Restoration of the dystrophin-associated glycoprotein complex after exon skipping therapy in duchenne muscular dystrophy

Molecular Therapy

Volumn 20, Issue 2, 2012, Pages 462-467

  Cirak, Sebahattin ^a   Feng, Lucy ^a   Anthony, Karen ^a   Arechavala Gomeza, Virginia ^a   Torelli, Silvia ^a   Sewry, Caroline ^a,b   Morgan, Jennifer E ^a   Muntoni, Francesco ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROBERT JONES AND AGNES HUNT ORTHOPAEDIC HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SARCOGLYCAN; BETA DYSTROGLYCAN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; ETEPLIRSEN; NEURONAL NITRIC OXIDE SYNTHASE;

ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; GENE DELETION; HUMAN; HUMAN TISSUE; OPEN READING FRAME; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; SARCOLEMMA; SINGLE DRUG DOSE;

EID: 84856546632     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.248     Document Type: Article

References (42)

1. Bushby, K, Finkel, R, Birnkrant, DJ, Case, LE, Clemens, PR, Cripe, L et al.; DMD Care Considerations Working Group. (2010). Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management. Lancet Neurol 9: 77-93.
2. Ervasti, JM and Campbell, KP (1993). A role for the dystrophin- glycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122: 809-823. (Pubitemid 23241091)
3. Ibraghimov-Beskrovnaya, O, Ervasti, JM, Leveille, CJ, Slaughter, CA, Sernett, SW and Campbell, KP (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355: 696-702.
4. Ishikawa-Sakurai, M, Yoshida, M, Imamura, M, Davies, KE and Ozawa, E (2004). ZZ domain is essentially required for the physiological binding of dystrophin and utrophin to-dystroglycan. Hum Mol Genet 13: 693-702. (Pubitemid 38455957)
5. Hnia, K, Zouiten, D, Cantel, S, Chazalette, D, Hugon, G, Fehrentz, JA et al. (2007). ZZ domain of dystrophin and utrophin: topology and mapping of a-dystroglycan interaction site. Biochem J 401: 667-677. (Pubitemid 46219261)
6. Crawford, GE, Faulkner, JA, Crosbie, RH, Campbell, KP, Froehner, SC and Chamberlain, JS (2000). Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150: 1399-1410.
7. Peters, MF, Adams, ME and Froehner, SC (1997). Differential association of syntrophin pairs with the dystrophin complex. J Cell Biol 138: 81-93. (Pubitemid 27337454)
8. Sadoulet-Puccio, HM, Rajala, M and Kunkel, LM (1997). Dystrobrevin and dystrophin: an interaction through coiled-coil motifs. Proc Natl Acad Sci USA 94: 12413-12418. (Pubitemid 27492542)
9. Millay, DP, Sargent, MA, Osinska, H, Baines, CP, Barton, ER, Vuagniaux, G et al. (2008). Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 14: 442-447. (Pubitemid 351499389)
10. Percival, JM, Anderson, KN, Huang, P, Adams, ME and Froehner, SC (2010). Golgi and sarcolemmal neuronal NOS differentially regulate contraction-induced fatigue and vasoconstriction in exercising mouse skeletal muscle. J Clin Invest 120: 816-826.
11. Bushby, KM, Gardner-Medwin, D, Nicholson, LV, Johnson, MA, Haggerty, ID, Cleghorn, NJ et al. (1993). The clinical, genetic and dystrophin characteristics of Becker muscular dystrophy. II. Correlation of phenotype with genetic and protein abnormalities. J Neurol 240: 105-112. (Pubitemid 23073201)
12. Alter, J, Lou, F, Rabinowitz, A, Yin, H, Rosenfeld, J, Wilton, SD et al. (2006). Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 12: 175-177. (Pubitemid 43214742)
