The mitochondrial ADP/ATP carrier: Structural, physiological and pathological aspects

Biochimie

Volumn 80, Issue 2, 1998, Pages 137-150

  Fiore, C ^a   Trezeguet V ^b   Le Saux, A ^b   Roux, P ^a   Schwimmer, C ^b   Dianoux, A C ^a   Noel, F ^a   Lauquin, G J M ^b   Brandolin, G ^a   Vignais, P V ^a  

^a UMR 314 CNRS   (France)

^b Institut de Biochimie et Genetique Cellulaires   (France)

Author keywords

ADP ATP carrier; Atractyloside; Bongkrekic acid; Fluorescence; Mitochondria; Muscular pathologies; Mutagenesis

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ATRACTYLOSIDE; BONGKREKIC ACID; CARBOXYATRACTYLOSIDE; CARRIER PROTEIN; ENZYME INHIBITOR; FLUORESCENT DYE;

ARTICLE; CONFORMATIONAL TRANSITION; FLUOROMETRY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MYOPATHY; NUCLEOTIDE TRANSPORT; PROTEIN CONFORMATION;

EID: 0032006449     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0300-9084(98)80020-5     Document Type: Article

References (71)

1. 1 Siekevitz PV, Potter VR (1955) Biochemical structure of mitochondria I. Intramitochondrial components and oxidative phosphorylation. J Biol Chem 215, 237-255
2. 2 Pressman BC (1958) Intramitochondrial nucleotides. I. Some factors affecting net interconversion of adenine nucleotides. J Biol Chem 232, 967-978
3. 3 Bruni A, Contessa AR, Luciani S (1962) Atractyloside as inhibitor of energy-transfer reactions in liver mitochondria. Biochim Biophys Acta 60, 301-316
4. 4 Vignais PV, Vignais PM, Stanislas E (1962) Action of potassium atractylate on oxidative phosphorylation in mitochondria and submitochondrial particles. Biochim Biophys Acta 60, 284-300
5. 5 Kemp A, Slater EC (1964) The site of action of atractyloside. Biochim Biophys Acta 92, 178-180
6. 6 Chappell JB, Crofts AR (1965) The effect of atractyloside and oligomycin on the behavior of mitochondria towards the adenine nucleotides. Biochem J 95, 707-716
7. 7 Pfaff E, Klingenberg M, Heldt HW (1965) Unspecific permeation and specific exchange of mitochondrial adenine nucleotides in liver mitochondria. Biochim Biophys Acta 104, 312-315
8. 8 Duée ED, Vignais PV (1965) Echange entre adénine-nucléotides extra-et intramitochondriaux. Biochim Biophys Acta 107, 184-188
9. 14C-labeled ADP and ATP and with atractyloside. Biochem Biophys Res Commun 18, 174-179
10. 10 Vignais PV (1976) Molecular and physiological aspects of adenine nucleotide transport in mitochondria. Biochim Biophys Acta 456, 1-38
11. 11 Vignais PV, Block MR, Boulay F, Brandolin G, Lauquin GJM (1985) Molecular aspects of structure function relationships in mitochondrial adenine nucleotide carrier. In: Structure and Properties of Cell Membranes, Vol II (Benga G, ed) CRC Press, Boca Raton, 139-179
12. 12 Higgins DG, Bleasby AJ, Fuchs R (1992) CLUSTAL V: improved software for multiple sequence alignment. CABIOS 8, 189-191
13. 13 Adrian GS, McCammon MT, Montgommery DL, Douglas MG (1986) Sequence required for delivery and localization of the ADP/ATP translocator to the mitochondrial inner membrane. Mol Cell Biol 6, 626-634
14. 14 Lawson JE, Douglas MG (1988) Separate genes encode functionally equivalent ADP/ATP carrier proteins in Sacchammyces cerevisiae. Isolation and analysis of AAC2. J Biol Chem 263, 14812-14818
15. 15 Kolarov J, Kolarova N, Nelson N (1990) A third ADP/ATP translocator gene in yeast. J Biol Chem 265, 12711-12716
16. 16 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
17. 17 O'Malley K, Pratt P, Robertson J, Lilly M, Douglas MG (1982) Selection of the nuclear gene for the mitochondrial adenine nucleotide translocator by genetic complementation of the opl mutation in yeast. J Biol Chem 257, 2097-2103
