Opportunities and challenges for the development of antisense treatment in neuromuscular disorders

Bibliography

• Emery AE. The muscular dystrophies. Lancet 2002;359:687-95
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, van Ommen GJ. Progress in therapeutic antisense applications for neuromuscular disorders. Eur J Hum Genet 2010;11:146-53
   Google Scholar
• Wood MJ, Gait MJ, Yin H. RNA-targeted splice-correction therapy for neuromuscular disease. Brain 2010;133:957-72
   Google Scholar
• Hoffman EP, Fischbeck KH, Brown RH, Characterization of dystrophin in muscle-biopsy specimens from patients with Duchenne's or Becker's muscular dystrophy. N Engl J Med 1988;318:1363-8
   PubMed Web of Science ®Google Scholar
• Monaco AP, Bertelson CJ, Liechti-Gallati S, An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 1988;2:90-5
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, van Vliet L, Hirschi M, Guidelines for antisense oligonucleotide design and insight into splice-modulating mechanisms. Mol Ther 2009;17:548-53
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, van Deutekom JC, Fokkema IF, 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;34:135-44
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Fokkema I, Verschuuren J, Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum Mutat 2009;30:293-9
   PubMed Web of Science ®Google Scholar
• Goemans NM, Tulinius M, van den Akker JT, Systemic administration of PRO051 in Duchenne's muscular dystrophy. N Engl J Med 2011; published online 23 March 2011, doi: 10.1056/NEJMoa1011367
   Google Scholar
• Kinali M, rechavala-Gomeza V, Feng L, 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 Neurol 2009;8:918-28
   PubMed Web of Science ®Google Scholar
• van Deutekom JC, Janson AA, Ginjaar IB, Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007;357:2677-86
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Janson AA, Kaman WE, Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet 2003;12:907-14
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Janson AA, Kaman WE, Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 2004;74:83-92
   PubMed Web of Science ®Google Scholar
• Alter J, Lou F, Rabinowitz A, Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 2006;12:175-7
   PubMed Web of Science ®Google Scholar
• Heemskerk H, de Winter C, van Kuik P, Preclinical PK and PD Studies on 2′-O-Methyl-phosphorothioate RNA antisense oligonucleotides in the mdx mouse model. Mol Ther 2010;18:1210-17
   PubMed Web of Science ®Google Scholar
• Heemskerk HA, De Winter CL, de Kimpe SJ, In vivo comparison of 2′-O-methyl phosphorothioate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping. J Gene Med 2009;11:257-66
   PubMed Web of Science ®Google Scholar
• Heemskerk H, De Winter CL, van Ommen GJ, Development of antisense-mediated exon skipping as a treatment for Duchenne muscular dystrophy. Ann NY Acad Sci 2009;1175:71-9
   PubMed Web of Science ®Google Scholar
• Wu B, Lu P, Benrashid E, Dose-dependent restoration of dystrophin expression in cardiac muscle of dystrophic mice by systemically delivered morpholino. Gene Ther 2010;17:132-40
   PubMed Web of Science ®Google Scholar
• Kim J, Wang Z, Heymsfield SB, Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr 2002;76:378-83
   PubMed Web of Science ®Google Scholar
• Goemans NM, Buyse G, Wilson R, 24 week follow-up data from a phase I/IIa extension study of PRO051/GSK2402968 in subjects with Duchenne muscular dystrophy. Neuromuscul Disord 2011;20:639
   Web of Science ®Google Scholar
• McDonald CM, Henricson EK, Han JJ, The 6-minute walk test in Duchenne/Becker muscular dystrophy: longitudinal observations. Muscle Nerve 2010;42:966-74
   PubMed Web of Science ®Google Scholar
• GlaxoSmithKline. Phase II Doubleblind Exploratory Study of GSK2402968 in Ambulant Subjects With Duchenne Muscular Dystrophy. ClinicalTrials.gov NCT01153932. Available from: http://clinicaltrials.gov/ct2/show/NCT01153932?term=NCT01153932&rank=1
   Google Scholar
• GlaxoSmithKline. A Clinical Study to Assess the Efficacy and Safety of GSK2402968 in Subjects With Duchenne Muscular Dystrophy. ClinicalTrials.gov NCT01254019. Available from: http://clinicaltrials.gov/ct2/show/NCT01254019?term=NCT01254019&rank=1
