Antisense suppression of donor splice site mutations in the dystrophin gene transcript

Molecular Genetics and Genomic Medicine

Volumn 1, Issue 3, 2013, Pages 162-173

  Fletcher, Sue ^a,b   Meloni, Penny L ^b   Johnsen, Russell D ^b   Wong, Brenda L ^c   Muntoni, Francesco ^d   Wilton, Stephen D ^a,b  

^a MURDOCH UNIVERSITY   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Duchenne muscular dystrophy; Exonskipping; Splice mutation; Splice switchingoligomer

Indexed keywords

EID: 84932147351     PISSN: None     EISSN: 23249269     Source Type: Journal    
DOI: 10.1002/mgg3.19     Document Type: Article

References (48)

1. Aartsma-Rus, A., I. Fokkema, J. Verschuuren, I. Ginjaar, J. van Deutekom, G. J. van Ommen, et al. 2009. Theoreticapplicability of antisense-mediated exon skipping forDuchenne muscular dystrophy mutations. Hum. Mutat.30:293–299.
2. Adachi, K., Y. Takeshima, H. Wada, M. Yagi, H. Nakamura, and M. Matsuo. 2003. Heterogous dystrophin mRNAproduced by a novel splice acceptor site mutation inintermediate dystrophinopathy. Pediatr. Res. 53:125–131.
3. Adams, A. M., P. L. Harding, P. L. Iversen, C. Coleman, S. Fletcher, and S. D. Wilton. 2007. Antisense oligonucleotideinduced exon skipping and the dystrophin gene transcript:cocktails and chemistries. BMC Mol. Biol. 8:57.
4. Adkin, C. F., P. L. Meloni, S. Fletcher, A. M. Adams, F. Muntoni, B. Wong, et al. 2012. Multiple exon skipping strategies to by-pass dystrophin mutations. Neuromuscul. Disord. 22:297–305.
5. Arechavala-Gomeza, V., I. R. Graham, L. J. Popplewell, A. M. Adams, A. Aartsma-Rus, M. Kinali, et al. 2007. Comparativeanalysis of antisense oligonucleotide sequences for targetedskipping of exon 51 during dystrophin Pre-MRNA splicingin human muscle. Hum. Gene Ther. 18:798–810.
6. Baralle, D., and M. Baralle. 2005. Splicing in action: assessingdisease causing sequence changes. J. Med. Genet. 42:737–748.
7. Baralle, D., A. Lucassen, and E. Buratti. 2009. Missed threads.the impact of pre-mRNA splicing defects on clinicalpractice. EMBO Rep. 10:810–816.
8. Buratti, E., M. Chivers, J. Kralovicova, M. Romano, M. Baralle, A. R. Krainer, et al. 2007. Aberrant 5’ splice sites inhuman disease genes: mutation pattern, nucleotide structureand comparison of computational tools that predict theirutilization. Nucleic Acids Res. 35:4250–4263.
9. Cirak, S., V. Arechavala-Gomeza, M. Guglieri, L. Feng, S. Torelli, K. Anthony, et al. 2011. Exon skipping and dystrophin restoration in patients with Duchenne musculardystrophy after systemic phosphorodiamidate morpholinooligomer treatment: an open-label, phase 2, dose-escalationstudy. Lancet 378:595–605.
10. Cooper, S. T., H. P. Lo, and K. N. North. 2003. Single sectionWestern blot: improving the molecular diagnosis of themuscular dystrophies. Neurology 61:93–97.
11. Davidson, L., A. Kerr, and S. West. 2012. Co-transcriptionaldegradation of aberrant pre-mRNA by Xrn2. EMBO J.31:2566–2578.
12. De Conti, L., N. Skoko, E. Buratti, and M. Baralle. 2012. Complexities of 5’splice site definition: implications in clinical analyses. RNA Biol. 9:911–923.
13. van Deutekom, J. C., and G. J. van Ommen. 2003. Advancesin Duchenne muscular dystrophy gene therapy. Nat. Rev.Genet. 4:774–783.
14. van Deutekom, J. C., A. A. Janson, I. B. Ginjaar, W. S. Frankhuizen, A. Aartsma-Rus, M. Bremmer-Bout, et al. 2007. Local dystrophin restoration with antisenseoligonucleotide PRO051. N. Engl. J. Med. 357:2677–2686.
15. Dominski, Z., and R. Kole. 1993. Restoration of correctsplicing in thalassemic pre-mRNA by antisense oligonucleotides. Proc. Natl. Acad. Sci. USA 90:8673–8677.
