- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Annual Issues ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 184393, 8 pages
Mammalian Models of Duchenne Muscular Dystrophy: Pathological Characteristics and Therapeutic Applications
1Department of Medicine (Neurology and Rheumatology), School of Medicine Shinshu University, 3-1-1 Ahahi, Matsumoto 390-8621, Japan
2Department of Molecular Therapy, National Institute of Neuroscience, National Center of Neurology and Psychiatry, 4-1-1 Ogawa-higashi, Kodaira, Tokyo 187-8502, Japan
Received 14 October 2010; Accepted 19 December 2010
Academic Editor: Andrea Vecchione
Copyright © 2011 Akinori Nakamura and Shin'ichi Takeda. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- H. Moser, “Duchenne muscular dystrophy: pathogenetic aspects and genetic prevention,” Human Genetics, vol. 66, no. 1, pp. 17–40, 1984.
- E. P. Hoffman, R. H. Brown Jr., and L. M. Kunkel, “Dystrophin: the protein product of the Duchenne muscular dystrophy locus,” Cell, vol. 51, no. 6, pp. 919–928, 1987.
- K. P. Campbell, “Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage,” Cell, vol. 80, no. 5, pp. 675–679, 1995.
- G. D. Shelton and E. Engvall, “Canine and feline models of human inherited muscle diseases,” Neuromuscular Disorders, vol. 15, no. 2, pp. 127–138, 2005.
- E. W. Yeung, N. P. Whitehead, T. M. Suchyna, P. A. Gottlieb, F. Sachs, and D. G. Allen, “Effects of stretch-activated channel blockers on and muscle damage in the mdx mouse,” Journal of Physiology, vol. 562, no. 2, pp. 367–380, 2005.
- M. Koening, A. H. Beggs, M. Moyer et al., “The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion,” American Journal of Human Genetics, vol. 45, no. 4, pp. 498–506, 1989.
- C. Wilson and A. D. Keefe, “Building oligonucleotide therapeutics using non-natural chemistries,” Current Opinion in Chemical Biology, vol. 10, no. 6, pp. 607–614, 2006.
- S. Karkare and D. Bhatnagar, “Promising nucleic acid analogs and mimics: characteristic features and applications of PNA, LNA, and morpholino,” Applied Microbiology and Biotechnology, vol. 71, no. 5, pp. 575–586, 2006.
- M. Yoshimura, M. Sakamoto, M. Ikemoto et al., “AAV vector-mediated microdystrophin expression in a relatively small percentage of mdx myofibers improved the mdx phenotype,” Molecular Therapy, vol. 10, no. 5, pp. 821–828, 2004.
- P. Gregorevic, J. M. Allen, E. Minami et al., “rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice,” Nature Medicine, vol. 12, no. 7, pp. 787–789, 2006.
- G. R. Coulton, N. A. Curtin, J. E. Morgan, and T. A. Partridge, “The mdx mouse skeletal muscle myopathy: II. Contractile properties,” Neuropathology and Applied Neurobiology, vol. 14, no. 4, pp. 299–314, 1988.
- W. B. Im, S. F. Phelps, E. H. Copen, E. G. Adams, J. L. Slightom, and J. S. Chamberlain, “Differential expression of dystrophin isoforms in strains of mdx mice with different mutations,” Human Molecular Genetics, vol. 5, no. 8, pp. 1149–1153, 1996.
- E. Araki, K. Nakamura, K. Nakao et al., “Targeted disruption of exon 52 in the mouse dystrophin gene induced muscle degeneration similar to that observed in duchenne muscular dystrophy,” Biochemical and Biophysical Research Communications, vol. 238, no. 2, pp. 492–497, 1997.
- A. E. Deconinck, J. A. Rafael, J. A. Skinner et al., “Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy,” Cell, vol. 90, no. 4, pp. 717–727, 1997.
- G. Bulfield, W. G. Siller, P. A. L. Wight, and K. J. Moore, “X chromosome-linked muscular dystrophy (mdx) in the mouse,” Proceedings of the National Academy of Sciences of the United States of America, vol. 81, no. 4 I, pp. 1189–1192, 1984.