   Google Scholar
• GlaxoSmithKline. A Double-blind, Escalating Dose, Randomized, Placebo-controlled Study Assessing PK, Safety, Tolearbility in Non-ambulant DMD Subjects. ClinicalTrials.gov NCT01128855. Available from: http://clinicaltrials.gov/ct2/show/NCT01128855?term=NCT01128855&rank=1
   Google Scholar
• Kole R. Progress in systemic delivery of AVI-4658 for treatment of Duchenne muscular dystrophy. Bothell, WA: AVI BioPharma, 2010. Available from: http://www.avibio.com/wp-content/uploads/2010/10/OTS_2010_DMD.pdf [Last accessed 14 April 2011]
   Google Scholar
• AVI BioPharma's Investigational Drug Candidate AVI-4658 Demonstrates Broadly Favorable Profile of Safety and Tolerability, New Dystrophin Expression, Stable Clinical Performance and Inflammatory Modulation in the Treatment of Duchenne Muscular Dystrophy. Bothell, WA: AVI BioPharma, 2010. Available from: http://investorrelations.avibio.com/phoenix.zhtml?c=64231&p=irol-newsArticle&ID=1483148&highlight= [Last accessed 14 April 2011]
   Google Scholar
• Aartsma-Rus A, van Ommen GJ. Less is more: therapeutic exon skipping for Duchenne muscular dystrophy. Lancet Neurol 2009;8:873-5
   PubMed Web of Science ®Google Scholar
• Shrewsbury S. Current prodgress and preliminary results with the systemic administration trioal of AVI-4658, a novel Phosphorodiamidate Morpholino Oligomer (PMO) skipping dystrophin exon 51 in Duchenne muscular dystrophy (DMD). Bothell, WA: AVI BioPharma, 2010. Available from: http://www.avibio.com/wp-content/uploads/2010/10/AVI-4658-28-WMS-FINAL.101510.pdf [Last accessed 14 April 2011]
   Google Scholar
• Bansal D, Campbell KP. Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol 2004;14:206-13
   PubMed Web of Science ®Google Scholar
• Bashir R, Britton S, Strachan T, A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat Genet 1998;20:37-42
   PubMed Web of Science ®Google Scholar
• Illa I, Serrano-Munuera C, Gallardo E, Distal anterior compartment myopathy: a dysferlin mutation causing a new muscular dystrophy phenotype. Ann Neurol 2001;49:130-4
   PubMed Web of Science ®Google Scholar
• Liu J, Aoki M, Illa I, Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat Genet 1998;20:31-6
   PubMed Web of Science ®Google Scholar
• Therrien C, Dodig D, Karpati G, Sinnreich M. Mutation impact on dysferlin inferred from database analysis and computer-based structural predictions. J Neurol Sci 2006;250:71-8
   PubMed Web of Science ®Google Scholar
• Sinnreich M, Therrien C, Karpati G. Lariat branch point mutation in the dysferlin gene with mild limb-girdle muscular dystrophy. Neurology 2006;66:1114-16
   PubMed Web of Science ®Google Scholar
• Krahn M, Wein N, Lostal W, Partial functionality of a Mini-dysferlin molecule identified in a patient affected with moderately severe primary dysferlinopathy. Neuromuscul Disord 2008;18:781
   Web of Science ®Google Scholar
• Aartsma-Rus A, van der Maarel S. Reply to Levy, et al. Eur J Hum Genet 2010;18:971
   Google Scholar
• Wein N, Avril A, Bartoli M, Efficient bypass of mutations in dysferlin deficient patient cells by antisense-induced exon skipping. Hum Mutat 2010;31:136-42
   PubMed Web of Science ®Google Scholar
• Aartsma-Rus A, Singh KH, Fokkema IF, Therapeutic exon skipping for dysferlinopathies? Eur J Hum Genet 2010;18:889-94
   PubMed Web of Science ®Google Scholar
• Yokota T, Lu QL, Partridge T, Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 2009;65:667-76
   PubMed Web of Science ®Google Scholar
• Frugier T, Nicole S, Cifuentes-Diaz C, Melki J. The molecular bases of spinal muscular atrophy. Curr Opin Genet Dev 2002;12:294-8
   PubMed Web of Science ®Google Scholar
• Lefebvre S, Burglen L, Reboullet S, Identification and characterization of a spinal muscular atrophy-determining gene. Cell 1995;80:155-65
   PubMed Web of Science ®Google Scholar
• Monani UR, Lorson CL, Parsons DW, A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum Mol Genet 1999;8:1177-83
   PubMed Web of Science ®Google Scholar
• Lorson CL, Strasswimmer J, Yao JM, SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat Genet 1998;19:63-6
   PubMed Web of Science ®Google Scholar
