Antisense mediated exon skipping therapy for duchenne muscular dystrophy (DMD)

Artificial DNA: PNA and XNA

Volumn 2, Issue 1, 2011, Pages 6-15

  Brolin, Camilla ^a   Shiraishi, Takehiko ^b  

^a Mental Health Center Glostrup   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Antisense; DMD; Exon skipping; In vivo; Splicing modulation; Therapy

Indexed keywords

2' O METHYL PHOSPHOROTHIOATE; AMINOCAPROIC ACID; ANTISENSE OLIGONUCLEOTIDE; ARGININE; AVI 4658; DYSTROPHIN; GUANIDINE; LIPOFECTIN; MACROGOL; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; PEPTIDE NUCLEIC ACID; PHOSPHORODIAMIDATE MORPHOLINO OLIGOMER; POLOXAMER; POLY(METHYL METHACRYLATE); POLYETHYLENEIMINE; POLYGLACTIN; PRO 051; PYRIDINIUM DERIVATIVE; UNCLASSIFIED DRUG;

ABSENCE OF SIDE EFFECTS; ANTISENSE THERAPY; ARTICLE; DISEASE MODEL; DRUG STRUCTURE; DRUG TOLERABILITY; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN GENE; ELECTROPORATION; EXON; EXON SKIPPING; GENE; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC);

ANIMALIA;

EID: 79955564274     PISSN: 1949095X     EISSN: 19490968     Source Type: Journal    
DOI: 10.4161/adna.2.1.15425     Document Type: Article

References (61)

