Mitochondrial transfection for studying organellar DNA repair, genome maintenance and aging

Mechanisms of Ageing and Development

Volumn 132, Issue 8-9, 2011, Pages 412-423

  Mileshina, Daria ^a,b   Ibrahim, Noha ^a   Boesch, Pierre ^a,c   Lightowlers, Robert N ^c   Dietrich, André ^a   Weber Lotfi, Frédérique ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b SIBERIAN INSTITUTE OF PLANT PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

DNA repair; Mitochondria; Nanocarrier; Natural competence; Transfection

Indexed keywords

DEQUALINIUM; DNA FRAGMENT; MITOCHONDRIAL DNA;

AGING; ARTICLE; BIOLISTIC TRANSFORMATION; CELL ORGANELLE; CHLAMYDOMONAS REINHARDTII; DNA DAMAGE; DNA METABOLISM; DNA REPAIR; DNA SYNTHESIS; DNA TRANSFER; GENE MUTATION; HUMAN; MITOCHONDRIAL GENOME; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; PROTEIN TRANSPORT; TRANSGENE;

AGING; ANIMALS; DNA REPAIR; DNA, MITOCHONDRIAL; GENOME, MITOCHONDRIAL; HUMANS; TRANSFECTION;

CHLAMYDOMONAS REINHARDTII;

EID: 80053118301     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2011.05.002     Document Type: Article

References (122)

1. Aamann M.D., Sorensen M.M., Hvitby C., Berquist B.R., Muftuoglu M., Tian J., de Souza-Pinto N.C., Scheibye-Knudsen M., Wilson Iii D.M., Stevnsner T., Bohr V.A. Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane. FASEB J. 2010, 24:2334-2346.
2. Akbari M., Visnes T., Krokan H.E., Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst.) 2008, 7:605-616.
3. Alexeyev M.F., Venediktova N., Pastukh V., Shokolenko I., Bonilla G., Wilson G.L. Selective elimination of mutant mitochondrial genomes as therapeutic strategy for the treatment of NARP and MILS syndromes. Gene Ther. 2008, 15:516-523.
4. Bacman S.R., Williams S.L., Garcia S., Moraes C.T. Organ-specific shifts in mtDNA heteroplasmy following systemic delivery of a mitochondria-targeted restriction endonuclease. Gene Ther. 2010, 17:713-720.
5. Bacman S.R., Williams S.L., Hernandez D., Moraes C.T. Modulating mtDNA heteroplasmy by mitochondria-targeted restriction endonucleases in a 'differential multiple cleavage-site' model. Gene Ther. 2007, 14:1309-1318.
6. Bayona-Bafaluy M.P., Blits B., Battersby B.J., Shoubridge E.A., Moraes C.T. Rapid directional shift of mitochondrial DNA heteroplasmy in animal tissues by a mitochondrially targeted restriction endonuclease. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:14392-14397.
7. Boddapati S.V., Tongcharoensirikul P., Hanson R.N., D'Souza G.G., Torchilin V.P., Weissig V. Mitochondriotropic liposomes. J. Liposome Res. 2005, 15:49-58.
8. Boesch P., Ibrahim N., Dietrich A., Lightowlers R.N. Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria. Nucleic Acids Res. 2010, 38:1478-1488.
9. Boesch P., Ibrahim N., Paulus F., Cosset A., Tarasenko V., Dietrich A. Plant mitochondria possess a short-patch base excision DNA repair pathway. Nucleic Acids Res. 2009, 37:5690-5700.
10. Boesch P., Weber-Lotfi F., Ibrahim N., Tarasenko V., Cosset A., Paulus F., Lightowlers R.N., Dietrich A. DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Biochim. Biophys. Acta 2010, 1813:186-200.
11. Bokori-Brown M., Holt I.J. Expression of algal nuclear ATP synthase subunit 6 in human cells results in protein targeting to mitochondria but no assembly into ATP synthase. Rejuvenation Res. 2006, 9:455-469.
