Forelimb Treatment in a Large Cohort of Dystrophic Dogs Supports Delivery of a Recombinant AAV for Exon Skipping in Duchenne Patients

Molecular Therapy

Volumn 22, Issue 11, 2014, Pages 1923-1935

  Le Guiner, Caroline ^a,b   Montus, Marie ^b   Servais, Laurent ^c   Cherel, Yan ^d   Francois, Virginie ^a   Thibaud, Jean Laurent ^e,f   Wary, Claire ^e   Matot, Béatrice ^e   Larcher, Thibaut ^d   Guigand, Lydie ^d   Dutilleul, Maeva ^d   Domenger, Claire ^a   Allais, Marine ^a   Beuvin, Maud ^g   Moraux, Amélie ^c   Le Duff, Johanne ^a   Devaux, Marie ^a   Jaulin, Nicolas ^a   Guilbaud, Mickaël ^a   Latournerie, Virginie ^b   Veron, Philippe ^b   Boutin, Sylvie ^b   Leborgne, Christian ^b   Desgue, Diana ^b   Deschamps, Jack Yves ^d   Moullec, Sophie ^d   Fromes, Yves ^d   Vulin, Adeline ^h   Smith, Richard H ⁱ   Laroudie, Nicolas ^b   Barnay Toutain, Frédéric ^b   Rivière, Christel ^b   Bucher, Stéphanie ^b   Le, Thanh Hoa ^b   Delaunay, Nicolas ^b   Gasmi, Mehdi ^b   Kotin, Robert M ⁱ   Bonne, Gisèle ^g,j   Adjali, Oumeya ^a   Masurier, Carole ^b   Hogrel, Jean Yves ^c   Carlier, Pierre ^e   Moullier, Philippe ^a,b,k   Voit, Thomas ^g   more..

^a UNIVERSITÉ DE NANTES   (France)

^b GÉNÉTHON   (France)

^c Institut de Myologie   (France)

^d LUNAM UNIVERSITÉ   (France)

^e AIM CEA   (France)

^f ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^g INSERM   (France)

^h THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

ⁱ NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^j PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^k UNIVERSITY OF FLORIDA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; PARVOVIRUS VECTOR; SMALL NUCLEAR RNA; U7SNRNA; UNCLASSIFIED DRUG; U7 SMALL NUCLEAR RNA;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; DOG; DOSE RESPONSE; DRUG ADMINISTRATION ROUTE; DRUG TOLERABILITY; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; FORELIMB; GOLDEN RETRIEVER; HISTOPATHOLOGY; LOCOREGIONAL TRANSVENOUS INJECTION; MALE; MUSCLE STRENGTH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN EXPRESSION; RNA VECTOR; SEROTYPE; VIRAL GENE THERAPY; VIRUS RECOMBINANT; ADMINISTRATION AND DOSAGE; ANIMAL; DEPENDOPARVOVIRUS; DISEASE MODEL; EXON; GENE THERAPY; GENE VECTOR; GENETICS; HUMAN; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; MUSCULAR DYSTROPHY, DUCHENNE; PATHOPHYSIOLOGY;

ANIMALS; COHORT STUDIES; DEPENDOVIRUS; DISEASE MODELS, ANIMAL; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; DYSTROPHIN; EXONS; FORELIMB; GENETIC THERAPY; GENETIC VECTORS; HUMANS; INFUSIONS, INTRAVENOUS; MUSCULAR DYSTROPHY, DUCHENNE; RNA, SMALL NUCLEAR;

EID: 84964313862     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.151     Document Type: Article

References (50)