1. Aartsma-Rus A, Van Deutekom JC, Fokkema IF, Van Ommen GJ, Den Dunnen JT. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the reading-frame rule. Muscle & nerve 2006; 34:135-144.
2. van Ommen GJ, van Deutekom J, Aartsma-Rus A. The therapeutic potential of antisense-mediated exon skipping. Current opinion in molecular therapeutics 2008; 10:140-149.
3. Wu B, Moulton HM, Iversen PL, Jiang J, Li J, Li J, et al. Effective rescue of dystrophin improves cardiac function in dystrophin-deficient mice by a modified morpholino oligomer. Proceedings of the National Academy of Sciences of the United States of America 2008; 105:14814-14819.
4. Yin H, Moulton HM, Betts C, Merritt T, Seow Y, Ashraf S, et al. Functional rescue of dystrophin-deficient mdx mice by a chimeric peptide-PMO. Mol Ther 2010; 18:1822-1829.
5. Jearawiriyapaisarn N, Moulton HM, Sazani P, Kole R, Willis MS. Long-term improvement in mdx cardiomyopathy after therapy with peptide-conjugated morpholino oligomers. Cardiovascular research 2010; 85:444-453.
6. Extance A. Targeting RNA: an emerging hope for treating muscular dystrophy. Nature reviews 2009; 8:917-918.
7. Hammond SM, Wood MJ. PRO-051, an antisense oligonucleotide for the potential treatment of Duchenne muscular dystrophy. Current opinion in molecular therapeutics 2010; 12:478-486.
8. J skipping corrects the nonsense mutation in dystrophic mouse muscle and produces functional revertant fibers by clonal expansion. The Journal of cell biology 2000; 148:985-996.
9. Kunkel LM, Beggs AH, Hoffman EP. Molecular genetics of Duchenne and Becker muscular dystrophy: emphasis on improved diagnosis. Clinical chemistry 1989; 35:21-24.
10. Aartsma-Rus A, Fokkema I, Verschuuren J, Ginjaar I, van Deutekom J, van Ommen GJ, den Dunnen JT. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Human mutation 2009; 30:293-299.
11. Nakamura A, Takeda S. Exon-skipping therapy for Duchenne muscular dystrophy. Neuropathology 2009; 29:494-501.
12. Grounds MD, Radley HG, Lynch GS, Nagaraju K, De Luca A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiology of disease 2008; 31:1-19.
13. Mann CJ, Honeyman K, Cheng AJ, Ly T, Lloyd F, Fletcher S, et al. Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proceedings of the National Academy of Sciences of the United States of America 2001; 98:42-47.
14. th 2009. Neuromuscul Disord 20:355-362.
15. Goyenvalle A, Babbs A, Powell D, Kole R, Fletcher S, Wilton SD, Davies KE. Prevention of dystrophic pathology in severely affected dystrophin/utrophin-deficient mice by morpholino-oligomer-mediated exon-skipping. Mol Ther 2010; 18:198-205.
16. Bremmer-Bout M, Aartsma-Rus A, de Meijer EJ, Kaman WE, Janson AA, Vossen RH, et al. Targeted exon skipping in transgenic hDMD mice: A model for direct preclinical screening of human-specific antisense oligonucleotides. Mol Ther 2004; 10:232-240.
17. Aoki Y, Nakamura A, Yokota T, Saito T, Okazawa H, Nagata T, Takeda S. In-frame dystrophin following exon 51-skipping improves muscle pathology and function in the exon 52-deficient mdx mouse. Mol Ther 2010; 18:1995-2005.
18. Mitrpant C, Fletcher S, Iversen PL, Wilton SD. By-passing the nonsense mutation in the 4 CV mouse model of muscular dystrophy by induced exon skipping. The journal of gene medicine 2009; 11:46-56.
19. Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, Takeda S, Hoffman E. Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 2009; 65:667-676.
20. van Deutekom JC, Janson AA, Ginjaar IB, Frankhuizen WS, Aartsma-Rus A, Bremmer-Bout M, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007; 357:2677-2686.
21. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, Adkin C, et al. 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 neurology 2009; 8:918-928.
22. Lu QL, Rabinowitz A, Chen YC, Yokota T, Yin H, Alter J, et al. Systemic delivery of antisense oligoribo-nucleotide restores dystrophin expression in body-wide skeletal muscles. Proceedings of the National Academy of Sciences of the United States of America 2005; 102:198-203.
23. Alter J, Lou F, Rabinowitz A, Yin H, Rosenfeld J, Wilton SD, et al. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 2006; 12:175-177.