18. 18 Haraguchi Y, Chung AB, Torroni A, Stepien G, Shoffner JM, Wasmuth JJ, Costigan DA, Polak M, Altherr MR, Winokur ST (1993) Genetic mapping of human heart-skeletal muscle adenine nucleotide translocator and its relationship to the facioscapulohumeral muscular dystrophy locus. Genomics 16, 479-485
19. 19 Slim R, Levilliers J, Ludecke HJ, Claussen U, Nguyen VC, Gough NM, Horsthemke B, Petit C (1993) A human pseudoautosomal gene encodes the ANT3 ADP/ATP translocase and escapes X-inactivation. Genomics 16, 26-33
20. 20 Schiebel K, Weiss B, Wohrle D, Rappold G (1993) A human pseudoautosomal gene, ADP/ATP translocase, escapes X-inactivation whereas a homologue on Xq is subject to X-inactivation. Nature Genet 3, 82-87
21. 21 Wijmenga C, Padberg GW, Moerer P, Wiegant J, Liem L, Brouwer OF, Milner EC, Weber JL, Van Ommen G, Sandkuyl LA (1991) Mapping of facioscapulohumeral muscular dystrophy gene to chromosome 4q35-qter by multipoint linkage analysis and in situ hybridization. Genomics 9, 570-575
22. 22 Wijmenga C, Winokur ST, Padberg GW, Skraastad MI, Altherr MR, Wasmuth JJ, Murray JC, Hofker MH, Frants RR (1993) The human skeletal muscle adenine nucleotide translocator gene maps to chromosome 4q35 in the region of the facioscapulohumeral muscular dystrophy locus. Hum Genet 92, 198-203
23. 23 Schulteiss HP, Bolte HD (1985) Immunological analysis of autoantibodies against the adenine nucleotide translocator in dilated cardiomyopathy. J Mol Cell Cardiol 17, 603-617
24. 24 Stepien G, Torroni A, Chung AB, Hodge JA, Wallace DC (1992) Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. J Biol Chem 267, 14592-14597
25. 25 Lunardi J, Hurko O, Engel WK, Attardi G (1992) The multiple ADP/ATP translocase genes are differentially expressed during human muscle development. J Biol Chem 267, 15267-15270
26. 26 Li K, Hodge JA, Wallace DC (1990) OXBOX, a positive transcriptional element of the heart-skeletal muscle ADP/ATP translocator gene. J Biol Chem 265, 20585-20588
27. 27 Lunardi J, Attardi G (1991) Differential regulation of expression of the multiple ADP/ATP translocase genes in human cells. J Biol Chem 266, 16534-16540
28. 28 Luciakova K, Nelson BD (1992) Transcript levels for nuclear-encoded mammalian mitochondrial respiratory-chain components are regulated by thyroid hormone in an uncoordinated fashion. Eur J Biochem 207, 247-251
29. 29 Battini R, Ferrari S, Kaczmarek L, Calabretta B, Chen ST, Baserga R (1987) Molecular cloning of a cDNA for a human ADP/ATP carrier which is growth-regulated. J Biol Chem 262, 4355-4359
30. 30 Brandolin G, Le Saux A, Trézéguet V, Lauquin GJM, Vignais PV (1993) Chemical, immunological, enzymatic, and genetic approaches to studying the arrangement of the peptide chain of the ADP/ATP carrier in the mitochondrial membrane. J Bioenerg Biomembr 25, 459-472
31. 31 Brdiczka D, Schumacher D (1976) Iodination of the peripheral mitochondrial membrane proteins in correlation to the functional state of the ADP/ATP carrier. Biochem Biophys Res Commun 73, 823-832
32. 32 Buchanan BB, Eiermann W, Riccio P, Aquila H, Klingenberg M (1976) Antibody evidence for different conformational states of ADP/ATP translocator isolated from mitochondria. Proc Natl Sci Acad USA 73, 2280-2284
33. 33 Boulay F, Lauquin GJM, Vignais PV (1986) Localization of immunoreactive regions in the beef heart adenine nucleotide carrier using rabbit antisera against the carboxyatractyloside-liganded and the sodium dodecyl sulfate denaturated carrier forms. Biochemistry 25, 7567-7571
34. 34 Brandolin G, Boulay F, Dalbon P, Vignais PV (1989) Orientation of the N-terminal region of the membrane-bound ADP/ATP carrier protein explored by antipeptide antibodies and an arginine-specific endoprotease. Evidence that the accessibility of the N-terminal residues depends on the conformational state of the carrier. Biochemistry 28, 1093-1100
