Antisense pre-treatment increases gene therapy efficacy in dystrophic muscles

Human Molecular Genetics

Volumn 25, Issue 16, 2016, Pages 3555-3563

  Peccate, Cécile ^a   Mollard, Amédée ^a   Le Hir, Mäeva ^b   Julien, Laura ^a   McClorey, Graham ^c   Jarmin, Susan ^d   Le Heron, Anita ^d   Dickson, George ^d   Benkhelifa Ziyyat, Sofia ^a   Piétri Rouxel, France ^a   Wood, Matthew J ^c   Voit, Thomas ^a,e   Lorain, Stéphanie ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENO ASSOCIATED VIRUS VECTOR; COMPLEMENTARY DNA; DYSTROPHIN; MORPHOLINO OLIGONUCLEOTIDE; ANTISENSE OLIGONUCLEOTIDE;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS 7; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTISENSE THERAPY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; GENE TRANSFER; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPHYLAXIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SARCOLEMMA; SINGLE DRUG DOSE; THERAPY EFFECT; TISSUE SECTION; VIRAL GENE THERAPY; VIRUS GENOME; WESTERN BLOTTING; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; DRUG EFFECTS; EXON; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; PATHOLOGY; SKELETAL MUSCLE;

ANIMALS; DEPENDOVIRUS; DYSTROPHIN; EXONS; GENE TRANSFER TECHNIQUES; GENETIC THERAPY; GENETIC VECTORS; HUMANS; MICE, INBRED MDX; MORPHOLINOS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; OLIGONUCLEOTIDES, ANTISENSE; SARCOLEMMA;

EID: 85014380396     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw201     Document Type: Article

References (36)

