Stable nuclear expression of ATP8 and ATP6 genes rescues a mtDNA Complex v null mutant

Nucleic Acids Research

Volumn 44, Issue 19, 2016, Pages 9342-9357

  Boominathan, Amutha ^a   Vanhoozer, Shon ^a   Basisty, Nathan ^b   Powers, Kathleen ^a   Crampton, Alexandra L ^c   Wang, Xiaobin ^d   Friedricks, Natalie ^e   Schilling, Birgit ^b   Brand, Martin D ^b   O'Connor, Matthew S ^a  

^a SENS Foundation   (United States)

^b BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^c University of Minnesota   (United States)

^d Columbia University ^*  (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MITOCHONDRIAL DNA; ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; MEMBRANE PROTEIN; OLIGOMYCIN SENSITIVITY-CONFERRING PROTEIN;

ARTICLE; ATP6 GENE; ATP8 GENE; CELL VIABILITY; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME SYNTHESIS; GENE; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENE SEQUENCE; GENE TARGETING; GLYCOLYSIS; HUMAN; HUMAN CELL; HYDROLYSIS; LIMIT OF QUANTITATION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; CELL LINE; CELL NUCLEUS; DNA MUTATIONAL ANALYSIS; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MITOCHONDRIAL GENE; MITOCHONDRION; MUTATION;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; CARRIER PROTEINS; CELL LINE; CELL NUCLEUS; DNA MUTATIONAL ANALYSIS; GENE EXPRESSION; GENES, MITOCHONDRIAL; GENETIC COMPLEMENTATION TEST; HYDROLYSIS; MEMBRANE PROTEINS; MITOCHONDRIA; MUTATION;

EID: 84994583233     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw756     Document Type: Article

References (62)

