Adenine nucleotide translocase, mitochondrial stress, and degenerative cell death

Oxidative Medicine and Cellular Longevity

Volumn , Issue , 2013, Pages

  Liu, Yaxin ^a   Chen, Xin Jie ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; DEGENERATIVE DISEASE; INTRACELLULAR ORGANELLE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DNA (MTDNA); MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL STRESS;

CELL DEATH; METABOLISM; NUCLEIC ACIDS; NUCLEOTIDES; PROTEINS; TRANSPORT PROPERTIES; YEAST;

MITOCHONDRIA;

ADENINE NUCLEOTIDE TRANSLOCASE; MITOCHONDRIAL DNA; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MUTANT PROTEIN;

AGING; AMINO ACID SEQUENCE; BIOGENESIS; CARDIOMYOPATHY; CELL DEATH; CELL DEGENERATION; CELL STRESS; CELL VIABILITY; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; DEUTERIUM HYDROGEN EXCHANGE; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; GAIN OF FUNCTION MUTATION; GEL ELECTROPHORESIS; HEART VENTRICLE HYPERTROPHY; HUMAN; LACTIC ACIDOSIS; MASS SPECTROMETRY; MISSENSE MUTATION; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL MYOPATHY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NEUTRON SCATTERING; NONHUMAN; NUCLEOTIDE TRANSPORT; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RESPIRATORY CHAIN; REVIEW; ULTRACENTRIFUGATION; ANIMAL; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE;

ANIMALS; CELL DEATH; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL ADP, ATP TRANSLOCASES; PROTEIN STRUCTURE, SECONDARY;

EID: 84881494762     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2013/146860     Document Type: Review

References (93)

1. Wallace D. C., Why do we still have a maternally inherited mitochondrial DNA? insights from evolutionary medicine. Annual Review of Biochemistry 2007 76 781 821 2-s2.0-34548614520 10.1146/annurev.biochem.76.081205.150955
2. Eisenberg T., Büttner S., Kroemer G., Madeo F., The mitochondrial pathway in yeast apoptosis. Apoptosis 2007 12 5 1011 1023 2-s2.0-34247469791 10.1007/s10495-007-0758-0 (Pubitemid 46653302)
3. Guaragnella N., Antonacci L., Passarella S., Marra E., Giannattasio S., Hydrogen peroxide and superoxide anion production during acetic acid-induced yeast programmed cell death. Folia Microbiologica 2007 52 3 237 240 2-s2.0-34547327874 10.1007/BF02931304 (Pubitemid 47148560)
4. Caballero A., Ugidos A., Liu B., Öling D., Kvint K., Hao X., Mignat C., Nachin L., Molin M., Nyström T., Absence of mitochondrial translation control proteins extends life span by activating sirtuin-dependent silencing. Molecular Cell 2011 42 3 390 400 2-s2.0-79955501271 10.1016/j.molcel.2011.03.021
5. Chen X. J., The search for nonconventional mitochondrial determinants of aging. Molecular Cell 2011 42 3 271 273 2-s2.0-79955512116 10.1016/j.molcel. 2011.04.013
6. Jazwinski S. M., The retrograde response: when mitochondrial quality control is not enough. Biochimica et Biophysica Acta 2013 1833 2 400 409 2-s2.0-84857760213 10.1016/j.bbamcr.2012.02.010
7. Delaney J. R., Ahmed U., Chou A., Sim S., Carr D., Murakami C. J., Schleit J., Sutphin G. L., An E. H., Castanza A., Fletcher M., Higgins S., Jelic M., Klum S., Muller B., Peng Z. J., Rai D., Ros V., Singh M., Wende H. V., Kennedy B. K., Kaeberlein M., Stress profiling of longevity mutants identifies Afg3 as a mitochondrial determinant of cytoplasmic mRNA translation and aging. Aging Cell 2013 12 1 156 166