- J. Dangain and G. Vrbova, “Muscle development in mdx mutant mice,” Muscle and Nerve, vol. 7, no. 9, pp. 700–704, 1984.
- Y. Tanabe, K. Esaki, and T. Nomura, “Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse,” Acta Neuropathologica, vol. 69, no. 1-2, pp. 91–95, 1986.
- Q. L. Lu, C. J. Mann, F. Lou et al., “Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse,” Nature Medicine, vol. 9, no. 8, pp. 1009–1014, 2003.
- D. J. Wells, “Therapeutic restoration of dystrophin expression in Duchenne muscular dystrophy,” Journal of Muscle Research and Cell Motility, vol. 27, no. 5-7, pp. 387–398, 2006.
- S. Fletcher, K. Honeyman, A. M. Fall, P. L. Harding, R. D. Johnsen, and S. D. Wilton, “Dystrophin expression in the mdx mouse after localised and systemic administration of a morpholino antisense oligunucleotide,” Journal of Gene Medicine, vol. 8, no. 2, pp. 207–216, 2006.
- N. Jearawiriyapaisarn, H. M. Moulton, B. Buckley et al., “Sustained dystrophin expression induced by peptide-conjugated morpholino oligomers in the muscles of mdx mice,” Molecular Therapy, vol. 16, no. 9, pp. 1624–1629, 2008.
- A. Goyenvalle, A. Vulin, F. Fougerousse et al., “Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping,” Science, vol. 306, no. 5702, pp. 1796–1799, 2004.
- P. Gregorevic, M. J. Blankinship, J. M. Allen et al., “Systemic delivery of genes to striated muscles using adeno-associated viral vectors,” Nature Medicine, vol. 10, no. 8, pp. 828–834, 2004.
- Z. Wang, T. Zhu, C. Qiao et al., “Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart,” Nature Biotechnology, vol. 23, no. 3, pp. 321–328, 2005.
- L. T. Bish, K. Morine, M. M. Sleeper et al., “Adeno-associated virus (AAV) serotype 9 provides global cardiac gene transfer superior to AAV1, AAV6, AAV7, and AAV8 in the mouse and rat,” Human Gene Therapy, vol. 19, no. 12, pp. 1359–1368, 2008.
- S. Kameya, E. Araki, M. Katsuki et al., “Dp260 disrupted mice revealed prolonged implicit time of the b-wave in ERG and loss of accumulation of β-dystroglycan in the outer plexiform layer of the retina,” Human Molecular Genetics, vol. 6, no. 13, pp. 2195–2203, 1997.
- A. Aartsma-Rus, I. Fokkema, J. Verschuuren et al., “Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations,” Human Mutation, vol. 30, no. 3, pp. 293–299, 2009.
- M. Kinali, V. Arechavala-Gomeza, L. Feng 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,” The Lancet Neurology, vol. 8, no. 10, pp. 918–928, 2009.
- A. T. J. M. Helderman-van den Enden, C. S. M. Straathof, A. Aartsma-Rus et al., “Becker muscular dystrophy patients with deletions around exon 51; a promising outlook for exon skipping therapy in Duchenne patients,” Neuromuscular Disorders, vol. 20, no. 4, pp. 251–254, 2010.
- J. C. van Deutekom, A. A. Janson, I. B. Ginjaar et al., “Local dystrophin restoration with antisense oligonucleotide PRO051,” The New England Journal of Medicine, vol. 357, no. 26, pp. 2677–2686, 2007.
- F. Muntoni, K. Bushby, and G. Van Ommen, “128th ENMC International Workshop on 'Preclinical optimization and phase I/II clinical trials using antisense oligonucleotides in Duchenne muscular dystrophy' 22-24 October 2004, Naarden, The Netherlands,” Neuromuscular Disorders, vol. 15, no. 6, pp. 450–457, 2005.
