A duchenne muscular dystrophy gene hot spot mutation in dystrophin-deficient Cavalier King Charles Spaniels is amenable to exon 51 skipping

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Walmsley, Gemma L ^a   Arechavala Gomeza, Virginia ^b   Fernandez Fuente, Marta ^a,b   Burke, Margaret M ^c   Nagel, Nicole ^d   Holder, Angela ^a   Stanley, Rachael ^a   Chandler, Kate ^a   Marks, Stanley L ^e   Muntoni, Francesco ^b   Shelton, Diane G ^f   Piercy, Richard J ^a,b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c HAREFIELD HOSPITAL   (United Kingdom)

^d Alphapet Veterinary Clinic   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; DYSTROPHIN; MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAVALIER KING CHARLES SPANIEL; CELL CULTURE; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOG; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN GENE; EXON; EXON SKIPPING; EXPERIMENTAL MODEL; FEMALE; FRAMESHIFT MUTATION; GENE; GENE DELETION; GENE MUTATION; GENETIC TRANSCRIPTION; HISTOPATHOLOGY; HUMAN; MALE; MDX GENE; MISSENSE MUTATION; MOUSE; MUSCLE BIOPSY; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; RNA TRANSLATION; SKELETAL MUSCLE; UNITED KINGDOM; UNITED STATES;

ANIMALIA; CANIS FAMILIARIS;

EID: 77649263080     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008647     Document Type: Article

References (48)