8. Brand M. D., Pakay J. L., Ocloo A., Kokoszka J., Wallace D. C., Brookes P. S., Cornwall E. J., The basal proton conductance of mitochondria depends on adenine nucleotide translocase content. Biochemical Journal 2005 392 2 353 362 2-s2.0-29144515671 10.1042/BJ20050890 (Pubitemid 41796524)
9. Endres M., Neupert W., Brunner M., Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO Journal 1999 18 12 3214 3221 2-s2.0-0033564856 10.1093/emboj/18.12.3214 (Pubitemid 29276568)
10. Pfanner N., Hoeben P., Tropschug M., Neupert W., The carboxyl-terminal two-thirds of the ADP/ATP carrier polypeptide contains sufficient information to direct translocation into mitochondria. Journal of Biological Chemistry 1987 262 31 14851 14854 2-s2.0-0023645869
11. Ryan M. T., Müller H., Pfanner N., Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane. Journal of Biological Chemistry 1999 274 29 20619 20627 2-s2.0-0040610684 10.1074/jbc.274.29.20619 (Pubitemid 29340425)
12. Palmieri F., The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Archiv European Journal of Physiology 2004 447 5 689 709 2-s2.0-1242317666 10.1007/s00424-003-1099-7 (Pubitemid 38241455)
13. Wohlrab H., The human mitochondrial transport protein family: identification and protein regions significant for transport function and substrate specificity. Biochimica et Biophysica Acta 2005 1709 2 157 168 2-s2.0-23944435962 10.1016/j.bbabio.2005.07.003 (Pubitemid 41207743)
14. Duszyński J., Bogucka K., Letko G., Küster U., Kunz W., Wojtczak L., Relationship between the energy cost of ATP transport and ATP synthesis in mitochondria. Biochimica et Biophysica Acta 1981 637 2 217 223 2-s2.0-0019879891
15. Levy S. E., Chen Y.-S., Graham B. H., Wallace D. C., Expression and sequence analysis of the mouse adenine nucleotide translocase 1 and 2 genes. Gene 2000 254 1-2 57 66 2-s2.0-0034702878 10.1016/S0378-1119(00)00252-3
16. Stepien G., Torroni A., Chung A. B., Hodge J. A., Wallace D. C., Differential expression of adenine nucleotide translocator isoforms in mammalian tissues and during muscle cell differentiation. Journal of Biological Chemistry 1992 267 21 14592 14597 2-s2.0-0026718789
17. Chevrollier A., Leiseau D., Stepien G., What is the specific role of ANT2 in cancer cells? Medecine/Sciences 2005 21 2 156 161 2-s2.0-13944278753 (Pubitemid 40269055)
18. Brower J. V., Rodic N., Seki T., Jorgensen M., Fliess N., Yachnis A. T., McCarrey J. R., Oh S. P., Terada N., Evolutionarily conserved mammalian adenine nucleotide translocase 4 is essential for spermatogenesis. Journal of Biological Chemistry 2007 282 40 29658 29666 2-s2.0-35748978524 10.1074/jbc.M704386200 (Pubitemid 350043375)
19. Klingenberg M., The ADP and ATP transport in mitochondria and its carrier. Biochimica et Biophysica Acta 2008 1778 10 1978 2021 2-s2.0-52049113898 10.1016/j.bbamem.2008.04.011
20. Saraste M., Walker J. E., Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Letters 1982 144 2 250 254 2-s2.0-0020473533
21. Walker J. E., Runswick M. J., The mitochondrial transport protein superfamily. Journal of Bioenergetics and Biomembranes 1993 25 5 435 446 2-s2.0-0027136160 10.1007/BF01108401 (Pubitemid 24006371)
22. Brandolin G., le Saux A., Trezeguet V., Lauquin G. J. M., Vignais P. V., 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 1993 25 5 459 472 2-s2.0-0027133425 10.1007/BF01108403 (Pubitemid 24006373)
