Efficacy of systemic morpholino exon-skipping in duchenne dystrophy dogs

Annals of Neurology

Volumn 65, Issue 6, 2009, Pages 667-676

  Yokota, Toshifumi ^a   Lu, Qi Long ^b   Partridge, Terence ^a   Kobayashi, Masanori ^c   Nakamura, Akinori ^c   Takeda, Shin'ichi ^c   Hoffman, Eric ^a,d  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b CAROLINAS MEDICAL CENTER   (United States)

^c NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^d GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; MESSENGER RNA; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER EX6A; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER EX6B; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER EX8A; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; DOG; DRUG EFFICACY; DUCHENNE MUSCULAR DYSTROPHY; EXON; EXON SKIPPING; HUMAN; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; TREATMENT OUTCOME;

ANIMALS; DISEASE MODELS, ANIMAL; DOGS; EXONS; GENE THERAPY; MORPHOLINES; MUSCULAR DYSTROPHY, DUCHENNE; MYOBLASTS, CARDIAC; POINT MUTATION;

EID: 63449141811     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.21627     Document Type: Article

References (32)

1. Hoffman EP, Brown RH Jr, Kunkel LM. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987;51:919-928.
2. Matsumura K, Campbell KP. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 1994;17:2-15.
3. Koenig M, Beggs AH, Moyer M, et al. The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion. Am J Hum Genet 1989;45:498-506.
4. England SB, Nicholson LV, Johnson MA, et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 1990;343:180-182.
5. Dunckley MG, Manoharan M, Villiet P, et al. Modification of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 1998;7:1083-1090.
6. van Deutekom JC, Janson AA, Ginjaar IB, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007;357:2677-2686.
7. Yokota T, Duddy W, Partridge T. Optimizing exon skipping therapies for DMD. Acta Myol 2007;26:179-184.
8. Aartsma-Rus A, Janson AA, Kaman WE, et al. Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 2004;74:83-92.
9. Sharp NJ, Kornegay JN, Van Camp SD, et al. An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 1992;13:115-121.
10. McClorey G, Moulton HM, Iversen PL, et al. Antisense oligonucleotide- induced exon skipping restores dystrophin expression in vitro in a canine model of DMD. Gene Ther 2006;13:1373-1381.
11. Shimatsu Y, Katagiri K, Furuta T, et al. Canine X-linked muscular dystrophy in Japan (CXMDJ). Exp Anim 2003;52:93-97.
12. Summerton J, Weller D. Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev 1997;7:187-195.
13. Yokota T, Takeda S, Lu QL, et al. A renaissance for anti-sense oligonucleotide drugs in neurology: exon-skipping breaks new ground. Arch Neurol 2009;66:32-38.
14. Jankowski RJ, Haluszczak C, Trucco M, Huard J. Flow cytometric characterization of myogenic cell populations obtained via the preplate technique: potential for rapid isolation of muscle-derived stem cells. Hum Gene Ther 2001;12:619-628.
15. Yokota T, Lu QL, Morgan JE, et al. Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J Cell Sci 2006;119:2679-2687.
16. Abramoff MD, Magelhaes PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int 2004;11:36-42.
17. Araishi K, Sasaoka T, Imamura M, et al. Loss of the sarcoglycan complex and sarcospan leads to muscular dystrophy in beta-sarcoglycan-deficient mice. Hum Mol Genet 1999;8:1589-1598.
18. Shimatsu Y, Yoshimura M, Yuasa K, et al. Major clinical and histopathological characteristics of canine X-linked muscular dystrophy in Japan, CXMDJ. Acta Myol 2005;24:145-154.
19. Alter J, Lou F, Rabinowitz A, et al. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 2006;12:175-177.
20. Reiss J, Rininsland F. An explanation for the constitutive exon 9 cassette splicing of the DMD gene. Hum Mol Genet 1994;3:295-298.
21. Aartsma-Rus A, De Winter CL, Janson AA, et al. Functional analysis of 114 exon-internal AONs for targeted DMD exon skipping: indication for steric hindrance of SR protein binding sites. Oligonucleotides 2005;15:284-297.
22. Yoshimura M, Sakamoto M, Ikemoto M, et al. AAV vector-mediated microdystrophin expression in a relatively small percentage of mdx myofibers improved the mdx phenotype. Mol Ther 2004;10:821-828.
23. Liang KW, Nishikawa M, Liu F, et al. Restoration of dystrophin expression in mdx mice by intravascular injection of naked DNA containing full-length dystrophin cDNA. Gene Ther 2004;11:901-908.
24. Yokota T, Pistilli E, Duddy W, Nagaraju K. Potential of oligonucleotide-mediated exon-skipping therapy for Duchenne muscular dystrophy. Exp Opin Biol Ther 2007;7:831-842.
25. Yugeta N UN, Fujii Y, Yoshimura M, et al. Cardiac involvement in Beagle-based canine X-linked muscular dystrophy in Japan (CXMDJ): electrocardiographic, echocardiographic, and morphologic studies. BMC Cardiovasc Disord 2006;6:47.
26. Jearawiriyapaisarn N, Moulton HM, Buckley B, et al. Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol Ther 2008;16:1624-1629.
27. Vannan M, McCreery T, Li P, et al. Ultrasound-mediated transfection of canine myocardium by intravenous administration of cationic microbubble-linked plasmid DNA. J Am Soc Echocardiogr 2002;15:214-218.
28. Fall AM, Johnsen R, Honeyman K, et al. Induction of revertant fibres in the mdx mouse using antisense oligonucleotides. Genet Vaccines Ther 2006;4:3.
29. Aartsma-Rus A, Janson AA, van Ommen GJ, van Deutekom JC. Antisense-induced exon skipping for duplications in Duchenne muscular dystrophy. BMC Med Genet 2007;8:43.
30. Aartsma-Rus A, Kaman WE, Weij R, et al. Exploring the frontiers of therapeutic exon skipping for Duchenne muscular dystrophy by double targeting within one or multiple exons. Mol Ther 2006;14:401-407.
31. Nakamura A, Yoshida K, Fukushima K, et al. Follow-up of three patients with a large in-frame deletion of exons 45-55 in the Duchenne muscular dystrophy (DMD) gene. J Clin Neurosci 2008;15:757-763.
32. Beroud C, Tuffery-Giraud S, Matsuo M, et al. Multiexon skipping leading to an artificial DMD protein lacking amino acids from exons 45 through 55 could rescue up to 63% of patients with Duchenne muscular dystrophy. Hum Mutat 2007;28:196-202.