Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2013, Article ID 146860, 10 pages
http://dx.doi.org/10.1155/2013/146860
Review Article

Adenine Nucleotide Translocase, Mitochondrial Stress, and Degenerative Cell Death

Department of Biochemistry and Molecular Biology, State University of New York Upstate Medical University, Syracuse, NY 13210, USA

Received 10 May 2013; Revised 14 June 2013; Accepted 24 June 2013

Academic Editor: Sergio Giannattasio

Copyright © 2013 Yaxin Liu and Xin Jie Chen. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. C. Wallace, “Why do we still have a maternally inherited mitochondrial DNA? insights from evolutionary medicine,” Annual Review of Biochemistry, vol. 76, pp. 781–821, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. T. Eisenberg, S. Büttner, G. Kroemer, and F. Madeo, “The mitochondrial pathway in yeast apoptosis,” Apoptosis, vol. 12, no. 5, pp. 1011–1023, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Guaragnella, L. Antonacci, S. Passarella, E. Marra, and S. Giannattasio, “Hydrogen peroxide and superoxide anion production during acetic acid-induced yeast programmed cell death,” Folia Microbiologica, vol. 52, no. 3, pp. 237–240, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Caballero, A. Ugidos, B. Liu et al., “Absence of mitochondrial translation control proteins extends life span by activating sirtuin-dependent silencing,” Molecular Cell, vol. 42, no. 3, pp. 390–400, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. X. J. Chen, “The search for nonconventional mitochondrial determinants of aging,” Molecular Cell, vol. 42, no. 3, pp. 271–273, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. S. M. Jazwinski, “The retrograde response: when mitochondrial quality control is not enough,” Biochimica et Biophysica Acta, vol. 1833, no. 2, pp. 400–409, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. J. R. Delaney, U. Ahmed, A. Chou et al., “Stress profiling of longevity mutants identifies Afg3 as a mitochondrial determinant of cytoplasmic mRNA translation and aging,” Aging Cell, vol. 12, no. 1, pp. 156–166, 2013. View at Google Scholar
  8. M. D. Brand, J. L. Pakay, A. Ocloo et al., “The basal proton conductance of mitochondria depends on adenine nucleotide translocase content,” Biochemical Journal, vol. 392, no. 2, pp. 353–362, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Endres, W. Neupert, and M. Brunner, “Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex,” EMBO Journal, vol. 18, no. 12, pp. 3214–3221, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Pfanner, P. Hoeben, M. Tropschug, and W. Neupert, “The carboxyl-terminal two-thirds of the ADP/ATP carrier polypeptide contains sufficient information to direct translocation into mitochondria,” Journal of Biological Chemistry, vol. 262, no. 31, pp. 14851–14854, 1987. View at Google Scholar · View at Scopus
  11. M. T. Ryan, H. Müller, and N. Pfanner, “Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane,” Journal of Biological Chemistry, vol. 274, no. 29, pp. 20619–20627, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Palmieri, “The mitochondrial transporter family (SLC25): physiological and pathological implications,” Pflugers Archiv European Journal of Physiology, vol. 447, no. 5, pp. 689–709, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Wohlrab, “The human mitochondrial transport protein family: identification and protein regions significant for transport function and substrate specificity,” Biochimica et Biophysica Acta, vol. 1709, no. 2, pp. 157–168, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Duszyński, K. Bogucka, G. Letko, U. Küster, W. Kunz, and L. Wojtczak, “Relationship between the energy cost of ATP transport and ATP synthesis in mitochondria,” Biochimica et Biophysica Acta, vol. 637, no. 2, pp. 217–223, 1981. View at Google Scholar · View at Scopus