23. Riccio P., Aquila H., Klingenberg M., Purification of the carboxy atractylate binding protein from mitochondria. FEBS Letters 1975 56 1 133 138 2-s2.0-0016734199 10.1016/0014-5793(75)80127-X
24. Aquila H., Eiermann W., Babel W., Klingenberg M., Isolation of the ADP/ATP translocator from beef heart mitochondria as the bongkrekate-protein complex. The European Journal of Biochemistry 1978 85 2 549 560 2-s2.0-0017857902 (Pubitemid 8335278)
25. Pebay-Peyroula E., Dahout-Gonzalez C., Kahn R., Trézéguet V., Lauquin G. J.-M., Brandolin G., Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 2003 426 6962 39 44 2-s2.0-0242497235 10.1038/nature02056 (Pubitemid 37432535)
26. Rey M., Man P., Clémençon B., Trézéguet V., Brandolin G., Forest E., Pelosi L., Conformational dynamics of the bovine mitochondrial ADP/ATP carrier isoform 1 revealed by hydrogen/deuterium exchange coupled to mass spectrometry. Journal of Biological Chemistry 2010 285 45 34981 34990 2-s2.0-78049365353 10.1074/jbc.M110.146209
27. Clémençon B., Rey M., Trézé V., Forests E., Pelosis L., Yeast ADP/ATP carrier isoform 2: conformational dynamics and role of the RRRMMM signature sequence methionines. Journal of Biological Chemistry 2011 286 41 36119 36131 2-s2.0-80053907976 10.1074/jbc.M111.277376
28. Nury H., Dahout-Gonzalez C., Trézéguet V., Lauquin G. J. M., Brandolin G., Pebay-Peyroula E., Relations between structure and function of the mitochondrial ADP/ATP carrier. Annual Review of Biochemistry 2006 75 713 741 2-s2.0-33746337576 10.1146/annurev.biochem.75.103004.142747 (Pubitemid 44118050)
29. Heidkämper D., Müller V., Nelson D. R., Klingenberg M., 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 1996 35 50 16144 16152 2-s2.0-0030480093 10.1021/bi960668j (Pubitemid 27044076)
30. Dyall S. D., Agius S. C., de Marcos Lousa C., Trézéguet V., Tokatlidis K., The dynamic dimerization of the yeast ADP/ATP carrier in the inner mitochondrial membrane is affected by conserved cysteine residues. Journal of Biological Chemistry 2003 278 29 26757 26764 2-s2.0-0038035871 10.1074/jbc.M302700200 (Pubitemid 36876823)
31. Hackenberg H., Klingenberg M., Molecular weight and hydrodynamic parameters of the adenosine 5′-diphosphate-adenosine 5′-triphosphate carrier in triton X-100. Biochemistry 1980 19 3 548 555 2-s2.0-0019316912
32. Block M. R., Zaccaï G., Lauquin G. J. M., Vignais P. V., Small angle neutron scattering of the mitochondrial ADP ATP carrier protein in detergent. Biochemical and Biophysical Research Communications 1982 109 2 471 477 2-s2.0-0020494167
33. Hashimoto M., Majima E., Goto S., Shinohara Y., Terada H., 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 1999 38 3 1050 1056 2-s2.0-0033579942 10.1021/bi9822978 (Pubitemid 29052720)
34. Kihira Y., Majima E., Shinohara Y., Terada H., Cysteine labeling studies detect conformational changes in region 106-132 of the mitochondrial ADP/ATP carrier of Saccharomyces cerevisiae. Biochemistry 2005 44 1 184 192 2-s2.0-11844249290 10.1021/bi0488653 (Pubitemid 40095720)
35. Majima E., Ikawa K., Takeda M., Hashimoto M., Shinohara Y., Terada H., 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 1995 270 49 29548 29554 2-s2.0-0028840853 10.1074/jbc.270.49.29548
36. Trézéguet V., le Saux A., David C., Gourdet C., Fiore C., Dianoux A.-C., Brandolin G., Lauquin G. J.-M., A covalent tandem dimer of the mitochondrial ADP/ATP carrier is functional in vivo. Biochimica et Biophysica Acta 2000 1457 1-2 81 93 2-s2.0-0039742269 10.1016/S0005-2728(99)00115-2 (Pubitemid 30110732)