13. Arechavala-Gomeza, V, Graham, IR, Popplewell, LJ, Adams, AM, Aartsma-Rus, A, Kinali, M 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. (Pubitemid 47502846)
14. Lu, QL, Mann, CJ, Lou, F, Bou-Gharios, G, Morris, GE, Xue, SA et al. (2003). Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat Med 9: 1009-1014. (Pubitemid 37021780)
15. Yokota, T, Lu, QL, Partridge, T, Kobayashi, M, Nakamura, A, Takeda, S et al. (2009). Efficacy of systemic morpholino exon-skipping in Duchenne dystrophy dogs. Ann Neurol 65: 667-676.
16. Kinali, M, Arechavala-Gomeza, V, Feng, L, Cirak, S, Hunt, D, Adkin, C 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.
17. van Deutekom, JC, Janson, AA, Ginjaar, IB, Frankhuizen, WS, Aartsma-Rus, A, Bremmer-Bout, M et al. (2007). Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 357: 2677-2686.
18. Heemskerk, HA, de Winter, CL, de Kimpe, SJ, van Kuik-Romeijn, P, Heuvelmans, N, Platenburg, GJ et al. (2009). In vivo comparison of 2-O-methyl phosphorothioate and morpholino antisense oligonucleotides for Duchenne muscular dystrophy exon skipping. J Gene Med 11: 257-266.
19. Fletcher, S, Honeyman, K, Fall, AM, Harding, PL, Johnsen, RD and Wilton, SD (2006). Dystrophin expression in the mdx mouse after localised and systemic administration of a morpholino antisense oligonucleotide. J Gene Med 8: 207-216. (Pubitemid 43250701)
20. Mitrpant, C, Fletcher, S, Iversen, PL and Wilton, SD (2009). By-passing the nonsense mutation in the 4 CV mouse model of muscular dystrophy by induced exon skipping. J Gene Med 11: 46-56.
21. Anderson, LV and Davison, K (1999). Multiplex Western blotting system for the analysis of muscular dystrophy proteins. Am J Pathol 154: 1017-1022. (Pubitemid 29169736)
22. Chang, WJ, Iannaccone, ST, Lau, KS, Masters, BS, McCabe, TJ, McMillan, K et al. (1996). Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93: 9142-9147. (Pubitemid 26282032)
23. Dubowitz V, Sewry C. Muscle Biopsy: A Practical Approach, 3rd edn., Saunders: Elsevier, 2007.
24. Matsumura, K, Tomé, FM, Ionasescu, V, Ervasti, JM, Anderson, RD, Romero, NB et al. (1993). Deficiency of dystrophin-associated proteins in Duchenne muscular dystrophy patients lacking COOH-terminal domains of dystrophin. J Clin Invest 92: 866-871. (Pubitemid 23262409)
25. Ohlendieck, K, Matsumura, K, Ionasescu, VV, Towbin, JA, Bosch, EP, Weinstein, SL et al. (1993). Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology 43: 795-800. (Pubitemid 23121977)
26. Lenk, U, Oexle, K, Voit, T, Ancker, U, Hellner, KA, Speer, A et al. (1996). A cysteine 3340 substitution in the dystroglycan-binding domain of dystrophin associated with Duchenne muscular dystrophy, mental retardation and absence of the ERG b-wave. Hum Mol Genet 5: 973-975. (Pubitemid 26232277)
27. Goldberg, LR, Hausmanowa-Petrusewicz, I, Fidzianska, A, Duggan, DJ, Steinberg, LS and Hoffman, EP (1998). A dystrophin missense mutation showing persistence of dystrophin and dystrophin-associated proteins yet a severe phenotype. Ann Neurol 44: 971-976. (Pubitemid 28558262)
28. Muntoni, F, Gobbi, P, Sewry, C, Sherratt, T, Taylor, J, Sandhu, SK et al. (1994). Deletions in the 5 region of dystrophin and resulting phenotypes. J Med Genet 31: 843-847.