• Dickson A, Osman E, Lorson C. A negatively-acting bifunctional RNA increases survival motor neuron in vitro and in vivo. Hum Gene Ther 2008;19:1307-15
   PubMed Web of Science ®Google Scholar
• Hua Y, Vickers TA, Baker BF, Enhancement of SMN2 exon 7 inclusion by antisense oligonucleotides targeting the exon. PLoS Biol 2007;5:e73
   PubMed Web of Science ®Google Scholar
• Hua Y, Vickers TA, Okunola HL, Antisense masking of an hnRNP A1/A2 intronic splicing silencer corrects SMN2 splicing in transgenic mice. Am J Hum Genet 2008;82:834-48
   PubMed Web of Science ®Google Scholar
• Lim SR, Hertel KJ. Modulation of survival motor neuron pre-mRNA splicing by inhibition of alternative 3′ splice site pairing. J Biol Chem 2001;276:45476-83
   PubMed Web of Science ®Google Scholar
• Hua Y, Sahashi K, Hung G, Antisense correction of SMN2 splicing in the CNS rescues necrosis in a type III SMA mouse model. Genes Dev 2010;24:1634-44
   PubMed Web of Science ®Google Scholar
• Baughan T, Shababi M, Coady TH, Stimulating full-length SMN2 expression by delivering bifunctional RNAs via a viral vector. Mol Ther 2006;14:54-62
   PubMed Web of Science ®Google Scholar
• Marquis J, Meyer K, Angehrn L, Spinal muscular atrophy: SMN2 pre-mRNA splicing corrected by a U7 snRNA derivative carrying a splicing enhancer sequence. Mol Ther 2007;15:1479-86
   PubMed Web of Science ®Google Scholar
• Meyer K, Marquis J, Trub J, Rescue of a severe mouse model for spinal muscular atrophy by U7 snRNA-mediated splicing modulation. Hum Mol Genet 2009;18:546-55
   PubMed Web of Science ®Google Scholar
• Rosen DR. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993;364:362
   PubMed Web of Science ®Google Scholar
• Zamecnik PC, Stephenson ML. Inhibition of Rous sarcoma virus replication and cell transformation by a specific oligodeoxynucleotide. Proc Natl Acad Sci USA 1978;75:280-4
   PubMed Web of Science ®Google Scholar
• Dominski Z, Kole R. Restoration of correct splicing in thalassemic pre-mRNA by antisense oligonucleotides. Proc Natl Acad Sci USA 1993;90:8673-7
   PubMed Web of Science ®Google Scholar
• Kurreck J. Antisense technologies. Improvement through novel chemical modifications. Eur J Biochem 2003;270:1628-44
   PubMedGoogle Scholar
• Smith RA, Miller TM, Yamanaka K, Antisense oligonucleotide therapy for neurodegenerative disease. J Clin Invest 2006;116:2290-6
   PubMed Web of Science ®Google Scholar
• Isis Pharmaceuticals. Safety, Tolerability, and Activity Study of ISIS SOD1Rx to Treat Familial Amyotrophic Lateral Sclerosis (ALS) Caused by SOD1 Gene Mutations. ClinicalTrials.gov NCT01041222. Available from: http://clinicaltrials.gov/ct2/show/NCT01041222?term=NCT01041222&rank=1
   Google Scholar
• Caskey CT, Pizzuti A, Fu YH, Triplet repeat mutations in human disease. Science 1992;256:784-9
   PubMed Web of Science ®Google Scholar
• Brook JD, McCurrach ME, Harley HG, Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 1992;69:799-808
   Google Scholar
• Liquori CL, Ricker K, Moseley ML, Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science 2001;293:864-7
   PubMed Web of Science ®Google Scholar
• Lee JE, Cooper TA. Pathogenic mechanisms of myotonic dystrophy. Biochem Soc Trans 2009;37:1281-6
   PubMed Web of Science ®Google Scholar
• Pelletier R, Hamel F, Beaulieu D, Absence of a differentiation defect in muscle satellite cells from DM2 patients. Neurobiol Dis 2009;36:181-90
   Google Scholar
• Santoro M, Modoni A, Masciullo M, Analysis of MTMR1 expression and correlation with muscle pathological features in juvenile/adult onset myotonic dystrophy type 1 (DM1) and in myotonic dystrophy type 2 (DM2). Exp Mol Pathol 2010;89:158-68
   PubMed Web of Science ®Google Scholar
• Philips AV, Timchenko LT, Cooper TA. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 1998;280:737-41
   PubMed Web of Science ®Google Scholar
• Wheeler TM, Lueck JD, Swanson MS, Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J Clin Invest 2007;117:3952-7
   PubMed Web of Science ®Google Scholar
• Wheeler TM, Sobczak K, Lueck JD, Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science 2009;325:336-9
   PubMed Web of Science ®Google Scholar
• Mulders SA, van den Broek WJ, Wheeler TM, Triplet-repeat oligonucleotide-mediated reversal of RNA toxicity in myotonic dystrophy. Proc Natl Acad Sci USA 2009;106:13915-20