12. Bolender N., Sickmann A., Wagner R., Meisinger C., Pfanner N. Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep. 2008, 9:42-49.
13. Bolle N., Hinrichsen I., Kempken F. Plastid mRNAs are neither spliced nor edited in maize and cauliflower mitochondrial in organello systems. RNA 2007, 13:2061-2065.
14. Bolle N., Kempken F. Mono- and dicotyledonous plant-specific RNA editing sites are correctly edited in both in organello systems. FEBS Lett. 2006, 580:4443-4448.
15. Bonnefoy N., Fox T.D. Directed alteration of Saccharomyces cerevisiae mitochondrial DNA by biolistic transformation and homologous recombination. Methods Mol. Biol. 2007, 372:153-166.
16. Bonnefoy N., Remacle C., Fox T.D. Genetic transformation of Saccharomyces cerevisiae and Chlamydomonas reinhardtii mitochondria. Methods Cell Biol. 2007, 80:525-548.
17. Bonnet C., Augustin S., Ellouze S., Benit P., Bouaita A., Rustin P., Sahel J.A., Corral-Debrinski M. The optimized allotopic expression of ND1 or ND4 genes restores respiratory chain complex I activity in fibroblasts harboring mutations in these genes. Biochim. Biophys. Acta 2008, 1783:1707-1717.
18. Bonnet C., Kaltimbacher V., Ellouze S., Augustin S., Benit P., Forster V., Rustin P., Sahel J.A., Corral-Debrinski M. Allotopic mRNA localization to the mitochondrial surface rescues respiratory chain defects in fibroblasts harboring mitochondrial DNA mutations affecting complex I or v subunits. Rejuvenation Res. 2007, 10:127-144.
19. Cai S., Xu Y., Cooper R.J., Ferkowicz M.J., Hartwell J.R., Pollok K.E., Kelley M.R. Mitochondrial targeting of human O6-methylguanine DNA methyltransferase protects against cell killing by chemotherapeutic alkylating agents. Cancer Res. 2005, 65:3319-3327.
20. Canugovi C., Maynard S., Bayne A.C., Sykora P., Tian J., de Souza Pinto N.C., Croteau D.L., Bohr V.A. The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair (Amst.) 2010, 9:1080-1089.
21. Cappadocia L., Marechal A., Parent J.S., Lepage E., Sygusch J., Brisson N. Crystal structures of DNA-Whirly complexes and their role in Arabidopsis organelle genome repair. Plant Cell 2010, 22:1849-1867.
22. Castandet B., Choury D., Begu D., Jordana X., Araya A. Intron RNA editing is essential for splicing in plant mitochondria. Nucleic Acids Res. 2010, 38:7112-7121.
23. Chatterjee A., Mambo E., Zhang Y., Deweese T., Sidransky D. Targeting of mutant hogg1 in mammalian mitochondria and nucleus: effect on cellular survival upon oxidative stress. BMC Cancer 2006, 6:235.
24. Chatterjee A., Singh K.K. Uracil-DNA glycosylase-deficient yeast exhibit a mitochondrial mutator phenotype. Nucleic Acids Res. 2001, 29:4935-4940.
25. Chen I., Christie P.J., Dubnau D. The ins and outs of DNA transfer in bacteria. Science 2005, 310:1456-1460.
26. Choury D., Araya A. RNA editing site recognition in heterologous plant mitochondria. Curr. Genet. 2006, 50:405-416.
27. Choury D., Farre J.C., Jordana X., Araya A. Different patterns in the recognition of editing sites in plant mitochondria. Nucleic Acids Res. 2004, 32:6397-6406.
28. Choury D., Farre J.C., Jordana X., Araya A. Gene expression studies in isolated mitochondria: Solanum tuberosum rps10 is recognized by cognate potato but not by the transcription, splicing and editing machinery of wheat mitochondria. Nucleic Acids Res. 2005, 33:7058-7065.