29. Prior, TW, Papp, AC, Snyder, PJ, Burghes, AH, Bartolo, C, Sedra, MS et al. (1993). A missense mutation in the dystrophin gene in a Duchenne muscular dystrophy patient. Nat Genet 4: 357-360. (Pubitemid 23231483)
30. Malerba, A, Sharp, PS, Graham, IR, Arechavala-Gomeza, V, Foster, K, Muntoni, F et al. (2011). Chronic systemic therapy with low-dose morpholino oligomers ameliorates the pathology and normalizes locomotor behavior in mdx mice. Mol Ther 19: 345-354.
31. Lai, Y, Thomas, GD, Yue, Y, Yang, HT, Li, D, Long, C et al. (2009). Dystrophins carrying spectrin-like repeats 16 and 17 anchor nNOS to the sarcolemma and enhance exercise performance in a mouse model of muscular dystrophy. J Clin Invest 119: 624-635.
32. Torelli, S, Brown, SC, Jimenez-Mallebrera, C, Feng, L, Muntoni, F and Sewry, CA (2004). Absence of neuronal nitric oxide synthase (nNOS) as a pathological marker for the diagnosis of Becker muscular dystrophy with rod domain deletions. Neuropathol Appl Neurobiol 30: 540-545. (Pubitemid 39423041)
33. Wells, KE, Torelli, S, Lu, Q, Brown, SC, Partridge, T, Muntoni, F et al. (2003). Relocalization of neuronal nitric oxide synthase (nNOS) as a marker for complete restoration of the dystrophin associated protein complex in skeletal muscle. Neuromuscul Disord 13: 21-31. (Pubitemid 35430136)
34. Kobayashi, YM, Rader, EP, Crawford, RW, Iyengar, NK, Thedens, DR, Faulkner, JA et al. (2008). Sarcolemma-localized nNOS is required to maintain activity after mild exercise. Nature 456: 511-515. (Pubitemid 352759004)
35. Finanger Hedderick, EL, Simmers, JL, Soleimani, A, Andres-Mateos, E, Marx, R, Files, DC et al. (2011). Loss of sarcolemmal nNOS is common in acquired and inherited neuromuscular disorders. Neurology 76: 960-967.
36. Finanger Hedderick, EL, Simmers, JL, Soleimani, A, Andres-Mateos, E, Marx, R, Files, DC et al. (2011). Loss of sarcolemmal nNOS is common in acquired and inherited neuromuscular disorders. Neurology 76: 960-967.
37. Lawler, JM (2011). Exacerbation of pathology by oxidative stress in respiratory and locomotor muscles with Duchenne muscular dystrophy. J Physiol (Lond) 589(Pt 9): 2161-2170.
38. Muntoni, F, Di Lenarda, A, Porcu, M, Sinagra, G, Mateddu, A, Marrosu, G et al. (1997). Dystrophin gene abnormalities in two patients with idiopathic dilated cardiomyopathy. Heart 78: 608-612. (Pubitemid 28034215)
39. Melis, MA, Cau, M, Muntoni, F, Mateddu, A, Galanello, R, Boccone, L et al. (1998). Elevation of serum creatine kinase as the only manifestation of an intragenic deletion of the dystrophin gene in three unrelated families. Eur J Paediatr Neurol 2: 255-261. (Pubitemid 28553033)
40. Helderman-van den Enden, AT, Straathof, CS, Aartsma-Rus, A, den Dunnen, JT, Verbist, BM, Bakker, E et al. (2010). Becker muscular dystrophy patients with deletions around exon 51; a promising outlook for exon skipping therapy in Duchenne patients. Neuromuscul Disord 20: 251-254.
41. Rafael, JA, Townsend, ER, Squire, SE, Potter, AC, Chamberlain, JS and Davies, KE (2000). Dystrophin and utrophin influence fiber type composition and post-synaptic membrane structure. Hum Mol Genet 9: 1357-1367. (Pubitemid 30312484)
42. Arechavala-Gomeza, V, Kinali, M, Feng, L, Brown, SC, Sewry, C, Morgan, JE et al. (2010). Immunohistological intensity measurements as a tool to assess sarcolemmaassociated protein expression. Neuropathol Appl Neurobiol 36: 265-274.