  15. S. E. Levy, Y.-S. Chen, B. H. Graham, and D. C. Wallace, “Expression and sequence analysis of the mouse adenine nucleotide translocase 1 and 2 genes,” Gene, vol. 254, no. 1-2, pp. 57–66, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Stepien, A. Torroni, A. B. Chung, J. A. Hodge, and D. C. Wallace, “Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation,” Journal of Biological Chemistry, vol. 267, no. 21, pp. 14592–14597, 1992. View at Google Scholar · View at Scopus
  17. A. Chevrollier, D. Leiseau, and G. Stepien, “What is the specific role of ANT2 in cancer cells?” Medecine/Sciences, vol. 21, no. 2, pp. 156–161, 2005. View at Google Scholar · View at Scopus
  18. J. V. Brower, N. Rodic, T. Seki et al., “Evolutionarily conserved mammalian adenine nucleotide translocase 4 is essential for spermatogenesis,” Journal of Biological Chemistry, vol. 282, no. 40, pp. 29658–29666, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Klingenberg, “The ADP and ATP transport in mitochondria and its carrier,” Biochimica et Biophysica Acta, vol. 1778, no. 10, pp. 1978–2021, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Saraste and J. E. Walker, “Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase,” FEBS Letters, vol. 144, no. 2, pp. 250–254, 1982. View at Google Scholar · View at Scopus
  21. J. E. Walker and M. J. Runswick, “The mitochondrial transport protein superfamily,” Journal of Bioenergetics and Biomembranes, vol. 25, no. 5, pp. 435–446, 1993. View at Publisher · View at Google Scholar · View at Scopus
  22. G. Brandolin, A. le Saux, V. Trezeguet, G. J. M. Lauquin, and P. V. Vignais, “Chemical, immunological, enzymatic, and genetic approaches to studying the arrangement of the peptide chain of the ADP/ATP carrier in the mitochondrial membrane,” Journal of Bioenergetics and Biomembranes, vol. 25, no. 5, pp. 459–472, 1993. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Riccio, H. Aquila, and M. Klingenberg, “Purification of the carboxy atractylate binding protein from mitochondria,” FEBS Letters, vol. 56, no. 1, pp. 133–138, 1975. View at Publisher · View at Google Scholar · View at Scopus
  24. H. Aquila, W. Eiermann, W. Babel, and M. Klingenberg, “Isolation of the ADP/ATP translocator from beef heart mitochondria as the bongkrekate-protein complex,” The European Journal of Biochemistry, vol. 85, no. 2, pp. 549–560, 1978. View at Google Scholar · View at Scopus
  25. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trézéguet, G. J.-M. Lauquin, and G. Brandolin, “Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside,” Nature, vol. 426, no. 6962, pp. 39–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Rey, P. Man, B. Clémençon et al., “Conformational dynamics of the bovine mitochondrial ADP/ATP carrier isoform 1 revealed by hydrogen/deuterium exchange coupled to mass spectrometry,” Journal of Biological Chemistry, vol. 285, no. 45, pp. 34981–34990, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Clémençon, M. Rey, V. Trézé, E. Forests, and L. Pelosis, “Yeast ADP/ATP carrier isoform 2: conformational dynamics and role of the RRRMMM signature sequence methionines,” Journal of Biological Chemistry, vol. 286, no. 41, pp. 36119–36131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Nury, C. Dahout-Gonzalez, V. Trézéguet, G. J. M. Lauquin, G. Brandolin, and E. Pebay-Peyroula, “Relations between structure and function of the mitochondrial ADP/ATP carrier,” Annual Review of Biochemistry, vol. 75, pp. 713–741, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. D. Heidkämper, V. Müller, D. R. Nelson, and M. Klingenberg, “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, vol. 35, no. 50, pp. 16144–16152, 1996. View at Publisher · View at Google Scholar · View at Scopus