37. Hatanaka T., Hashimoto M., Majima E., Shinohara Y., Terada H., Functional expression of the tandem-repeated homodimer of the mitochondrial ADP/ATP carrier in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications 1999 262 3 726 730 2-s2.0-0033533487 10.1006/bbrc.1999.1283 (Pubitemid 29443726)
38. Huang S.-G., Odoy S., Klingenberg M., Chimers of two fused ADP/ATP carrier monomers indicate a single channel for ADP/ATP transport. Archives of Biochemistry and Biophysics 2001 394 1 67 75 2-s2.0-0035477049 10.1006/abbi.2001.2520 (Pubitemid 32948286)
39. Bamber L., Slotboom D.-J., Kunji E. R. S., Yeast mitochondrial ADP/ATP carriers are monomeric in detergents as demonstrated by differential affinity purification. Journal of Molecular Biology 2007 371 2 388 395 2-s2.0-34447277172 10.1016/j.jmb.2007.05.072 (Pubitemid 47048283)
40. Kunji E. R. S., Crichton P. G., Mitochondrial carriers function as monomers. Biochimica et Biophysica Acta 2010 1797 6-7 817 831 2-s2.0-77953807486 10.1016/j.bbabio.2010.03.023
41. 2+-induced membrane transition in mitochondria. The protective mechanisms. Archives of Biochemistry and Biophysics 1979 195 2 453 459 2-s2.0-0018332596 (Pubitemid 9235077)
42. 2+ trigger site. Archives of Biochemistry and Biophysics 1979 195 2 460 467 2-s2.0-0018332597 (Pubitemid 9235078)
43. Bernardi P., Broekemeier K. M., Pfeiffer D. R., Recent progress on regulation of the mitochondrial permeability transition pore; a cyclosporin-sensitive pore in the inner mitochondrial membrane. Journal of Bioenergetics and Biomembranes 1994 26 5 509 517 2-s2.0-0028053663 10.1007/BF00762735 (Pubitemid 24378753)
44. Zoratti M., Szabo I., The mitochondrial permeability transition. Biochimica et Biophysica Acta 1995 1241 2 139 176 2-s2.0-0029116916 10.1016/0304-4157(95)00003-A
45. Brust D., Daum B., Breunig C., Hamann A., Kühlbrandt W., Osiewacz H. D., Cyclophilin D links programmed cell death and organismal aging in Podospora anserina. Aging Cell 2010 9 5 761 775 2-s2.0-78349264668 10.1111/j.1474-9726. 2010.00609.x
46. Woodfield K., Rück A., Brdiczka D., Halestrap A. P., Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochemical Journal 1998 336 2 287 290 2-s2.0-0032387842 (Pubitemid 28564382)
47. Crompton M., Virji S., Ward J. M., 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 1998 258 2 729 735 2-s2.0-0032401567 (Pubitemid 28557940)
48. Kokoszka J. E., Waymire K. G., Levy S. E., Sligh J. E., Cai J., Jones D. P., MacGregor G. R., Wallace D. C., The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature 2004 427 6973 461 465 2-s2.0-0842307483 10.1038/nature02229 (Pubitemid 38168501)
49. Giorgio V., von Stockum S., Antoniel M., Fabbro A., Fogolari F., Forte M., Glick G. D., Petronilli V., Zoratti M., Szabo I., Lippe G., Bernardi P., Dimers of mitochondrial ATP synthase form the permeability transition pore. Proceedings of the National Academy of Sciences 2013 110 15 5887 5892
50. O ATP synthase in mitochondrial permeability transition. Cell Cycle 2013 12 4 674 683
51. Pereira C., Camougrand N., Manon S., Sousa M. J., Côrte-Real M., ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis. Molecular Microbiology 2007 66 3 571 582 2-s2.0-35448982828 10.1111/j.1365-2958.2007.05926.x (Pubitemid 47621847)
