Prevention of dystrophic pathology in severely affected dystrophin/utrophin-deficient mice by morpholino-oligomer-mediated exon-skipping

Molecular Therapy

Volumn 18, Issue 1, 2010, Pages 198-205

  Goyenvalle, Aurélie ^a   Babbs, Arran ^a   Powell, Dave ^a   Kole, Ryszard ^b   Fletcher, Sue ^c   Wilton, Steve D ^c   Davies, Kay E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b AVI BIOPHARMA INC   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; MESSENGER RNA PRECURSOR; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTISENSE THERAPY; ARTICLE; CONTROLLED STUDY; DRUG DOSE INCREASE; DRUG EFFICACY; DRUG MECHANISM; DUCHENNE MUSCULAR DYSTROPHY; EXON; GENE EXPRESSION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PHENOTYPE; PRIMARY PREVENTION; SYSTEMIC THERAPY;

ANIMALS; DYSTROPHIN; EXONS; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; MICE; MICE, INBRED MDX; MICE, KNOCKOUT; MORPHOLINES; MUSCULAR DYSTROPHY, ANIMAL; PEPTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UTROPHIN;

MUS;

EID: 74149093605     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2009.248     Document Type: Article

References (34)

1. Monaco, AP, Bertelson, CJ, Liechti-Gallati, S, Moser, H and Kunkel, LM (1988). An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2: 90-95.
2. 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.
3. Dunckley, MG, Manoharan, M, Villiet, P, Eperon, IC and Dickson, G (1998). Modifcation of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 7: 1083-1090.
4. Mann, CJ, Honeyman, K, Cheng, AJ, Ly, T, Lloyd, F, Fletcher, S et al. (2001). Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proc Natl Acad Sci USA 98: 42-47.
5. Lu, QL, Mann, CJ, Lou, F, Bou-Gharios, G, Morris, GE, Xue, SA et al. (2003). Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat Med 9: 1009-1014.
6. 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.
7. Kinali, M, Arechavala-Gomeza, V, Feng, L, Cirak, S, Hunt, D et al. (2009). Local restoration of dystrophin expression with the morpholino oligomer AV1-4658 in Duchenne muscular dystrophy: a single-blind, placebo-controlled, dose-escalation, proof-of-concept study. Lancet Neurol 8: 918-928.
8. Alter, J, Lou, F, Rabinowitz, A, Yin, H, Rosenfeld, J, Wilton, SD et al. (2006). Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 12: 175-177.
9. Fletcher, S, Honeyman, K, Fall, AM, Harding, PL, Johnsen, RD and Wilton, SD (2006). Dystrophin expression in the mdx mouse after localised and systemic administration of a morpholino antisense oligonucleotide. J Gene Med 8: 207-216.
10. Yokota, T, Lu, QL, Partridge, T, Kobayashi, M, Nakamura, A, Takeda, S et al. (2009). Effcacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65: 667-676.
11. Fletcher, S, Honeyman, K, Fall, AM, Harding, PL, Johnsen, RD, Steinhaus, JP et al. (2007). Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol Ther 15: 1587-1592.
12. Yin, H, Moulton, HM, Seow, Y, Boyd, C, Boutilier, J, Iverson, P et al. (2008). Cell-penetrating peptide-conjugated antisense oligonucleotides restore systemic muscle and cardiac dystrophin expression and function. Hum Mol Genet 17: 3909-3918.
13. Wu, B, Moulton, HM, Iversen, PL, Jiang, J, Li, J, Li, J et al. (2008). Effective rescue of dystrophin improves cardiac function in dystrophin-defcient mice by a modifed morpholino oligomer. Proc Natl Acad Sci USA 105: 14814-14819.
14. Jearawiriyapaisarn, N, Moulton, HM, Buckley, B, Roberts, J, Sazani, P, Fucharoen, S et al. (2008). Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol Ther 16: 1624-1629.