29. Clark M.A., Shay J.W. Mitochondrial transformation of mammalian cells. Nature 1982, 295:605-607.
30. Collombet J.M., Wheeler V.C., Vogel F., Coutelle C. Introduction of plasmid DNA into isolated mitochondria by electroporation. A novel approach toward gene correction for mitochondrial disorders. J. Biol. Chem. 1997, 272:5342-5347.
31. Cudd A., Labbe H., Gervais M., Nicolau C. Liposomes injected intravenously into mice associate with liver mitochondria. Biochim. Biophys. Acta 1984, 774:169-180.
32. Cudd A., Nicolau C. Intracellular fate of liposome-encapsulated DNA in mouse liver. Analysis using electron microscope autoradiography and subcellular fractionation. Biochim. Biophys. Acta 1985, 845:477-491.
33. Cudd A., Nicolau C. Interaction of intravenously injected liposomes with mouse liver mitochondria. A fluorescence and electron microscopy study. Biochim. Biophys. Acta 1986, 860:201-214.
34. D'Souza G.G., Boddapati S.V., Weissig V. Mitochondrial leader sequence - plasmid DNA conjugates delivered into mammalian cells by DQAsomes co-localize with mitochondria. Mitochondrion 2005, 5:352-358.
35. D'Souza G.G., Boddapati S.V., Weissig V. Gene therapy of the other genome: the challenges of treating mitochondrial DNA defects. Pharm. Res. 2007, 24:228-238.
36. D'Souza G.G., Rammohan R., Cheng S.M., Torchilin V.P., Weissig V. DQAsome-mediated delivery of plasmid DNA toward mitochondria in living cells. J. Control. Release 2003, 92:189-197.
37. Dassa E.P., Dufour E., Goncalves S., Paupe V., Hakkaart G.A., Jacobs H.T., Rustin P. Expression of the alternative oxidase complements cytochrome c oxidase deficiency in human cells. EMBO Mol. Med. 2009, 1:30-36.
38. de la Loza M.C., Wellinger R.E. A novel approach for organelle-specific DNA damage targeting reveals different susceptibility of mitochondrial DNA to the anticancer drugs camptothecin and topotecan. Nucleic Acids Res. 2009, 37:e26.
39. Dobson A.W., Xu Y., Kelley M.R., LeDoux S.P., Wilson G.L. Enhanced mitochondrial DNA repair and cellular survival after oxidative stress by targeting the human 8-oxoguanine glycosylase repair enzyme to mitochondria. J. Biol. Chem. 2000, 275:37518-37523.
40. Druzhyna N.M., Musiyenko S.I., Wilson G.L., LeDoux S.P. Cytokines induce nitric oxide-mediated mtDNA damage and apoptosis in oligodendrocytes. Protective role of targeting 8-oxoguanine glycosylase to mitochondria. J. Biol. Chem. 2005, 280:21673-21679.
41. Ellouze S., Augustin S., Bouaita A., Bonnet C., Simonutti M., Forster V., Picaud S., Sahel J.A., Corral-Debrinski M. Optimized allotopic expression of the human mitochondrial ND4 prevents blindness in a rat model of mitochondrial dysfunction. Am. J. Hum. Genet. 2008, 83:373-387.
42. Estevez A.M., Thiemann O.H., Alfonzo J.D., Simpson L. T7 RNA polymerase-driven transcription in mitochondria of Leishmania tarentolae and Trypanosoma brucei. Mol. Biochem. Parasitol. 1999, 103:251-259.
43. Farre J.C., Araya A. Gene expression in isolated plant mitochondria: high fidelity of transcription, splicing and editing of a transgene product in electroporated organelles. Nucleic Acids Res. 2001, 29:2484-2491.