52. Pereira C., Chaves S., Alves S., Salin B., Camougrand N., Manon S., Sousa M. J., Côrte-Real M., Mitochondrial degradation in acetic acid-induced yeast apoptosis: the role of Pep4 and the ADP/ATP carrier. Molecular Microbiology 2010 76 6 1398 1410 2-s2.0-77953492945 10.1111/j.1365-2958.2010. 07122.x
53. Pereira H., Azevedo F., Rego A., Sousa M. J., Chaves S. R., Corte-Real M., 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 2013 587 2 200 205
54. Graham B. H., Waymire K. G., Cottrell B., Trounce I. A., MacGregor G. R., Wallace D. C., A mouse model for mitochondrial myopathy and cardiomyopathy resulting from a deficiency in the heart/muscle isoform of the adenine nucleotide translocator. Nature Genetics 1997 16 3 226 234 2-s2.0-0031011211 10.1038/ng0797-226 (Pubitemid 27280204)
55. Jordens E. Z., Palmieri L., Huizing M., Van Den Heuvel L. P., Sengers R. C. A., Dörner A., Ruitenbeek W., Trijbels F. J., Valsson J., Sigfusson G., Palmieri F., Smeitink J. A. M., Adenine nucleotide translocator 1 deficiency associated with Sengers syndrome. Annals of Neurology 2002 52 1 95 99 2-s2.0-0036288502 10.1002/ana.10214 (Pubitemid 34693749)
56. Sharer J. D., The adenine nucleotide translocase type 1 (ANT1): a new factor in mitochondrial disease. IUBMB Life 2005 57 9 607 614 2-s2.0-27444433840 10.1080/15216540500217735 (Pubitemid 41530548)
57. Mayr J. A., Haack T. B., Graf E., Zimmermann F. A., Wieland T., Haberberger B., Superti-Furga A., Kirschner J., Steinmann B., Baumgartner M. R., Moroni I., Lamantea E., Zeviani M., Rodenburg R. J., Smeitink J., Strom T. M., Meitinger T., Sperl W., Prokisch H., Lack of the mitochondrial protein acylglycerol kinase causes sengers syndrome. The American Journal of Human Genetics 2012 90 2 314 320 2-s2.0-84857043743 10.1016/j.ajhg.2011.12.005
58. Strauss K. A., Dubiner L., Simon M., Zaragoza M., Sengupta P. P., Li P., Narula N., Dreike S., Platt J., Procaccio V., Ortiz-Gonzalez X. R., Puffenberger E. G., Kelley R. I., Morton D. H., Narula J., Wallace D. C., 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 2013 110 9 3453 3458
59. Padberg G. W., Lunt P. W., Koch M., Fardeau M., Diagnostic criteria for facioscapulohumeral muscular dystrophy. Neuromuscular Disorders 1991 1 4 231 234 2-s2.0-0026335673 10.1016/0960-8966(91)90094-9
60. Wijmenga C., Hewitt J. E., Sandkuijl L. A., Clark L. N., Wright T. J., Dauwerse H. G., Gruter A.-M., Hofker M. H., Moerer P., Williamson R., Van Ommen G.-J. B., Padberg G. W., Frants R. R., Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nature Genetics 1992 2 1 26 30 2-s2.0-0026922062
61. Gabellini D., Green M. R., Tupler R., Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 2002 110 3 339 348 2-s2.0-0037047439 10.1016/S0092-8674(02)00826-7
62. van der Maarel S. M., Frants R. R., The D4Z4 repeat-mediated pathogenesis of facioscapulohumeral muscular dystrophy. The American Journal of Human Genetics 2005 76 3 375 386 2-s2.0-13844251804 10.1086/428361 (Pubitemid 40250518)
63. Lemmers R. J. L. F., van der Vliet P. J., Klooster R., Sacconi S., Camaño P., Dauwerse J. G., Snider L., Straasheijm K. R., Van Ommen G. J., Padberg G. W., Miller D. G., Tapscott S. J., Tawil R., Frants R. R., Van Der Maarel S. M., A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 2010 329 5999 1650 1653 2-s2.0-77957327192 10.1126/science.1189044
64. Gabellini D., D'Antona G., Moggio M., Prelle A., Zecca C., Adami R., Angeletti B., Ciscato P., Pellegrino M. A., Bottinelli R., Green M. R., Tupler R., Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 2006 439 7079 973 977 2-s2.0-33644522383 10.1038/nature04422 (Pubitemid 43292415)
