleotides in Saccharomyces cerevisiae: bacterial expression, reconstitution and functional characterization. Biochem J 393:441–446

    Article  PubMed  CAS  Google Scholar 

  60. Floyd S, Favre C, Lasorsa FM, Leahy M, Trigiante G, Stroebel P, Marx A, Loughran G, O’Callaghan K, Marobbio CM, Slotboom DJ, Kunji ER, Palmieri F, O’Connor R (2007) The insulin-like growth factor-I-mTOR signaling pathway induces the mitochondrial pyrimidine nucleotide carrier to promote cell growth. Mol Biol Cell 18:3545–5355

    Article  PubMed  CAS  Google Scholar 

  61. Marobbio CM, Vozza A, Harding M, Bisaccia F, Palmieri F, Walker JE (2002) Identification and reconstitution of the yeast mitochondrial transporter for thiamine pyrophosphate. EMBO J 21:5653–5661

    Article  PubMed  CAS  Google Scholar 

  62. Lindhurst MJ, Fiermonte G, Song S, Struys E, De Leonardis F, Schwartzberg PL, Chen A, Castegna A, Verhoeven N, Mathews CK, Palmieri F, Biesecker LG (2006) Knockout of Slc25a19 causes mitochondrial thiamine pyrophosphate depletion, embryonic lethality, CNS malformations, and anemia. Proc Natl Acad Sci USA 103:15927–15932

    Article  PubMed  CAS  Google Scholar 

  63. Marobbio CM, Agrimi G, Lasorsa FM, Palmieri F (2003) Identification and functional reconstitution of yeast mitochondrial carrier for S-adenosylmethionine. EMBO J 22:5975–5982

    Article  PubMed  CAS  Google Scholar 

  64. Agrimi G, Di Noia MA, Marobbio CM, Fiermonte G, Lasorsa FM, Palmieri F (2004) Identification of the human mitochondrial S-adenosylmethionine transporter: bacterial expression, reconstitution, functional characterization and tissue distribution. Biochem J 379:183–190

    Article  PubMed  CAS  Google Scholar 

  65. Palmieri L, Arrigoni R, Blanco E, Carrari F, Zanor MI, Studart-Guimaraes C, Fernie AR, 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

    Article  PubMed  CAS  Google Scholar 

  66. Hjort K, Goldberg AV, Tsaousis AD, Hirt RP, Embley TM (2010) Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos Trans R Soc Lond B Biol Sci 365:713–727

    Article  PubMed  CAS  Google Scholar 

  67. Danovaro R, Dell’anno A, Pusceddu A, Gambi C, Heiner I, Kristensen RM (2010) The first metazoa living in permanently anoxic conditions. BMC Biol 8:30

    Article  PubMed  Google Scholar 

  68. Voncken F, Boxma B, Tjaden J, Akhmanova A, Huynen M, Verbeek F, Tielens AG, Haferkamp I, Neuhaus HE, Vogels G, Veenhuis M, Hackstein JH (2002) Multiple origins of hydrogenosomes: functional and phylogenetic evidence from the ADP/ATP carrier of the anaerobic chytrid Neocallimastix sp. Mol Microbiol 44:1441–1454

    Article  PubMed  CAS  Google Scholar 

  69. Boxma B, de Graaf RM, van der Staay GW, van Alen TA, Ricard G, Gabaldón T, van Hoek AH, Moon-van der Staay SY, Koopman WJ, van Hellemond JJ, Tielens AG, Friedrich T, Veenhuis M, Huynen MA, Hackstein JH (2005) An anaerobic mitochondrion that produces hydrogen. Nature 434:74–79

    Article  PubMed  CAS  Google Scholar 

  70. van der Giezen M, Slotboom DJ, Horner DS, Dyal PL, Harding M, Xue GP, Embley TM, Kunji ER (2002) Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J 21:572–579

    Article  PubMed  Google Scholar 

  71. Stechmann A, Hamblin K, Pérez-Brocal V, Gaston D, Richmond GS, van der Giezen M, Clark CG, Roger AJ (2008) Organelles in Blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr Biol 18:580–585

    Article  PubMed  CAS  Google Scholar 

  72. Perez-Brocal V, Clark CG (2008) Analysis of two genomes from the mitochondrion-like organelle of the intestinal parasite Blastocystis: complete sequences, gene content, and genome organization. Mol Biol Evol 25:2475–2482

