Muscle function recovery in golden retriever muscular dystrophy after AAV1-U7 exon skipping

Molecular Therapy

Volumn 20, Issue 11, 2012, Pages 2120-2133

  Vulin, Adeline ^a,b   Barthélémy, Inès ^c   Goyenvalle, Aurélie ^a   Thibaud, Jean Laurent ^c   Beley, Cyriaque ^a   Griffith, Graziella ^a   Benchaouir, Rachid ^a   Le Hir, Maëva ^a   Unterfinger, Yves ^b   Lorain, Stéphanie ^a   Dreyfus, Patrick ^a   Voit, Thomas ^a   Carlier, Pierre ^d   Blot, Stéphane ^a,c   Garcia, Luis ^a  

^a Sorbonne Université   (France)

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

^c UNIVERSITÉ PARIS EST   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; MESSENGER RNA; PARVOVIRUS VECTOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; U7E6 SMALL NUCLEAR RIBONUCLEOPROTEIN; U7E8 SMALL NUCLEAR RINONUCLEOPROTEIN; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOG; DOWN REGULATION; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; IN VITRO STUDY; LIMB PERFUSION; MUSCLE NECROSIS; MUSCLE STRENGTH; MUSCULAR DYSTROPHY; NONHUMAN; SKELETAL MUSCLE; VIRAL GENE THERAPY;

ADENO-ASSOCIATED VIRUS; CANIS FAMILIARIS;

EID: 84869086454     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.181     Document Type: Article

References (52)

