Dystrophin isoform induction in vivo by antisense-mediated alternative splicing

Molecular Therapy

Volumn 18, Issue 6, 2010, Pages 1218-1223

  Fletcher, Sue ^a   Adams, Abbie M ^a   Johnsen, Russell D ^a   Greer, Kane ^a   Moulton, Hong M ^b   Wilton, Steve D ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER; UNCLASSIFIED DRUG; ISOPROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; GENE SILENCING; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN DOMAIN; RNA PROCESSING; ANIMAL; BIOSYNTHESIS;

ALTERNATIVE SPLICING; ANIMALS; DYSTROPHIN; MICE; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN ISOFORMS;

ANIMALIA; MUS;

EID: 77953128623     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.45     Document Type: Article

References (46)

1. Wilton, SD and Fletcher, S (2006). Modifcation of pre-mRNA processing: application to dystrophin expression. Curr Opin Mol Ther 8: 130-135.
2. Deconinck, N and Dan, B (2007). Pathophysiology of duchenne muscular dystrophy: current hypotheses. Pediatr Neurol 36: 1-7.
3. Doran, P, Wilton, SD, Fletcher, S and Ohlendieck, K (2009). Proteomic profling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 9: 671-685.
4. 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.
5. Goyenvalle, A, Babbs, A, Powell, D, Kole, R, Fletcher, S, Wilton, SD et al. (2010). Prevention of dystrophic pathology in severely affected dystrophin/utrophin-defcient mice by morpholino-oligomer-mediated exon-skipping. Mol Ther 18: 198-205.
6. Aartsma-Rus, A, Bremmer-Bout, M, Janson, AA, den Dunnen, JT, van Ommen, GJ and van Deutekom, JC (2002). Targeted exon skipping as a potential gene correction therapy for Duchenne muscular dystrophy. Neuromuscul Disord 12 Suppl 1: S71-S77.
7. Aartsma-Rus, A, Janson, AA, Kaman, WE, Bremmer-Bout, M, den Dunnen, JT, Baas, F et al. (2003). Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet 12: 907-914.
8. McClorey, G, Fall, AM, Moulton, HM, Iversen, PL, Rasko, JE, Ryan, M et al. (2006). Induced dystrophin exon skipping in human muscle explants. Neuromuscul Disord 16: 583-590.
9. 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.
10. den Dunnen, JT, Bakker, E, Breteler, EG, Pearson, PL and van Ommen, GJ (1987). Direct detection of more than 50% of the Duchenne muscular dystrophy mutations by feld inversion gels. Nature 329: 640-642.
11. Prior, TW, Bartolo, C, Pearl, DK, Papp, AC, Snyder, PJ, Sedra, MS et al. (1995). Spectrum of small mutations in the dystrophin coding region. Am J Hum Genet 57: 22-33.
12. 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.
13. Yokota, T, Duddy, W and Partridge, T (2007). Optimizing exon skipping therapies for DMD. Acta Myol 26: 179-184.
14. Aartsma-Rus, A, Janson, AA, van Ommen, GJ and van Deutekom, JC (2007). Antisense-induced exon skipping for duplications in Duchenne muscular dystrophy. BMC Med Genet 8: 43.
15. Aartsma-Rus, A, Kaman, WE, Weij, R, den Dunnen, JT, van Ommen, GJ and van Deutekom, JC (2006). Exploring the frontiers of therapeutic exon skipping for Duchenne muscular dystrophy by double targeting within one or multiple exons. Mol Ther 14: 401-407.
16. Aartsma-Rus, A, Janson, AA, Kaman, WE, Bremmer-Bout, M, van Ommen, GJ, den Dunnen, JT et al. (2004). Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 74: 83-92.
17. 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.
18. Fall, AM, Johnsen, R, Honeyman, K, Iversen, P, Fletcher, S and Wilton, SD (2006). Induction of revertant fbres in the mdx mouse using antisense oligonucleotides. Genet Vaccines Ther 4: 3.
19. Mitrpant, C, Fletcher, S, Iversen, PL and Wilton, SD (2009). By-passing the nonsense mutation in the 4 CV mouse model of muscular dystrophy by induced exon skipping. J Gene Med 11: 46-56.
20. Corrado, K, Mills, PL and Chamberlain, JS (1994). Deletion analysis of the dystrophin-actin binding domain. FEBS Lett 344: 255-260.
21. 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.
22. Chamberlain, JS, Corrado, K, Rafael, JA, Cox, GA, Hauser, M and Lumeng, C (1997). Interactions between dystrophin and the sarcolemma membrane. Soc Gen Physiol Ser 52: 19-29.