44. Farre J.C., Araya A. RNA splicing in higher plant mitochondria: determination of functional elements in group II intron from a chimeric cox II gene in electroporated wheat mitochondria. Plant J. 2002, 29:203-213.
45. Farre J.C., Leon G., Jordana X., Araya A. cis Recognition elements in plant mitochondrion RNA editing. Mol. Cell. Biol. 2001, 21:6731-6737.
46. Fishel M.L., Seo Y.R., Smith M.L., Kelley M.R. Imbalancing the DNA base excision repair pathway in the mitochondria; targeting and overexpressing N-methylpurine DNA glycosylase in mitochondria leads to enhanced cell killing. Cancer Res. 2003, 63:608-615.
47. Flierl A., Jackson C., Cottrell B., Murdock D., Seibel P., Wallace D.C. Targeted delivery of DNA to the mitochondrial compartment via import sequence-conjugated peptide nucleic acid. Mol. Ther. 2003, 7:550-557.
48. Fox T.D., Sanford J.C., McMullin T.W. Plasmids can stably transform yeast mitochondria lacking endogenous mtDNA. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:7288-7292.
49. Frossi B., Tell G., Spessotto P., Colombatti A., Vitale G., Pucillo C. H(2)O(2) induces translocation of APE/Ref-1 to mitochondria in the Raji B-cell line. J. Cell. Physiol. 2002, 193:180-186.
50. Fukui H., Moraes C.T. Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons. Hum. Mol. Genet. 2009, 18:1028-1036.
51. Griffiths L.M., Swartzlander D., Meadows K.L., Wilkinson K.D., Corbett A.H., Doetsch P.W. Dynamic compartmentalization of base excision repair proteins in response to nuclear and mitochondrial oxidative stress. Mol. Cell. Biol. 2009, 29:794-807.
52. Guy J., Qi X., Pallotti F., Schon E.A., Manfredi G., Carelli V., Martinuzzi A., Hauswirth W.W., Lewin A.S. Rescue of a mitochondrial deficiency causing Leber Hereditary Optic Neuropathy. Ann. Neurol. 2002, 52:534-542.
53. Ho R., Rachek L.I., Xu Y., Kelley M.R., LeDoux S.P., Wilson G.L. Yeast apurinic/apyrimidinic endonuclease Apn1 protects mammalian neuronal cell line from oxidative stress. J. Neurochem. 2007, 102:13-24.
54. Ikeda S., Kohmoto T., Tabata R., Seki Y. Differential intracellular localization of the human and mouse endonuclease III homologs and analysis of the sorting signals. DNA Repair (Amst.) 2002, 1:847-854.
55. Inoki Y., Hakamata Y., Hamamoto T., Kinouchi T., Yamazaki S., Kagawa Y., Endo H. Proteoliposomes colocalized with endogenous mitochondria in mouse fertilized egg. Biochem. Biophys. Res. Commun. 2000, 278:183-191.
56. Iyer S., Thomas R.R., Portell F.R., Dunham L.D., Quigley C.K., Bennett J.P. Recombinant mitochondrial transcription factor A with N-terminal mitochondrial transduction domain increases respiration and mitochondrial gene expression. Mitochondrion 2009, 9:196-203.
57. Johnston S.A., Anziano P.Q., Shark K., Sanford J.C., Butow R.A. Mitochondrial transformation in yeast by bombardment with microprojectiles. Science 1988, 240:1538-1541.
58. Kagawa Y., Hayashi J.I. Gene therapy of mitochondrial diseases using human cytoplasts. Gene Ther. 1997, 4:6-10.
59. Kaltimbacher V., Bonnet C., Lecoeuvre G., Forster V., Sahel J.A., Corral-Debrinski M. mRNA localization to the mitochondrial surface allows the efficient translocation inside the organelle of a nuclear recoded ATP6 protein. RNA 2006, 12:1408-1417.