1. Bushby K, Bourke J, Bullock R, Eagle M, Gibson M, et al. (2005) The multidisciplinary management of Duchenne muscular dystrophy. Current Paediatrics 15: 292-300.
2. Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, et al. (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517.
3. Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
4. Ahn AH, Kunkel LM (1993) The structural and functional diversity of dystrophin. Nat Genet 3: 283-291.
5. Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7: 762-773.
6. Feron M, Guevel L, Rouger K, Dubreil L, Arnaud MC, et al. (2009) PTEN contributes to profound PI3K/Akt signaling pathway deregulation in dystrophin-deficient dog muscle. Am J Pathol 174: 1459-1470.
7. Aartsma-Rus A, Van Deutekom JC, Fokkema IF, Van Ommen GJ, Den Dunnen JT (2006) 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 34: 135-144.
8. Koenig M, Beggs AH, Moyer M, Scherpf S, Heindrich K, et al. (1989) The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion. Am J Hum Genet 45: 498-506.
9. Den Dunnen JT, Grootscholten PM, Bakker E, Blonden LA, Ginjaar HB, et al. (1989) Topography of the Duchenne muscular dystrophy (DMD) gene: FIGE and cDNA analysis of 194 cases reveals 115 deletions and 13 duplications. Am J Hum Genet 45: 835-847.
10. Nobile C, Marchi J, Nigro V, Roberts RG, Danieli GA (1997) Exon-intron organization of the human dystrophin gene. Genomics 45: 421-424.
11. Aartsma-Rus A, van Ommen GJ (2007) Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. RNA 13: 1609-1624.
12. van Deutekom JC, van Ommen GJ (2003) Advances in Duchenne muscular dystrophy gene therapy. Nat Rev Genet 4: 774-783.
13. Kinali M, Arechavala-Gomeza V, Feng L, Cirak S, Hunt D, et al. (2009) 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 8: 918-928.
14. Aartsma-Rus A, Janson AA, Kaman WE, Bremmer-Bout M, van Ommen GJ, et al. (2004) Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 74: 83-92.
15. Arechavala-Gomeza V, Graham IR, Popplewell LJ, Adams AM, Aartsma-Rus A, et al. (2007) Comparative analysis of antisense oligonucleotide sequences for targeted skipping of exon 51 during dystrophin pre-mRNA splicing in human muscle. Hum Gene Ther 18: 798-810.
16. Schatzberg SJ, Olby NJ, Breen M, Anderson LV, Langford CF, et al. (1999) Molecular analysis of a spontaneous dystrophin 'knockout' dog. Neuromuscul Disord 9: 289-295.
17. Shelton GD, Engvall E (2005) Canine and feline models of human inherited muscle diseases. Neuromuscul Disord 15: 127-138.
18. Banks GB, Chamberlain JS (2008) The value of mammalian models for duchenne muscular dystrophy in developing therapeutic strategies. Curr Top Dev Biol 84: 431-453.
19. Sampaolesi M, Blot S, D'Antona G, Granger N, Tonlorenzi R, et al. (2006) Mesoangioblast stem cells ameliorate muscle function in dystrophic dogs. Nature 444: 574-579.
20. McClorey G, Moulton HM, Iversen PL, Fletcher S, Wilton SD (2006) Antisense oligonucleotide-induced exon skipping restores dystrophin expression in vitro in a canine model of DMD. Gene Ther 13: 1373-1381.
21. Shimatsu Y, Katagiri K, Furuta T, Nakura M, Tanioka Y, et al. (2003) Canine X-linked muscular dystrophy in Japan (CXMDJ). Exp Anim 52: 93-97.
22. Yokota T, Lu QL, Partridge T, Kobayashi M, Nakamura A, et al. (2009) Efficacy of systemic morpholino exon-skipping in duchenne dystrophy dogs. Ann Neurol.
23. Matsumura K, Campbell KP (1994) Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle Nerve 17: 2-15.
24. Chapman VM, Miller DR, Armstrong D, Caskey CT (1989) Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc Natl Acad Sci U S A 86: 1292-1296.
25. Im WB, Phelps SF, Copen EH, Adams EG, Slightom JL, et al. (1996) Differential expression of dystrophin isoforms in strains of mdx mice with different mutations. Hum Mol Genet 5: 1149-1153.
26. Duan D (2006) Challenges and opportunities in dystrophin-deficient cardiomyopathy gene therapy. Hum Mol Genet 15 Spec No 2: R253-261.
27. Gaschen FP, Hoffman EP, Gorospe JR, Uhl EW, Senior DF, et al. (1992) Dystrophin deficiency causes lethal muscle hypertrophy in cats. J Neurol Sci 110: 149-159.
28. Winand NJ, Edwards M, Pradhan D, Berian CA, Cooper BJ (1994) Deletion of the dystrophin muscle promoter in feline muscular dystrophy. Neuromuscul Disord 4: 433-445.
29. Gaschen F, Burgunder JM (2001) Changes of skeletal muscle in young dystrophin-deficient cats: a morphological and morphometric study. Acta Neuropathol 101: 591-600.
30. Cooper BJ, Winand NJ, Stedman H, Valentine BA, Hoffman EP, et al. (1988) The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 334: 154-156.
31. Sharp NJ, Kornegay JN, Van Camp SD, Herbstreith MH, Secore SL, et al. (1992) An error in dystrophin mRNA processing in golden retriever muscular dystrophy, an animal homologue of Duchenne muscular dystrophy. Genomics 13: 115-121.
32. Schatzberg SJ, Shelton GD (2004) Newly identified neuromuscular disorders. Vet Clin North Am Small Anim Pract 34: 1497-1524.
33. Shimatsu Y, Yoshimura M, Yuasa K, Urasawa N, Tomohiro M, et al. (2005) Major clinical and histopathological characteristics of canine X-linked muscular dystrophy in Japan, CXMDJ. Acta Myol 24: 145-154.
34. Ambrosio CE, Valadares MC, Zucconi E, Cabral R, Pearson PL, et al. (2008) Ringo, a Golden Retriever Muscular Dystrophy (GRMD) dog with absent dystrophin but normal strength. Neuromuscul Disord 18: 892-893.
35. Schatzberg SJ, Anderson LV, Wilton SD, Kornegay JN, Mann CJ, et al. (1998) Alternative dystrophin gene transcripts in golden retriever muscular dystrophy. Muscle Nerve 21: 991-998.
36. Dubowitz V (2006) Enigmatic conflict of clinical and molecular diagnosis in Duchenne/Becker muscular dystrophy. Neuromuscul Disord 16: 865-866.
37. Karpati G, Carpenter S, Morris GE, Davies KE, Guerin C, et al. (1993) Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J Neuropathol Exp Neurol 52: 119-128.
38. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE (1998) Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19: 79-82.
39. Cerletti M, Negri T, Cozzi F, Colpo R, Andreetta F, et al. (2003) Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther 10: 750-757.
40. Muntoni F, Torelli S, Ferlini A (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol 2: 731-740.
41. Yugeta N, Urasawa N, Fujii Y, Yoshimura M, Yuasa K, et al. (2006) Cardiac involvement in Beagle-based canine X-linked muscular dystrophy in Japan (CXMDJ): electrocardiographic, echocardiographic, and morphologic studies. BMC Cardiovasc Disord 6: 47.
42. Valentine BA, Cummings JF, Cooper BJ (1989) Development of Duchenne-type cardiomyopathy. Morphologic studies in a canine model. Am J Pathol 135: 671-678.
43. Oudet C, Hanauer A, Clemens P, Caskey T, Mandel JL (1992) Two hot spots of recombination in the DMD gene correlate with the deletion prone regions. Hum Mol Genet 1: 599-603.
44. Sironi M, Pozzoli U, Comi GP, Riva S, Bordoni A, et al. (2006) A region in the dystrophin gene major hot spot harbors a cluster of deletion breakpoints and generates double-strand breaks in yeast. FASEB J 20: 1910-1912.
45. Rusbridge C, Knowler SP (2004) Inheritance of occipital bone hypoplasia (Chiari type I malformation) in Cavalier King Charles Spaniels. J Vet Intern Med 18: 673-8.
46. Fanin M, Danieli GA, Cadaldini M, Miorin M, Vitiello L, et al. (1995) Dystrophin-positive fibers in Duchenne dystrophy: origin and correlation to clinical course. Muscle Nerve 18: 1115-1120.
47. Yokota T, Lu QL, Morgan JE, Davies KE, Fisher R, et al. (2006) Expansion of revertant fibers in dystrophic mdx muscles reflects activity of muscle precursor cells and serves as an index of muscle regeneration. J Cell Sci 119: 2679-2687.
48. Dubowitz V, Sewry CA (2007) Muscle Biopsy. A Practical Approach: Elsevier. pp 11-39.