  30. S. D. Dyall, S. C. Agius, C. de Marcos Lousa, V. Trézéguet, and K. Tokatlidis, “The dynamic dimerization of the yeast ADP/ATP carrier in the inner mitochondrial membrane is affected by conserved cysteine residues,” Journal of Biological Chemistry, vol. 278, no. 29, pp. 26757–26764, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. H. Hackenberg and M. Klingenberg, “Molecular weight and hydrodynamic parameters of the adenosine 5′-diphosphate-adenosine 5′-triphosphate carrier in triton X-100,” Biochemistry, vol. 19, no. 3, pp. 548–555, 1980. View at Google Scholar · View at Scopus
  32. M. R. Block, G. Zaccaï, G. J. M. Lauquin, and P. V. Vignais, “Small angle neutron scattering of the mitochondrial ADP ATP carrier protein in detergent,” Biochemical and Biophysical Research Communications, vol. 109, no. 2, pp. 471–477, 1982. View at Google Scholar · View at Scopus
  33. M. Hashimoto, E. Majima, S. Goto, Y. Shinohara, and H. Terada, “Fluctuation of the first loop facing the matrix of the mitochondrial ADP/ATP carrier deduced from intermolecular cross-linking of Cys56 residues by bifunctional dimaleimides,” Biochemistry, vol. 38, no. 3, pp. 1050–1056, 1999. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. Kihira, E. Majima, Y. Shinohara, and H. Terada, “Cysteine labeling studies detect conformational changes in region 106-132 of the mitochondrial ADP/ATP carrier of Saccharomyces cerevisiae,” Biochemistry, vol. 44, no. 1, pp. 184–192, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. E. Majima, K. Ikawa, M. Takeda, M. Hashimoto, Y. Shinohara, and H. Terada, “Translocation of loops regulates transport activity of mitochondrial ADP/ATP carrier deduced from formation of a specific intermolecular disulfide bridge catalyzed by copper-o-phenanthroline,” Journal of Biological Chemistry, vol. 270, no. 49, pp. 29548–29554, 1995. View at Publisher · View at Google Scholar · View at Scopus
  36. V. Trézéguet, A. le Saux, C. David et al., “A covalent tandem dimer of the mitochondrial ADP/ATP carrier is functional in vivo,” Biochimica et Biophysica Acta, vol. 1457, no. 1-2, pp. 81–93, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Hatanaka, M. Hashimoto, E. Majima, Y. Shinohara, and H. Terada, “Functional expression of the tandem-repeated homodimer of the mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae,” Biochemical and Biophysical Research Communications, vol. 262, no. 3, pp. 726–730, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. S.-G. Huang, S. Odoy, and M. Klingenberg, “Chimers of two fused ADP/ATP carrier monomers indicate a single channel for ADP/ATP transport,” Archives of Biochemistry and Biophysics, vol. 394, no. 1, pp. 67–75, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Bamber, D.-J. Slotboom, and E. R. S. Kunji, “Yeast mitochondrial ADP/ATP carriers are monomeric in detergents as demonstrated by differential affinity purification,” Journal of Molecular Biology, vol. 371, no. 2, pp. 388–395, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. E. R. S. Kunji and P. G. Crichton, “Mitochondrial carriers function as monomers,” Biochimica et Biophysica Acta, vol. 1797, no. 6-7, pp. 817–831, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. D. R. Hunter and R. A. Haworth, “The Ca2+-induced membrane transition in mitochondria. The protective mechanisms,” Archives of Biochemistry and Biophysics, vol. 195, no. 2, pp. 453–459, 1979. View at Google Scholar · View at Scopus
  42. R. A. Haworth and D. R. Hunter, “The Ca2+-induced membrane transition in mitochondria. II. Nature of the Ca2+ trigger site,” Archives of Biochemistry and Biophysics, vol. 195, no. 2, pp. 460–467, 1979. View at Google Scholar · View at Scopus
  43. P. Bernardi, K. M. Broekemeier, and D. R. Pfeiffer, “Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane,” Journal of Bioenergetics and Biomembranes, vol. 26, no. 5, pp. 509–517, 1994. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Zoratti and I. Szabo, “The mitochondrial permeability transition,” Biochimica et Biophysica Acta, vol. 1241, no. 2, pp. 139–176, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. D. Brust, B. Daum, C. Breunig, A. Hamann, W. Kühlbrandt, and H. D. Osiewacz, “Cyclophilin D links programmed cell death and organismal aging in Podospora anserina,” Aging Cell, vol. 9, no. 5, pp. 761–775, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. K. Woodfield, A. Rück, D. Brdiczka, and A. P. Halestrap, “Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition,” Biochemical Journal, vol. 336, no. 2, pp. 287–290, 1998. View at Google Scholar · View at Scopus