   PubMed Web of Science ®Google Scholar
• Francois V, Klein AF, Beley C, Selective silencing of mutated mRNAs in DM1 by using modified hU7-snRNAs. Nat Struct Mol Biol 2011;18:85-7
   Google Scholar
• Li D, Yue Y, Duan D. Preservation of muscle force in Mdx3cv mice correlates with low-level expression of a near full-length dystrophin protein. Am J Pathol 2008;172:1332-41
   PubMed Web of Science ®Google Scholar
• Sharp PS, 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;19:165-71
   PubMed Web of Science ®Google Scholar
• Ferreiro V, Giliberto F, Muniz GM, Asymptomatic Becker muscular dystrophy in a family with a multiexon deletion. Muscle Nerve 2009;39:239-43
   PubMed Web of Science ®Google Scholar
• Townsend D, Yasuda S, Li S, Emergent dilated cardiomyopathy caused by targeted repair of dystrophic skeletal muscle. Mol Ther 2008;16:832-5
   PubMed Web of Science ®Google Scholar
• Malerba A, Sharp PS, Graham IR, Chronic systemic therapy with low-dose morpholino oligomers ameliorates the pathology and normalizes locomotor behavior in mdx mice. Mol Ther 2011;19:345-54
   PubMed Web of Science ®Google Scholar
• Crisp A, Yin H, Goyenvalle A, Diaphragm rescue alone prevents heart dysfunction in dystrophic mice. Hum Mol Genet 2011;20:413-21
   PubMed Web of Science ®Google Scholar
• Moulton HM, Moulton JD. Morpholinos and their peptide conjugates: Therapeutic promise and challenge for Duchenne muscular dystrophy. Biochim Biophys Acta 2010;1798:2296-303
   PubMed Web of Science ®Google Scholar
• Our Programs, Duchenne Muscular Dystrophy. Bothell, WA: AVI BioPharma, 2011. Available from: http://www.avibio.com/our-programs/rare-diseases/duchenne-muscular-dystrophy/ [Last accessed 14 April 2011]
   Google Scholar
• Denti MA, Rosa A, D'Antona G, Body-wide gene therapy of Duchenne muscular dystrophy in the mdx mouse model. Proc Natl Acad Sci USA 2006;103:3758-63
   PubMed Web of Science ®Google Scholar
• Goyenvalle A, Vulin A, Fougerousse F, Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 2004;306:1796-9
   PubMed Web of Science ®Google Scholar
• Denti MA, Incitti T, Sthandier O, Long-term benefit of adeno-associated virus/antisense-mediated exon skipping in dystrophic mice. Hum Gene Ther 2008;19:601-8
   PubMed Web of Science ®Google Scholar
• Goyenvalle A, Babbs A, van Ommen GJ, Enhanced exon-skipping induced by U7 snRNA carrying a splicing silencer sequence: promising tool for DMD therapy. Mol Ther 2009;17:1234-40
   PubMed Web of Science ®Google Scholar
• Incitti T, De Angelis FG, Cazzella V, Exon Skipping and Duchenne Muscular Dystrophy Therapy: Selection of the Most Active U1 snRNA Antisense Able to Induce Dystrophin Exon 51 Skipping. Mol Ther 2010;18:1675-82
   PubMed Web of Science ®Google Scholar
• Muntoni F. The development of antisense oligonucleotide therapies for Duchenne muscular dystrophy: report on a TREAT-NMD workshop hosted by the European Medicines Agency (EMA), on September 25th 2009. Neuromuscul Disord 2010;20:355-62
   PubMedGoogle Scholar
• Prosensa Therapeutics. Phase I/II Study of PRO044 in Duchenne Muscular Dystrophy (DMD). ClinicalTrials.gov NCT01037309. Available from: http://clinicaltrials.gov/ct2/show/NCT01037309?term=NCT01037309&rank=1
   Google Scholar
• Aartsma-Rus A. The risks of therapeutic misconception and individual patient (n=1) "trials" in rare diseases such as Duchenne dystrophy. Neuromuscul Disord 2011;21:13-15
   PubMed Web of Science ®Google Scholar
• Mendell JR, Campbell K, Rodino-Klapac L, Dystrophin immunity in Duchenne's muscular dystrophy. N Engl J Med 2010;363:1429-37
   PubMed Web of Science ®Google Scholar
• Moodie Z, Price L, Gouttefangeas C, Response definition criteria for ELISPOT assays revisited. Cancer Immunol Immunother 2010;59:1489-501
   PubMed Web of Science ®Google Scholar
• Wilson JM. Autoimmunity, recessive diseases, and gene replacement therapy. Mol Ther 2010;18:2045-7
   PubMed Web of Science ®Google Scholar
• AVI BioPharma, Inc. Dose-Ranging Study of AVI-4658 to Induce Dystrophin Expression in Selected Duchenne Muscular Dystrophy (DMD) Patients. ClinicalTrials.gov NCT00844597. Available from: http://clinicaltrials.gov/ct2/show/NCT00844597?term=NCT00844597&rank=1
   Google Scholar