Long-term rescue of dystrophin expression and improvement in muscle pathology and function in dystrophic mdx mice by peptide-conjugated morpholino

American Journal of Pathology

Volumn 181, Issue 2, 2012, Pages 392-400

  Wu, Bo ^a   Lu, Peijuan ^a   Cloer, Caryn ^a   Shaban, Mona ^a   Grewal, Snimar ^a   Milazi, Stephanie ^a   Shah, Sapana N ^a   Moulton, Hong M ^b   Lu, Qi Long ^a  

^a Neuromuscular/ALS Center   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CREATINE KINASE; DYSTROPHIN; MORPHOLINO OLIGONUCLEOTIDE; PHOSPHORODIAMIDATE MORPHOLINO; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DUCHENNE MUSCULAR DYSTROPHY; EXON; GRIP STRENGTH; HEART MUSCLE; HISTOPATHOLOGY; LD 50; MOUSE; MUSCLE DISEASE; MUSCLE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; SKELETAL MUSCLE; WESTERN BLOTTING;

ADMINISTRATION, INTRAVENOUS; ANIMALS; DRUG ADMINISTRATION SCHEDULE; DYSTROPHIN; HALF-LIFE; LETHAL DOSE 50; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MORPHOLINOS; MUSCLES; MUSCULAR DYSTROPHY, ANIMAL; PEPTIDES; RECOVERY OF FUNCTION; TIME FACTORS;

EID: 84864119843     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.04.006     Document Type: Article

References (28)