1. Moser, H (1984). Duchenne muscular dystrophy: pathogenetic aspects and genetic prevention. Hum Genet 66: 17-40.
2. Rodino-Klapac, LR, Mendell, JR and Sahenk, Z (2013). Update on the treatment of Duchenne muscular dystrophy. Curr Neurol Neurosci Rep 13: 332.
3. Muntoni, F, Torelli, S and Ferlini, A (2003). Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol 2: 731-740.
4. Aartsma-Rus, A (2012). Overview on DMD exon skipping. Methods Mol Biol 867: 97-116.
5. Echigoya, Y and Yokota, T (2014). Skipping multiple exons of dystrophin transcripts using cocktail antisense oligonucleotides. Nucleic Acid Ther 24: 57-68.
6. Cirak, S, Arechavala-Gomeza, V, Guglieri, M, Feng, L, Torelli, S, Anthony, K 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.
7. Goemans, NM, Tulinius, M, van den Akker, JT, Burm, BE, Ekhart, PF, Heuvelmans, N et al. (2011). Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 364: 1513-1522.
8. Mendell, JR, Rodino-Klapac, LR, Sahenk, Z, Roush, K, Bird, L, Lowes, LP et al.; Eteplirsen Study Group. (2013). Eteplirsen for the treatment of Duchenne muscular dystrophy. Ann Neurol 74: 637-647.
9. Goemans, N (2013). Drisapersen Efficacy and Safety in Duchenne Muscular Dystrophy: Results of a Phase III, Randomized, Double-Blind, Placebo-Controlled Trial (Study DMD114044). World Muscle Society Congress: Late breaking news.
10. Gorman, L, Suter, D, Emerick, V, Schümperli, D and Kole, R (1998). Stable alteration of pre-mRNA splicing patterns by modified U7 small nuclear RNAs. Proc Natl Acad Sci USA 95: 4929-4934.
11. Jiang, H, Pierce, GF, Ozelo, MC, de Paula, EV, Vargas, JA, Smith, P et al. (2006). Evidence of multiyear factor IX expression by AAV-mediated gene transfer to skeletal muscle in an individual with severe hemophilia B. Mol Ther 14: 452-455.
12. Goyenvalle, A, Vulin, A, Fougerousse, F, Leturcq, F, Kaplan, JC, Garcia, L et al. (2004). Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306: 1796-1799.
13. Bish, LT, Sleeper, MM, Forbes, SC, Wang, B, Reynolds, C, Singletary, GE 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.
14. Goyenvalle, A, Babbs, A, Wright, J, Wilkins, V, Powell, D, Garcia, L et al. (2012). Rescue of severely affected dystrophin/utrophin-deficient mice through scAAV-U7snRNAmediated exon skipping. Hum Mol Genet 21: 2559-2571.
15. Vulin, A, Barthélémy, I, Goyenvalle, A, Thibaud, JL, Beley, C, Griffith, G et al. (2012). Muscle function recovery in golden retriever muscular dystrophy after AAV1-U7 exon skipping. Mol Ther 20: 2120-2133.
16. Barbash, IM, Cecchini, S, Faranesh, AZ, Virag, T, Li, L, Yang, Y et al. (2013). MRI roadmap-guided transendocardial delivery of exon-skipping recombinant adenoassociated virus restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Gene Ther 20: 274-282.
17. Kornegay, JN, Bogan, JR, Bogan, DJ, Childers, MK, Li, J, Nghiem, P et al. (2012). Canine models of Duchenne muscular dystrophy and their use in therapeutic strategies. Mamm Genome 23: 85-108.
18. Sharp, NJ, Kornegay, JN, Van Camp, SD, Herbstreith, MH, Secore, SL, Kettle, S et al. (1992). An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 13: 115-121.
19. Su, LT, Gopal, K, Wang, Z, Yin, X, Nelson, A, Kozyak, BW et al. (2005). Uniform scale-independent gene transfer to striated muscle after transvenular extravasation of vector. Circulation 112: 1780-1788.