1. Schaefer, A. M., McFarland, R., Blakely, E. L., He, L., Whittaker, R. G., Taylor, R. W., Chinnery, P. F., Turnbull, D. M. (2008) Prevalence of mitochondrial DNA disease in adults. Ann. Neurol., 63, 35-39.
2. Arpa, J., Cruz-Martinez, A., Campos, Y., Gutierrez-Molina, M., Garcia-Rio, F., Perez-Conde, C., Martin, M. A., Rubio, J. C., Del Hoyo, P., Arpa-Fernandez, A. et al. (2003) Prevalence and progression of mitochondrial diseases: A study of 50 patients. Muscle Nerve, 28, 690-695.
3. Chinnery, P. F., Johnson, M. A., Wardell, T. M., Singh-Kler, R., Hayes, C., Brown, D. T., Taylor, R. W., Bindoff, L. A., Turnbull, D. M. (2000) The epidemiology of pathogenic mitochondrial DNA mutations. Ann. Neurol., 48, 188-193.
4. Elliott, H. R., Samuels, D. C., Eden, J. A., Relton, C. L., Chinnery, P. F. (2008) Pathogenic mitochondrial DNA mutations are common in the general population. Am. J. Hum. Genet., 83, 254-260.
5. Cwerman-Thibault, H., Sahel, J. A., Corral-Debrinski, M. (2011) Mitochondrial medicine: To a new era of gene therapy for mitochondrial DNA mutations. J. Inherit. Metab. Dis., 34, 327-344.
6. Wallace, D. C., Singh, G., Lott, M. T., Hodge, J. A., Schurr, T. G., Lezza, A. M., Elsas, L. J. 2nd and Nikoskelainen, E. K. (1988) Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science, 242, 1427-1430.
7. Howell, N., Kubacka, I., Xu, M., McCullough, D. A. (1991) Leber hereditary optic neuropathy: Involvement of the mitochondrial ND1 gene and evidence for an intragenic suppressor mutation. Am. J. Hum. Genet., 48, 935-942.
8. Gerbitz, K. D., Obermaier-Kusser, B., Lestienne, P., Zierz, S., Muller-Hocker, J., Pongratz, D., Paetzke-Brunner, I., Deufel, T. (1990) Mutations of the mitochondrial DNA: the contribution of DNA techniques to the diagnosis of mitochondrial encephalomyopathies. J. Clin. Chem. Clin. Biochem, 28, 241-250.
9. Shoffner, J. M., Lott, M. T., Voljavec, A. S., Soueidan, S. A., Costigan, D. A., Wallace, D. C. (1989) Spontaneous Kearns-Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy. Proc. Natl. Acad. Sci. U. S. A., 86, 7952-7956.
10. van den Ouweland, J. M., de Klerk, J. B., van de Corput, M. P., Dirks, R. W., Raap, A. K., Scholte, H. R., Huijmans, J. G., Hart, L. M., Bruining, G. J., Maassen, J. A. (2000) Characterization of a novel mitochondrial DNA deletion in a patient with a variant of the Pearson marrow-pancreas syndrome. Eur. J. Hum. Genet., 8, 195-203.
11. Wallace, D. C., Chalkia, D. (2013) Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold. Spring Harb. Perspect. Biol., 5, a021220.
12. Hargreaves, I. P. (2014) Coenzyme Q10 as a therapy for mitochondrial disease. Int. J. Biochem. Cell Biol., 49, 105-111.
13. Pfeffer, G., Majamaa, K., Turnbull, D. M., Thorburn, D., Chinnery, P. F. (2012) Treatment for mitochondrial disorders. Cochrane Database Syst. Rev., 4, CD004426.
14. Nagley, P., Farrell, L. B., Gearing, D. P., Nero, D., Meltzer, S., Devenish, R. J. (1988) Assembly of functional proton-translocating ATPase complex in yeast mitochondria with cytoplasmically synthesized subunit 8, a polypeptide normally encoded within the organelle. Proc. Natl. Acad. Sci. U. S. A., 85, 2091-2095.
15. Manfredi, G., Fu, J., Ojaimi, J., Sadlock, J. E., Kwong, J. Q., Guy, J., Schon, E. A. (2002) Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat. Genet., 30, 394-399.
16. Zullo, S. J., Parks, W. T., Chloupkova, M., Wei, B., Weiner, H., Fenton, W. A., Eisenstadt, J. M., Merril, C. R. (2005) Stable transformation of CHO Cells and human NARP cybrids confers oligomycin resistance (oli(r)) following transfer of a mitochondrial DNA-encoded oli(r) ATPase6 gene to the nuclear genome: a model system for mtDNA gene therapy. Rejuvenation Res., 8, 18-28.