35. 35 Boulay F, Vignais PV (1984) Localization of the N-ethylmaleimide reactive cysteine in the beef heart mitochondrial ADP/ATP carrier protein. Biochemistry 23, 4807-4812
36. 36 Many I, Brandolin G, Gagnon J, Brasseur R, Vignais PV (1992) Topography of the membrane-bound ADP/ATP carrier assessed by enzymatic proteolysis. Biochemistry 31, 4058-4065
37. 37 Block MR, Lauquin GJM, Vignais PV (1983) Use of 3′-O-naphthoyladenosine 5′-diphosphate to probe distinct conformational states of membrane-bound adenosine 5′-diphosphate/adenosine 5′-triphosphate carrier. Biochemistry 22, 2202-2208
38. 38 Klingenberg M (1985) Principles of carrier catalysis elucidated by comparing two similar membrane translocators from mitochondria, the ADP/ATP carrier and the uncoupling protein. Ann NY Acad Sci 456, 279-288
39. 39 Porath J, Carlsson J, Olsson I, Belfrage G (1975) Metal chelate affinity chromatography, a new approach to protein fractionation. Nature 258, 598-599
40. 40 Hochuli E, Döbeli H, Schacher A (1987) New metal chelate adsorbent selective for proteins and peptide containing neighbouring histidine residues. J Chromatogr 411, 177-184
41. 41 Hackenberg H, Klingenberg M (1980) Molecular weight and hydrodynamic parameters of the adenosine 5′-diphosphate/adenosine 5′-triphosphate carrier in Triton X-100. Biochemistry 19, 548-555
42. 42 Block MR, Zaccai G, Lauquin GJM, Vignais PV (1982) Small angle neutron scattering of the mitochondrial ADP/ATP carrier protein in detergent. Biochem Biophys Res Commun 109, 471-477
43. 43 Dupont Y, Brandolin G, Vignais PV (1982) Exploration of the nucleotide binding sites of the isolated ADP/ATP carrier protein from beef heart mitochondria. 1. Probing of the nucleotide sites by Naphthoyl-ATP, a fluorescent nontransportable analogue of ATP. Biochemistry 21, 6343-6347
44. 44 Brandolin G, Dupont Y, Vignais PV (1982) Exploration of the nucleotide binding sites of the isolated ADP/ATP carrier protein from beef heart mitochondria. 2. Probing of the nucleotide sites by formycin triphosphate, a fluorescent transportable analogue of ATP. Biochemistry 21, 6348-6353
45. 14C]acetylcarboxyatractyloside to the mitochondrial ADP/ATP carrier. FEBS Lett 117, 335-340
46. 46 Block MR, Vignais PV (1984) Substrate-site interactions in the membrane-bound adenine-nucleotide carrier as disclosed by ADP and ATP analogs. Biochim Biophys Acta 767, 369-376
47. 47 Vignais PV, Vignais PM, Defaye G (1971) Gummiferin, an inhibitor of the adenine-nucleotide translocation. Study of its binding properties to mitochondria. FEBS Lett 17, 281-287
48. 48 Brandolin G, Dupont Y, Vignais PV (1985) Substrate-induced modifications of the intrinsic fluorescence of the isolated adenine nucleotide carrier protein: demonstration of distinct conformational states. Biochemistry 24, 1991-1997
49. 49 Saraste M, Walker JE (1982) Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Lett 144, 250-254
50. 50 Walker JE, Runswick MJ (1993) The mitochondrial transport protein superfamily. J Bioenerg Biomembr 25, 435-446
51. 51 Brandolin G, Dupont Y, Vignais PV (1981) Substrate-induced fluorescence changes of the isolated ADP/ATP carrier protein in solution. Biochem Biophys Res Commun 98, 28-35
52. 52 Brandolin G, Le Saux A, Trézéguet V, Vignais PV, Lauquin GJM (1993) Biochemical characterization of the isolated Anc2 adenine nucleotide carrier from Saccharomyces cerevisiae mitochondria. Biochem Biophys Res Commun 192, 143-150
53. 53 Le Saux A, Roux P, Trézéguel V, Fiore C, Schwimmer C, Dianoux AC, Vignais PV, Brandolin G, Lauquin GJM (1996) Conformational changes of the yeast mitochondrial adenosine diphosphate/adenosine triphosphate carrier studied through its intrinsic fluorescence. 1. Tryptophanyl residues of the carrier can be mutated without impairing protein activity. Biochemistry 35, 16116-16124