    Article  PubMed  CAS  Google Scholar 

  73. Tjaden J, Haferkamp I, Boxma B, Tielens AG, Huynen M, Hackstein JH (2004) A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles. Mol Microbiol 51:1439–1446

    Article  PubMed  CAS  Google Scholar 

  74. Hrdý I, Hirt RP, Dolezal P, Bardonova L, Foster PG, Tachezy J, Embley TM (2004) Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618–622

    Article  PubMed  Google Scholar 

  75. Dolezal P, Dagley MJ, Kono M, Wolynec P, Likić VA, Foo JH, Sedinová M, Tachezy J, Bachmann A, Bruchhaus I, Lithgow T (2010) The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6:e1000812

    Article  PubMed  Google Scholar 

  76. Chan KW, Slotboom DJ, Cox S, Embley TM, Fabre O, van der Giezen M, Harding M, Horner DS, Kunji ER, León-Avila G, Tovar J (2005) A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr Biol 15:737–742

    Article  PubMed  CAS  Google Scholar 

  77. Maralikova B, Ali V, Nakada-Tsukui K, Nozaki T, van der Giezen M, Henze K, Tovar J (2010) Bacterial-type oxygen detoxification and iron-sulfur cluster assembly in amoebal relict mitochondria. Cell Microbiol 12:331–342

    Article  PubMed  CAS  Google Scholar 

  78. Hampl V, Silberman JD, Stechmann A, Diaz-Triviño S, Johnson PJ, Roger AJ (2008) Genetic evidence for a mitochondriate ancestry in the ‘amitochondriate’ flagellate Trimastix pyriformis. PLoS ONE 3:e1383

    Article  PubMed  Google Scholar 

  79. de Graaf RM, Duarte I, van Alen TA, Kuiper JW, Schotanus K, Rosenberg J, Huynen MA, Hackstein JH (2009) The hydrogenosomes of Psalteriomonas lanterna. BMC Evol Biol 9:287

    Article  PubMed  Google Scholar 

  80. Williams BA, Haferkamp I, Keeling PJ (2008) An ADP/ATP-specific mitochondrial carrier protein in the microsporidian Antonospora locustae. J Mol Biol 375:1249–1257

    Article  PubMed  CAS  Google Scholar 

  81. Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453:553–556

    Article  PubMed  CAS  Google Scholar 

  82. Möhlmann T, Tjaden J, Schwöppe C, Winkler HH, Kampfenkel K, Neuhaus HE (1998) Occurrence of two plastidic ATP/ADP transporters in Arabidopsis thaliana L.—molecular characterisation and comparative structural analysis of similar ATP/ADP translocators from plastids and Rickettsia prowazekii. Eur J Biochem 252:353–359

    Article  PubMed  Google Scholar 

  83. Trentmann O, Jung B, Neuhaus HE, Haferkamp I (2008) Nonmitochondrial ATP/ADP transporters accept phosphate as third substrate. J Biol Chem 283:36486–36493

    Article  PubMed  CAS  Google Scholar 

  84. Reinhold T, Alawady A, Grimm B, Beran KC, Jahns P, Conrath U, Bauer J, Reiser J, Melzer M, Jeblick W, Neuhaus HE (2007) Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage. Plant J 50:293–304

    Article  PubMed  CAS  Google Scholar 

  85. Thuswaldner S, Lagerstedt JO, Rojas-Stütz M, Bouhidel K, Der C, Leborgne-Castel N, Mishra A, Marty F, Schoefs B, Adamska I, Persson BL, Spetea C (2007) Identification, expression, and functional analyses of a thylakoid ATP/ADP carrier from Arabidopsis. J Biol Chem 282:8848–8859

    Article  PubMed  CAS  Google Scholar 

  86. Yin L, Lundin B, Bertrand M, Nurmi M, Solymosi K, Kangasjärvi S, Aro EM, Schoefs B, Spetea C (2010) Role of thylakoid ATP/ADP carrier in photoinhibition and photoprotection of photosystem II in Arabidopsis. Plant Physiol 153:666–677

