Complete loss-of-function of the heart/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy

Human Molecular Genetics

Volumn 14, Issue 20, 2005, Pages 3079-3088

  Palmieri, Luigi ^a,b   Alberio, Simona ^c   Pisano, Isabella ^a   Lodi, Tiziana ^d   Meznaric Petrusa, Mija ^e   Zidar, Janez ^e   Santoro, Antonella ^a,b   Scarcia, Pasquale ^a   Fontanesi, Flavia ^d,f   Lamantea, Eleonora ^c   Ferrero, Iliana ^d   Zeviani, Massimo ^c  

^a UNIVERSITY OF BARI   (Italy)

^b CNR   (Italy)

^c DEPARTMENT OF NEUROSURGERY   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e UNIVERSITY MEDICAL CENTRE LJUBLJANA   (Slovenia)

^f UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE TRIPHOSPHATE; ALANINE; ASPARTIC ACID; MITOCHONDRIAL DNA; MUSCLE PROTEIN; REACTIVE OXYGEN METABOLITE; SCAVENGER;

ADULT; AMINO ACID SUBSTITUTION; ARTICLE; CASE REPORT; CELL VIABILITY; CLINICAL FEATURE; DISEASE ASSOCIATION; DISEASE SEVERITY; ELECTROCARDIOGRAM; ELECTROMYOGRAM; EXERCISE TOLERANCE; GENE FUNCTION; GENE MUTATION; GENOME ANALYSIS; HEART LEFT VENTRICLE HYPERTROPHY; HUMAN; HUMAN TISSUE; HYPERTROPHIC CARDIOMYOPATHY; LACTIC ACIDOSIS; MALE; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL MYOPATHY; MUSCLE BIOPSY; MUSCLE MITOCHONDRION; NUCLEIC ACID BASE SUBSTITUTION; OPHTHALMOPLEGIA; ORTHOLOGY; OXIDATION REDUCTION REACTION; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOLIPOSOME; RECESSIVE INHERITANCE; SOUTHERN BLOTTING; SYSTOLIC HEART MURMUR;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; ADULT; AMINO ACID SEQUENCE; ANIMALS; CARDIOMYOPATHIES; CELL SURVIVAL; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; HUMANS; MICE; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MITOCHONDRIAL MYOPATHIES; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MYOCARDIUM; PHENOTYPE; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT;

EID: 27544494568     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi341     Document Type: Article

References (40)