60. Kamenisch Y., Fousteri M., Knoch J., von Thaler A.K., Fehrenbacher B., Kato H., Becker T., Dolle M.E., Kuiper R., Majora M., Schaller M., van der Horst G.T., van Steeg H., Rocken M., Rapaport D., Krutmann J., Mullenders L.H., Berneburg M. Proteins of nucleotide and base excision repair pathways interact in mitochondria to protect from loss of subcutaneous fat, a hallmark of aging. J. Exp. Med. 2010, 207:379-390.
61. Katrangi E., D'Souza G., Boddapati S.V., Kulawiec M., Singh K.K., Bigger B., Weissig V. Xenogenic transfer of isolated murine mitochondria into human rho0 cells can improve respiratory function. Rejuvenation Res. 2007, 10:561-570.
62. Keeney P.M., Quigley C.K., Dunham L.D., Papageorge C.M., Iyer S., Thomas R.R., Schwarz K.M., Trimmer P.A., Khan S.M., Portell F.R., Bergquist K.E., Bennett J.P. Mitochondrial gene therapy augments mitochondrial physiology in a Parkinson's disease cell model. Hum. Gene Ther. 2009, 20:897-907.
63. Khan S.M., Bennett J.P. Development of mitochondrial gene replacement therapy. J. Bioenerg. Biomembr. 2004, 36:387-393.
64. King M.P., Attardi G. Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA. Cell 1988, 52:811-819.
65. King M.P., Attardi G. Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 1989, 246:500-503.
66. King M.P., Koga Y., Davidson M., Schon E.A. Defects in mitochondrial protein synthesis and respiratory chain activity segregate with the tRNA(Leu(UUR)) mutation associated with mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. Mol. Cell. Biol. 1992, 12:480-490.
67. Koczor C.A., Snyder J.W., Shokolenko I.N., Dobson A.W., Wilson G.L., Ledoux S.P. Targeting repair proteins to the mitochondria of mammalian cells through stable transfection, transient transfection, viral transduction, and TAT-mediated protein transduction. Methods Mol. Biol. 2009, 554:233-249.
68. Koulintchenko M., Konstantinov Y., Dietrich A. Plant mitochondria actively import DNA via the permeability transition pore complex. EMBO J. 2003, 22:1245-1254.
69. Koulintchenko M., Temperley R.J., Mason P.A., Dietrich A., Lightowlers R.N. Natural competence of mammalian mitochondria allows the molecular investigation of mitochondrial gene expression. Hum. Mol. Genet. 2006, 15:143-154.
70. Li M.X., Wang D., Zhong Z.Y., Xiang D.B., Li Z.P., Xie J.Y., Yang Z.Z., Jin F., Qing Y. Targeting truncated APE1 in mitochondria enhances cell survival after oxidative stress. Free Radic. Biol. Med. 2008, 45:592-601.
71. Liu P., Demple B. DNA repair in mammalian mitochondria: much more than we thought?. Environ. Mol. Mutagen. 2010, 51:417-426.
72. Liu P., Qian L., Sung J.S., de Souza-Pinto N.C., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson D.M., Shen B., Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008, 28:4975-4987.
73. Liu Z., Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 2006, 40:159-185.
74. Manfredi G., Fu J., Ojaimi J., Sadlock J.E., Kwong J.Q., Guy J., Schon E.A. Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat. Genet. 2002, 30:394-399.
75. Minczuk M., Kolasinska-Zwierz P., Murphy M.P., Papworth M.A. Construction and testing of engineered zinc-finger proteins for sequence-specific modification of mtDNA. Nat. Protoc. 2010, 5:342-356.
76. Minczuk M., Papworth M.A., Kolasinska P., Murphy M.P., Klug A. Sequence-specific modification of mitochondrial DNA using a chimeric zinc finger methylase. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:19689-19694.
77. Minczuk M., Papworth M.A., Miller J.C., Murphy M.P., Klug A. Development of a single-chain, quasi-dimeric zinc-finger nuclease for the selective degradation of mutated human mitochondrial DNA. Nucleic Acids Res. 2008, 36:3926-3938.
