Phenotypic rescue of a Drosophila model of mitochondrial ANT1 disease

DMM Disease Models and Mechanisms

Volumn 7, Issue 6, 2014, Pages 635-648

  Vartiainen, Suvi ^a   Chen, Shanjun ^a   George, Jack ^a   Tuomela, Tea ^a   Luoto, Kaisa R ^a   O'Dell, Kevin M C ^b   Jacobs, Howard T ^a,c  

^a TAMPERE UNIVERSITY HOSPITAL   (Finland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Adenine nucleotide translocase; Alternative oxidase; Mitochondrial biogenesis; Mitochondrial disease

Indexed keywords

ADENINE NUCLEAR TRANSLOCASE 1; ADENOSINE TRIPHOSPHATE; ALTERNATIVE OXIDASE; CARRIER PROTEIN; CYTOCHROME C OXIDASE; LACTATE DEHYDROGENASE; LACTIC ACID; MITOCHONDRIAL DNA; OXIDOREDUCTASE; UNCLASSIFIED DRUG; ADENINE NUCLEOTIDE TRANSLOCASE; DNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASCIDIACEA; BIOENERGY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; DROSOPHILA MELANOGASTER; EMBRYO; FEMALE; FEMALE STERILITY; FERTILIZATION; GENE EXPRESSION; GLYCOLYSIS; MALE; MECHANICAL STRESS; METABOLIC STRESS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; RESPIRATION CONTROL; SEIZURE; AMINO ACID SEQUENCE; ANIMAL; DISEASE MODEL; DROSOPHILA; GENETICS; MOLECULAR GENETICS; OXIDATIVE PHOSPHORYLATION;

ADENINE NUCLEOTIDE TRANSLOCATOR 1; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA; DROSOPHILA; FEMALE; MALE; MITOCHONDRIAL DISEASES; MOLECULAR SEQUENCE DATA; OXIDATIVE PHOSPHORYLATION; PHENOTYPE; POINT MUTATION;

EID: 84902259954     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.016527     Document Type: Article

References (78)