54. 54 Roux P, Le Saux A, Trézéguet V, Fiore C, Schwimmer C, Dianoux AC, Vignais PV, Lauquin GJM, Brandolin G (1996) Conformational changes of the yeast mitochondrial adenosine diphosphate/adenosine triphosphate carrier studied through its intrinsic fluorescence. 2. Assignment of tryptophanyl residues of the carrier to the responses to specific ligands. Biochemistry 35, 16125-16131
55. 55 Klingenberg M, Nelson DR (1994) Structure-function relationships of the ADP/ATP carrier. Biochim Biophys Acta 1187, 241-244
56. 56 Nelson DR, Lawson JE, Klingenberg M, Douglas MG (1993) Site-directed mutagenesis of the yeast mitochondrial ADP/ATP translocator. Six arginines and one lysine are essential. J Mol Biol 230, 1159-1170
57. 57 Klingenberg M, Nelson DR (1994) Structure-function relationships of the ADP/ATP carrier. Biochim Biophys Acta 1187, 241-244
58. 58 Muller V, Basset G, Nelson DR, Klingenberg M (1996) Probing the role of positive residues in the ADP/ATP carrier from yeast. The effect of six arginine mutations of oxidative phosphorylation and AAC expression. Biochemistry 35, 16132-16143
59. 59 Heidkamper D, Muller V, Nelson DR, Klingenberg M (1996) Probing the role of positive residues in the ADP/ATP carrier from yeast. The effect of six arginine mutations on transport and the four ATP versus ADP exchange modes. Biochemistry 35, 16144-16152
60. 60 Nelson DR, Douglas MG (1993) Function-based mapping of the yeast mitochondrial ADP/ATP translocator by selection for second site revenants. J Mol Biol 230, 1171-1182
61. 61 Nelson DR (1996) The yeast ADP/ATP carrier. Mutagenesis and second-site revertants. Biochim Biophys Acta 1275, 133-137
62. 62 Huizing M, DePinto V, Ruitenbeek W, Trijbels FJM, Van den Heuvel LP, Wendel U (1996) Importance of mitochondrial transmembrane processes in human mitochondriopathies. J Bioenerg Biomembr 28, 109-114
63. 63 Bakker HD, Scholte HR, Van den Bogert C, Ruitenbeek W, Jeneson JA, Wanders RJ, Abeling NG, Dorland B, Sengers RC, Van Gennip AH (1993) Deficiency of the adenine nucleotide translocator in muscle of a patient with myopathy and lactic acidosis: a new mitochondrial defect. Pediatr Res 33, 412-417
64. 64 Graham BH, Waymine KG, Cottrell B, Trounce IA, MacGregor GR, Wallace DC (1997) A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nature Genet 16, 226-234
65. 65 Heddi A, Lestienne P, Wallace DC, Stepien G (1993) Mitochondrial DNA expression in mitochondrial myopathies and coordinated expression of nuclear genes involved in ATP production. J Biol Chem 268. 12156-12163
66. 66 Torroni A, Stepien G, Hodge JA, Wallace DC (1990) Neoplastic transformation is associated with coordinate induction of nuclear and cytoplasmic oxidative phosphorylation genes. J Biol Chem 265, 20589-20593
67. 67 Heddi A, Faure-Vigny H, Wallace DC, Stepien G (1996) Coordinate expression of nuclear and mitochondrial genes involved in energy production in carcinoma and oncocytoma. Biochim Biophys Acta 1316, 203-209
68. 68 Bakker HD, Scholte H, Van den Bogert C, Jeneson JA, Ruitenbeek W, Wanders RJ, Abeling NG, Van Gennip AH (1993) Adenine nucleotide translocator deficiency in muscle: potential therapeutic value of vitamin E. J Inherit Metab Dis 16, 548-552
69. 69 Bakker HD, Scholte HR, Jeneson JA (1993) Vitamin E in a mitochondrial myopathy with proliferating mitochondria. Lancet 342, 175-176
70. 70 Roux P, Le Saux A, Fiore C, Schwimmer C, Dianoux AC, Trézéguet V, Vignais PV, Lauquin GJM, Brandolin G (1996) Fluorometric titration of the mitochondrial ADP/ATP carrier protein in muscle homogenate with atractyloside derivatives. Anal Biochem 234, 31-37
71. 71 Boulay F, Brandolin G, Lauquin GJM, Vignais PV (1983) Synthesis and properties of fluorescent derivatives of atractyloside as potential probes of the mitochondrial ADP/ATP carrier protein. Anal Biochem 128, 323-330