24. Heemskerk HA, de Winter CL, de Kimpe SJ, van Kuik-Romeijn P, Heuvelmans N, Platenburg GJ, et al. In vivo comparison of 2'-O-methyl phosphorothio-ate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping. The journal of gene medicine 2009; 11:257-266.
25. Wang Q, Yin H, Camelliti P, Betts C, Moulton H, Lee H, et al. In vitro evaluation of novel antisense oligonucleotides is predictive of in vivo exon skipping activity for Duchenne muscular dystrophy. The journal of gene medicine 2010; 12:354-364.
26. Aartsma-Rus A, Janson AA, Kaman WE, Bremmer-Bout M, den Dunnen JT, Baas F, et al. Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Human molecular genetics 2003; 12:907-914.
27. Guglieri M, Bushby K. Molecular treatments in Duchenne muscular dystrophy. Current opinion in pharmacology 2010; 10:331-337.
28. Flanigan KM, Dunn DM, von Niederhausern A, Soltanzadeh P, Gappmaier E, Howard MT, et al. Mutational spectrum of DMD mutations in dystro-phinopathy patients: application of modern diagnostic techniques to a large cohort. Human mutation 2009; 30:1657-1666.
29. Wood MJ, Gait MJ, Yin H. RNA-targeted splice-correction therapy for neuromuscular disease. Brain 2010; 133:957-972.
30. van Vliet L, de Winter CL, van Deutekom JC, van Ommen GJ, Aartsma-Rus A. Assessment of the feasibility of exon 45-55 multiexon skipping for Duchenne muscular dystrophy. BMC Med Genet 2008; 9:105.
31. Lu QL, Partridge TA. Antisense therapy corrects nonsense mutation by exon skipping. Discov Med 2003; 3:39-44.
32. Wells KE, Fletcher S, Mann CJ, Wilton SD, Wells DJ. Enhanced in vivo delivery of antisense oligonucleotides to restore dystrophin expression in adult mdx mouse muscle. FEBS letters 2003; 552:145-149.
33. Gebski BL, Mann CJ, Fletcher S, Wilton SD. Morpholino antisense oligonucleotide induced dystrophin exon 23 skipping in mdx mouse muscle. Human molecular genetics 2003; 12:1801-1811.
34. Graham IR, Hill VJ, Manoharan M, Inamati GB, Dickson G. Towards a therapeutic inhibition of dystrophin exon 23 splicing in mdx mouse muscle induced by antisense oligoribonucleotides (splicomers): target sequence optimisation using oligonucleotide arrays. The journal of gene medicine 2004; 6:1149-1158.
35. Takeshima Y, Yagi M, Wada H, Matsuo M. Intraperitoneal administration of phosphorothioate antisense oligodeoxynucleotide against splicing enhancer sequence induced exon skipping in dystrophin mRNA expressed in mdx skeletal muscle. Brain Dev 2005; 27:488-493.
36. Williams JH, Sirsi SR, Latta DR, Lutz GJ. Induction of dystrophin expression by exon skipping in mdx mice following intramuscular injection of antisense oligonucleotides complexed with PEG-PEI copolymers. Mol Ther 2006; 14:88-96.
37. Fall AM, Johnsen R, Honeyman K, Iversen P, Fletcher S, Wilton SD. Induction of revertant fibres in the mdx mouse using antisense oligonucleotides. Genet Vaccines Ther 2006; 4:3.
38. Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Wilton SD. Dystrophin expression in the mdx mouse after localised and systemic administration of a morpholino antisense oligonucleotide. The journal of gene medicine 2006; 8:207-216.
39. Fletcher S, Honeyman K, Fall AM, Harding PL, Johnsen RD, Steinhaus JP, et al. Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol Ther 2007; 15:1587-1592.
40. Laws N, Cornford-Nairn RA, Irwin N, Johnsen R, Fletcher S, Wilton SD, Hoey AJ. Long-term administration of antisense oligonucleotides into the paraspinal muscles of mdx mice reduces kyphosis. J Appl Physiol 2008; 105:662-668.
41. Williams JH, Schray RC, Sirsi SR, Lutz GJ. Nanopolymers improve delivery of exon skipping oligonucleotides and concomitant dystrophin expression in skeletal muscle of mdx mice. BMC biotechnology 2008; 8:35.
42. Jearawiriyapaisarn N, Moulton HM, Buckley B, Roberts J, Sazani P, Fucharoen S, et al. Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice. Mol Ther 2008; 16:1624-1629.
43. Vitiello L, Bassi N, Campagnolo P, Zaccariotto E, Occhi G, Malerba A, et al. In vivo delivery of naked antisense oligos in aged mdx mice: analysis of dystrophin restoration in skeletal and cardiac muscle. Neuromuscul Disord 2008; 18:597-605.