78. Mitra S., Izumi T., Boldogh I., Bhakat K.K., Chattopadhyay R., Szczesny B. Intracellular trafficking and regulation of mammalian AP-endonuclease 1 (APE1), an essential DNA repair protein. DNA Repair (Amst.) 2007, 6:461-469.
79. Muratovska A., Lightowlers R.N., Taylor R.W., Turnbull D.M., Smith R.A., Wilce J.A., Martin S.W., Murphy M.P. Targeting peptide nucleic acid (PNA) oligomers to mitochondria within cells by conjugation to lipophilic cations: implications for mitochondrial DNA replication, expression and disease. Nucleic Acids Res. 2001, 29:1852-1863.
80. Nagley P., Farrell L.B., Gearing D.P., Nero D., Meltzer S., Devenish R.J. 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. 1988, 85:2091-2095.
81. Oca-Cossio J., Kenyon L., Hao H., Moraes C.T. Limitations of allotopic expression of mitochondrial genes in mammalian cells. Genetics 2003, 165:707-720.
82. Ojaimi J., Pan J., Santra S., Snell W.J., Schon E.A. An algal nucleus-encoded subunit of mitochondrial ATP synthase rescues a defect in the analogous human mitochondrial-encoded subunit. Mol. Biol. Cell 2002, 13:3836-3844.
83. Paul R., Dalibart R., Lemoine S., Lestienne P. Expression of E. coli RecA targeted to mitochondria of human cells. Mutat. Res. 2001, 486:11-19.
84. Perales-Clemente E., Fernandez-Silva P., Acin-Perez R., Perez-Martos A., Enriquez J.A. Allotopic expression of mitochondrial-encoded genes in mammals: achieved goal, undemonstrated mechanism or impossible task?. Nucleic Acids Res. 2010, 39:225-234.
85. Pinkert C.A., Irwin M.H., Johnson L.W., Moffatt R.J. Mitochondria transfer into mouse ova by microinjection. Transgenic Res. 1997, 6:379-383.
86. Pinkert C.A., Trounce I.A. Production of transmitochondrial mice. Methods 2002, 26:348-357.
87. Rachek L.I., Grishko V.I., Alexeyev M.F., Pastukh V.V., LeDoux S.P., Wilson G.L. Endonuclease III and endonuclease VIII conditionally targeted into mitochondria enhance mitochondrial DNA repair and cell survival following oxidative stress. Nucleic Acids Res. 2004, 32:3240-3247.
88. Rachek L.I., Grishko V.I., Musiyenko S.I., Kelley M.R., LeDoux S.P., Wilson G.L. Conditional targeting of the DNA repair enzyme hOGG1 into mitochondria. J. Biol. Chem. 2002, 277:44932-44937.
89. Rachek L.I., Thornley N.P., Grishko V.I., LeDoux S.P., Wilson G.L. Protection of INS-1 cells from free fatty acid-induced apoptosis by targeting hOGG1 to mitochondria. Diabetes 2006, 55:1022-1028.
90. Randolph-Anderson B.L., Boynton J.E., Gillham N.W., Harris E.H., Johnson A.M., Dorthu M.P., Matagne R.F. Further characterization of the respiratory deficient dum-1 mutation of Chlamydomonas reinhardtii and its use as a recipient for mitochondrial transformation. Mol. Gen. Genet. 1993, 236:235-244.
91. Rasmussen A.K., Rasmussen L.J. Targeting of O6-MeG DNA methyltransferase (MGMT) to mitochondria protects against alkylation induced cell death. Mitochondrion 2005, 5:411-417.
92. Remacle C., Cardol P., Coosemans N., Gaisne M., Bonnefoy N. High-efficiency biolistic transformation of Chlamydomonas mitochondria can be used to insert mutations in complex I genes. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:4771-4776.