1. Barca, E., Aguennouz, M., Mazzeo, A., Messina, S., Toscano, A., Vita, G. L., Portaro, S., Parisi, D. and Rodolico, C. (2013). ANT1 is reduced in sporadic inclusion body myositis. Neurol. Sci. 34, 217-224.
2. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
3. 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. (Pubitemid 41796524)
4. Charlier, C., Montfort, J., Chabrol, O., Brisard, D., Nguyen, T., Le Cam, A., Richard-Parpaillon, L., Moreews, F., Pontarotti, P., Uzbekova, S. et al. (2012). Oocyte-somatic cells interactions, lessons from evolution. BMC Genomics 13, 560.
5. Chaturvedi, R. K. and Beal, M. F. (2013). Mitochondria targeted therapeutic approaches in Parkinson's and Huntington's diseases. Mol. Cell. Neurosci. 55, 101-114.
6. Chen, S., Oliveira, M. T., Sanz, A., Kemppainen, E., Fukuoh, A., Schlicht, B., Kaguni, L. S. and Jacobs, H. T. (2012). A cytoplasmic suppressor of a nuclear mutation affecting mitochondrial functions in Drosophila. Genetics 192, 483-493.
7. Chevrollier, A., Loiseau, D., Reynier, P. and Stepien, G. (2011). Adenine nucleotide translocase 2 is a key mitochondrial protein in cancer metabolism. Biochim. Biophys. Acta 1807, 562-567.
8. Deng, W. M. and Bownes, M. (1998). Patterning and morphogenesis of the follicle cell epithelium during Drosophila oogenesis. Int. J. Dev. Biol. 42, 541-552.
9. Deng, H., Dodson, M. W., Huang, H. and Guo, M. (2008). The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl. Acad. Sci. USA 105, 14503-14508.
10. Deschauer, M., Hudson, G., Müller, 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. (Pubitemid 40431937)
11. Dillon, L. M., Williams, S. L., Hida, A., Peacock, J. D., Prolla, T. A., Lincoln, J. and Moraes, C. T. (2012). Increased mitochondrial biogenesis in muscle improves aging phenotypes in the mtDNA mutator mouse. Hum. Mol. Genet. 21, 2288-2297.
12. Dobson, S. L., Marsland, E. J. and Rattanadechakul, W. (2002). Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160, 1087-1094. (Pubitemid 34263471)
13. El-Khoury, R., Dufour, E., Rak, M., Ramanantsoa, N., Grandchamp, N., Csaba, Z., Duvillié, B., Bénit, P., Gallego, J., Gressens, P. et al. (2013). Alternative oxidase expression in the mouse enables bypassing cytochrome c oxidase blockade and limits mitochondrial ROS overproduction. PLoS Genet. 9, e1003182.
14. El-Khoury, R., Kemppainen, K. K., Dufour, E., Szibor, M., Jacobs, H. T. and Rustin, P. (2014). Engineering the alternative oxidase gene to better understand and counteract mitochondrial defects: state of the art and perspectives. Br. J. Pharmacol. 171, 2243-2249.
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. (Pubitemid 29214495)
16. Farhadian, S. F., Suárez-Fariñas, M., Cho, C. E., Pellegrino, M. and Vosshall, L. B. (2012). Post-fasting olfactory, transcriptional, and feeding responses in Drosophila. Physiol. Behav. 105, 544-553.
17. Fergestad, T., Bostwick, B. and Ganetzky, B. (2006). Metabolic disruption in Drosophila bang-sensitive seizure mutants. Genetics 173, 1357-1364. (Pubitemid 44127641)
18. Fernández-Ayala, D. J., Sanz, A., Vartiainen, S., Kemppainen, K. K., Babusiak, M., Mustalahti, E., Costa, R., Tuomela, T., Zeviani, M., Chung, J. et al. (2009). Expression of the Ciona intestinalis alternative oxidase (AOX) in Drosophila complements defects in mitochondrial oxidative phosphorylation. Cell Metab. 9, 449-460.
19. Fernández-Ayala, D. J., Chen, S., Kemppainen, E., O'Dell, K. M. and Jacobs, H. T. (2010). Gene expression in a Drosophila model of mitochondrial disease. PLoS ONE 5, e8549.
20. 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. (Pubitemid 38628428)
21. Forlani, G., Giarda, E., Ala, U., Di Cunto, F., Salani, M., Tupler, R., Kilstrup-Nielsen, C. and Landsberger, N. (2010). The MeCP2/YY1 interaction regulates ANT1 expression at 4q35: novel hints for Rett syndrome pathogenesis. Hum. Mol. Genet. 19, 3114-3123.