17. Cwerman-Thibault, H., Augustin, S., Lechauve, C., Ayache, J., Ellouze, S., Sahel, J. A., Corral-Debrinski, M. (2015) Nuclear expression of mitochondrial ND4 leads to the protein assembling in complex I and prevents optic atrophy and visual loss. Mol. Ther. Methods Clin. Dev., 2, 15003.
18. Koilkonda, R., Yu, H., Talla, V., Porciatti, V., Feuer, W. J., Hauswirth, W. W., Chiodo, V., Erger, K. E., Boye, S. L., Lewin, A. S. et al. (2014) LHON gene therapy vector prevents visual loss and optic neuropathy induced by G11778A mutant mitochondrial DNA: biodistribution and toxicology profile. Invest. Ophthalmol. Vis. Sci., 55, 7739-7753.
19. Ellouze, S., Augustin, S., Bouaita, A., Bonnet, C., Simonutti, M., Forster, V., Picaud, S., Sahel, J. A., Corral-Debrinski, M. (2008) Optimized allotopic expression of the human mitochondrial ND4 prevents blindness in a rat model of mitochondrial dysfunction. Am. J. Hum. Genet., 83, 373-387.
20. Calabrese, C., Iommarini, L., Kurelac, I., Calvaruso, M. A., Capristo, M., Lollini, P. L., Nanni, P., Bergamini, C., Nicoletti, G., Giovanni, C. D. et al. (2013) Respiratory complex I is essential to induce a Warburg profile in mitochondria-defective tumor cells. Cancer Metab., 1, 11.
21. Gasparre, G., Kurelac, I., Capristo, M., Iommarini, L., Ghelli, A., Ceccarelli, C., Nicoletti, G., Nanni, P., De Giovanni, C., Scotlandi, K. et al. (2011) A mutation threshold distinguishes the antitumorigenic effects of the mitochondrial gene MTND1, an oncojanus function. Cancer Res., 71, 6220-6229.
22. Lim, S. C., Hroudova, J., Van Bergen, N. J., Lopez Sanchez, M. I., Trounce, I. A., McKenzie, M. (2016) Loss of mitochondrial DNA-encoded protein ND1 results in disruption of complex I biogenesis during early stages of assembly. FASEB J., 30, 2236-2248.
23. McKenzie, M., Chiotis, M., Hroudova, J., Lopez Sanchez, M. I., Lim, S. C., Cook, M. J., McKelvie, P., Cotton, R. G., Murphy, M., St John, J. C. et al. (2014) Capture of somatic mtDNA point mutations with severe effects on oxidative phosphorylation in synaptosome cybrid clones from human brain. Hum. Mutat., 35, 1476-1484.
24. Perales-Clemente, E., Fernandez-Silva, P., Acin-Perez, R., Perez-Martos, A., Enriquez, J. A. (2011) Allotopic expression of mitochondrial-encoded genes in mammals: achieved goal, undemonstrated mechanism or impossible task? Nucleic Acids Res., 39, 225-234.
25. Oca-Cossio, J., Kenyon, L., Hao, H., Moraes, C. T. (2003) Limitations of allotopic expression of mitochondrial genes in mammalian cells. Genetics, 165, 707-720.
26. Bai, R. K., Wong, L. J. (2004) Detection and quantification of heteroplasmic mutant mitochondrial DNA by real-time amplification refractory mutation system quantitative PCR analysis: a single-step approach. Clin. Chem., 50, 996-1001.
27. Johnston, A. J., Hoogenraad, J., Dougan, D. A., Truscott, K. N., Yano, M., Mori, M., Hoogenraad, N. J., Ryan, M. T. (2002) Insertion and assembly of human tom7 into the preprotein translocase complex of the outer mitochondrial membrane. J. Biol. Chem., 277, 42197-42204.
28. Keshishian, H., Addona, T., Burgess, M., Kuhn, E., Carr, S. A. (2007) Quantitative, multiplexed assays for low abundance proteins in plasma by targeted mass spectrometry and stable isotope dilution. Mol. Cell. Proteomics, 6, 2212-2229.
29. Kuhn, M. L., Zemaitaitis, B., Hu, L. I., Sahu, A., Sorensen, D., Minasov, G., Lima, B. P., Scholle, M., Mrksich, M., erson, W. F. et al. (2014) Structural, kinetic and proteomic characterization of acetyl phosphate-dependent bacterial protein acetylation. PLoS One, 9, e94816.
30. Schilling, B., Rardin, M. J., MacLean, B. X., Zawadzka, A. M., Frewen, B. E., Cusack, M. P., Sorensen, D. J., Bereman, M. S., Jing, E., Wu, C. C. et al. (2012) Platform-independent and label-free quantitation of proteomic data using MS1 extracted ion chromatograms in skyline: application to protein acetylation and phosphorylation. Mol. Cell. Proteomics, 11, 202-214.