93. Schatz G. The protein import system of mitochondria. J. Biol. Chem. 1996, 271:31763-31766.
94. Seibel M., Bachmann C., Schmiedel J., Wilken N., Wilde F., Reichmann H., Isaya G., Seibel P., Pfeiler D. Processing of artificial peptide-DNA-conjugates by the mitochondrial intermediate peptidase (MIP). Biol. Chem. 1999, 380:961-967.
95. Seibel P., Trappe J., Villani G., Klopstock T., Papa S., Reichmann H. Transfection of mitochondria: strategy towards a gene therapy of mitochondrial DNA diseases. Nucleic Acids Res. 1995, 23:10-17.
96. Seo B.B., Nakamaru-Ogiso E., Flotte T.R., Matsuno-Yagi A., Yagi T. In vivo complementation of complex I by the yeast Ndi1 enzyme. Possible application for treatment of Parkinson disease. J. Biol. Chem. 2006, 281:14250-14255.
97. Shinmura K., Yokota J. The OGG1 gene encodes a repair enzyme for oxidatively damaged DNA and is involved in human carcinogenesis. Antioxid. Redox Signal. 2001, 3:597-609.
98. Shokolenko I.N., Alexeyev M.F., Robertson F.M., LeDoux S.P., Wilson G.L. The expression of Exonuclease III from E. coli in mitochondria of breast cancer cells diminishes mitochondrial DNA repair capacity and cell survival after oxidative stress. DNA Repair (Amst.) 2003, 2:471-482.
99. Srivastava S., Moraes C.T. Manipulating mitochondrial DNA heteroplasmy by a mitochondrially targeted restriction endonuclease. Hum. Mol. Genet. 2001, 10:3093-3099.
100. Staudinger M., Bolle N., Kempken F. Mitochondrial electroporation and in organello RNA editing of chimeric atp6 transcripts. Mol. Genet. Genomics 2005, 273:130-136.
101. Staudinger M., Kempken F. Electroporation of isolated higher-plant mitochondria: transcripts of an introduced cox2 gene, but not an atp6 gene, are edited in organello. Mol. Genet. Genomics 2003, 269:553-561.
102. Stevnsner T., Muftuoglu M., Aamann M.D., Bohr V.A. The role of Cockayne Syndrome group B (CSB) protein in base excision repair and aging. Mech. Ageing Dev. 2008, 129:441-448.
103. Swartzlander D.B., Griffiths L.M., Lee J., Degtyareva N.P., Doetsch P.W., Corbett A.H. Regulation of base excision repair: Ntg1 nuclear and mitochondrial dynamic localization in response to genotoxic stress. Nucleic Acids Res. 2010, 38:3963-3974.
104. Szczesny B., Tann A.W., Longley M.J., Copeland W.C., Mitra S. Long patch base excision repair in mammalian mitochondrial genomes. J. Biol. Chem. 2008, 283:26349-26356.
105. Tanaka M., Borgeld H.J., Zhang J., Muramatsu S., Gong J.S., Yoneda M., Maruyama W., Naoi M., Ibi T., Sahashi K., Shamoto M., Fuku N., Kurata M., Yamada Y., Nishizawa K., Akao Y., Ohishi N., Miyabayashi S., Umemoto H., Muramatsu T., Furukawa K., Kikuchi A., Nakano I., Ozawa K., Yagi K. Gene therapy for mitochondrial disease by delivering restriction endonuclease SmaI into mitochondria. J. Biomed. Sci. 2002, 9:534-541.
106. Taylor R.W., Wardell T.M., Smith P.M., Muratovska A., Murphy M.P., Turnbull D.M., Lightowlers R.N. An antigenomic strategy for treating heteroplasmic mtDNA disorders. Adv. Drug Deliv. Rev. 2001, 49:121-125.
107. Vestweber D., Schatz G. DNA-protein conjugates can enter mitochondria via the protein import pathway. Nature 1989, 338:170-172.