22. Fregoso Lomas, M., Hails, F., Lachance, J. F. and Nilson, L. A. (2013). Response to the dorsal anterior gradient of EGFR signaling in Drosophila oogenesis is prepatterned by earlier posterior EGFR activation. Cell Rep. 4, 791-802.
23. 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. (Pubitemid 27280204)
24. Hofer, A., Noe, N., Tischner, C., Kladt, N., Lellek, V., Schauß, A. and Wenz, T. (2014). Defining the action spectrum of potential PGC-1α activators on a mitochondrial and cellular level in vivo. Hum. Mol. Genet. 23, 2400-2415.
25. Humphrey, D. M., Parsons, R. B., Ludlow, Z. N., Riemensperger, T., Esposito, G., Verstreken, P., Jacobs, H. T., Birman, S. and Hirth, F. (2012). Alternative oxidase rescues mitochondria-mediated dopaminergic cell loss in Drosophila. Hum. Mol. Genet. 21, 2698-2712.
26. Hurd, T. R., DeGennaro, M. and Lehmann, R. (2012). Redox regulation of cell migration and adhesion. Trends Cell Biol. 22, 107-115.
27. Jacobs, H. T. and Turnbull, D. M. (2005). Nuclear genes and mitochondrial translation: a new class of genetic disease. Trends Genet. 21, 312-314. (Pubitemid 40726384)
28. Jordens, E. Z., Palmieri, L., Huizing, M., van den Heuvel, L. P., Sengers, R. C., Dörner, 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. (Pubitemid 34693749)
29. 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. (Pubitemid 30650199)
30. Kawamata, H., Tiranti, V., Magrané, J., Chinopoulos, C. and Manfredi, G. (2011). adPEO mutations in ANT1 impair ADP-ATP translocation in muscle mitochondria. Hum. Mol. Genet. 20, 2964-2974.
31. 25t) by duplication of the mutant gene in its natural chromosomal context. Mitochondrion 9, 353-363.
32. Kemppainen, K. K., Rinne, J., Sriram, A., Lakanmaa, M., Zeb, A., Tuomela, T., Popplestone, A., Singh, S., Sanz, A., Rustin, P. et al. (2014). Expression of alternative oxidase in Drosophila ameliorates diverse phenotypes due to cytochrome oxidase deficiency. Hum. Mol. Genet. 23, 2078-2093.
33. 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.
34. Komen, J. C. and Thorburn, D. R. (2014). Turn up the power - pharmacological activation of mitochondrial biogenesis in mouse models. Br. J. Pharmacol. 171, 1818-1836.
35. Lee, J., Schriner, S. E. and Wallace, D. C. (2009). Adenine nucleotide translocator 1 deficiency increases resistance of mouse brain and neurons to excitotoxic insults. Biochim. Biophys. Acta 1787, 364-370.
36. Longley, M. J., Clark, S., Yu Wai Man, C., Hudson, G., Durham, S. E., Taylor, R. W., Nightingale, S., Turnbull, D. M., Copeland, W. C. and Chinnery, P. F. (2006). Mutant POLG2 disrupts DNA polymerase gamma subunits and causes progressive external ophthalmoplegia. Am. J. Hum. Genet. 78, 1026-1034. (Pubitemid 43787693)
37. 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. et al. (2012). Lack of the mitochondrial protein acylglycerol kinase causes Sengers syndrome. Am. J. Hum. Genet. 90, 314-320.
38. Michaud, S., Morrow, G., Marchand, J. and Tanguay, R. M. (2002). Drosophila small heat shock proteins: cell and organelle-specific chaperones? Prog. Mol. Subcell. Biol. 28, 79-101.
39. Miwa, S., St-Pierre, J., Partridge, L. and Brand, M. D. (2003). Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med. 35, 938-948. (Pubitemid 37211448)
40. Morrow, G., Inaguma, Y., Kato, K. and Tanguay, R. M. (2000). The small heat shock protein Hsp22 of Drosophila melanogaster is a mitochondrial protein displaying oligomeric organization. J. Biol. Chem. 275, 31204-31210.
41. 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. (Pubitemid 34016466)
