Dominant membrane uncoupling by mutant adenine nucleotide translocase in mitochondrial diseases

Human Molecular Genetics

Volumn 17, Issue 24, 2008, Pages 4036-4044

  Wang, Xiaowen ^a   Salinas, Kelly ^a   Zuo, Xiaoming ^b   Kucejova, Blanka ^b   Chen, Xin Jie ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ALANINE; ASPARTIC ACID; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; FUNGAL PROTEIN; METHIONINE; MITOCHONDRIAL DNA; PROLINE; PROTEIN AAC2; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; AUTOSOMAL DOMINANT DISORDER; BIOGENESIS; CARDIOMYOPATHY; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; CONTROLLED STUDY; CYTOSOL; DISEASE COURSE; GENE MUTATION; GENE OVEREXPRESSION; GENETIC STABILITY; MEDICAL AUDIT; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MUTATIONAL ANALYSIS; MYOPATHY; NONHUMAN; NUCLEOTIDE TRANSPORT; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; YEAST;

AMINO ACID SUBSTITUTION; ENERGY METABOLISM; GENES, DOMINANT; HUMANS; MITOCHONDRIAL ADP, ATP TRANSLOCASES; MITOCHONDRIAL DISEASES; MITOCHONDRIAL MEMBRANES; MODELS, BIOLOGICAL; OPHTHALMOPLEGIA, CHRONIC PROGRESSIVE EXTERNAL; PHENOTYPE; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UNCOUPLING AGENTS;

EID: 57049091540     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn306     Document Type: Article

References (35)