    Article  PubMed  CAS  Google Scholar 

  87. Kirchberger S, Tjaden J, Neuhaus HE (2008) Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J 56:51–63

    Article  PubMed  CAS  Google Scholar 

  88. Leroch M, Kirchberger S, Haferkamp I, Wahl M, Neuhaus HE, Tjaden J (2005) Identification and characterization of a novel plastidic adenine nucleotide uniporter from Solanum tuberosum. J Biol Chem 280:17992–18000

    Article  PubMed  CAS  Google Scholar 

  89. Kirchberger S, Leroch M, Huynen MA, Wahl M, Neuhaus HE, Tjaden J (2007) Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays. J Biol Chem 282:22481–22491

    Article  PubMed  CAS  Google Scholar 

  90. Lasorsa FM, Scarcia P, Erdmann R, Palmieri F, Rottensteiner H, Palmieri L (2004) The yeast peroxisomal adenine nucleotide transporter: characterization of two transport modes and involvement in DeltapH formation across peroxisomal membranes. Biochem J 381:581–585

    Article  PubMed  CAS  Google Scholar 

  91. Palmieri L, Rottensteiner H, Girzalsky W, Scarcia P, Palmieri F, Erdmann R (2001) Identification and functional reconstitution of the yeast peroxisomal adenine nucleotide transporter. EMBO J 20:5049–5059

    Article  PubMed  CAS  Google Scholar 

  92. Visser WF, van Roermund CW, Waterham HR, Wanders RJ (2002) Identification of human PMP34 as a peroxisomal ATP transporter. Biochem Biophys Res Commun 299:494–497

    Article  PubMed  CAS  Google Scholar 

  93. Linka N, Theodoulou FL, Haslam RP, Linka M, Napier JA, Neuhaus HE, Weber AP (2008) Peroxisomal ATP import is essential for seedling development in Arabidopsis thaliana. Plant Cell 20:3241–3257

    Article  PubMed  CAS  Google Scholar 

  94. Michels PA, Bringaud F, Herman M, Hannaert V (2006) Metabolic functions of glycosomes in trypanosomatids. Biochim Biophys Acta 1763:1463–1477

    Article  PubMed  CAS  Google Scholar 

  95. Leroch M, Neuhaus HE, Kirchberger S, Zimmermann S, Melzer M, Gerhold J, Tjaden J (2008) Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:438–451

    Article  PubMed  CAS  Google Scholar 

  96. Sawada K, Echigo N, Juge N, Miyaji T, Otsuka M, Omote H, Yamamoto A, Moriyama Y (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105:5683–5686

    Article  PubMed  CAS  Google Scholar 

  97. Miyaji T, Echigo N, Hiasa M, Senoh S, Omote H, Moriyama Y (2008) Identification of a vesicular aspartate transporter. Proc Natl Acad Sci USA 105:11720–11724

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from Ministerio de Educación y Ciencia (BFU2008-04084/BMC), Comunidad de Madrid (S-GEN-0269-2006 MITOLAB-CM), the European Union (LSHM-CT-2006-518153), and CIBERER (an initiative of the ISCIII) to J.S.; by grants from the ISCIII (PI080610) to A. del A. and by an institutional grant from the Fundación Ramón Areces to the Centro de Biología Molecular Severo Ochoa. J.T. is a recipient of a fellowship from the Comunidad de Madrid.

Author information

Authors and Affiliations

  1. Departamento de Biología Molecular, Centro de Biología Molecular Severo Ochoa UAM-CSIC, CIBER de Enfermedades Raras (CIBERER), Universidad Autónoma de Madrid, Madrid, Spain

    Javier Traba, Jorgina Satrústegui & Araceli del Arco

  2. Área de Bioquímica, Facultad de Ciencias del Medio Ambiente, Centro Regional de Investigaciones Biomédicas (CRIB), Universidad de Castilla-La Mancha, Toledo, Spain

    Araceli del Arco

Authors
  1. Javier Traba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorgina Satrústegui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Araceli del Arco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Traba.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 94 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Traba, J., Satrústegui, J. & del Arco, A. Adenine nucleotide transporters in organelles: novel genes and functions. Cell. Mol. Life Sci. 68, 1183–1206 (2011). https://doi.org/10.1007/s00018-010-0612-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-010-0612-3

Keywords

Search

Navigation