Highly efficient in vivo delivery of PMO into regenerating myotubes and rescue in laminin-α2 chain-null congenital muscular dystrophy mice

Human Molecular Genetics

Volumn 22, Issue 24, 2013, Pages 4914-4928

  Aoki, Yoshitsugu ^a,b   Nagata, Tetsuya ^a   Yokota, Toshifumi ^c,d   Nakamura, Akinori ^e,f   Wood, Matthew J A ^b   Partridge, Terence ^g,h   Takeda, Shin'ichi ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF ALBERTA   (Canada)

^d Friends of Garrett Cumming Research   (Canada)

^e SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f SHINSHU UNIVERSITY HOSPITAL   (Japan)

^g CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^h GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2' O METHYLPHOSPHOROTHIOLATE; CARDIOTOXIN; DMD POTEIN; DYSTROPHIN; LAMININ ALPHA2; MDX52 PROTEIN; MEROSIN; MORPHOLINO OLIGONUCLEOTIDE; MUSCLE PROTEIN; MYOSIN HEAVY CHAIN; PHOSPHOROTHIOIC ACID DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DRUG DELIVERY SYSTEM; DRUG MEGADOSE; EXON; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE FIBER MEMBRANE; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; TIBIALIS ANTERIOR MUSCLE;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BROMODEOXYURIDINE; CARDIOTOXINS; CELL LINE; CELL MEMBRANE PERMEABILITY; DISEASE MODELS, ANIMAL; DYSTROPHIN; EXONS; GENE EXPRESSION; GENE ORDER; HUMANS; LAMININ; MICE; MICE, KNOCKOUT; MORPHOLINOS; MUSCLE FIBERS, SKELETAL; MUSCULAR DYSTROPHIES; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; REGENERATION;

EID: 84888143527     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt341     Document Type: Article

References (46)