42. Narula, N., Zaragoza, M. V., Sengupta, P. P., Li, P., Haider, N., Verjans, J., Waymire, K., Vannan, M. and Wallace, D. C. (2011). Adenine nucleotide translocase 1 deficiency results in dilated cardiomyopathy with defects in myocardial mechanics, histopathological alterations, and activation of apoptosis. JACC Cardiovasc. Imaging 4, 1-10.
43. Neuman-Silberberg, F. S. and Schüpbach, T. (1996). The Drosophila TGF-alpha-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev. 59, 105-113. (Pubitemid 26379332)
44. Noe, N., Dillon, L., Lellek, V., Diaz, F., Hida, A., Moraes, C. T. and Wenz, T. (2013). Bezafibrate improves mitochondrial function in the CNS of a mouse model of mitochondrial encephalopathy. Mitochondrion 13, 417-426.
45. 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. (Pubitemid 41535472)
46. Parker, L., Padilla, M., Du, Y., Dong, K. and Tanouye, M. A. (2011). Drosophila as a model for epilepsy: bss is a gain-of-function mutation in the para sodium channel gene that leads to seizures. Genetics 187, 523-534.
47. Pavlidis, P., Ramaswami, M. and Tanouye, M. A. (1994). The Drosophila easily shocked gene: a mutation in a phospholipid synthetic pathway causes seizure, neuronal failure, and paralysis. Cell 79, 23-33. (Pubitemid 24309510)
48. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézé guet, V., Lauquin, G. J. and Brandolin, G. (2003). Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426, 39-44. (Pubitemid 37432535)
49. Phillips, M. J., Webb-Wood, S., Faulkner, A. E., Jabbar, S. B., Biousse, V., Newman, N. J., Do, V. T., Boatright, J. H., Wallace, D. C. and Pardue, M. T. (2010). Retinal function and structure in Ant1-deficient mice. Invest. Ophthalmol. Vis. Sci. 51, 6744-6752.
50. Poulton, J. S. and Deng, W. M. (2007). Cell-cell communication and axis specification in the Drosophila oocyte. Dev. Biol. 311, 1-10. (Pubitemid 47588234)
51. Rikhy, R., Ramaswami, M. and Krishnan, K. S. (2003). A temperature-sensitive allele of Drosophila sesB reveals acute functions for the mitochondrial adenine nucleotide translocase in synaptic transmission and dynamin regulation. Genetics 165, 1243-1253. (Pubitemid 38020246)
52. Rørth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
53. Rørth, P., Szabo, K. and Texido, G. (2000). The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol. Cell 6, 23-30.
54. Roth, S., Neuman-Silberberg, F. S., Barcelo, G. and Schüpbach, T. (1995). cornichon and the EGF receptor signaling process are necessary for both anteriorposterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967-978.
55. Royden, C. S., Pirrotta, V. and Jan, L. Y. (1987). The tko locus, site of a behavioral mutation in D. melanogaster, codes for a protein homologous to prokaryotic ribosomal protein S12. Cell 51, 165-173.
56. Saada, A. (2004). Deoxyribonucleotides and disorders of mitochondrial DNA integrity. DNA Cell Biol. 23, 797-806.
57. Sanz, A., Soikkeli, M., Portero-Otín, M., Wilson, A., Kemppainen, E., McIlroy, G., Ellilä, S., Kemppainen, K. K., Tuomela, T., Lakanmaa, M. et al. (2010a). Expression of the yeast NADH dehydrogenase Ndi1 in Drosophila confers increased lifespan independently of dietary restriction. Proc. Natl. Acad. Sci. USA 107, 9105-9110.
58. Sanz, A., Fernández-Ayala, D. J., Stefanatos, R. K. and Jacobs, H. T. (2010b). Mitochondrial ROS production correlates with, but does not directly regulate lifespan in Drosophila. Aging 2, 200-223.
59. Shah, Z. H., O'Dell, K. M., Miller, S. C., An, X. and Jacobs, H. T. (1997). Metazoan nuclear genes for mitoribosomal protein S12. Gene 204, 55-62. (Pubitemid 28022170)
60. Sharer, J. D. (2005). The adenine nucleotide translocase type 1 (ANT1): a new factor in mitochondrial disease. IUBMB Life 57, 607-614.
61. 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. (Pubitemid 32626024)