23. Ishikawa-Sakurai, M, Yoshida, M, Imamura, M, Davies, KE and Ozawa, E (2004). ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to beta-dystroglycan. Hum Mol Genet 13: 693-702.
24. Yang, B, Jung, D, Rafael, JA, Chamberlain, JS and Campbell, KP (1995). Identifcation of α-syntrophin binding to syntrophin triplet, dystrophin, and utrophin. J Biol Chem 270: 4975-4978.
25. Crawford, GE, Faulkner, JA, Crosbie, RH, Campbell, K P, Froehner, SC and Chamberlain, JS (2000). Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150: 1399-1410.
26. 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.
27. 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.
28. Yin, H, Lu, Q and Wood, M (2008). Effective exon skipping and restoration of dystrophin expression by peptide nucleic acid antisense oligonucleotides in mdx mice. Mol Ther 16: 38-45.
29. Yin, H, Moulton, HM, Betts, C, Seow, Y, Boutilier, J, Iverson, PL et al. (2009). A fusion peptide directs enhanced systemic dystrophin exon skipping and functional restoration in dystrophin-defcient mdx mice. Hum Mol Genet 18: 4405-4414.
30. 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.
31. Aartsma-Rus, A, Van Deutekom, JC, Fokkema, IF, Van Ommen, GJ and Den Dunnen, JT (2006). Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confrm the reading-frame rule. Muscle Nerve 34: 135-144.
32. Bushby, K, Lynn, S and Straub, T (2009). Collaborating to bring new therapies to the patient-the TREAT-NMD model. Acta Myol 28: 12-15.
33. Mercuri, E, Mayhew, A, Muntoni, F, Messina, S, Straub, V, Van Ommen, GJ et al. (2008). Towards harmonisation of outcome measures for DMD and SMA within TREAT-NMD; report of three expert workshops: TREAT-NMD/ENMC workshop on outcome measures, 12th-13th May 2007, Naarden, The Netherlands; TREAT-NMD workshop on outcome measures in experimental trials for DMD, 30th June-1st July 2007, Naarden, The Netherlands; conjoint Institute of Myology TREAT-NMD meeting on physical activity monitoring in neuromuscular disorders, 11th July 2007, Paris, France. Neuromuscul Disord 18: 894-903.
34. Matsuo, M, Masumura, T, Nishio, H, Nakajima, T, Kitoh, Y, Takumi, T et al. (1991). Exon skipping during splicing of dystrophin mRNA precursor due to an intraexon deletion in the dystrophin gene of Duchenne muscular dystrophy kobe. J Clin Invest 87: 2127-2131.
35. Takeshima, Y, Wada, H, Yagi, M, Ishikawa, Y, Ishikawa, Y, Minami, R et al. (2001). Oligonucleotides against a splicing enhancer sequence led to dystrophin production in muscle cells from a Duchenne muscular dystrophy patient. Brain Dev 23: 788-790.
36. Arora, V, Devi, GR and Iversen, PL (2004). Neutrally charged phosphorodiamidate morpholino antisense oligomers: uptake, effcacy and pharmacokinetics. Curr Pharm Biotechnol 5: 431-439.
37. Heasman, J (2002). Morpholino oligos: making sense of antisense? Dev Biol 243: 209-214.
38. Stein, DA (2008). Inhibition of RNA virus infections with peptide-conjugated morpholino oligomers. Curr Pharm Des 14: 2619-2634.
39. Grounds, MD (2008). Two-tiered hypotheses for Duchenne muscular dystrophy. Cell Mol Life Sci 65: 1621-1625.
40. Errington, SJ, Mann, CJ, Fletcher, S and Wilton, SD (2003). Target selection for antisense oligonucleotide induced exon skipping in the dystrophin gene. J Gene Med 5: 518-527. (Pubitemid 40310395)
41. Adams, AM, Harding, PL, Iversen, PL, Coleman, C, Fletcher, S and Wilton, SD (2007). Antisense oligonucleotide induced exon skipping and the dystrophin gene transcript: cocktails and chemistries. BMC Mol Biol 8: 57.
42. 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)
43. Koenig, M, Monaco, AP and Kunkel, LM (1988). The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53: 219-228.
44. Levine, BA, Moir, AJ, Patchell, VB and Perry, SV (1990). The interaction of actin with dystrophin. FEBS Lett 263: 159-162.
45. Levine, BA, Moir, AJ, Patchell, VB and Perry, SV (1992). Binding sites involved in the interaction of actin with the N-terminal region of dystrophin. FEBS Lett 298: 44-48.
46. Lai, Y, Thomas, GD, Yue, Y, Yang, HT, Li, D, Long, C et al. (2009). Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 119: 624-635