1. Hoffman, E.P., Brown, R.H. and Kunkel, L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
2. Monaco, A.P., Bertelson, C.J., Liechti-Gallati, S., Moser, H. and Kunkel, L.M. (1988) An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics, 2, 90-95.
3. Matsuo, M., Masumura, T., Nishio, H., Nakajima, T., Kitoh, Y., Takumi, T., Koga, J. and Nakamura, H. (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.
4. Wood, M.J.A. (2010) Toward an oligonucleotide therapy for Duchenne muscular dystrophy: a complex development challenge. Sci. Transl. Med., 2, 25ps15.
5. Aoki, Y., Nakamura, A., Yokota, T., Saito, T., Okazawa, H., Nagata, T. and Takeda, S. (2010) In-frame dystrophin following exon 51-skipping improves muscle pathology and function in the exon 52-deficient mdx mouse. Mol. Ther., 18, 1995-2005.
6. Aoki, Y., Yokota, T., Nagata, T., Nakamura, A., Tanihata, J., Saito, T., Duguez, S.M.R., Nagaraju, K., Hoffman, E.P., Partridge, T. et al. (2012) Bodywide s kipping of exons 45-55 in dystrophic mdx52 mice by systemic antisense delivery. Proc. Natl. Acad. Sci. USA, 109, 13763-13768.
7. Yokota, T., Lu, Q.-L., Partridge, T., Kobayashi, M., Nakamura, A., Takeda, S. and Hoffman, E. (2009) Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann. Neurol., 65, 667-676.
8. Lu, Q.L., Rabinowitz, A., Chen, Y.C., Yokota, T., Yin, H., Alter, J., Jadoon, A., Bou-Gharios, G. and Partridge, T. (2005) Systemic delivery of antisense oligoribonucleotide restores dystrophin expression in body-wide skeletal muscles. Proc. Natl. Acad. Sci. USA, 102, 198-203.
9. Cirak, S., Arechavala-Gomeza, V., Guglieri, M., Feng, L., Torelli, S., Anthony, K., Abbs, S., Garralda, M.E., Bourke, J., Wells, D.J. et al. (2011) 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, 595-605.
10. Goemans, N.M., Tulinius, M.,Vanden Akker, J.T., Burm, B.E., Ekhart, P.F., Heuvelmans, N., Holling, T., Janson, A.A., Platenburg, G.J., Sipkens, J.A. et al. (2011) Systemic administration of PRO051 in Duchenne's muscular dystrophy. N. Engl. J. Med., 364, 1513-1522.
11. Arora, V., Devi, GR. and Iversen, PL. (2004) Neutrally charged phosphorodiamidate morpholino antisense oligomers: uptake, efficacy and pharmacokinetics. Curr. Pharm. Biotechnol., 5, 431-439.
12. Ghosh, C. and Iversen, P.L. (2000) Intracellular delivery strategies for antisense phosphorodiamidate morpholino oligomers. Antisense Nucleic Acid Drug Dev., 10, 263-274.
13. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. and Sweeney, H.L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA, 90, 3710-3714.
14. McArdle, A., Edwards, R.H. and Jackson, M.J. (1994) Time course of changes in plasma membrane permeability in the dystrophin-deficient mdx mouse. Muscle Nerve, 17, 1378-1384.
15. Araki, E., Nakamura, K., Nakao, K., Kameya, S., Kobayashi, O., Nonaka, I., Kobayashi, T. and Katsuki, M. (1997) Targeted disruption of exon 52 in the mouse dystrophin gene induced muscle degeneration similar to that observed in Duchenne muscular dystrophy. Biochem. Biophys. Res. Commun., 238, 492-497.
16. Miyagoe, Y., Hanaoka, K., Nonaka, I., Hayasaka, M., Nabeshima, Y., Arahata, K. and Takeda, S. (1997) Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett., 415, 33-39.
17. Saito, T., Nakamura, A., Aoki, Y., Yokota, T., Okada, T., Osawa, M. and Takeda, S. (2010) Antisense PMO found in dystrophic dog model was effective in cells from Exon 7-deleted DMD patient. PLoS ONE, 5, 8.
18. Amantana,A. and Iversen, PL. (2005) Pharmacokinetics and biodistribution of phosphorodiamidate morpholino antisense oligomers. Curr. Opin. Pharmacol., 5, 550-555.
19. Hudziak, R.M., Barofsky, E., Barofsky, D.F., Weller, D.L., Huang, S.B. and Weller, D.D. (1996) Resistance of morpholino phosphorodiamidate oligomers to enzymatic degradation. Antisense Nucleic Acid Drug Dev., 6, 267-272.
20. Moulton, H.M. and Moulton, J.D. (2010) Morpholinos and their peptide conjugates: therapeutic promise and challenge for Duchenne muscular dystrophy. Biochim. Biophys. Acta, 1798, 2296-2303.
21. Popplewell, L.J., Malerba, A. and Dickson, G. (2012) Optimizing antisense oligonucleotides using phosphorodiamidate morpholino oligomers. Methods Mol. Biol., 867, 143-167.
22. Iversen, P.L., Aird, K.M., Wu, R., Morse, M.M. and Devi, G.R. (2009) Cellular uptake of neutral phosphorodiamidate morpholino oligomers. Curr. Pharm. Biotechnol., 10, 579-588.
23. Mokri, B. and Engel, A.G. (1975) Duchenne dystrophy: electron microscopic findings pointing to a basic or early abnormality in the plasma membrane of the muscle fiber. Neurology, 25, 1111-1120.
