Gene correction of a duchenne muscular dystrophy mutation by meganuclease-enhanced exon knock-in

Human Gene Therapy

Volumn 24, Issue 7, 2013, Pages 692-701

  Popplewell, Linda ^a   Koo, Taeyoung ^a   Leclerc, Xavier ^b   Duclert, Aymeric ^c   Mamchaoui, Kamel ^b   Gouble, Agnés ^c   Mouly, Vincent ^b   Voit, Thomas ^b   Pâques, Frédéric ^c   Cédrone, Frédéric ^c   Isman, Olga ^a   Yáñez Muñoz, Rafael J ^a   Dickson, George ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b SORBONNE UNIVERSITÉ   (France)

^c Arvid Wallgrens Backe 20   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; LENTIVIRUS VECTOR; MEGANUCLEASE; MESSENGER RNA; NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; DUCHENNE MUSCULAR DYSTROPHY; ENZYME ACTIVITY; EXON; GENE DELETION; GENE LOCATION; GENE MUTATION; GENE SEQUENCE; GENE TARGETING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; INTRON; MYOBLAST; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RECOMBINATION REPAIR; VIRAL GENE THERAPY; WESTERN BLOTTING; X CHROMOSOME;

BLOTTING, WESTERN; DEOXYRIBONUCLEASES; DNA REPAIR; EXONS; GENE KNOCK-IN TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INDEL MUTATION; LENTIVIRUS; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION; MYOBLASTS; OLIGONUCLEOTIDES, ANTISENSE; TARGETED GENE REPAIR;

EID: 84880581726     PISSN: 10430342     EISSN: 15577422     Source Type: Journal    
DOI: 10.1089/hum.2013.081     Document Type: Article

References (39)