1. Hoffman, EP, Brown, RH Jr and Kunkel, LM (1987). Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
2. Chelly, J, Kaplan, JC, Maire, P, Gautron, S and Kahn, A (1988). Transcription of the dystrophin gene in human muscle and non-muscle tissue. Nature 333: 858-860.
3. Bonilla, E, Samitt, CE, Miranda, AF, Hays, AP, Salviati, G, DiMauro, S et al. (1988). Duchenne muscular dystrophy: Deficiency of dystrophin at the muscle cell surface. Cell 54: 447-452.
4. Petrof, BJ, Shrager, JB, Stedman, HH, Kelly, AM and Sweeney, HL (1993). Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710-3714. (Pubitemid 23111437)
5. Emery, AEH (1993). Duchenne Muscular Dystrophy. 2nd edn., 1-392.
6. Cotton, S, Voudouris, NJ and Greenwood, KM (2001). Intelligence and Duchenne muscular dystrophy: Full-scale, verbal, and performance intelligence quotients. Dev Med Child Neurol 43: 497-501. (Pubitemid 32651798)
7. Koenig, M, Hoffman, EP, Bertelson, CJ, Monaco, AP, Feener, C and Kunkel, LM (1987). Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517. (Pubitemid 18098338)
8. Muntoni, F, Torelli, S and Ferlini, A (2003). Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol 2: 731-740. (Pubitemid 37443515)
9. Matsuo, M (1996). Duchenne/Becker muscular dystrophy: From molecular diagnosis to gene therapy. Brain Dev 18: 167-172. (Pubitemid 26253920)
10. Lu, QL, Yokota, T, Takeda, S, Garcia, L, Muntoni, F and Partridge, T (2011). The status of exon skipping as a therapeutic approach to duchenne muscular dystrophy. Mol Ther 19: 9-15.
11. Aartsma-Rus, A (2010). Antisense-mediated modulation of splicing: Therapeutic implications for Duchenne muscular dystrophy. RNA Biol 7: 453-461.
12. 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.
13. 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.
14. Kinali, M, Arechavala-Gomeza, V, Feng, L, Cirak, S, Hunt, D, Adkin, C et al. (2009). Local restoration of dystrophin expression with the morpholino oligomer AVI-4658 in Duchenne muscular dystrophy: A single-blind, placebo-controlled, dose-Escalation, proof-of-concept study. Lancet Neurol 8: 918-928.
15. Van Deutekom, JC, Janson, AA, Ginjaar, IB, Frankhuizen, WS, Aartsma-Rus, A, Bremmer-Bout, M et al. (2007). Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357: 2677-2686.
16. 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. (Pubitemid 28208527)
17. 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. (Pubitemid 39601401)
18. Goyenvalle, A, Babbs, A, van Ommen, GJ, Garcia, L and Davies, KE (2009). Enhanced exon-skipping induced by U7 snRNA carrying a splicing silencer sequence: Promising tool for DMD therapy. Mol Ther 17: 1234-1240.
19. Valentine, BA, Winand, NJ, Pradhan, D, Moise, NS, de Lahunta, A, Kornegay, JN et al. (1992). Canine X-linked muscular dystrophy as an animal model of Duchenne muscular dystrophy: A review. Am J Med Genet 42: 352-356.
20. 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.
21. Barbash, IM, Cecchini, S, Faranesh, AZ, Virag, T, Li, L, Yang, Y et al. (2012). MRI roadmap-guided transendocardial delivery of exon-skipping recombinant adenoassociated virus restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Gene Ther.
22. 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.
23. 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.
24. Schatzberg, SJ, Anderson, LV, Wilton, SD, Kornegay, JN, Mann, CJ, Solomon, GG et al. (1998). Alternative dystrophin gene transcripts in golden retriever muscular dystrophy. Muscle Nerve 21: 991-998. (Pubitemid 28287988)
25. McClorey, G, Moulton, HM, Iversen, PL, Fletcher, S and Wilton, SD (2006). Antisense oligonucleotide-induced exon skipping restores dystrophin expression in vitro in a canine model of DMD. Gene Ther 13: 1373-1381. (Pubitemid 44420632)
26. Blake, DJ, Tinsley, JM and Davies, KE (1996). Utrophin: A structural and functional comparison to dystrophin. Brain Pathol 6: 37-47. (Pubitemid 26078653)
27. Valentine, BA, Cooper, BJ and Gallagher, EA (1989). Intracellular calcium in canine muscle biopsies. J Comp Pathol 100: 223-230. (Pubitemid 19126342)
28. 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. (Pubitemid 46920965)
29. Kornegay, JN, Bogan, DJ, Bogan, JR, Childers, MK, Cundiff, DD, Petroski, GF et al. (1999). Contraction force generated by tarsal joint flexion and extension in dogs with golden retriever muscular dystrophy. J Neurol Sci 166: 115-121. (Pubitemid 29339082)
30. Deconinck, N, Tinsley, J, De Backer, F, Fisher, R, Kahn, D, Phelps, S et al. (1997). Expression of truncated utrophin leads to major functional improvements in dystrophin-Deficient muscles of mice. Nat Med 3: 1216-1221. (Pubitemid 27508821)