31. Rardin, M. J., Schilling, B., Cheng, L. Y., MacLean, B. X., Sorensen, D. J., Sahu, A. K., MacCoss, M. J., Vitek, O., Gibson, B. W. (2015) MS1 peptide ion intensity chromatograms in MS2 (SWATH) data independent acquisitions. Improving post acquisition analysis of proteomic experiments. Mol. Cell. Proteomics, 14, 2405-2419.
32. Shilov, I. V., Seymour, S. L., Patel, A. A., Loboda, A., Tang, W. H., Keating, S. P., Hunter, C. L., Nuwaysir, L. M., Schaeffer, D. A. (2007) The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell. Proteomics, 6, 1638-1655.
33. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., MacCoss, M. J. (2010) Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics, 26, 966-968.
34. Scharschmidt, B. F., Keeffe, E. B., Blankenship, N. M., Ockner, R. K. (1979) Validation of a recording spectrophotometric method for measurement of membrane-associated Mg-and NaK-ATPase activity. J. Lab. Clin. Med., 93, 790-799.
35. Wu, M., Neilson, A., Swift, A. L., Moran, R., Tamagnine, J., Parslow, D., Armistead, S., Lemire, K., Orrell, J., Teich, J. et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol., 292, C125-C136.
36. Jonckheere, A. I., Hogeveen, M., Nijtmans, L. G., van den Brand, M. A., Janssen, A. J., Diepstra, J. H., van den Brandt, F. C., van den Heuvel, L. P., Hol, F. A., Hofste, T. G. et al. (2008) A novel mitochondrial ATP8 gene mutation in a patient with apical hypertrophic cardiomyopathy and neuropathy. J. Med. Genet., 45, 129-133.
37. Bietenhader, M., Martos, A., Tetaud, E., Aiyar, R. S., Sellem, C. H., Kucharczyk, R., Clauder-Munster, S., Giraud, M. F., Godard, F., Salin, B. et al. (2012) Experimental relocation of the mitochondrial ATP9 gene to the nucleus reveals forces underlying mitochondrial genome evolution. PLoS Genet., 8, e1002876.
38. Koilkonda, R. D., Chou, T. H., Porciatti, V., Hauswirth, W. W., Guy, J. (2010) Induction of rapid and highly efficient expression of the human ND4 complex I subunit in the mouse visual system by self-complementary adeno-associated virus. Arch. Ophthalmol., 128, 876-883.
39. Dunn, D. A., Pinkert, C. A. (2015) Allotopic expression of ATP6 in the mouse as a transgenic model of mitochondrial disease. Methods Mol. Biol., 1265, 255-269.
40. Koilkonda, R. D., Yu, H., Chou, T. H., Feuer, W. J., Ruggeri, M., Porciatti, V., Tse, D., Hauswirth, W. W., Chiodo, V., Boye, S. L. et al. (2014) Safety and effects of the vector for the Leber hereditary optic neuropathy gene therapy clinical trial. JAMA Ophthalmol., 132, 409-420.
41. Vignal, C. (2015) Safety evaluation of gene therapy in Leber Hereditary Optic Neuropathy (LHON) patients.
42. Houstek, J., Klement, P., Hermanska, J., Houstkova, H., Hansikova, H., Van den Bogert, C., Zeman, J. (1995) Altered properties of mitochondrial ATP-synthase in patients with a T->G mutation in the ATPase 6 (subunit a) gene at position 8993 of mtDNA. Biochim. Biophys. Acta, 1271, 349-357.
43. Houstek, J., Pickova, A., Vojtiskova, A., Mracek, T., Pecina, P., Jesina, P. (2006) Mitochondrial diseases and genetic defects of ATP synthase. Biochim. Biophys. Acta, 1757, 1400-1405.
44. Nijtmans, L. G., Henderson, N. S., Attardi, G., Holt, I. J. (2001) Impaired ATP synthase assembly associated with a mutation in the human ATP synthase subunit 6 gene. J. Biol. Chem., 276, 6755-6762.
45. Jesina, P., Tesarova, M., Fornuskova, D., Vojtiskova, A., Pecina, P., Kaplanova, V., Hansikova, H., Zeman, J., Houstek, J. (2004) Diminished synthesis of subunit a (ATP6) and altered function of ATP synthase and cytochrome c oxidase due to the mtDNA 2 bp microdeletion of TA at positions 9205 and 9206. Biochem. J., 383, 561-571.
