Mitochondrially targeted ZFNs for selective degradation of pathogenic mitochondrial genomes bearing large-scale deletions or point mutations

EMBO Molecular Medicine

Volumn 6, Issue 4, 2014, Pages 458-466

  Gammage, Payam A ^a   Rorbach, Joanna ^a   Vincent, Anna I ^b   Rebar, Edward J ^b   Minczuk, Michal ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b SANGAMO BIOSCIENCES INC   (United States)

Author keywords

Gene therapy; Heteroplasmy; Mitochondrial disease; Zinc finger nuclease

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIALLY TARGETED OBLIGATE HETERODIMERIC ZINC FINGER NUCLEASE; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; DEOXYRIBONUCLEASE;

ARTICLE; ATAXIA; CELLULAR DISTRIBUTION; CHRONIC PROGRESSIVE EXTERNAL OPHTHALMOPLEGIA; CYBRID; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENETIC MANIPULATION; HAPLOTYPE; HETEROPLASMY; HUMAN; HUMAN CELL; KEARNS SAYRE SYNDROME; MITOCHONDRIAL GENE; MITOCHONDRIAL GENOME; MITOCHONDRIAL TARGETING SIGNAL; NEUROPATHY; ONSET AGE; PEARSON SYNDROME; POINT MUTATION; PRIORITY JOURNAL; RESPIRATORY FUNCTION; RETINITIS PIGMENTOSA; WILD TYPE; ENZYMOLOGY; GENE THERAPY; GENETICS; METABOLISM; MITOCHONDRIAL DISEASES; MITOCHONDRION; PROTEIN TRANSPORT;

DEOXYRIBONUCLEASES; DNA, MITOCHONDRIAL; GENETIC THERAPY; GENOME, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; POINT MUTATION; PROTEIN TRANSPORT; SEQUENCE DELETION;

EID: 84898602295     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201303672     Document Type: Article

References (42)