- Y. Aoki, A. Nakamura, T. Yokota et al., “In-frame dystrophin following exon 51-skipping improves muscle pathology and function in the exon 52-deficient mdx mouse,” Molecular Therapy, vol. 18, no. 11, pp. 1995–2005, 2010.
- N. J. H. Sharp, J. N. Kornegay, S. D. van Camp et al., “An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy,” Genomics, vol. 13, no. 1, pp. 115–121, 1992.
- N. Winand, D. Pradham, and B. Cooper, “Molecular characterization of severe Duchenne-type muscular dystrophy in a family of Rottwiler dogs,” in Molecular Mechanism of Neuromuscular Disease, Muscular Dystrophy Association, Tucson, Ariz, USA, 1994.
- S. J. Schatzberg, N. J. Olby, M. Breen et al., “Molecular analysis of a spontaneous dystrophin 'knockout' dog,” Neuromuscular Disorders, vol. 9, no. 5, pp. 289–295, 1999.
- G. L. Walmsley, V. Arechavala-Gomeza, M. Fernandez-Fuente et al., “A duchenne muscular dystrophy gene hot spot mutation in dystrophin-deficient cavalier king charles spaniels is amenable to exon 51 skipping,” PloS one, vol. 5, no. 1, Article ID e8647, 2010.
- B. J. Cooper, N. J. Winand, H. Stedman et al., “The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs,” Nature, vol. 334, no. 6178, pp. 154–156, 1988.
- B. A. Valentine, B. J. Cooper, A. De Lahunta, R. O'Quinn, and J. T. Blue, “Canine X-linked muscular dystrophy. An animal model of Duchenne muscular dystrophy: clinical studies,” Journal of the Neurological Sciences, vol. 88, no. 1-3, pp. 69–81, 1988.
- F. Nguyen, Y. Cherel, L. Guigand, I. Goubault-Leroux, and M. Wyers, “Muscle lesions associated with dystrophin deficiency in neonatal golden retriever puppies,” Journal of Comparative Pathology, vol. 126, no. 2-3, pp. 100–108, 2002.
- N. S. Moise, B. A. Valentine, C. A. Brown et al., “Duchenne's cardiomyopathy in a canine model: electrocardiographic and echocardiographic studies,” Journal of the American College of Cardiology, vol. 17, no. 3, pp. 812–820, 1991.
- J. K. Perloff, W. C. Roberts, A. C. de Leon Jr., and D. O'Doherty, “The distinctive electrocardiogram of Duchenne's progressive muscular dystrophy. An electrocardiographic-pathologic correlative study,” The American Journal of Medicine, vol. 42, no. 2, pp. 179–188, 1967.
- J. M. Howell, S. Fletcher, B. A. Kakulas, M. O'Hara, H. Lochmuller, and G. Karpati, “Use of the dog model for Duchenne muscular dystrophy in gene therapy trials,” Neuromuscular Disorders, vol. 7, no. 5, pp. 325–328, 1997.
- J. M. Howell, H. Lochmüller, A. O'Hara et al., “High-level dystrophin expression after adenovirus-mediated dystrophin minigene transfer to skeletal muscle of dystrophic dogs: prolongation of expression with immunosuppression,” Human Gene Therapy, vol. 9, no. 5, pp. 629–634, 1998.
- J. N. Kornegay, J. Li, J. R. Bogan et al., “Widespread muscle expression of an AAV9 human mini-dystrophin vector after intravenous injection in neonatal dystrophin-deficient dogs,” Molecular Therapy, vol. 19, no. 8, pp. 1501–1508, 2010.
- R. J. Bartlett, S. Stockinger, M. M. Denis et al., “In vivo targeted repair of a point mutation in the canine dystrophin gene by a chimeric RNA/DNA oligonucleotide,” Nature Biotechnology, vol. 18, no. 6, pp. 615–622, 2000.
- G. McClorey, H. M. Moulton, P. L. Iversen, S. Fletcher, and S. D. Wilton, “Antisense oligonucleotide-induced exon skipping restores dystrophin expression in vitro in a canine model of DMD,” Gene Therapy, vol. 13, no. 19, pp. 1373–1381, 2006.