  47. M. Crompton, S. Virji, and J. M. Ward, “Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore,” The European Journal of Biochemistry, vol. 258, no. 2, pp. 729–735, 1998. View at Google Scholar · View at Scopus
  48. J. E. Kokoszka, K. G. Waymire, S. E. Levy et al., “The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore,” Nature, vol. 427, no. 6973, pp. 461–465, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. V. Giorgio, S. von Stockum, M. Antoniel et al., “Dimers of mitochondrial ATP synthase form the permeability transition pore,” Proceedings of the National Academy of Sciences, vol. 110, no. 15, pp. 5887–5892, 2013. View at Google Scholar
  50. M. Bonora, A. Bononi, E. de Marchi et al., “Role of the c subunit of the FO ATP synthase in mitochondrial permeability transition,” Cell Cycle, vol. 12, no. 4, pp. 674–683, 2013. View at Google Scholar
  51. C. Pereira, N. Camougrand, S. Manon, M. J. Sousa, and M. Côrte-Real, “ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis,” Molecular Microbiology, vol. 66, no. 3, pp. 571–582, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Pereira, S. Chaves, S. Alves et al., “Mitochondrial degradation in acetic acid-induced yeast apoptosis: the role of Pep4 and the ADP/ATP carrier,” Molecular Microbiology, vol. 76, no. 6, pp. 1398–1410, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Pereira, F. Azevedo, A. Rego, M. J. Sousa, S. R. Chaves, and M. Corte-Real, “The protective role of yeast Cathepsin D in acetic acid-induced apoptosis depends on ANT, (Aac2p) but not on the voltage-dependent channel (Por1p),” FEBS Letters, vol. 587, no. 2, pp. 200–205, 2013. View at Google Scholar
  54. B. H. Graham, K. G. Waymire, B. Cottrell, I. A. Trounce, G. R. MacGregor, and D. C. Wallace, “A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator,” Nature Genetics, vol. 16, no. 3, pp. 226–234, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. E. Z. Jordens, L. Palmieri, M. Huizing et al., “Adenine nucleotide translocator 1 deficiency associated with Sengers syndrome,” Annals of Neurology, vol. 52, no. 1, pp. 95–99, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. J. D. Sharer, “The adenine nucleotide translocase type 1 (ANT1): a new factor in mitochondrial disease,” IUBMB Life, vol. 57, no. 9, pp. 607–614, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. J. A. Mayr, T. B. Haack, E. Graf et al., “Lack of the mitochondrial protein acylglycerol kinase causes sengers syndrome,” The American Journal of Human Genetics, vol. 90, no. 2, pp. 314–320, 2012. View at Publisher · View at Google Scholar · View at Scopus
  58. K. A. Strauss, L. Dubiner, M. Simon et al., “Severity of cardiomyopathy associated with adenine nucleotide translocator-1 deficiency correlates with mtDNA haplogroup,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 9, pp. 3453–3458, 2013. View at Google Scholar
  59. G. W. Padberg, P. W. Lunt, M. Koch, and M. Fardeau, “Diagnostic criteria for facioscapulohumeral muscular dystrophy,” Neuromuscular Disorders, vol. 1, no. 4, pp. 231–234, 1991. View at Publisher · View at Google Scholar · View at Scopus
  60. C. Wijmenga, J. E. Hewitt, L. A. Sandkuijl et al., “Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy,” Nature Genetics, vol. 2, no. 1, pp. 26–30, 1992. View at Google Scholar · View at Scopus