16. Emery, A. E. 2002. The muscular dystrophies. Lancet 359:687–695.
17. Fernandez-Cadenas, I., A. L. Andreu, J. Gamez, R. Gonzalo, M. A. Martin, J. C. Rubio, et al. 2003. Splicing mosaic ofthe myophosphorylase gene due to a silent mutation in McArdle disease. Neurology 61:1432–1434.
18. Fletcher, S., K. Honeyman, A. M. Fall, P. L. Harding, R. D. Johnsen, and S. D. Wilton. 2006. Dystrophin expression inthe mdx mouse after localised and systemic administrationof a morpholino antisenseoligonucleotide. J. Gene Med.8:207–216.
19. Forrest, S., P. L. Meloni, F. Muntoni, J. Kim, S. Fletcher, and S. D. Wilton. 2010. Personalized exon skipping strategies toaddress clustered non-deletion dystrophin mutations. Neuromuscul. Disord. 20:810–816.
20. Fragall, C. T., A. M. Adams, R. D. Johnsen, R. Kole, S. Fletcher, and S. D. Wilton. 2011. Mismatched singlestranded antisense oligonucleotides can induce efficientdystrophin splice switching. BMC Med. Genet. 12:141.
21. Goemans, N. M., M. Tulinius, J. T. van den Akker, B. E. Burm, P. F. Ekhart, N. Heuvelmans, et al. 2011. Systemicadministration of pro051 in duchenne’s muscular dystrophy. N. Engl. J. Med. 364:1513–1522.
22. Gurvich, O. L., T. M. Tuohy, M. T. Howard, R. S. Finkel, L. Medne, C. B. Anderson, et al. 2008. DMD pseudoexonmutations: splicing efficiency, phenotype, and potentialtherapy. Ann. Neurol. 63:81–89.
23. Harding, P. L., A. M. Fall, K. Honeyman, S. Fletcher, and S. D. Wilton. 2006. The influence of antisenseoligonucleotide length on dystrophin exon skipping. Mol.Ther. 15:157–166.
24. Jearawiriyapaisarn, N., H. M. Moulton, B. Buckley, J. Roberts, P. Sazani, S. Fucharoen, et al. 2008. Sustained dystrophinexpression induced by peptide-conjugated morpholinooligomers in the muscles of mdx mice. Mol. Ther. 16:1624–1629.
25. Jensen, C. J., B. J. Oldfield, and J. P. Rubio. 2009. Splicing, cisgenetic variation and disease. Biochem. Soc.Trans. 37:1311–1315.
26. Kinali, M., V. Arechavala-Gomeza, L. Feng, S. Cirak, D. Hunt, C. Adkin, et al. 2009. Local restoration of dystrophinexpression with the morpholino oligomer AVI-4658 inDuchenne muscular dystrophy: a single-blind, placebocontrolled,dose-escalation, proof-of-concept study. LancetNeurol. 8:918–928.
27. Krawczak, M., J. Reiss, and D. N. Cooper. 1992. Themutational spectrum of single base-pair substitutions inmRNA splice junctions of human genes: causes andconsequences. Hum. Genet. 90:41–54.
28. Krawczak, M., N. S. Thomas, B. Hundrieser, M. Mort, M. Wittig, J. Hampe, et al. 2007. Single base-pair substitutionsin exon-intron junctions of human genes: nature,distribution, and consequences for mRNA splicing. Hum.Mutat. 28:150–158.
29. Lattanzi, L., G. Salvatori, M. Coletta, C. Sonnino, M. G. Cusella De Angelis, L. Gioglio, et al. 1998. High efficiencymyogenic conversion of human fibroblasts by adenoviralvector-mediated MyoD gene transfer. An alternative strategyfor ex vivo gene therapy of primary myopathies. J. Clin.Invest. 101:2119–2128.
30. Magri, F., R. Del Bo, M. G. D’Angelo, A. Govoni, S. Ghezzi, S. Gandossini, et al. 2011. Clinical and molecularcharacterization of a cohort of patients with novelnucleotide alterations of the Dystrophin gene detected bydirect sequencing. BMC Med. Genet. 12:37.
31. Mann, C. J., K. Honeyman, A. J. Cheng, T. Ly, F. Lloyd, S. Fletcher, et al. 2001. Antisense-induced exon skippingand synthesis of dystrophin in the mdx mouse. Proc. Natl.Acad. Sci. USA 98:42–47.