62. Srivastava, S., Diaz, F., Iommarini, L., Aure, K., Lombes, A. and Moraes, C. T. (2009). PGC-1alpha/beta induced expression partially compensates for respiratory chain defects in cells from patients with mitochondrial disorders. Hum. Mol. Genet. 18, 1805-1812.
63. Stein, D., Cho, Y. S. and Stevens, L. M. (2013). Localized serine protease activity and the establishment of Drosophila embryonic dorsoventral polarity. Fly (Austin) 7, 161-167.
64. Strauss, K. A., DuBiner, L., Simon, M., Zaragoza, M., Sengupta, P. P., Li, P., Narula, N., Dreike, S., Platt, J., Procaccio, V. et al. (2013). Severity of cardiomyopathy associated with adenine nucleotide translocator-1 deficiency correlates with mtDNA haplogroup. Proc. Natl. Acad. Sci. USA 110, 3453-3458.
65. Subramaniam, V., Golik, P., Murdock, D. G., Levy, S., Kerstann, K. W., Coskun, P. E., Melkonian, G. A. and Wallace, D. C. (2008). MITOCHIP assessment of differential gene expression in the skeletal muscle of Ant1 knockout mice: coordinate regulation of OXPHOS, antioxidant, and apoptotic genes. Biochim. Biophys. Acta 1777, 666-675.
66. Suomalainen, A. and Kaukonen, J. (2001). Diseases caused by nuclear genes affecting mtDNA stability. Am. J. Med. Genet. 106, 53-61.
67. Terhzaz, S., Cabrero, P., Chintapalli, V. R., Davies, S. A. and Dow, J. A. (2010). Mislocalization of mitochondria and compromised renal function and oxidative stress resistance in Drosophila SesB mutants. Physiol. Genomics 41, 33-41.
68. Tiefenböck, S. K., Baltzer, C., Egli, N. A. and Frei, C. (2010). The Drosophila PGC-1 homologue Spargel coordinates mitochondrial activity to insulin signalling. EMBO J. 29, 171-183.
69. Toivonen, J. M., O'Dell, K. M., Petit, N., Irvine, S. C., Knight, G. K., Lehtonen, M., Longmuir, M., Luoto, K., Touraille, S., Wang, Z. et al. (2001). Technical knockout, a Drosophila model of mitochondrial deafness. Genetics 159, 241-254. (Pubitemid 32917374)
70. Tyynismaa, H., Ylikallio, E., Patel, M., Molnar, M. J., Haller, R. G. and Suomalainen, A. (2009). A heterozygous truncating mutation in RRM2B causes autosomal-dominant progressive external ophthalmoplegia with multiple mtDNA deletions. Am. J. Hum. Genet. 85, 290-295.
71. Van Goethem, G., Dermaut, B., Löfgren, 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. (Pubitemid 32626018)
72. Veal, E. and Day, A. (2011). Hydrogen peroxide as a signaling molecule. Antioxid. Redox Signal. 15, 147-151.
73. Wang, X., Salinas, K., Zuo, X., Kucejova, B. and Chen, X. J. (2008). Dominant membrane uncoupling by mutant adenine nucleotide translocase in mitochondrial diseases. Hum. Mol. Genet. 17, 4036-4044. (Pubitemid 352762862)
74. Wang, Y., Ebermann, L., Sterner-Kock, A., Wika, S., Schultheiss, H. P., Dörner, A. and Walther, T. (2009). Myocardial overexpression of adenine nucleotide translocase 1 ameliorates diabetic cardiomyopathy in mice. Exp. Physiol. 94, 220-227.
75. Wenz, T., Diaz, F., Spiegelman, B. M. and Moraes, C. T. (2008). Activation of the PPAR/PGC-1alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Cell Metab. 8, 249-256.
76. Yamamoto, M., Uematsu, S., Okamoto, T., Matsuura, Y., Sato, S., Kumar, H., Satoh, T., Saitoh, T., Takeda, K., Ishii, K. J. et al. (2007). Enhanced TLR-mediated NF-IL6 dependent gene expression by Trib1 deficiency. J. Exp. Med. 204, 2233-2239. (Pubitemid 47360882)
77. Zhang, Y. Q., Roote, J., Brogna, S., Davis, A. W., Barbash, D. A., Nash, D. and Ashburner, M. (1999). stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster. Genetics 153, 891-903. (Pubitemid 29482343)
78. Zhang, H., Tan, J., Reynolds, E., Kuebler, D., Faulhaber, S. and Tanouye, M. (2002). The Drosophila slamdance gene: a mutation in an aminopeptidase can cause seizure, paralysis and neuronal failure. Genetics 162, 1283-1299. (Pubitemid 35417519)