44. Yin H, Moulton HM, Seow Y, Boyd C, Boutilier J, Iverson P, Wood MJ. Cell-penetrating peptide-conjugated antisense oligonucleotides restore systemic muscle and cardiac dystrophin expression and function. Human molecular genetics 2008; 17:3909-3918.
45. Ivanova GD, Arzumanov A, Abes R, Yin H, Wood MJ, Lebleu B, Gait MJ. Improved cell-penetrating peptide-PNA conjugates for splicing redirection in HeLa cells and exon skipping in mdx mouse muscle. Nucleic acids research 2008; 36:6418-6428.
46. Yin H, Lu Q, Wood M. Effective exon skipping and restoration of dystrophin expression by peptide nucleic acid antisense oligonucleotides in mdx mice. Mol Ther 2008; 16:38-45.
47. Kim Y, Tewari M, Pajerowski JD, Cai S, Sen S, Williams JH, et al. Polymersome delivery of siRNA and antisense oligonucleotides. J Control Release 2009; 134:132-140.
48. Rimessi P, Sabatelli P, Fabris M, Braghetta P, Bassi E, Spitali P, et al. Cationic PMMA nanoparticles bind and deliver antisense oligoribonucleotides allowing restoration of dystrophin expression in the mdx mouse. Mol Ther 2009; 17:820-827.
49. Sirsi SR, Schray RC, Wheatley MA, Lutz GJ. Formulation of polylactide-co-glycolic acid nano-spheres for encapsulation and sustained release of poly(ethylene imine)-poly(ethylene glycol) copolymers complexed to oligonucleotides. Journal of nanobiotech-nology 2009; 7:1.
50. Malerba A, Thorogood FC, Dickson G, Graham IR. Dosing regimen has a significant impact on the efficiency of morpholino oligomer-induced exon skipping in mdx mice. Hum Gene Ther 2009; 20:955-965.
51. Wu B, Li Y, Morcos PA, Doran TJ, Lu P, Lu QL. Octa-guanidine morpholino restores dystrophin expression in cardiac and skeletal muscles and ameliorates pathology in dystrophic mdx mice. Mol Ther 2009; 17:864-871.
52. Yin H, Moulton HM, Betts C, Seow Y, Boutilier J, Iverson PL, Wood MJ. A fusion peptide directs enhanced systemic dystrophin exon skipping and functional restoration in dystrophin-deficient mdx mice. Human molecular genetics 2009; 18:4405-4414.
53. Ferlini A, Sabatelli P, Fabris M, Bassi E, Falzarano S, Vattemi G, Perrone D, et al. Dystrophin restoration in skeletal, heart and skin arrector pili smooth muscle of mdx mice by ZM2 NP-AON complexes. Gene therapy 2010; 17:432-438.
54. Heemskerk H, de Winter C, van Kuik P, Heuvelmans N, Sabatelli P, Rimessi P, et al. Preclinical PK and PD studies on 2'-O-methyl-phosphorothioate RNA anti-sense oligonucleotides in the mdx mouse model. Mol Ther 2010; 18:1210-1217.
55. Hu Y, Wu B, Zillmer A, Lu P, Benrashid E, Wang M, et al. Guanine analogues enhance antisense oligonucleotide-induced exon skipping in dystrophin gene in vitro and in vivo. Mol Ther 2010; 18:812-818.
56. Wu B, Lu P, Benrashid E, Malik S, Ashar J, Doran TJ, Lu QL. Dose-dependent restoration of dystrophin expression in cardiac muscle of dystrophic mice by systemically delivered morpholino. Gene therapy 2010; 17:132-140.
57. Yin H, Betts C, Saleh AF, Ivanova GD, Lee H, Seow Y, et al. Optimization of peptide nucleic acid antisense oligonucleotides for local and systemic dystrophin splice correction in the mdx mouse. Mol Ther 2010; 18:819-827.
58. Sharp PS, Bye-a-Jee H, Wells DJ. Physiological characterization of muscle strength with variable levels of dystrophin restoration in mdx mice following local antisense therapy. Mol Ther 2011; 19:165-171.
59. Arechavala-Gomeza V, Graham IR, Popplewell LJ, Adams AM, Aartsma-Rus A, Kinali M, et al. Comparative analysis of antisense oligonucleotide sequences for targeted skipping of exon 51 during dystrophin pre-mRNA splicing in human muscle. Hum Gene Ther 2007; 18:798-810.
60. Popplewell LJ, Adkin C, Arechavala-Gomeza V, Aartsma-Rus A, de Winter CL, Wilton SD, et al. Comparative analysis of antisense oligonucleotide sequences targeting exon 53 of the human DMD gene: Implications for future clinical trials. Neuromuscul Disord 2010; 20:102-110.
61. Takeshima Y, Yagi M, Wada H, Ishibashi K, Nishiyama A, Kakumoto M, et al. Intravenous infusion of an anti-sense oligonucleotide results in exon skipping in muscle dystrophin mRNA of Duchenne muscular dystrophy. Pediatr Res 2006; 59:690-694.