- Y. Shimatsu, K. Katagiri, T. Furuta et al., “Canine X-linked muscular dystrophy in Japan (CXMD),” Experimental Animals, vol. 52, no. 2, pp. 93–97, 2003.
- Y. Shimatsu, M. Yoshimura, K. Yuasa et al., “Major clinical and histopathological characteristics of canine X-linked muscular dystrophy in Japan, CXMD,” Acta Myologica, vol. 24, no. 2, pp. 145–154, 2005.
- N. Yugeta, N. Urasawa, Y. Fujii et al., “Cardiac involvement in Beagle-based canine X-linked muscular dystrophy in Japan (CXMD): electrocardiographic, echocardiographic, and morphologic studies,” BMC Cardiovascular Disorders, vol. 6, article 47, 2006.
- N. Urasawa, M. R. Wada, N. Machida et al., “Selective vacuolar degeneration in dystrophin-deficient canine Purkinje fibers despite preservation of dystrophin-associated proteins with overexpression of Dp71,” Circulation, vol. 117, no. 19, pp. 2437–2448, 2008.
- T. Yokota, Q. L. Lu, T. Partridge et al., “Efficacy of systemic morpholino exon-skipping in duchenne dystrophy dogs,” Annals of Neurology, vol. 65, no. 6, pp. 667–676, 2009.
- T. Saito, A. Nakamura, Y. Aoki et al., “Antisense PMO found in dystrophic dog model was effective in cells from exon 7-deleted DMD patient,” PLoS One, vol. 5, no. 8, Article ID e12239, 2010.
- K. Yuasa, M. Yoshimura, N. Urasawa et al., “Injection of a recombinant AAV serotype 2 into canine skeletal muscles evokes strong immune responses against transgene products,” Gene Therapy, vol. 14, no. 17, pp. 1249–1260, 2007.
- S. Ohshima, J. H. Shin, K. Yuasa et al., “Transduction efficiency and immune response associated with the administration of AAV8 vector into dog skeletal muscle,” Molecular Therapy, vol. 17, no. 1, pp. 73–80, 2009.
- J. Alter, F. Lou, A. Rabinowitz et al., “Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology,” Nature Medicine, vol. 12, no. 2, pp. 175–177, 2006.
- A. Aartsma-Rus, A. A. M. Janson, W. E. Kaman et al., “Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense,” American Journal of Human Genetics, vol. 74, no. 1, pp. 83–92, 2004.
- V. Arechavala-Gomeza, I. R. Graham, L. J. Popplewell et al., “Comparative analysis of antisense oligonucleotide sequences for targeted skipping of exon 51 during dystrophin pre-mRNA splicing in human muscle,” Human Gene Therapy, vol. 18, no. 9, pp. 798–810, 2007.
- A. Nakamura and S. Takeda, “Exon-skipping therapy for Duchenne muscular dystrophy,” Neuropathology, vol. 29, no. 4, pp. 494–501, 2009.
- J. H. Vos, J. S. van der Linde-Sipman, and S. A. Goedegebuure, “Dystrophy-like myopathy in the cat,” Journal of Comparative Pathology, vol. 96, no. 3, pp. 335–341, 1986.
- J. L. Carpenter, E. P. Hoffmann, F. C. A. Romanul et al., “Feline muscular dystrophy with dystrophin deficiency,” The American Journal of Pathology, vol. 135, no. 5, pp. 909–919, 1989.
- F. P. Gaschen, E. P. Hoffman, J. R. M. Gorospe et al., “Dystrophin deficiency causes lethal muscle hypertrophy in cats,” Journal of the Neurological Sciences, vol. 110, no. 1-2, pp. 149–159, 1992.
- N. J. Winand, M. Edwards, D. Pradhan, C. A. Berian, and B. J. Cooper, “Deletion of the dystrophin muscle promoter in feline muscular dystrophy,” Neuromuscular Disorders, vol. 4, no. 5-6, pp. 433–445, 1994.