20. Toromanoff, A, Chérel, Y, Guilbaud, M, Penaud-Budloo, M, Snyder, RO, Haskins, ME et al. (2008). Safety and efficacy of regional intravenous (r.i.) versus intramuscular (i.m.) delivery of rAAV1 and rAAV8 to nonhuman primate skeletal muscle. Mol Ther 16: 1291-1299.
21. Arruda, VR, Stedman, HH, Haurigot, V, Buchlis, G, Baila, S, Favaro, P et al. (2010). Peripheral transvenular delivery of adeno-associated viral vectors to skeletal muscle as a novel therapy for hemophilia B. Blood 115: 4678-4688.
22. Fan, Z, Kocis, K, Valley, R, Howard, JF, Chopra, M, An, H et al. (2012). Safety and feasibility of high-pressure transvenous limb perfusion with 0.9% saline in human muscular dystrophy. Mol Ther 20: 456-461.
23. Nguyen, F, Cherel, Y, Guigand, L, Goubault-Leroux, I and Wyers, M (2002). Muscle lesions associated with dystrophin deficiency in neonatal golden retriever puppies. J Comp Pathol 126: 100-108.
24. Dubowitz, V and Sewry, C (2007). Duchenne and Becker muscular dystrophy. In: Muscle Biopsy: A Practical Approach, 3rd edn. Elsevier: Philadelphia. pp. 297-304.
25. Thibaud, JL, Monnet, A, Bertoldi, D, Barthélémy, I, Blot, S and Carlier, PG (2007). Characterization of dystrophic muscle in golden retriever muscular dystrophy dogs by nuclear magnetic resonance imaging. Neuromuscul Disord 17: 575-584.
26. Wary, C, Naulet, T, Thibaud, JL, Monnet, A, Blot, S and Carlier, PG (2012). Splitting of Pi and other 31P NMR anomalies of skeletal muscle metabolites in canine muscular dystrophy. NMR Biomed 25: 1160-1169.
27. Yokota, T, Lu, QL, Partridge, T, Kobayashi, M, Nakamura, A, Takeda, S et al. (2009). Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65: 667-676.
28. Yokota, T, Nakamura, A, Nagata, T, Saito, T, Kobayashi, M, Aoki, Y et al. (2012). Extensive and prolonged restoration of dystrophin expression with vivo-morpholinomediated multiple exon skipping in dystrophic dogs. Nucleic Acid Ther 22: 306-315.
29. Neri, M, Torelli, S, Brown, S, Ugo, I, Sabatelli, P, Merlini, L et al. (2007). Dystrophin levels as low as 30% are sufficient to avoid muscular dystrophy in the human. Neuromuscul Disord 17: 913-918.
30. Anthony, K, Cirak, S, Torelli, S, Tasca, G, Feng, L, Arechavala-Gomeza, V et al. (2011). Dystrophin quantification and clinical correlations in Becker muscular dystrophy: implications for clinical trials. Brain 134(Pt 12): 3547-3559.
31. Sharp, PS, Bye-a-Jee, H and Wells, DJ (2011). Physiological characterization of muscle strength with variable levels of dystrophin restoration in mdx mice following local antisense therapy. Mol Ther 19: 165-171.
32. van Putten, M, Hulsker, M, Nadarajah, VD, van Heiningen, SH, van Huizen, E, van Iterson, M et al. (2012). The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS ONE 7: e31937.
33. Banks, GB and Chamberlain, JS (2008). The value of mammalian models for duchenne muscular dystrophy in developing therapeutic strategies. Curr Top Dev Biol 84: 431-453.
34. Niemeyer, GP, Herzog, RW, Mount, J, Arruda, VR, Tillson, DM, Hathcock, J et al. (2009). Long-term correction of inhibitor-prone hemophilia B dogs treated with liverdirected AAV2-mediated factor IX gene therapy. Blood 113: 797-806.