46. Tatuch, Y., Robinson, B. H. (1993) The mitochondrial DNA mutation at 8993 associated with NARP slows the rate of ATP synthesis in isolated lymphoblast mitochondria. Biochem. Biophys. Res. Commun., 192, 124-128.
47. Carrozzo, R., Tessa, A., Vazquez-Memije, M. E., Piemonte, F., Patrono, C., Malandrini, A., Dionisi-Vici, C., Vilarinho, L., Villanova, M., Schagger, H. et al. (2001) The T9176G mtDNA mutation severely affects ATP production and results in Leigh syndrome. Neurology, 56, 687-690.
48. Mattiazzi, M., Vijayvergiya, C., Gajewski, C. D., DeVivo, D. C., Lenaz, G., Wiedmann, M., Manfredi, G. (2004) The mtDNA T8993G (NARP) mutation results in an impairment of oxidative phosphorylation that can be improved by antioxidants. Hum. Mol. Genet., 13, 869-879.
49. Pallotti, F., Baracca, A., Hernandez-Rosa, E., Walker, W. F., Solaini, G., Lenaz, G., Melzi D'Eril, G. V., Dimauro, S., Schon, E. A., Davidson, M. M. (2004) Biochemical analysis of respiratory function in cybrid cell lines harbouring mitochondrial DNA mutations. Biochem. J., 384, 287-293.
50. Hejzlarova, K., Kaplanova, V., Nuskova, H., Kovarova, N., Jesina, P., Drahota, Z., Mracek, T., Seneca, S., Houstek, J. (2015) Alteration of structure and function of ATP synthase and cytochrome c oxidase by lack of Fo-a and Cox3 subunits caused by mitochondrial DNA 9205delTA mutation. Biochem. J., 466, 601-611.
51. Ware, S. M., El-Hassan, N., Kahler, S. G., Zhang, Q., Ma, Y. W., Miller, E., Wong, B., Spicer, R. L., Craigen, W. J., Kozel, B. A. et al. (2009) Infantile cardiomyopathy caused by a mutation in the overlapping region of mitochondrial ATPase 6 and 8 genes. J. Med. Genet., 46, 308-314.
52. rews, R. M., Kubacka, I., Chinnery, P. F., Lightowlers, R. N., Turnbull, D. M., Howell, N. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet., 23, 147.
53. Mayr, J. A., Haack, T. B., Freisinger, P., Karall, D., Makowski, C., Koch, J., Feichtinger, R. G., Zimmermann, F. A., Rolinski, B., Ahting, U. et al. (2015) Spectrum of combined respiratory chain defects. J. Inherit. Metab. Dis., 38, 629-640.
54. Kulawiak, B., Hopker, J., Gebert, M., Guiard, B., Wiedemann, N., Gebert, N. (2013) The mitochondrial protein import machinery has multiple connections to the respiratory chain. Biochim. Biophys. Acta, 1827, 612-626.
55. Mick, D. U., Dennerlein, S., Wiese, H., Reinhold, R., Pacheu-Grau, D., Lorenzi, I., Sasarman, F., Weraarpachai, W., Shoubridge, E. A., Warscheid, B. et al. (2012) MITRAC links mitochondrial protein translocation to respiratory-chain assembly and translational regulation. Cell, 151, 1528-1541.
56. Aiyar, R. S., Bohnert, M., Duvezin-Caubet, S., Voisset, C., Gagneur, J., Fritsch, E. S., Couplan, E., von der Malsburg, K., Funaya, C., Soubigou, F. et al. (2014) Mitochondrial protein sorting as a therapeutic target for ATP synthase disorders. Nat. Commun., 5, 5585.
57. Dunn, D. A., Pinkert, C. A. (2012) Nuclear expression of a mitochondrial DNA gene: mitochondrial targeting of allotopically expressed mutant ATP6 in transgenic mice. J. Biomed. Biotechnol., 2012, 541245.
58. Li, B. (2015) Safety and Efficacy Study of rAAV2-ND4 Treatment of Leber Hereditary Optic Neuropathy (LHON) (rAAV2-ND4).
59. Guy, J. (2015) Safety Study of an Adeno-associated Virus Vector for Gene Therapy of Leber's Hereditary Optic Neuropathy (LHON).
60. Fitoussi, S. (2016) Efficacy Study of GS010 for the Treatment of Vision Loss up to 6 Months From Onset in LHON Due to the ND4 Mutation (RESCUE).
61. Fitoussi, S. (2016) Efficacy Study of GS010 for Treatment of Vision Loss From 7 Months to 1 Year From Onset in LHON Due to the ND4 Mutation (REVERSE).
62. Michaud, M., Ubrig, E., Filleur, S., Erhardt, M., Ephritikhine, G., Marechal-Drouard, L., Duchene, A. M. (2014) Differential targeting of VDAC3 mRNA isoforms influences mitochondria morphology. Proc. Natl. Acad. Sci. U. S. A., 111, 8991-8996.