1. Arnoud, S., Perez, C., Cabaniols, J.P., et al. (2007). Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells. J. Mol. Biol. 371, 49-65.
2. Beytía, M. de los Angeles, Vry, J., and Kirschner, J. (2012). Drug treatment of Duchenne muscular dystrophy: Available evidence and perspectives. Acta Myol. 31, 4-8.
3. Carroll, D. (2011). Genome engineering with zinc-finger nucleases. Genetics 188, 773-782.
4. Chapdelaine, P., Pichavant, C., Rousseau, J., et al. (2010). Meganucleases can restore the reading frame of a mutated dystrophin. Gene Ther. 17, 846-858.
5. Chaouch, S., Mouly, V., Goyenvalle, A., et al. (2009). Immortalized skin fibroblasts expressing conditional MyoD as a renewable and reliable source of converted human muscle cells to assess therapeutic strategies for muscular dystrophies: Validation of an exon-skipping approach to restore dystrophin in Duchenne muscular dystrophy cells. Hum. Gene Ther. 20, 784-790.
6. Choulika, A., Perrin, A., Dujon, B., and Nicolas, J.F. (1995). Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol. Cell. Biol. 15, 1968-1973.
7. Cirak, S., Arechavala-Gomeza, V., Guglieri, M., et al. (2011). Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: An open-label, phase 2, dose-escalation study. Lancet 378, 595-605.
8. Daboussi, F., Zaslavskly, M., Poirot, L., et al. (2012) Chromosomal context and epigenetic mechanisms control the efficacy of genome editing by rare-cutting endonucleases. Nucleic Acids Res. 40, 6367-6379.
9. Goemans, N.M., Tulinius, M., van den Akker, J.T., et al. (2011). Systemic administration of PRO051 in Duchenne's muscular dystrophy. N. Engl. J. Med. 364, 1513-1522.
10. Goyenvalle, A., Babbs, A., Wright, J., et al. (2012). Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNA-mediated exon skipping. Hum. Mol. Genet. 21, 2559-2571.
11. Grizot, S., Smith, J., Daboussi, F., et al. (2009). Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res. 37, 5405-5419.
12. Grizot, S., Duclert, A., Thomas, S., et al. (2011). Context dependence between subdomains in the DNA binding interface of the I-CreI homing endonuclease. Nucleic Acids Res. 39, 6124-6136.
13. Herzog, R.W. (2007). Immune responses to AAV capsid: Are mice not humans after all? Mol. Ther. 15, 649-650.
14. Jacome, A., Navarro, S., Rio, P., et al. (2009) Lentiviral mediated genetic correction of hematopoietic and mesenchymal progenitor cells from Fanconi anemia patients. Mol. Ther. 17, 1083-1092.
15. Jearawiriyapaisarn, N., Moulton, H.M., Buckley, B., et al. (2008). Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol. Ther. 16, 1624-1629.
16. Jensen, N.M., Dalsgaard, T., Jakobsen, M., et al. (2011). An update on targeted gene repair in mammalian cells: Methods and mechanisms. J. Biomed. Sci. 1, 10.
17. Li, H., Haurigot, V., Doyon, Y., et al. (2011). In vivo genome editing restores haemostasis in a mouse model of haemophilia. Nature 47, 217-221.
18. Li, Y.H., Wang, X., Pan, Y., et al. (2012). Inhibition of non-homologous end joining repair impairs pancreatic cancer growth and enhances radiation response. PLoS One 7, e39588.
19. Liu, M., Yue, Y., Harper, S.Q., et al. (2005). Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle from contraction-induced injury. Mol. Ther. 11, 245-256.
20. Lombardo, A., Genovese, P., Beausejour, C.M., et al. (2007). Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat. Biotechnol. 25, 1298-1306.
21. Longhese, M.P., Bonetti, D., Manfrini, N., and Clerici, M. (2010). Mechanisms and regulation of DNA end resection. EMBO J. 29, 2864-2874.
22. Martin, S.A., Lord, C.J., and Ashworth, A. (2010). Therapeutic targeting of the DNA mismatch repair pathway. Clin. Cancer Res. 16, 5107-5113.
23. Muntoni, F., Torelli, S., and Ferlini, A. (2003). Dystrophin and mutations: One gene, several proteins, multiple phenotypes. Lancet Neurol. 2, 731-740.
24. Paques, F., and Duchateau, P. (2007). Meganucleases and DNA double-strand break-induced recombination: Perspectives for gene therapy. Curr. Gene Ther. 7, 49-66.
25. Peng, G., and Lin, S.Y. (2011). Exploiting the homologous recombination DNA repair network for targeted cancer therapy. World J. Clin. Oncol. 2, 73-79.
26. Pichavant, C., and Tremblay, J.P. (2012). Generation of lentiviral vectors for use in skeletal muscle research. Methods Mol. Biol. 798, 285-295.
27. Popplewell, L.J., Adkin, C., Arechavala-Gomeza, V., et al. (2010). Comparative analysis of antisense oligonucleotide sequences targeting exon 53 of the human DMD gene: Implications for future clinical trials. Neuromuscul. Disord. 20, 102-110.
28. Popplewell, L.J., Graham, I.R., Malerba, A., and Dickson, G. (2011). Bioinformatic and functional optimization of antisense phosphorodiamidate morpholino oligomers (PMOs) for therapeutic modulation of RNA splicing in muscle. Methods Mol. Biol. 709, 153-178.
29. Rouet, P., Smith, F., and Jasin, M. (1994). Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14, 8096-8106.
30. Schnepp, B.C., Clark, K.R., Klemanski, D.L., et al. (2003). Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J. Virol. 77, 3495-3504.
31. Seth, P., Miller, H.B., Lasda, E.L., et al. (2008). Identification of an intronic splicing enhancer essential for the inclusion of FGFR2 exon IIIc. J. Biol. Chem. 283, 10058-10067.
32. Shapiro, M.B., and Senapathy, P. (1987). RNA splice junctions of different classes of eukaryotes: Sequence statistics and functional implications in gene expression. Nucleic Acids Res. 15, 7155-7174.
33. Smith, J., Grizot, S., Arnould, S., et al. (2006). A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res. 34, e149.
34. Urnov, F.D., Miller, J.C., Lee, Y.L., et al. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651.
35. Wang, Z., Allen, J.M., Riddell, S.R., et al. (2007a). Immunity to adeno-associated virus-mediated gene transfer in a randombred canine model of Duchenne muscular dystrophy. Hum. Gene Ther. 18, 18-26.
36. Wang, Z., Kuhr, C.S., Allen, J.M., et al. (2007b). Sustained AAV mediated dystrophin expression in a canine model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol. Ther. 15, 1160-1166.
37. Welch, E.M., Barton, E.R., Zhuo, J., et al. (2007). PTC124 targets genetic disorders caused by nonsense mutations. Nature 447, 87-91.
38. Wilton, S. (2007). PTC124, nonsense mutations and Duchenne muscular dystrophy. Neuromuscul. Disord. 17, 719-720.
39. Yáñez-Muñoz, R.J., Balaggan, K.S., MacNeil, A., et al. (2006). Effective gene therapy with nonintegrating lentiviral vectors. Nat. Med. 12, 348-353.