1. Harper, S.Q., Hauser, M.A., DelloRusso, C., Duan, D., Crawford, R.W., Phelps, S.F., Harper, H.A., Robinson, A.S., Engelhardt, J.F., Brooks, S.V. and Chamberlain, J.S. (2002) Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat. Med., 8, 253-261.
2. Gregorevic, P., Allen, J.M., Minami, E., Blankinship, M.J., Haraguchi, M., Meuse, L., Finn, E., Adams, M.E., Froehner, S.C., Murry, C.E. and Chamberlain, J.S. (2006) rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat. Med., 12, 787-789.
3. Koo, T., Okada, T., Athanasopoulos, T., Foster, H., Takeda, S. and Dickson, G. (2011) Long-term functional adenoassociated virus-microdystrophin expression in the dystrophic CXMDj dog. J. Gene Med., 13, 497-506.
4. Shin, J.H., Pan, X., Hakim, C.H., Yang, H.T., Yue, Y., Zhang, K., Terjung, R.L. and Duan, D. (2013) Microdystrophin ameliorates muscular dystrophy in the canine model of duchenne muscular dystrophy. Mol. Ther., 21, 750-757.
5. Mendell, J.R., Campbell, K., Rodino-Klapac, L., Sahenk, Z., Shilling, C., Lewis, S., Bowles, D., Gray, S., Li, C., Galloway, G., et al. (2010) Dystrophin immunity in Duchenne's muscular dystrophy. N. Engl. J. Med., 363, 1429-1437.
6. Goemans, N.M., Tulinius, M., van den Akker, J.T., Burm, B.E., Ekhart, P.F., Heuvelmans, N., Holling, T., Janson, A.A., Platenburg, G.J., Sipkens, J.A., et al. (2011) Systemic administration of PRO051 in Duchenne's muscular dystrophy. N. Engl. J. Med., 364, 1513-1522.
7. Cirak, S., Arechavala-Gomeza, V., Guglieri, M., Feng, L., Torelli, S., Anthony, K., Abbs, S., Garralda, M.E., Bourke, J., Wells, D.J., 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. Mendell, J.R., Rodino-Klapac, L.R., Sahenk, Z., Roush, K., Bird, L., Lowes, L.P., Alfano, L., Gomez, A.M., Lewis, S., Kota, J., et al. (2013) Eteplirsen for the treatment of Duchenne muscular dystrophy. Ann. Neurol., 74, 637-647.
9. Voit, T., Topaloglu, H., Straub, V., Muntoni, F., Deconinck, N., Campion, G., de Kimpe, S.J., Eagle, M., Guglieri, M., Hood, S., et al. (2014) Safety and efficacy of drisapersen for the treatment of Duchenne muscular dystrophy (DEMAND II): an exploratory, randomised, placebo-controlled phase 2 study. Lancet Neurol., 13, 987-996.
10. Goyenvalle, A., Griffith, G., Babbs, A., El Andaloussi, S., Ezzat, K., Avril, A., Dugovic, B., Chaussenot, R., Ferry, A., Voit, T., et al. (2015) Functional correction in mouse models of muscular dystrophy using exon-skipping tricyclo-DNA oligomers. Nat. Med., 21, 270-275.
11. Betts, C., Saleh, A.F., Arzumanov, A.A., Hammond, S.M., Godfrey, C., Coursindel, T., Gait, M.J. and Wood, M.J. (2012) Pip6-PMO, A New Generation of Peptide-oligonucleotide Conjugates With Improved Cardiac Exon Skipping Activity for DMD Treatment. Mol. Ther. Nucleic Acids, 1, e38.
12. Betts, C.A., Saleh, A.F., Carr, C.A., Hammond, S.M., Coenen-Stass, A.M., Godfrey, C., McClorey, G., Varela, M.A., Roberts, T.C., Clarke, K., et al. (2015) Prevention of exercised induced cardiomyopathy following Pip-PMO treatment in dystrophic mdx mice. Sci. Rep., 5, 8986.
13. Brun, C., Suter, D., Pauli, C., Dunant, P., Lochmuller, H., Burgunder, J.M., Schumperli, D. and Weis, J. (2003) U7 snRNAs induce correction of mutated dystrophin pre-mRNA by exon skipping. Cell Mol. Life Sci., 60, 557-566.
14. Goyenvalle, A., Vulin, A., Fougerousse, F., Leturcq, F., Kaplan, J.C., Garcia, L. and Danos, O. (2004) Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science, 306, 1796-1799.
15. Denti, M.A., Rosa, A., D'Antona, G., Sthandier, O., De Angelis, F.G., Nicoletti, C., Allocca, M., Pansarasa, O., Parente, V., Musaro, A., et al. (2006) Chimeric adeno-associated virus/antisense U1 small nuclear RNA effectively rescues dystrophin synthesis and muscle function by local treatment of mdx mice. Hum. Gene Ther., 17, 565-574
16. Goyenvalle, A., Babbs, A., Wright, J., Wilkins, V., Powell, D., Garcia, L. and Davies, K.E. (2012) Rescue of severely affected dystrophin/utrophin-deficient mice through scAAVU7snRNA-mediated exon skipping. Hum. Mol. Genet., 21, 2559-2571.
17. Bish, L.T., Sleeper, M.M., Forbes, S.C., Wang, B., Reynolds, C., Singletary, G.E., Trafny, D., Morine, K.J., Sanmiguel, J., Cecchini, S., et al. (2012) Long-term restoration of cardiac dystrophin expression in golden retriever muscular dystrophy following rAAV6-mediated exon skipping. Mol. Ther., 20, 580-589.
18. Vulin, A., Barthelemy, I., Goyenvalle, A., Thibaud, J.L., Beley, C., Griffith, G., Benchaouir, R., Le Hir, M., Unterfinger, Y., Lorain, S., et al. (2012) Muscle function recovery in golden retriever muscular dystrophy after AAV1-U7 exon skipping. Mol. Ther., 20, 2120-2133.