24. Yokota, T., Takeda, S., Lu, Q.-L., Partridge, T.A., Nakamura, A. and Hoffman, E.P. (2009) A renaissance for antisense oligonucleotide drugs in neurology: exon skipping breaks new ground. Arch. Neurol., 66, 32-38.
25. Hoffman, E.P., Bronson, A., Levin, A.A., Takeda, S., Yokota, T., Baudy, A.R. and Connor, E.M. (2011) Restoring dystrophin expression in Duchenne muscular dystrophy muscle progress in exon skipping and stop codon read through. Am. J. Pathol., 179, 12-22.
26. Florence, J.M., Fox, P.T., Planer, G.J. and Brooke, M.H. (1985) Activity, creatine kinase, and myoglobin in Duchenne muscular dystrophy: a clue to etiology? Neurology, 35, 758-761.
27. Ozawa, E. (2010) Our trails and trials in the subsarcolemmal cytoskeleton network and muscular dystrophy researches in the dystrophin era. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci., 86, 798-821.
28. Heemskerk, H., De Winter, C., Van Kuik, P., Heuvelmans, N., Sabatelli, P., Rimessi, P., Braghetta, P., Van Ommen, G.-J.B., De Kimpe, S., Ferlini, A. et al. (2010) Preclinical PK and PD studies on 2'-O-methyl-phosphorothioate RNA antisense oligonucleotides in the mdx mouse model. Mol. Ther., 18, 1210-1217.
29. Matsuda, R., Nishikawa, A. and Tanaka, H. (1995) Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem., 118, 959-964.
30. Straub, V., Rafael, J.A., Chamberlain, J.S. and Campbell, K.P. (1997) Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol., 139, 375-385.
31. Wood, M.J.A., Gait, M.J. and Yin, H. (2010) RNA-targeted splice-correction therapy for neuromuscular disease. Brain, 133, 957-972.
32. Nakamura, A. and Takeda, S. (2011) Exon-skipping therapy for Duchenne muscular dystrophy. Lancet, 378, 546-547.
33. Yokota, T., Nakamura, A., Nagata, T., Saito, T., Kobayashi, M., Aoki, Y., Echigoya, Y., Partridge, T., Hoffman, E.P. and Takeda, S. (2012) Extensive and prolonged restoration of dystrophin expression with vivo-morpholino-mediated multiple exon skipping in dystrophic dogs. Nucleic Acid Ther., 22, 306-315.
34. Ezzat, K., Helmfors, H., Tudoran, O., Juks, C., Lindberg, S., Padari, K., El-Andaloussi, S., Pooga, M. and Langel, U. (2012) Scavenger receptor-mediated uptake of cell-penetrating peptide nanocomplexes with oligonucleotides. FASEB J., 26, 1172-1180.
35. Moulton, H.M., Fletcher, S., Neuman, B.W., McClorey, G., Stein, D.A., Abes, S., Wilton, S.D., Buchmeier, M.J., Lebleu, B. and Iversen, P.L. (2007) Cell-penetrating peptide-morpholino conjugates alter pre-mRNA splicing of DMD (Duchenne muscular dystrophy) and inhibit murine coronavirus replication in vivo. Biochem. Soc. Trans., 35, 826-828.
36. Yin, H., Moulton, H.M., Betts, C., Merritt, T., Seow, Y., Ashraf, S., Wang, Q., Boutilier, J. and Wood, M.J. (2010) Functional rescue of dystrophin-deficient mdx mice by a chimeric peptide-PMO. Mol. Ther., 18, 1822-1829.
37. Moulton, H.M., Nelson, M.H., Hatlevig, S.A., Reddy, M.T. and Iversen, P.L. (2004) Cellular uptake of antisense morpholino oligomers conjugated to arginine-rich peptides. Bioconjug. Chem., 15, 290-299.
38. Amantana, A., Moulton, H.M., Cate, M.L., Reddy, M.T., Whitehead, T., Hassinger, J.N., Youngblood, D.S. and Iversen, P.L. (2007) Pharmacokinetics, biodistribution, stability and toxicity of a cell-penetrating peptide-morpholino oligomer conjugate. Bioconjug. Chem., 18, 1325-1331.
39. Henry, S.P., Giclas, P.C., Leeds, J., Pangburn, M., Auletta, C., Levin, A.A. and Kornbrust, D.J. (1997) Activation of the alternative pathway of complement by a phosphorothioate oligonucleotide: potential mechanismof action. J. Pharmacol. Exp. Ther., 281, 810-816.
40. Sheehan, J.P. and Lan, H.C. (1998) Phosphorothioate oligonucleotides inhibit the intrinsic tenase complex. Blood, 92, 1617-1625.
41. Hawke, T.J. and Garry, D.J. (2001) Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol., 91, 534-551.
42. Miyagoe-Suzuki, Y., Nakagawa, M. and Takeda, S. (2000) Merosin and congenital muscular dystrophy. Microsc. Res. Tech., 48, 181-191.
43. Gawlik, K.I. and Durbeej, M. (2011) Skeletal muscle laminin and MDC1A: pathogenesis and treatment strategies. Skeletal Muscle, 1, 9.
44. Sunada, Y., Bernier, S.M., Utani, A., Yamada, Y. and Campbell, K.P. (1995) Identification of a novel mutant transcript of laminin alpha 2 chain gene responsible for muscular dystrophy and dysmyelination in dy2J mice. Hum. Mol. Genet., 4, 1055-1061.
45. Allamand, V. and Guicheney, P. (2002) Merosin-deficient congenital muscular dystrophy, autosomal recessive (MDC1A, MIM#156225, LAMA2 gene coding for alpha2 chain of laminin). Eur. J. Hum. Genet., 10, 91-94.
46. Cartegni, L., Wang, J., Zhu, Z., Zhang, MQ. and Krainer, AR. (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res., 31, 3568-3571.