1. Kaukonen, J., Juselius, J.K., Tiranti, V., Kyttälä, A., Zeviani, M., Comi, G.P., Keränen, S., Peltonen, L. and Suomalainen, A. (2000) Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science, 289, 782-785.
2. Spelbrink, J.N., Li, F.Y., Tiranti, V., Nikali, K., Yuan, Q.P., Tariq, M., Wanrooij, S., Garrido, N., Comi, G., Morandi, L. et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet., 28, 223-231.
3. Van Goethem, G., Dermaut, B., Lofgren, A., Martin, J.J. and Van Broeckhoven, C. (2001) Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nat. Genet., 28, 211-212.
4. Lamantea, E., Tiranti, V., Bordoni, A., Toscano, A., Bono, F., Servidei, S., Papadimitriou, A., Spelbrink, H., Silvestri, L., Casari, G. et al. (2002) Mutations of mitochondrial DNA polymerase gammaA are a frequent cause of autosomal dominant or recessive progressive external ophthalmoplegia. Ann. Neurol., 52, 211-219.
5. Napoli, L., Bordoni, A., Zeviani, M., Hadjigeorgiou, G.M., Sciacco, M., Tiranti, V., Terentiou, A., Moggio, M., Papadimitriou, A., Scarlato, G. et al. (2001) A novel missense adenine nucleotide translocator-1 gene mutation in a Greek adPEO family. Neurology, 57, 2295-2298.
6. Siciliano, G., Tessa, A., Petrini, S., Mancuso, M., Bruno, C., Grieco, G.S., Malandrini, A., De Florio, L., Martini, B., Federico, A. et al. (2003) Autosomal dominant external ophthalmoplegia and bipolar affective disorder associated with a mutation in the ANT1 gene. Neuromuscul. Disord., 13, 162-165.
7. Deschauer, M., Hudson, G., Muller, T., Taylor, R.W., Chinnery, P.F. and Zierz, S. (2005) A novel ANT1 gene mutation with probable germline mosaicism in autosomal dominant progressive external ophthalmoplegia. Neuromuscul. Disord, 15, 311-315.
8. Komaki, H., Fukazawa, T., Houzen, H., Yoshida, K., Nonaka, I. and Goro, Y. (2002) A novel D104G mutation in the adenine nucleotide translocator 1 gene in autosomal dominant progressive external ophthalmoplegia patients with mitochondrial DNA with multiple deletions. Ann. Neurol., 51, 645-648.
9. Dolce, V., Scarcia, P., Iacopetta, D. and Palmieri, F. (2005) A fourth ADP/ATP carrier isoform in man: Identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett., 579, 633-637.
10. Klingenberg, M. (1989) Molecular aspects of the adenine nucleotide carrier from mitochondria. Arch. Biochem. Biophys., 270, 1-14.
11. Fiore, C., Trezeguet, V., Le Saux, A., Roux, P., Schwimmer, C., Dianoux, A.C., Noel, F., Lauquin, G.J., Brandolin, G., and Vignais, P.V. (1998) The mitochondrial ADP/ATP carrier: Structural, physiological and pathological aspects. Biochemie, 80, 137-150.
12. Bauer, M.K.A., Schubert, A., Rocks, O. and Grimm, S. (1999) Adenine nucleotide translocase-1, a component of the permeability transition pore, can dominantly induce apoptosis. J. Cell. Biol., 147, 1493-1502.
13. Esposito, L.A., Melov, S., Panov, A., Cottrell, B.A. and Wallace, D.C. (1999) Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl. Acad. Sci. USA, 96, 4820-4825.
14. Graham, B.H., Waymire, K.G., Cottrell, B., Trounce, I.A., MacGregor, G.R. and Wallace, D.C. (1997) A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nat. Genet., 16, 226-234.
15. Fontanesi, F., Palmieri, L., Scarcia, P., Lodi, T., Donnini, C., Limongelli, A., Tiranti, V., Zeviani, M., Ferrero, I. and Viola, A.M. (2004) Mutations in AAC2, equivalent to human adPEO-associated ANT1 mutations, lead to defective oxidative phosphorylation in Saccharomyces cerevisiae and affect mitochondrial DNA stability. Hum. Mol. Genet., 13, 923-934.
16. Kramer, R. and Klingenberg, M. (1979) Reconstitution of adenine nucleotide transport from beef heart mitochondria. Biochemistry, 18, 4209-4215.
17. Fiermonte, G., Walker, J.E. and Palmieri, F. (1993) Abundant bacterial expression and reconstitution of an intrinsic membrane-transport protein from bovine mitochondria. Biochem. J., 294, 293-299.
18. Fiermonte, G., De Leonardis, F., Todisco, S., Palmieri, L., Lasorsa, F.M. and 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.