35. Bartoli, M, Poupiot, J, Goyenvalle, A, Perez, N, Garcia, L, Danos, O et al. (2006). Noninvasive monitoring of therapeutic gene transfer in animal models of muscular dystrophies. Gene Ther 13: 20-28.
36. Le Hir, M, Goyenvalle, A, Peccate, C, Précigout, G, Davies, KE, Voit, T et al. (2013). AAV genome loss from dystrophic mouse muscles during AAV-U7 snRNA-mediated exon-skipping therapy. Mol Ther 21: 1551-1558.
37. Nowrouzi, A, Penaud-Budloo, M, Kaeppel, C, Appelt, U, Le Guiner, C, Moullier, P et al. (2012). Integration frequency and intermolecular recombination of rAAV vectors in non-human primate skeletal muscle and liver. Mol Ther 20: 1177-1186.
38. Schmidt, WM, Uddin, MH, Dysek, S, Moser-Thier, K, Pirker, C, Höger, H et al. (2011). DNA damage, somatic aneuploidy, and malignant sarcoma susceptibility in muscular dystrophies. PLoS Genet 7: e1002042.
39. Colussi, C, Gurtner, A, Rosati, J, Illi, B, Ragone, G, Piaggio, G et al. (2009). Nitric oxide deficiency determines global chromatin changes in Duchenne muscular dystrophy. FASEB J 23: 2131-2141.
40. Wu, B, Cloer, C, Lu, P, Milazi, S, Shaban, M, Shah, SN et al. (2014). Exon skipping restores dystrophin expression, but fails to prevent disease progression in later stage dystrophic dko mice. Gene Ther. doi:10.1038/gt.2014.53 [Epub ahead of print].
41. Toromanoff, A, Adjali, O, Larcher, T, Hill, M, Guigand, L, Chenuaud, P et al. (2010). Lack of immunotoxicity after regional intravenous (RI) delivery of rAAV to nonhuman primate skeletal muscle. Mol Ther 18: 151-160.
42. Haurigot, V, Mingozzi, F, Buchlis, G, Hui, DJ, Chen, Y, Basner-Tschakarjan, E et al. (2010). Safety of AAV factor IX peripheral transvenular gene delivery to muscle in hemophilia B dogs. Mol Ther 18: 1318-1329.
43. Sherratt, TG, Vulliamy, T, Dubowitz, V, Sewry, CA and Strong, PN (1993). Exon skipping and translation in patients with frameshift deletions in the dystrophin gene. Am J Hum Genet 53: 1007-1015.
44. Mendell, JR, Campbell, K, Rodino-Klapac, L, Sahenk, Z, Shilling, C, Lewis, S et al. (2010). Dystrophin immunity in Duchenne's muscular dystrophy. N Engl J Med 363: 1429-1437.
45. Flanigan, KM, Campbell, K, Viollet, L, Wang, W, Gomez, AM, Walker, CM et al. (2013). Anti-dystrophin T cell responses in Duchenne muscular dystrophy: prevalence and a glucocorticoid treatment effect. Hum Gene Ther 24: 797-806.
46. Smith, RH, Levy, JR and Kotin, RM (2009). A simplified baculovirus-AAV expression vector system coupled with one-step affinity purification yields high-titer rAAV stocks from insect cells. Mol Ther 17: 1888-1896.
47. Le Guiner, C, Moullier, P and Arruda, VR (2011). Biodistribution and shedding of AAV vectors. Methods Mol Biol 807: 339-359.
48. Thibaud, JL, Azzabou, N, Barthelemy, I, Fleury, S, Cabrol, L, Blot, S et al. (2012). Comprehensive longitudinal characterization of canine muscular dystrophy by serial NMR imaging of GRMD dogs. Neuromuscul Disord 22 (suppl. 2): S85-S99.
49. Dueck, MH, Oberthuer, A, Wedekind, C, Paul, M and Boerner, U (2003). Propofol impairs the central but not the peripheral part of the motor system. Anesth Analg 96: 449-55, table of contents.
50. Reiss, J and Rininsland, F (1994). An explanation for the constitutive exon 9 cassette splicing of the DMD gene. Hum Mol Genet 3: 295-298.