31. 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.
32. Schümperli, D and Pillai, RS (2004). The special Sm core structure of the U7 snRNP: Far-reaching significance of a small nuclear ribonucleoprotein. Cell Mol Life Sci 61: 2560-2570. (Pubitemid 39586517)
33. Clerk, A, Morris, GE, Dubowitz, V, Davies, KE and Sewry, CA (1993). Dystrophinrelated protein, utrophin, in normal and dystrophic human fetal skeletal muscle. Histochem J 25: 554-561. (Pubitemid 23248307)
34. Beggs, AH, Hoffman, EP, Snyder, JR, Arahata, K, Specht, L, Shapiro, F et al. (1991). Exploring the molecular basis for variability among patients with Becker muscular dystrophy: Dystrophin gene and protein studies. Am J Hum Genet 49: 54-67. (Pubitemid 21891653)
35. Banks, GB, Gregorevic, P, Allen, JM, Finn, EE and Chamberlain, JS (2007). Functional capacity of dystrophins carrying deletions in the N-Terminal actin-binding domain. Hum Mol Genet 16: 2105-2113. (Pubitemid 47354893)
36. Manno, CS, Chew, AJ, Hutchison, S, Larson, PJ, Herzog, RW, Arruda, VR et al. (2003). AAV-mediated factor IX gene transfer to skeletal muscle in patients with severe hemophilia B. Blood 101: 2963-2972. (Pubitemid 36857981)
37. Chenuaud, P, Larcher, T, Rabinowitz, JE, Provost, N, Joussemet, B, Bujard, H et al. (2004). Optimal design of a single recombinant adeno-Associated virus derived from serotypes 1 and 2 to achieve more tightly regulated transgene expression from nonhuman primate muscle. Mol Ther 9: 410-418. (Pubitemid 38404530)
38. Rivera, VM, Gao, GP, Grant, RL, Schnell, MA, Zoltick, PW, Rozamus, LW et al. (2005). Long-Term pharmacologically regulated expression of erythropoietin in primates following AAV-mediated gene transfer. Blood 105: 1424-1430. (Pubitemid 40223657)
39. Herzog, RW, Hagstrom, JN, Kung, SH, Tai, SJ, Wilson, JM, Fisher, KJ et al. (1997). Stable gene transfer and expression of human blood coagulation factor IX after intramuscular injection of recombinant adeno-Associated virus. Proc Natl Acad Sci USA 94: 5804-5809. (Pubitemid 27241852)
40. Wang, Z, Allen, JM, Riddell, SR, Gregorevic, P, Storb, R, Tapscott, SJ et al. (2007). Immunity to adeno-Associated virus-mediated gene transfer in a random-bred canine model of Duchenne muscular dystrophy. Hum Gene Ther 18: 18-26. (Pubitemid 46105461)
41. Wang, Z, Tapscott, SJ, Chamberlain, JS and Storb, R (2011). Immunity and AAVMediated Gene Therapy for Muscular Dystrophies in Large Animal Models and Human Trials. Front Microbiol 2: 201.
42. Mendell, JR, Rodino-Klapac, LR, Rosales, XQ, Coley, BD, Galloway, G, Lewis, S et al. (2010). Sustained alpha-sarcoglycan gene expression after gene transfer in limb-girdle muscular dystrophy, type 2D. Ann Neurol 68: 629-638.
43. Herson, S, Hentati, F, Rigolet, A, Behin, A, Romero, NB, Leturcq, F et al. (2012). A phase I trial of adeno-Associated virus serotype 1-?-sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C. Brain 135(Pt 2): 483-492.
44. Mingozzi, F, Meulenberg, JJ, Hui, DJ, Basner-Tschakarjan, E, Hasbrouck, NC, Edmonson, SA et al. (2009). AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-Dependent activation of capsid-specific T cells. Blood 114: 2077-2086.
45. Bowles, DE, McPhee, SW, Li, C, Gray, SJ, Samulski, JJ, Camp, AS et al. (2012). Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector. Mol Ther 20: 443-455.
46. 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.
47. Lorain, S, Gross, DA, 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. (Pubitemid 351314994)
48. Kornegay, JN, Li, J, Bogan, JR, Bogan, DJ, Chen, C, Zheng, H et al. (2010). Widespread muscle expression of an AAV9 human mini-Dystrophin vector after intravenous injection in neonatal dystrophin-Deficient dogs. Mol Ther 18: 1501-1508.
49. Romero, NB, Braun, S, Benveniste, O, Leturcq, F, Hogrel, JY, Morris, GE et al. (2004). Phase I study of dystrophin plasmid-based gene therapy in Duchenne/Becker muscular dystrophy. Hum Gene Ther 15: 1065-1076. (Pubitemid 39552288)
50. Hagstrom, JE, Hegge, J, Zhang, G, Noble, M, Budker, V, Lewis, DL et al. (2004). A facile nonviral method for delivering genes and siRNAs to skeletal muscle of mammalian limbs. Mol Ther 10: 386-398. (Pubitemid 39117883)
51. Thibaud, JL, Huss, T, Hegge, J, Thioudellet, C, Granger, N, Gnirs, Ket al. (2006). Intravascular administration of dystrophin plasmid DNA in a canine model of Duchenne Muscular Dsytrophy: early side effects and long term biological efficacy. J Vet Intern Med 20: 1270-1270.
52. Sampaolesi, M, Blot, S, D'Antona, G, Granger, N, Tonlorenzi, R, Innocenzi, A et al. (2006). Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444: 574-579. (Pubitemid 44864430)