19. Bonneaud, N., Ozier-Kalogeropoulos, O., Li, G.Y., Labouesse, M., Minvielle-Sebastia, L. and Lacroute, F. (1991) A family of low and high copy replicative, integrative and single-stranded S. cerevisiae/E. coli shuttle vectors. Yeast, 7, 609-615.
20. Bennetzen, J.L. and Hall, B.D. (1982) Codon selection in yeast. J. Biol. Chem., 257, 3026-3031.
21. Kovácova, V., Irmlerová, J. and Kovác, L. (1968) Oxidative phosphorylation in yeast. IV. Combination of a nuclear mutation affecting oxidative phosphorylation with a cytoplasmic mutation to respiratory deficiency. Biochim. Biophys. Acta, 162, 157-162.
22. Bulder, C.J.E.A. (1964) Lethality of the petite mutation in petite-negative yeasts. Antonie Van Leeuwenhoek 30, 442-454.
23. Jordens, E.Z., Palmieri, L., Huizing, M., van den Heuvel, L.P., Sengers, R.C., Dorner, A., Ruitenbeek, W., Trijbels, F.J., Valsson, J., Sigfusson, G. et al. (2002) Adenine nucleotide translocator 1 deficiency associated with Sengers syndrome. Ann. Neurol., 52, 95-99.
24. Chen, X.J. (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.
25. 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, 26, 39-44.
26. MacKenzie, K.R., Prestegard, J.H. and Engelman, D.M. (1997) A transmembrane helix dimer: Structure and implications. Science, 276, 131-133.
27. Curran, A.R. and Engelman, D.M. (2003) Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Curr. Opin. Struct. Biol., 13, 412-417.
28. Dyall, S.D., Agius, S.C., De Marcos Lousa, C., Trezeguet, V. and Tokatlidis, K. (2003) The dynamic dimerization of the yeast ADP/ATP carrier in the inner mitochondrial membrane is affected by conserved cysteine residues. J. Biol. Chem., 278, 26757-26764.
29. Schroers, A., Burkovski, A., Wohlrab, H. and Kramer, R. (1998) The phosphate carrier from yeast mitochondria. Dimerization is a prerequisite for function. J. Biol. Chem., 273, 14269-14276.
30. Dujon, B. (1981) Mitochondrial genetics and functions. In The Molecular Biology of the Yeast Saccharomyces, Life Cycle and Inheritance, Cold Spring Harbor Laboratory, pp. 505-635.
31. Marzo, I., Brenner, C., Zamzami, N., Jurgensmeier, J.M., Susin, S.A., Vieira, H.L., Prevost, M.C., Xie, Z., Matsuyama, S., Reed, J.C. and Kroemer, G. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science, 281, 2027-2031.
32. McKenzie, M., Liolitsa, D. and Hanna, M.G. (2004) Mitochondrial disease: mutations and mechanisms. Neurochem. Res., 29, 589-600.
33. Doudican, N.A., Song, B., Shadel, G.S. and Doetsch, P.W. (2005) Oxidative DNA damage causes mitochondrial genomic instability in Saccharomyces cerevisiae. Mol. Cell Biol., 25, 5196-5204.
34. Fagiolari, G., Sciacco, M., Chiveri, L., Lamperti, C., Comi, G.P., Scarlato, G., Moggio, M. and Prelle, A. (2002) Lack of apoptosis in patients with progressive external ophthalmoplegia and mutated adenine nucleotide translocator-1 gene. Muscle Nerve, 26, 265-269.
35. Tiranti, V., Galimberti, C., Nijtmans, L., Bovolenta, S., Perini, M.P. and Zeviani, M. (1999) Characterization of SURF-1 expression and Surf-1p function in normal and disease conditions. Hum. Mol. Genet., 8, 2533-2540.
36. Ferrari, G., Lamantea, E., Donati, A., Filosto, M., Briem, E., Carrara, F., Parini, R., Simonati, A., Santer, R. and Zeviani, M. (2005) Infantile hepatocerebral syndromes associated with mutations in the mitochondrial DNA polymerase-gamma A. Brain, 128, 723-731.
37. Hashimoto, M., Shinohara, Y., Majima, E., Hatanaka, T., Yamazaki, N. and Terada, H. (1999) Expression of the bovine heart mitochondrial ADP/ATP carrier in yeast mitochondria: Significantly enhanced expression by replacement of the N-terminal region of the bovine carrier by the corresponding regions of the yeast carriers. Biochim. Biophys. Acta, 1409, 113-124.
38. Sherman, F. (1991) Getting started with yeast. Methods Enzymol., 194, 3-21.
39. Ogur, M., St. John, R. and Nagai, S. (1957) Tetrazolium overlay technique for population studies of respiratory deficiency in yeast. Science, 125, 928-929.
40. Palmieri, F., Indiveri, C., Bisaccia, F. and Iacobazzi, V. (1995) Mitochondrial metabolite carrier proteins: Purification, reconstitution, and transport studies. Methods Enzymol., 260, 349-369.