108. Vongsamphanh R., Fortier P.K., Ramotar D. Pir1p mediates translocation of the yeast Apn1p endonuclease into the mitochondria to maintain genomic stability. Mol. Cell. Biol. 2001, 21:1647-1655.
109. Weber-Lotfi F., Ibrahim N., Boesch P., Cosset A., Konstantinov Y., Lightowlers R.N., Dietrich A. Developing a genetic approach to investigate the mechanism of mitochondrial competence for DNA import. Biochim. Biophys. Acta 2009, 1787:320-327.
110. Weissig V., D'Souza G.G., Torchilin V.P. DQAsome/DNA complexes release DNA upon contact with isolated mouse liver mitochondria. J. Control. Release 2001, 75:401-408.
111. Weissig V., Lasch J., Erdos G., Meyer H.W., Rowe T.C., Hughes J. DQAsomes: a novel potential drug and gene delivery system made from Dequalinium. Pharm. Res. 1998, 15:334-337.
112. Weissig V., Torchilin V.P. Mitochondriotropic cationic vesicles: a strategy towards mitochondrial gene therapy. Curr. Pharm. Biotechnol. 2000, 1:325-346.
113. Xu H., DeLuca S.Z., O'Farrell P.H. Manipulating the metazoan mitochondrial genome with targeted restriction enzymes. Science 2008, 321:575-577.
114. Yagi T., Seo B.B., Nakamaru-Ogiso E., Marella M., Barber-Singh J., Yamashita T., Kao M.C., Matsuno-Yagi A. Can a single subunit yeast NADH dehydrogenase (Ndi1) remedy diseases caused by respiratory complex I defects?. Rejuvenation Res. 2006, 9:191-197.
115. Yagi T., Seo B.B., Nakamaru-Ogiso E., Marella M., Barber-Singh J., Yamashita T., Matsuno-Yagi A. Possibility of transkingdom gene therapy for complex I diseases. Biochim. Biophys. Acta 2006, 1757:708-714.
116. Yamada Y., Akita H., Kamiya H., Kogure K., Yamamoto T., Shinohara Y., Yamashita K., Kobayashi H., Kikuchi H., Harashima H. MITO-Porter: a liposome-based carrier system for delivery of macromolecules into mitochondria via membrane fusion. Biochim. Biophys. Acta 2008, 1778:423-432.
117. Yasuzaki Y., Yamada Y., Harashima H. Mitochondrial matrix delivery using MITO-Porter, a liposome-based carrier that specifies fusion with mitochondrial membranes. Biochem. Biophys. Res. Commun. 2010, 397:181-186.
118. Yoon Y.G., Koob M.D. Efficient cloning and engineering of entire mitochondrial genomes in Escherichia coli and transfer into transcriptionally active mitochondria. Nucleic Acids Res. 2003, 31:1407-1415.
119. Yoon Y.G., Koob M.D. Transformation of isolated mammalian mitochondria by bacterial conjugation. Nucleic Acids Res. 2005, 33:e139.
120. Yoshida Y., Izumi H., Torigoe T., Ishiguchi H., Itoh H., Kang D., Kohno K. P53 physically interacts with mitochondrial transcription factor A and differentially regulates binding to damaged DNA. Cancer Res. 2003, 63:3729-3734.
121. Zhang H., Mizumachi T., Carcel-Trullols J., Li L., Naito A., Spencer H.J., Spring P.M., Smoller B.R., Watson A.J., Margison G.P., Higuchi M., Fan C.Y. Targeting human 8-oxoguanine DNA glycosylase (hOGG1) to mitochondria enhances cisplatin cytotoxicity in hepatoma cells. Carcinogenesis 2007, 28:1629-1637.
122. Zhou J., Liu L., Chen J. Mitochondrial DNA heteroplasmy in Candida glabrata after mitochondrial transformation. Eukaryot. Cell 2010, 9:806-814.