1. Klingenberg, M. (2008) The ADP and ATP transport in mitochondria and its carrier. Biochim. Biophys. Acta, 1778, 1978-2021.
2. 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, 426 39-44.
3. + transport by free fatty acids, which is further stimulated by mersalyl. J. Biol. Chem., 269, 27329-27336.
4. Brand, M.D., Pakay, J.L., Ocloo, A., Kokoszka, J., Wallace, D.C., Brookes, P.S. and Cornwall, E.J. (2005) The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochem. J., 392, 353-362.
5. Kaukonen, J., Juselius, J.K., Tiranti, V., Kyttala, A., Zeviani, M., Comi, G.P., Keranen, S., Peltonen, L. and Suomalainen, A. (2000) Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science, 289, 782-785.
6. 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.
7. Komaki, H., Fukazawa, T., Houzen, H., Yoshida, K., Nonaka, I. and Goto, 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.
8. Siciliano, G., Tessa, A., Petrini, S., Mancuso, M., Bruno, C., Grieco, G.S., Malandrini, A., DeFlorio, 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.
9. 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.
10. Spinazzola, A. and Zeviani, M. (2005) Disorders of nuclear-mitochondrial intergenomic signaling. Gene, 354, 162-168.
11. Chen, X.J. (2002) Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia. Hum. Mol. Genet., 11, 1835-1843.
12. 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.
13. Wang, X.W., Zuo, X.M., Kucejova, B. and Chen, X.J. (2008) Reduced cytosolic protein synthesis suppresses mitochondrial degeneration. Nat. Cell Biol., 10, 1090-1097.
14. Palmieri, L., Alberio, S., Pisano, I., Lodi, T., Meznaric-Petrusa, M., Zidar, J., Santoro, A., Scarcia, P., Fontanesi, F., Lamantea, E. et al. (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.
15. 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.
16. 1-ATPase are required for survival of petite mutants in Saccharomyces cerevisiae. Mol. Gen. Genet., 262, 898-908.
17. Betina, S., Gavurnikova, G., Haviernik, P., Sabova, L. and Kolarov, J. (1995) Expression of the AAC2 gene encoding the major mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae is controlled at the transcriptional level by oxygen, heme and HAP2 factor. Eur. J. Biochem., 229, 651-657.
18. Thorsness, P.E., White, K.H. and Fox, T.D. (1993) Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell Biol., 13, 5418-5426.
19. Leonhard, K., Herrmann, J.M., Stuart, R.A., Mannhaupt, G., Neupert, W. and Langer, T. (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J., 15, 4218-4229.
20. Pearce, D.A. and Sherman, F. (1995) Degradation of cytochrome oxidase subunits in mutants of yeast lacking cytochrome c and suppression of the degradation by mutation of yme1. J. Biol. Chem., 270, 20879-20882.
21. Weber, E.R., Hanekamp, T. and Thorsness, P.E. (1996) Biochemical and functional analysis of the YME1 gene product, an ATP and zinc-dependent mitochondrial protease from S. cerevisiae. Mol. Biol. Cell, 7, 307-317.
22. Kominsky, D.J., Brownson, M.P., Updike, D.L. and Thorsness, P.E. (2002) Genetic and biochemical basis for viability of yeast lacking mitochondrial genomes. Genetics, 162, 1595-1604.
23. Chen, X.J. and Butow, R.A. (2005) The organization and inheritance of the mitochondrial genome. Nat. Rev. Genet., 6, 815-825.
24. 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.
25. 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.
26. Copeland, W.C. (2008) Inherited mitochondrial diseases of DNA replication. Annu. Rev. Med., 59, 131-146.
27. Amati-Bonneau, P., Valentino, M.L., Reynier, P., Gallardo, M.E., Bornstein, B., Boissiere, A., Campos, Y., Rivera, H., de la Aleja, J.G., Carroccia, R. et al. (2008) OPA1 mutations induce mitochondrial DNA instability and optic atrophy 'plus' phenotypes. Brain, 131, 338-351.
28. Hudson, G., Amati-Bonneau, P., Blakely, E.L., Stewart, J.D., He, L., Schaefer, A.M., Griffiths, P.G., Ahlqvist, K., Suomalainen, A., Reynier, P. et al. (2008) Mutation of OPA1 causes dominant optic atrophy with external ophthalmoplegia, ataxia, deafness and multiple mitochondrial DNA deletions: A novel disorder of mtDNA maintenance. Brain, 131, 329-337.
29. Ferraris, S., Clark, S., Garelli, E., Davidzon, G., Moore, S.A., Kardon, R.H., Bienstock, R.J., Longley, M.J., Mancuso, M., Gutierrez Rios, P. et al. (2008) Progressive external ophthalmoplegia and vision and hearing loss in a patient with mutations in POLG2 and OPA1. Arch. Neurol., 65, 125-131.
30. Kihira, Y., Iwahashi, A., Majima, E., Terada, H. and Shinohara, Y. (2004) Twisting of the second transmembrane alpha-helix of the mitochondrial ADP/ATP carrier during the transition between two carrier conformational states. Biochemistry, 43, 15204-15209.
31. Polcic, P., Sabova, L. and Kolarov, J. (1997) Fatty acids induced uncoupling of Saccharomyces cerevisiae mitochondria requires an intact ADP/ATP carrier. FEBS Lett., 412, 207-210.
32. Crompton, M. (2004) Mitochondria and aging: A role for the permeability transition? Aging Cell, 3, 3-6.
33. Talbot, D.A., Duchamp, C., Rey, B., Hanuise, N., Rouanet, J.L., Sibille, B. and Brand, M.D. (2004) Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins. J. Physiol., 558, 123-135.
34. Jacotot, E., Ferri, K.F., El Hamel, C., Brenner, C., Druillennec, S., Hoebeke, J., Rustin, P., Metivier, D., Lenoir, C., Geuskens, M. et al. (2001) Control of mitochondrial membrane permeabilization by adenine nucleotide translocator interacting with HIV-1 viral protein R and Bcl-2. J. Exp. Med., 193, 509-519.
35. Nicholls, D.G. (2004) Mitochondrial membrane potential and aging. Aging Cell, 3, 35-40.