1. Alexeyev MF, Venediktova N, Pastukh V, Shokolenko I, Bonilla G, Wilson GL (2008) Selective elimination of mutant mitochondrial genomes as therapeutic strategy for the treatment of NARP and MILS syndromes. Gene Ther 15: 516-523
2. Bacman SR, Williams SL, Duan D, Moraes CT (2012) Manipulation of mtDNA heteroplasmy in all striated muscles of newborn mice by AAV9-mediated delivery of a mitochondria-targeted restriction endonuclease. Gene Ther 19: 1101-1106
3. Bacman SR, Williams SL, Garcia S, Moraes CT (2010) Organ-specific shifts in mtDNA heteroplasmy following systemic delivery of a mitochondria-targeted restriction endonuclease. Gene Ther 17: 713-720
4. Bacman SR, Williams SL, Moraes CT (2009) Intra- and inter-molecular recombination of mitochondrial DNA after in vivo induction of multiple double-strand breaks. Nucleic Acids Res 37: 4218-4226
5. Bacman SR, Williams SL, Pinto M, Peralta S, Moraes CT. Specific elimination of mutant mitochondrial genomes in patient-derived cells by mitoTALENs. Nat Med (2013) 19: 1111-1113.
6. Bayona-Bafaluy MP, Blits B, Battersby BJ, Shoubridge EA, Moraes CT (2005) Rapid directional shift of mitochondrial DNA heteroplasmy in animal tissues by a mitochondrially targeted restriction endonuclease. Proc Natl Acad Sci USA 102: 14392-14397
7. Carling PJ, Cree LM, Chinnery PF (2011) The implications of mitochondrial DNA copy number regulation during embryogenesis. Mitochondrion 11: 686-692
8. Carroll D, Morton JJ, Beumer KJ, Segal DJ. Design, construction and in vitro testing of zinc finger nucleases. Nat Protoc 2006;1:1329-1341.
9. Carroll J, Fearnley IM, Wang Q, Walker JE Measurement of the molecular masses of hydrophilic and hydrophobic subunits of ATP synthase and complex I in a single experiment. Anal Biochem 2009;395:249-255.
10. Chinnery PF, Johnson MA, Wardell TM, Singh-Kler R, Hayes C, Brown DT, Taylor RW, Bindoff LA, Turnbull DM (2000) The epidemiology of pathogenic mitochondrial DNA mutations. Ann Neurol 48: 188-193
11. Doyon Y, Vo TD, Mendel MC, Greenberg SG, Wang J, Xia DF, Miller JC, Urnov FD, Gregory PD, Holmes MC Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 2011;8:74-79.
12. Ellis BL, Hirsch ML, Porter SN, Samulski RJ, Porteus MH (2013) Zinc-finger nuclease-mediated gene correction using single AAV vector transduction and enhancement by Food and Drug Administration-approved drugs. Gene Ther 20: 35-42
13. Fernandez-Martinez J, Brown CV, Diez E, Tilburn J, Arst HN Jr, Penalva MA, Espeso EA Overlap of nuclear localisation signal and specific DNA-binding residues within the zinc finger domain of PacC. J Mol Biol 2003;334:667-684.
14. Gaj T, Gersbach CA, Barbas CF III. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 2013;31:397-405.
15. Grady JP, Campbell G, Ratnaike T, Blakely EL, Falkous G, Nesbitt V, Schaefer AM, McNally RJ, Gorman GS, Taylor RW et al Disease progression in patients with single, large-scale mitochondrial DNA deletions. Brain DOI 10.1093/brain/awt321
16. Holt IJ, Harding AE, Petty RK, Morgan-Hughes JA A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am J Hum Genet 1990;46:428-433.
17. Kim S, Lee MJ, Kim H, Kang M, Kim JS (2011) Preassembled zinc-finger arrays for rapid construction of ZFNs. Nat Methods 8: 7
18. Kim YG, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci USA 93: 1156-1160
19. Lightowlers RN (2011) Mitochondrial transformation: time for concerted action. EMBO Rep 12: 480-481
20. Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA et al (2008) Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31: 294-301
21. Maniura-Weber K, Goffart S, Garstka HL, Montoya J, Wiesner RJ Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells. Nucleic Acids Res 2004;32:6015-6027.
22. Matheny C, Day ML, Milbrandt J The nuclear localization signal of NGFI-A is located within the zinc finger DNA binding domain. J Biol Chem 1994;269:8176-8181.
23. Miller JC, Holmes MC, Wang J, Guschin DY, Lee YL, Rupniewski I, Beausejour CM, Waite AJ, Wang NS, Kim KA et al (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25: 778-785
24. Minczuk M (2010) Engineered zinc finger proteins for manipulation of the human mitochondrial genome. Methods Mol Biol 649: 257-270
25. Minczuk M, He J, Duch AM, Ettema TJ, Chlebowski A, Dzionek K, Nijtmans LG, Huynen MA, Holt IJ TEFM (c17orf42) is necessary for transcription of human mtDNA. Nucleic Acids Res 2011;39:4284-4299.
26. Minczuk M, Kolasinska-Zwierz P, Murphy MP, Papworth MA Construction and testing of engineered zinc-finger proteins for sequence-specific modification of mtDNA. Nat Protoc 2010;5:342-356.
27. Minczuk M, Papworth MA, Kolasinska P, Murphy MP, Klug A Sequence-specific modification of mitochondrial DNA using a chimeric zinc finger methylase. Proc Natl Acad Sci USA 2006;103:19689-19694.
28. Minczuk M, Papworth MA, Miller JC, Murphy MP, 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.
29. Palpant NJ, Dudzinski D (2013) Zinc finger nucleases: looking toward translation. Gene Ther 20: 121-127
30. Papworth M, Kolasinska P, Minczuk M (2006) Designer zinc-finger proteins and their applications. Gene 366: 27-38
31. Pearson H (2008) Protein engineering: the fate of fingers. Nature 455: 160-164
32. Pfeffer G, Horvath R, Klopstock T, Mootha VK, Suomalainen A, Koene S, Hirano M, Zeviani M, Bindoff LA, Yu-Wai-Man P et al (2013) New treatments for mitochondrial disease-no time to drop our standards. Nat Rev Neurol 9: 474-481
33. Porteous WK, James AM, Sheard PW, Porteous CM, Packer MA, Hyslop SJ, Melton JV, Pang CY, Wei YH, Murphy MP (1998) Bioenergetic consequences of accumulating the common 4977-bp mitochondrial DNA deletion. Eur J Biochem 257: 192-201
34. Rorbach J, Gammage PA, Minczuk M (2012) C7orf30 is necessary for biogenesis of the large subunit of the mitochondrial ribosome. Nucleic Acids Res 40: 4097-4109
35. Sander JD, Dahlborg EJ, Goodwin MJ, Cade L, Zhang F, Cifuentes D, Curtin SJ, Blackburn JS, Thibodeau-Beganny S, Qi Y et al (2011) Selection-free zinc-finger-nuclease engineering by context-dependent assembly (CoDA). Nat Methods 8: 67-69
36. Schaefer AM, McFarland R, Blakely EL, He L, Whittaker RG, Taylor RW, Chinnery PF, Turnbull DM (2008) Prevalence of mitochondrial DNA disease in adults. Ann Neurol 63: 35-39
37. Smith J, Bibikova M, Whitby FG, Reddy AR, Chandrasegaran S, Carroll D (2000) Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Res 28: 3361-3369.
38. Suzuki Y, Holmes JB, Cerritelli SM, Sakhuja K, Minczuk M, Holt IJ, Crouch RJ (2010) An upstream open reading frame and the context of the two AUG codons affect the abundance of mitochondrial and nuclear RNase H1. Mol Cell Biol 30: 5123-5134.
39. Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25: 786-793
40. Tanaka M, Borgeld HJ, Zhang J, Muramatsu S, Gong JS, Yoneda M, Maruyama W, Naoi M, Ibi T, Sahashi K et al (2002) Gene therapy for mitochondrial disease by delivering restriction endonuclease SmaI into mitochondria. J Biomed Sci 9: 534-541
41. Taylor RW, Chinnery PF, Turnbull DM, Lightowlers RN (1997) Selective inhibition of mutant human mitochondrial DNA replication in vitro by peptide nucleic acids. Nat Genet 15: 212-215
42. Vafai SB, Mootha VK (2012) Mitochondrial disorders as windows into an ancient organelle. Nature 491: 374-383