15. Grady, RM, Teng, H, Nichol, MC, Cunningham, JC, Wilkinson, RS and Sanes, JR (1997). Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90: 729-738.
16. Deconinck, AE, Rafael, JA, Skinner, JA, Brown, SC, Potter, AC, Metzinger, L et al. (1997). Utrophin-dystrophin-defcient mice as a model for Duchenne muscular dystrophy. Cell 90: 717-727.
17. Mann, CJ, Honeyman, K, McClorey, G, Fletcher, S and Wilton, SD (2002). Improved antisense oligonucleotide induced exon skipping in the mdx mouse model of muscular dystrophy. J Gene Med 4: 644-654.
18. Brenman, JE, Chao, DS, Gee, SH, McGee, AW, Craven, SE, Santillano, DR et al. (1996). Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α1-syntrophin mediated by PDZ domains. Cell 84: 757-767.
19. Newey, SE, Benson, MA, Ponting, CP, Davies, KE and Blake, DJ (2000). Alternative splicing of dystrobrevin regulates the stoichiometry of syntrophin binding to the dystrophin protein complex. Curr Biol 10: 1295-1298.
20. Oliver, PL, Keays, DA and Davies, KE (2007). Behavioural characterisation of the robotic mouse mutant. Behav Brain Res 181: 239-247.
21. Qiao, C, Li, J, Jiang, J, Zhu, X, Wang, B, Li, J et al. (2008). Myostatin propeptide gene delivery by adeno-associated virus serotype 8 vectors enhances muscle growth and ameliorates dystrophic phenotypes in mdx mice. Hum Gene Ther 19: 241-254.
22. Wells, DJ (2006). Therapeutic restoration of dystrophin expression in Duchenne muscular dystrophy. J Muscle Res Cell Motil 27: 387-398.
23. Bogdanovich, S, Perkins, KJ, Krag, TO and Khurana, TS (2004). Therapeutics for Duchenne muscular dystrophy: current approaches and future directions. J Mol Med 82: 102-115.
24. Gebski, BL, Mann, CJ, Fletcher, S and Wilton, SD (2003). Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Hum Mol Genet 12: 1801-1811. (Pubitemid 36944135)
25. Lu, QL, Rabinowitz, A, Chen, YC, Yokota, T, Yin, H, Alter, J et al. (2005). Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc Natl Acad Sci USA 102:198-203.
26. Muntoni, F, Mateddu, A, Marchei, F, Clerk, A and Serra, G (1993). Muscular weakness in the mdx mouse. J Neurol Sci 120: 71-77.
27. Hirst, RC, McCullagh, KJ and Davies, KE (2005). Utrophin upregulation in Duchenne muscular dystrophy. Acta Myol 24: 209-216.
28. Malerba, A, Thorogood, FC, Dickson, G and Graham, IR (2009). Dosing regimen has a significant impact on the efficiency of morpholino oligomer-induced exon skipping in mdx mice. Hum Gene Ther 20: 955-965.
29. Gregorevic, P, Allen, JM, Minami, E, Blankinship, MJ, Haraguchi, M, Meuse, L et al. (2006). rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 12: 787-789.
30. Odom, GL, Gregorevic, P, Allen, JM, Finn, E and Chamberlain, JS (2008). Microutrophin delivery through rAAV6 increases lifespan and improves muscle function in dystrophic dystrophin/utrophin-defcient mice. Mol Ther 16: 1539-1545.
31. Wang, B, Li, J, Fu, FH and Xiao, X (2009). Systemic human minidystrophin gene transfer improves functions and life span of dystrophin and dystrophin/ utrophin-defcient mice. J Orthop Res 27: 421-426.
32. Barclay, CJ, Woledge, RC and Curtin, NA (2009). Effects of UCP3 genotype, temperature and muscle type on energy turnover of resting mouse skeletal muscle. Pfugers Arch 457: 857-864.
33. Lynch, GS, Hinkle, RT and Faulkner, JA (2000). Power output of fast and slow skeletal muscles of mdx (dystrophic) and control mice after clenbuterol treatment. Exp Physiol 85: 295-299.
34. Brooks, SV and Faulkner, JA (1988). Contractile properties of skeletal muscles from young, adult and aged mice. J Physiol (Lond) 404: 71-82.