32. Mann, C. J., K. Honeyman, G. McClorey, S. Fletcher, and S. D. Wilton. 2002. Improved antisense oligonucleotide induced exon skipping in the mdx mouse model ofmuscular dystrophy. J. Gene Med. 4:644–654.
33. McClorey, G., H. M. Moulton, P. L. Iversen, S. Fletcher, and S. D. Wilton. 2006. Antisense oligonucleotide-induced exonskipping restores dystrophin expression in vitro in a caninemodel of DMD. Gene Ther. 13:1373–1381.
34. Mitrpant, C., A. M. Adams, P. L. Meloni, F. Muntoni, S. Fletcher, and S. D. Wilton. 2009. Rational design of antisense oligomers to induce dystrophin exon skipping. Mol. Ther. 17:1418–1426.
35. Moulton, H. M., and J. D. Moulton. 2010. Morpholinos andtheir peptide conjugates: therapeutic promise and challengefor Duchenne muscular dystrophy. Biochim. Biophys. Acta 1798:2296–2303.
36. Moulton, H. M., S. Fletcher, B. W. Neuman, G. McClorey, D. A. Stein, S. Abes, et al. 2007. Cell-penetrating peptidemorpholinoconjugates alter pre-mRNA splicing of DMD(Duchenne muscular dystrophy) and inhibit murinecoronavirus replication in vivo. Biochem. Soc. Trans.35:826–828.
37. Moulton, H. M., B. Wu, N. Jearawiriyapaisarn, P. Sazani, Q. L. Lu, and R. Kole. 2009. Peptide-morpholino conjugate:a promising therapeutic for Duchenne muscular dystrophy. Ann. N. Y. Acad. Sci. 1175:55–60.
38. Nicholson, L. V., K. Davison, G. Falkous, C. Harwood, E. O’Donnell, C. R. Slater, et al. 1989. Dystrophin in skeletalmuscle. I. Western blot analysis using a monoclonalantibody. J. Neurol. Sci. 94:125–136.
39. Roberts, R. G., R. J. Gardner, and M. Bobrow. 1994. Searchingfor the 1 in 2,400,000: a review of dystrophin gene pointmutations. Hum. Mutat. 4:1–11.
40. Schwartz, M., M. Duno, A. L. Palle, T. Krag, and J. Vissing.2007. Deletion of exon 16 of the dystrophin gene is notassociated with disease. Hum. Mutat. 28:205.
41. Sharp, N. J., J. N. Kornegay, S. D. Van Camp, M. H. Herbstreith, S. L. Secore, S. Kettle, et al. 1992. An error indystrophin mRNA processing in golden retriever musculardystrophy, an animal homologue of Duchenne musculardystrophy. Genomics 13:115–121.
42. Sherratt, T. G., T. Vulliamy, V. Dubowitz, C. A. Sewry, and P. N. Strong. 1993. Exon skipping and translation in patients with frameshift deletions in the dystrophin gene. Am. J. Hum. Genet. 53:1007–1015.
43. Sironi, M., S. Corti, F. Locatelli, R. Cagliani, and G. P. Comi.2001. A novel splice site mutation (3157 + 1G>T) in thedystrophin gene causing total exon skipping and DMDphenotype. Hum. Mutat. 17:239.
44. Takeshima, Y., H. Nishio, H. Sakamoto, H. Nakamura, and M. Matsuo. 1995. Modulation of in vitro splicing of theupstream intron by modifying an intra-exon sequence whichis deleted from the dystrophin gene in dystrophin Kobe.J. Clin. Invest. 95:515–520.
45. Takeshima, Y., M. Yagi, Y. Okizuka, H. Awano, Z. Zhang, Y. Yamauchi, et al. 2010. Mutation spectrum of the dystrophingene in 442 Duchenne/Becker muscular dystrophy casesfrom one Japanese referral center. J. Hum. Genet. 55:379–388.
46. Thi Tran, H. T., Y. Takeshima, A. Surono, M. Yagi, H. Wada, and M. Matsuo. 2005. A G-to-A transition at the fifthposition of intron-32 of the dystrophin gene inactivatesa splice-donor site both in vivo and in vitro. Mol. Genet. Metab. 85:213–219.
47. Winnard, A. V., C. J. Klein, D. D. Coovert, T. Prior, A. Papp, P. Snyder, et al. 1993. Characterization of translationalframe exception patients in Duchenne/Becker musculardystrophy. Hum. Mol. Genet. 2:737–744.
48. Yokota, T., Q. L. Lu, T. Partridge, M. Kobayashi, A. Nakamura, S. Takeda, et al. 2009. Efficacy of systemicmorpholino exon-skipping in Duchenne dystrophy dogs. Ann. Neurol. 65:667–676.