65. Laoudj-Chenivesse D., Carnac G., Bisbal C., Hugon G., Bouillot S., Desnuelle C., Vassetzky Y., Fernandez A., 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 2005 83 3 216 224 2-s2.0-16844364725 10.1007/s00109-004-0583-7 (Pubitemid 40487410)
66. Clemencon B., Babot M., Trezeguet V., The mitochondrial ADP/ATP carrier (SLC25 family): pathological implications of its dysfunction. Molecular Aspects of Medicine 2013 34 2-3 485 493
67. le Bras M., Borgne-Sanchez A., Touat Z., El Dein O. S., Deniaud A., Maillier E., Lecellier G., Rebouillat D., Lemaire C., Kroemer G., Jacotot E., Brenner C., Chemosensitization by knockdown of adenine nucleotide translocase-2. Cancer Research 2006 66 18 9143 9152 2-s2.0-33749489663 10.1158/0008-5472.CAN- 05-4407 (Pubitemid 44521134)
68. Moreno-Sanchez R., Rodriguez-Enriquez S., Marin-Hernandez A., Saavedra E., Energy metabolism in tumor cells. FEBS Journal 2007 274 6 1393 1418 (Pubitemid 46333738)
69. 1 The European Journal of Biochemistry 1997 245 3 813 818 2-s2.0-0030990662 (Pubitemid 27223918)
70. Chen X. J., Clark-Walker G. D., Specific mutations in α and γ -subunits of F1-ATPase affect mitochondrial genome integrity in the petite-negative yeast Kluyveromyces lactis. EMBO Journal 1995 14 13 3277 3286 2-s2.0-0028979314
71. 1-ATPase. Genetics 1996 144 4 1445 1454 2-s2.0-0040386551 (Pubitemid 26427894)
72. Chen X. J., Clark-Walker G. D., The petite mutation in yeasts: 50 years on. International Review of Cytology 2000 194 197 238 2-s2.0-0032849910 (Pubitemid 29423649)
73. Chevrollier A., Loiseau D., Reynier P., Stepien G., Adenine nucleotide translocase 2 is a key mitochondrial protein in cancer metabolism. Biochimica et Biophysica Acta 2011 1807 6 562 567 2-s2.0-79955581213 10.1016/j.bbabio.2010. 10.008
74. 1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted ρ °cells. Journal of Biological Chemistry 1998 273 36 22983 22989 2-s2.0-0032483497 10.1074/jbc.273.36.22983 (Pubitemid 28417475)
75. Kaukonen J., Juselius J. K., Tiranti V., Kyttala A., Zeviani M., Comi G. P., Keranen S., Peltonen L., Suomalainen A., Role of adenine nucleotide translocator 1 in mtDNA maintenance. Science 2000 289 5480 782 785 2-s2.0-0034604506 10.1126/science.289.5480.782 (Pubitemid 30650199)
76. Napoli L., Bordoni A., Zeviani M., Hadjigeorgiou G. M., Sciacco M., Tiranti V., Terentiou A., Moggio M., Papadimitriou A., Scarlato G., Comi G. P., A novel missense adenine nucleotide translocator-1 gene mutation in a greek adPEO family. Neurology 2001 57 12 2295 2298 2-s2.0-0035956491 (Pubitemid 34016466)
77. Komaki H., Fukazawa T., Houzen H., Yoshida K., Nonaka I., Goto -I Y., 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 2002 51 5 645 648 10.1002/ana.10172 (Pubitemid 34438708)
78. van Goethem G., Dermaut B., Löfgren A., Martin J.-J., van Broeckhoven C., Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions. Nature Genetics 2001 28 3 211 212 2-s2.0-0034943967 10.1038/90034 (Pubitemid 32626018)
79. Spelbrink J. N., Li F. Y., Tiranti V., Nikali K., Yuan Q. P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G. M., Somer H., Croxen R., Beeson D., Poulton L., Suomalainen A., Jacobs H. T., Zeviani M., Larsson C., Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nature Genetics 2001 28 3 223 231 (Pubitemid 32626024)