1. E.P. Hoffman, R.H. Brown Jr, L.M. Kunkel Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 51 1987 919 928
2. N.G. Laing Molecular genetics and genetic counselling for Duchenne/Becker muscular dystrophy Molecular and Cell Biology of Muscular Dystrophy T. Partridge, 1993 Chapman & Hall London 37 77
3. A.P. Monaco, C.J. Bertelson, S. Liechti-Gallati, H. Moser, L.M. Kunkel An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus Genomics 2 1988 90 95
4. T. Athanasopoulos, I.R. Graham, H. Foster, G. Dickson Recombinant adeno-associated viral (rAAV) vectors as therapeutic tools for Duchenne muscular dystrophy (DMD) Gene Ther 11 Suppl 1 2004 S109 S121
5. S.B. England, L.V. Nicholson, M.A. Johnson, S.M. Forrest, D.R. Love, E.E. Zubrzycka-Gaarn, D.E. Bulman, J.B. Harris, K.E. Davies Very mild muscular dystrophy associated with the deletion of 46% of dystrophin Nature 343 1990 180 182
6. P. Gregorevic, M.J. Blankinship, J.M. Allen, R.W. Crawford, L. Meuse, D.G. Miller, D.W. Russell, J.S. Chamberlain Systemic delivery of genes to striated muscles using adeno-associated viral vectors Nat Med 10 2004 828 834
7. T.G. Sherratt, T. Vulliamy, V. Dubowitz, C.A. Sewry, P.N. Strong Exon skipping and translation in patients with frameshift deletions in the dystrophin gene Am J Hum Genet 53 1993 1007 1015
8. M.G. Dunckley, M. Manoharan, P. Villiet, I.C. Eperon, G. Dickson Modification of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides Hum Mol Genet 7 1998 1083 1090
9. C.J. Mann, K. Honeyman, A.J. Cheng, T. Ly, F. Lloyd, S. Fletcher, J.E. Morgan, T.A. Partridge, S.D. Wilton Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse Proc Natl Acad Sci USA 98 2001 42 47
10. G. Dickson, V. Hill, I.R. Graham Screening for antisense modulation of dystrophin pre-mRNA splicing Neuromuscul Disord 12 Suppl 1 2002 S67 S70
11. A. Aartsma-Rus, M. Bremmer-Bout, A.A. Janson, J.T. den Dunnen, G.J. van Ommen, J.C. van Deutekom Targeted exon skipping as a potential gene correction therapy for Duchenne muscular dystrophy Neuromuscul Disord 12 Suppl 1 2002 S71 S77
12. Q.L. Lu, C.J. Mann, F. Lou, G. Bou-Gharios, G.E. Morris, S.A. Xue, S. Fletcher, T.A. Partridge, S.D. Wilton Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse Nat Med 9 2003 1009 1014
13. Q.L. Lu, A. Rabinowitz, Y.C. Chen, T. Yokota, H. Yin, J. Alter, A. Jadoon, G. Bou-Gharios, T. Partridge Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles Proc Natl Acad Sci USA 102 2005 198 203
14. J. Alter, F. Lou, A. Rabinowitz, H. Yin, J. Rosenfeld, S.D. Wilton, T.A. Partridge, Q.L. Lu Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology Nat Med 12 2006 175 177
15. B. Wu, H.M. Moulton, P.L. Iversen, J. Jiang, J. Li, C.F. Spurney, A. Sali, A.D. Guerron, K. Nagaraju, T. Doran, P. Lu, X. Xiao, Q.L. Lu Effective rescue of dystrophin improves cardiac function in dystrophin-deficient mice by a modified morpholino oligomer Proc Natl Acad Sci USA 105 2008 14814 14819
16. B. Wu, Y. Li, P.A. Morcos, T.J. Doran, P. Lu, Q.L. Lu Octa-guanidine morpholino restores dystrophin expression in cardiac and skeletal muscles and ameliorates pathology in dystrophic mdx mice Mol Ther 17 2009 864 871
17. B. Wu, P. Lu, E. Benrashid, S. Malik, J. Ashar, T.J. Doran, Q.L. Lu Dose-dependent restoration of dystrophin expression in cardiac muscle of dystrophic mice by systemically delivered morpholino Gene Ther 17 2010 132 140
18. T. Yokota, Q.L. Lu, T. Partridge, M. Kobayashi, A. Nakamura, S. Takeda, E. Hoffman Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs Ann Neurol 65 2009 667 676
19. M. Kinali, V. Arechavala-Gomeza, L. Feng, S. Cirak, D. Hunt, C. Adkin, M. Guglieri, E. Ashton, S. Abbs, P. Nihoyannopoulos, M.E. Garralda, M. Rutherford, C. McCulley, L. Popplewell, I.R. Graham, G. Dickson, M.J. Wood, D.J. Wells, S.D. Wilton, R. Kole, V. Straub, K. Bushby, C. Sewry, J.E. Morgan, F. Muntoni 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 [Erratum appeared in Lancet Neurol 2009, 8:1083] Lancet Neurol 8 2009 918 928
20. J.C. van Deutekom, A.A. Janson, I.B. Ginjaar, W.S. Frankhuizen, A. Aartsma-Rus, M. Bremmer-Bout, J.T. den Dunnen, K. Koop, A.J. van der Kooi, N.M. Goemans, S.J. de Kimpe, P.F. Ekhart, E.H. Venneker, G.J. Platenburg, J.J. Verschuuren, G.J. van Ommen Local dystrophin restoration with antisense oligonucleotide PRO051 N Engl J Med 357 2007 2677 2686
21. N.M. Goemans, M. Tulinius, J.T. van den Akker, B.E. Burm, P.F. Ekhart, N. Heuvelmans, T. Holling, A.A. Janson, G.J. Platenburg, J.A. Sipkens, J.M. Sitsen, A. Aartsma-Rus, G.J. van Ommen, G. Buyse, N. Darin, J.J. Verschuuren, G.V. Campion, S.J. de Kimpe, J.C. van Deutekom Systemic administration of PRO051 in Duchenne's muscular dystrophy [Erratum appeared in N Engl J Med 2011, 365:1361] N Engl J Med 364 2011 1513 1522
22. S. Cirak, V. Arechavala-Gomeza, M. Guglieri, L. Feng, S. Torelli, K. Anthony, S. Abbs, M.E. Garralda, J. Bourke, D.J. Wells, G. Dickson, M.J. Wood, S.D. Wilton, V. Straub, R. Kole, S.B. Shrewsbury, C. Sewry, J.E. Morgan, K. Bushby, F. Muntoni Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study Lancet 378 2011 595 604
23. B. Wu, B. Xiao, C. Cloer, M. Shaban, A. Sali, P. Lu, J. Li, K. Nagaraju, X. Xiao, Q.L. Lu One-year treatment of morpholino antisense oligomer improves skeletal and cardiac muscle functions in dystrophic mdx mice Mol Ther 19 2011 576 583
24. N. Jearawiriyapaisarn, H.M. Moulton, B. Buckley, J. Roberts, P. Sazani, S. Fucharoen, P.L. Iversen, R. Kole Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice Mol Ther 16 2008 1624 1629
25. H. Yin, H.M. Moulton, Y. Seow, C. Boyd, J. Boutilier, P. Iverson, M.J. Wood Cell-penetrating peptide-conjugated antisense oligonucleotides restore systemic muscle and cardiac dystrophin expression and function Hum Mol Genet 17 2008 3909 3918
26. R. Abes, A.A. Arzumanov, H.M. Moulton, S. Abes, G.D. Ivanova, P.L. Iversen, M.J. Gait, B. Lebleu Cell-penetrating-peptide-based delivery of oligonucleotides: an overview Biochem Soc Trans 35 2007 775 779
27. H.M. Moulton, J.D. Moulton Morpholinos and their peptide conjugates: therapeutic promise and challenge for Duchenne muscular dystrophy Biochim Biophys Acta 1798 2010 2296 2303
28. A. Amantana, H.M. Moulton, M.L. Cate, M.T. Reddy, T. Whitehead, J.N. Hassinger, D.S. Youngblood, P.L. Iversen Pharmacokinetics, biodistribution, stability and toxicity of a cell-penetrating peptide-morpholino oligomer conjugate Bioconjug Chem 18 2007 1325 1331