  61. D. Gabellini, M. R. Green, and R. Tupler, “Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle,” Cell, vol. 110, no. 3, pp. 339–348, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. S. M. van der Maarel and R. R. Frants, “The D4Z4 repeat-mediated pathogenesis of facioscapulohumeral muscular dystrophy,” The American Journal of Human Genetics, vol. 76, no. 3, pp. 375–386, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. R. J. L. F. Lemmers, P. J. van der Vliet, R. Klooster et al., “A unifying genetic model for facioscapulohumeral muscular dystrophy,” Science, vol. 329, no. 5999, pp. 1650–1653, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. D. Gabellini, G. D'Antona, M. Moggio et al., “Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1,” Nature, vol. 439, no. 7079, pp. 973–977, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. D. Laoudj-Chenivesse, G. Carnac, C. Bisbal et al., “Increased levels of adenine nucleotide translocator 1 protein and response to oxidative stress are early events in facioscapulohumeral muscular dystrophy muscle,” Journal of Molecular Medicine, vol. 83, no. 3, pp. 216–224, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. B. Clemencon, M. Babot, and V. Trezeguet, “The mitochondrial ADP/ATP carrier (SLC25 family): pathological implications of its dysfunction,” Molecular Aspects of Medicine, vol. 34, no. 2-3, pp. 485–493, 2013. View at Google Scholar
  67. M. le Bras, A. Borgne-Sanchez, Z. Touat et al., “Chemosensitization by knockdown of adenine nucleotide translocase-2,” Cancer Research, vol. 66, no. 18, pp. 9143–9152, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. R. Moreno-Sanchez, S. Rodriguez-Enriquez, A. Marin-Hernandez, and E. Saavedra, “Energy metabolism in tumor cells,” FEBS Journal, vol. 274, no. 6, pp. 1393–1418, 2007. View at Google Scholar
  69. M.-F. Giraud and J. Velours, “The absence of the mitochondrial ATP synthase δ subunit promotes a slow growth phenotype of rho- yeast cells by a lack of assembly of the catalytic sector F1,” The European Journal of Biochemistry, vol. 245, no. 3, pp. 813–818, 1997. View at Google Scholar · View at Scopus
  70. X. J. Chen and G. D. Clark-Walker, “Specific mutations in α and γ-subunits of F1-ATPase affect mitochondrial genome integrity in the petite-negative yeast Kluyveromyces lactis,” EMBO Journal, vol. 14, no. 13, pp. 3277–3286, 1995. View at Google Scholar · View at Scopus
  71. X. J. Chen and G. D. Clark-Walker, “The mitochondrial genome integrity gene, MGI1, of Kluyveromyces lactis encodes the β-subunit of F1-ATPase,” Genetics, vol. 144, no. 4, pp. 1445–1454, 1996. View at Google Scholar · View at Scopus
  72. X. J. Chen and G. D. Clark-Walker, “The petite mutation in yeasts: 50 years on,” International Review of Cytology, vol. 194, pp. 197–238, 2000. View at Google Scholar · View at Scopus
  73. A. Chevrollier, D. Loiseau, P. Reynier, and G. Stepien, “Adenine nucleotide translocase 2 is a key mitochondrial protein in cancer metabolism,” Biochimica et Biophysica Acta, vol. 1807, no. 6, pp. 562–567, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Buchet and C. Godinot, “Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted ρ°cells,” Journal of Biological Chemistry, vol. 273, no. 36, pp. 22983–22989, 1998. View at Publisher · View at Google Scholar · View at Scopus
  75. J. Kaukonen, J. K. Juselius, V. Tiranti et al., “Role of adenine nucleotide translocator 1 in mtDNA maintenance,” Science, vol. 289, no. 5480, pp. 782–785, 2000. View at Publisher · View at Google Scholar · View at Scopus
  76. L. Napoli, A. Bordoni, M. Zeviani et al., “A novel missense adenine nucleotide translocator-1 gene mutation in a greek adPEO family,” Neurology, vol. 57, no. 12, pp. 2295–2298, 2001. View at Google Scholar · View at Scopus
  77. H. Komaki, T. Fukazawa, H. Houzen, K. Yoshida, I. Nonaka, and Y. Goto -I, “A novel D104G mutation in the adenine nucleotide translocator 1 gene in autosomal dominant progressive external ophthalmoplegia patients with mitochondrial DNA with multiple deletions.,” Annals of Neurology, vol. 51, no. 5, pp. 645–648, 2002. View at Publisher · View at Google Scholar