80. Deschauer M., Hudson G., Müller T., Taylor R. W., Chinnery P. F., Zierz S., A novel ANT 1 gene mutation with probable germline mosaicism in autosomal dominant progressive external ophthalmoplegia. Neuromuscular Disorders 2005 15 4 311 315 2-s2.0-15944414797 10.1016/j.nmd.2004.12.004 (Pubitemid 40431937)
81. Palmieri L., Alberio S., Pisano I., Lodi T., Meznaric-Petrusa M., Zidar J., Santoro A., Scarcia P., Fontanesi F., Lamantea E., Ferrero I., Zeviani M., Complete loss-of-function of the heart/muscle-specific adenine nucleotide translocator is associated with mitochondrial myopathy and cardiomyopathy. Human Molecular Genetics 2005 14 20 3079 3088 2-s2.0-27544494568 10.1093/hmg/ddi341 (Pubitemid 41535472)
82. Kihira Y., Iwahashi A., Majima E., Terada H., Shinohara Y., Twisting of the second transmembrane α -helix of the mitochondrial ADP/ATP carrier during the transition between two carrier conformational states. Biochemistry 2004 43 48 15204 15209 2-s2.0-10044249898 10.1021/bi0494222 (Pubitemid 39602181)
83. Galassi G., Lamantea E., Invernizzi F., Tavani F., Pisano I., Ferrero I., Palmieri L., Zeviani M., Additive effects of POLG1 and ANT1 mutations in a complex encephalomyopathy. Neuromuscular Disorders 2008 18 6 465 470 2-s2.0-45449120033 10.1016/j.nmd.2008.03.013
84. de Marcos Lousa C., Trézéguet V., Dianoux A.-C., Brandolin G., Lauquin G. J.-M., The human mitochondrial ADP/ATP carriers: kinetic properties and biogenesis of wild-type and mutant proteins in the yeast S. cerevisiae. Biochemistry 2002 41 48 14412 14420 2-s2.0-2242438967 10.1021/bi0261490 (Pubitemid 35407431)
85. Fontanesi F., Palmieri L., Scarcia P., Lodi T., Donnini C., Limongelli A., Tiranti V., Zeviani M., Ferrero I., Viola A. M., 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 2004 13 9 923 934 2-s2.0-16544382212 10.1093/hmg/ddh108 (Pubitemid 38628428)
86. Kawamata H., Tiranti V., Magrané J., Chinopoulos C., Manfredi G., adPEO mutations in ANT1 impair ADP-ATP translocation in muscle mitochondria. Human Molecular Genetics 2011 20 15 2964 2974 2-s2.0-79960131601 10.1093/hmg/ddr200 ddr200
87. Chen X. J., Induction of an unregulated channel by mutations in adenine nucleotide translocase suggests an explanation for human ophthalmoplegia. Human Molecular Genetics 2002 11 16 1835 1843 2-s2.0-0036667983
88. Wang X., Salinas K., Zuo X., Kucejova B., Chen X. J., Dominant membrane uncoupling by mutant adenine nucleotide translocase in mitochondrial diseases. Human Molecular Genetics 2008 17 24 4036 4044 2-s2.0-57049091540 10.1093/hmg/ddn306 (Pubitemid 352762862)
89. Wang X., Zuo X., Kucejova B., Chen X. J., Reduced cytosolic protein synthesis suppresses mitochondrial degeneration. Nature Cell Biology 2008 10 9 1090 1097 2-s2.0-51049094187 10.1038/ncb1769
90. El-Khoury R., Sainsard-Chanet A., Suppression of mitochondrial DNA instability of autosomal dominant forms of progressive external ophthalmoplegia-associated ANT1 mutations in Podospora anserina. Genetics 2009 183 3 861 871 2-s2.0-72449195206 10.1534/genetics.109.107813
91. Bratic A., Larsson N.-G., The role of mitochondria in aging. Journal of Clinical Investigation 2013 123 3 951 957
92. Osiewacz H. D., Bernhardt D., Mitochondrial quality control: impact on aging and life span-a mini review. Gerontology. In press
93. Breitenbach M., Jazwinski S. M., Laun P., The retrograde response and other pathways of interorganelle communication in yeast replicative aging. Aging Research in Yeast 2012 57 Amsterdam, The Netherlands Springer 79 100