19. Le Guiner, C., Montus, M., Servais, L., Cherel, Y., Francois, V., Thibaud, J.L., Wary, C., Matot, B., Larcher, T., Guigand, L., et al. (2014) Forelimb treatment in a large cohort of dystrophic dogs supports delivery of a recombinant AAV for exon skipping in Duchenne patients. Mol. Ther., 22, 1923-1935.
20. Le Hir, M., Goyenvalle, A., Peccate, C., Precigout, G., Davies, K.E., Voit, T., Garcia, L. and Lorain, S. (2013) AAV Genome Loss From Dystrophic Mouse Muscles During AAV-U7 snRNA-mediated Exon-skipping Therapy. Mol. Ther., 21, 1551-1558.
21. Lorain, S., Gross, D.A., Goyenvalle, A., Danos, O., Davoust, J. and Garcia, L. (2008) Transient immunomodulation allows repeated injections of AAV1 and correction of muscular dystrophy in multiple muscles. Mol. Ther., 16, 541-547.
22. Aartsma-Rus, A., Fokkema, I., Verschuuren, J., Ginjaar, I., van Deutekom, J., van Ommen, G.J. and den Dunnen, J.T. (2009) Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum. Mutat., 30, 293-299.
23. Sicinski, P., Geng, Y., Ryder-Cook, A.S., Barnard, E.A., Darlison, M.G. and Barnard, P.J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science, 244, 1578-1580.
24. Foster, H., Sharp, P.S., Athanasopoulos, T., Trollet, C., Graham, I.R., Foster, K., Wells, D.J. and Dickson, G. (2008) Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol. Ther, 16, 1825-1832.
25. Deconinck, A.E., Rafael, J.A., Skinner, J.A., Brown, S.C., Potter, A.C., Metzinger, L., Watt, D.J., Dickson, J.G., Tinsley, J.M. and Davies, K.E. (1997) Utrophin-dystrophin-deficient mice as amodel for Duchenne muscular dystrophy. Cell, 90, 717-727.
26. Grady, R.M., Teng, H., Nichol, M.C., Cunningham, J.C., Wilkinson, R.S. and Sanes, J.R. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell, 90, 729-738.
27. Valentine, B.A., Winand, N.J., Pradhan, D., Moise, N.S., de Lahunta, A., Kornegay, J.N. and Cooper, B.J. (1992) Canine Xlinked muscular dystrophy as an animal model of Duchenne muscular dystrophy: a review. Am. J. Med. Genet., 42, 352-356.
28. Louboutin, J.P., Wang, L. and Wilson, J.M. (2005) Gene transfer into skeletal muscle using novel AAV serotypes. J. Gene Med., 7, 442-451.
29. Wang, Z., Storb, R., Halbert, C.L., Banks, G.B., Butts, T.M., Finn, E.E., Allen, J.M., Miller, A.D., Chamberlain, J.S. and Tapscott, S.J. (2012) Successful regional delivery and longterm expression of a dystrophin gene in canine muscular dystrophy: a preclinical model for human therapies. Mol. Ther., 20, 1501-1507.
30. Yuasa, K., Sakamoto, M., Miyagoe-Suzuki, Y., Tanouchi, A., Yamamoto, H., Li, J., Chamberlain, J.S., Xiao, X. and Takeda, S. (2002) Adeno-associated virus vector-mediated gene transfer into dystrophin-deficient skeletal muscles evokes enhanced immune response against the transgene product. Gene Ther., 9, 1576-1588.
31. Straub, V., Rafael, J.A., Chamberlain, J.S. and Campbell, K.P. (1997) Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol., 139, 375-385.
32. Cea, L.A., Puebla, C., Cisterna, B.A., Escamilla, R., Vargas, A.A., Frank, M., Martinez-Montero, P., Prior, C., Molano, J., Esteban-Rodriguez, I., et al. (2016) Fast skeletal myofibers of mdx mouse, model of Duchenne muscular dystrophy, express connexin hemichannels that lead to apoptosis. Cell Mol. Life Sci, 73(13):2583-2599.
33. Maguire, C.A., Balaj, L., Sivaraman, S., Crommentuijn, M.H., Ericsson, M., Mincheva-Nilsson, L., Baranov, V., Gianni, D., Tannous, B.A., Sena-Esteves, M., et al. (2012) Microvesicle-associated AAV vector as a novel gene delivery system. Mol. Ther., 20, 960-971.
34. Duguez, S., Duddy, W., Johnston, H., Laine, J., Le Bihan, M.C., Brown, K.J., Bigot, A., Hathout, Y., Butler-Browne, G. and Partridge, T. (2013) Dystrophin deficiency leads to disturbance of LAMP1-vesicle-associated protein secretion. Cell Mol. Life Sci., 70, 2159-2174.
35. Dupont, J.B., Tournaire, B., Georger, C., Marolleau, B., Jeanson-Leh, L., Ledevin, M., Lindenbaum, P., Lecomte, E., Cogne, B., Dubreil, L., et al. (2015) Short-lived recombinant adeno-associated virus transgene expression in dystrophic muscle is associated with oxidative damage to transgene mRNA. Mol. Ther. Methods Clin. Dev., 2, 15010.
36. Bartlett, R.J., Stockinger, S., Denis, M.M., Bartlett, W.T., Inverardi, L., Le, T.T., thi Man, N., Morris, G.E., Bogan, D.J., Metcalf-Bogan, J. and Kornegay, J.N. (2000) In vivo targeted repair of a point mutation in the canine dystrophin gene by a chimeric RNA/DNA oligonucleotide. Nat. Biotechnol., 18, 615-622.