  78. G. van Goethem, B. Dermaut, A. Löfgren, J.-J. Martin, and C. van Broeckhoven, “Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions,” Nature Genetics, vol. 28, no. 3, pp. 211–212, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. J. N. Spelbrink, F. Y. Li, V. Tiranti et al., “Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria,” Nature Genetics, vol. 28, no. 3, pp. 223–231, 2001. View at Google Scholar
  80. M. Deschauer, G. Hudson, T. Müller, R. W. Taylor, P. F. Chinnery, and S. Zierz, “A novel ANT1 gene mutation with probable germline mosaicism in autosomal dominant progressive external ophthalmoplegia,” Neuromuscular Disorders, vol. 15, no. 4, pp. 311–315, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. L. Palmieri, S. Alberio, I. Pisano et al., “Complete loss-of-function of the heart/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy,” Human Molecular Genetics, vol. 14, no. 20, pp. 3079–3088, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Kihira, A. Iwahashi, E. Majima, H. Terada, and Y. Shinohara, “Twisting of the second transmembrane α-helix of the mitochondrial ADP/ATP carrier during the transition between two carrier conformational states,” Biochemistry, vol. 43, no. 48, pp. 15204–15209, 2004. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Galassi, E. Lamantea, F. Invernizzi et al., “Additive effects of POLG1 and ANT1 mutations in a complex encephalomyopathy,” Neuromuscular Disorders, vol. 18, no. 6, pp. 465–470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  84. C. de Marcos Lousa, V. Trézéguet, A.-C. Dianoux, G. Brandolin, and G. J.-M. Lauquin, “The human mitochondrial ADP/ATP carriers: kinetic properties and biogenesis of wild-type and mutant proteins in the yeast S. cerevisiae,” Biochemistry, vol. 41, no. 48, pp. 14412–14420, 2002. View at Publisher · View at Google Scholar · View at Scopus
  85. F. Fontanesi, L. Palmieri, P. Scarcia et al., “Mutation in AAC2, equivalent to human adPEO-associated ANT1 mutations, lead to defective oxidative phosphorylation in Saccharomyces cerevisiae and affect mitochondrial DNA stability,” Human Molecular Genetics, vol. 13, no. 9, pp. 923–934, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. H. Kawamata, V. Tiranti, J. Magrané, C. Chinopoulos, and G. Manfredi, “adPEO mutations in ANT1 impair ADP-ATP translocation in muscle mitochondria,” Human Molecular Genetics, vol. 20, no. 15, Article ID ddr200, pp. 2964–2974, 2011. View at Publisher · View at Google Scholar · View at Scopus
  87. X. J. Chen, “Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia,” Human Molecular Genetics, vol. 11, no. 16, pp. 1835–1843, 2002. View at Google Scholar · View at Scopus
  88. X. Wang, K. Salinas, X. Zuo, B. Kucejova, and X. J. Chen, “Dominant membrane uncoupling by mutant adenine nucleotide translocase in mitochondrial diseases,” Human Molecular Genetics, vol. 17, no. 24, pp. 4036–4044, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. X. Wang, X. Zuo, B. Kucejova, and X. J. Chen, “Reduced cytosolic protein synthesis suppresses mitochondrial degeneration,” Nature Cell Biology, vol. 10, no. 9, pp. 1090–1097, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. R. El-Khoury and A. Sainsard-Chanet, “Suppression of mitochondrial DNA instability of autosomal dominant forms of progressive external ophthalmoplegia-associated ANT1 mutations in Podospora anserina,” Genetics, vol. 183, no. 3, pp. 861–871, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Bratic and N.-G. Larsson, “The role of mitochondria in aging,” Journal of Clinical Investigation, vol. 123, no. 3, pp. 951–957, 2013. View at Google Scholar
  92. H. D. Osiewacz and D. Bernhardt, “Mitochondrial quality control: impact on aging and life span—a mini review,” Gerontology. In press.
  93. M. Breitenbach, S. M. Jazwinski, and P. Laun, “The retrograde response and other pathways of interorganelle communication in yeast replicative aging,” in Aging Research in Yeast, vol. 57, pp. 79–100, Springer, Amsterdam, The Netherlands, 2012. View at Google Scholar