Advances in genetic therapeutic strategies for Duchenne muscular dystrophy

Experimental Physiology

Volumn 100, Issue 12, 2015, Pages 1458-1467

  Guiraud, Simon ^a   Chen, Huijia ^a   Burns, David T ^a   Davies, Kay E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; UTROPHIN;

CLINICAL TRIAL (TOPIC); CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; DNA MODIFICATION; DUCHENNE MUSCULAR DYSTROPHY; EXON SKIPPING; GENE EXPRESSION; GENE REPLACEMENT THERAPY; GENE REPRESSION; GENE THERAPY; HUMAN; MUSCLE FUNCTION; NONHUMAN; REVIEW; RNA SPLICING; RNA TRANSLATION; STOP CODON; ANIMAL; GENETICS; METABOLISM; MUSCULAR DYSTROPHY, DUCHENNE; PROCEDURES; SKELETAL MUSCLE;

ANIMALS; CLINICAL TRIALS AS TOPIC; DYSTROPHIN; GENETIC THERAPY; HUMANS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; UTROPHIN;

EID: 84949313313     PISSN: 09580670     EISSN: 1469445X     Source Type: Journal    
DOI: 10.1113/EP085308     Document Type: Review

References (62)

1. Al-Rewashdy H, Ljubicic V, Lin W, Renaud JM & Jasmin BJ (2015). Utrophin A is essential in mediating the functional adaptations of mdx mouse muscle following chronic AMPK activation. Hum Mol Genet 24, 1243-1255.
2. Bach JR, O'Brien J, Krotenberg R & Alba AS (1987). Management of end stage respiratory failure in Duchenne muscular dystrophy. Muscle Nerve 10, 177-182.
3. Belanto JJ, Mader TL, Eckhoff MD, Strandjord DM, Banks GB, Gardner MK, Lowe, DA Ervasti, JM (2014). Microtubule binding distinguishes dystrophin from utrophin. Proc Natl Acad Sci USA 111, 5723-5728.
4. Béroud C, Tuffery-Giraud S, Matsuo M, Hamroun D, Humbertclaude V, Monnier N et al. (2007). Multiexon skipping leading to an artificial DMD protein lacking amino acids from exons 45 through 55 could rescue up to 63% of patients with Duchenne muscular dystrophy. Hum Mutat 28, 196-202.
5. Betts CA, Saleh AF, Carr CA, Hammond SM, Coenen-Stass AM, Godfrey C et al. (2015). Prevention of exercised induced cardiomyopathy following Pip-PMO treatment in dystrophic mdx mice. Sci Rep 5, 8986.
6. Bladen CL, Salgado D, Monges S, Foncuberta ME, Kekou K, Kosma K et al. (2015). The TREAT-NMD DMD Global Database: analysis of more than 7, 000 Duchenne muscular dystrophy mutations. Hum Mutat 36, 395-402.
7. Bulfield G, Siller WG, Wight PAL & Moore KJ (1984). X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81, 1189-1192.
8. Bushby K, Finkel R, Wong B, Barohn R, Campbell C, Comi GP et al. (2014). Ataluren treatment of patients with nonsense mutation dystrophinopathy. Muscle Nerve 50, 477-487.
9. Cerletti M, Negri T, Cozzi F, Colpo R, Andreetta F, Croci D et al. (2003). Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther 10, 750-757.
10. Chakkalakal JV, Harrison M-A, Carbonetto S, Chin E, Michel RN & Jasmin BJ (2004). Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum Mol Genet 13, 379-388.
11. Chamberlain JS (1997). Dystrophin levels required for genetic correction of Duchenne muscular dystrophy. Basic Appl Myol 7, 255-257.
12. Cohn RD & Campbell KP (2000). Molecular basis of muscular dystrophies. Muscle Nerve 23, 1456-1471.
13. Davies KE & Nowak KJ (2006). Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7, 762-773.
14. Dunckley MG, Manoharan M, Villiet P, Eperon IC & Dickson G (1998). Modification of splicing in the dystrophin gene in cultured Mdx muscle cells by antisense oligoribonucleotides. Hum Mol Genet 7, 1083-1090.
15. Emery AE (1990). Dystrophin function. Lancet 335, 1289.
16. Emery AEH (1993). Duchenne muscular dystrophy-Meryon's disease. Neuromuscul Disord 3, 263-266.
17. England SB, Nicholson LV, Johnson MA, Forrest SM, Love DR, Zubrzycka-Gaarn EE et al. (1990). Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343, 180-182.
18. Ervasti JM (2007). Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim Biophys Acta 1772, 108-117.
19. Fairclough RJ, Wood MJ & Davies KE (2013). Therapy for Duchenne muscular dystrophy: renewed optimism from genetic approaches. Nat Rev Genet 14, 373-378.
20. Fisher R, Tinsley JM, Phelps SR, Squire SE, Townsend ER, Martin JE et al. (2001). Non-toxic ubiquitous over-expression of utrophin in the mdx mouse. Neuromuscul Disord 11, 713-721.
21. Goyenvalle A, Griffith G, Babbs A, Andaloussi SE, Ezzat K, Avril A, Garcia L et al. (2015). Functional correction in mouse models of muscular dystrophy using exon-skipping tricyclo-DNA oligomers. Nat Med 21, 270-275.
22. Goyenvalle A, Vulin A, Fougerousse F, Leturcq F, Kaplan JC, Garcia L et al. (2004). Rescue of dystrophic muscle through U7 snRNA-mediated exon skipping. Science 306, 1796-1799.
23. Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, vanOmmen GJ & Kunkel LM (2015a). The pathogenesis and therapy of muscular dystrophies. Annu Rev Genomics Hum Genet 16, 281-308.
24. Guiraud S, Squire SE, Edwards B, Chen H, Burns DT, Shah N et al. (2015b). Second-generation compound for the modulation of utrophin in the therapy of DMD. Hum Mol Genet 24, 4212-4224.
25. Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, Phelps SF et al. (2002). Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8, 253-261.
26. Hayashita-Kinoh H, Yugeta N, Okada H, Nitahara-Kasahara Y, Chiyo T, Okada T et al. (2015). Intra-amniotic rAAV-mediated microdystrophin gene transfer improves canine X-linked muscular dystrophy and may induce immune tolerance. Mol Ther 23, 627-637.
27. Helliwell TR, Man NT, Morris GE & Davies KE (1992). The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromuscul Disord 2, 177-184.
28. Hollinger K, Gardan-Salmon D, Santana C, Rice D, Snella E & Selsby JT (2013). Rescue of dystrophic skeletal muscle by PGC-1α involves restored expression of dystrophin-associated protein complex components and satellite cell signaling. Am J Physiol Regul Integr Comp Physiol 305, R13-R23.
29. Jinek M, Chylinski K, Fonfara I, Hauer JA, Doudna JA & Charpentier E (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821.
30. 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.
31. Kleopa KA, Drousiotou A, Mavrikiou E, Ormiston A & Kyriakides T (2006). Naturally occurring utrophin correlates with disease severity in Duchenne muscular dystrophy. Hum Mol Genet 15, 1623-1628.
32. Koo T, Popplewell L, Athanasopoulos T & Dickson G (2014). Triple trans-splicing adeno-associated virus vectors capable of transferring the coding sequence for full-length dystrophin protein into dystrophic mice. Hum Gene Ther 25, 98-108.
33. Krag TO, Bogdanovich S, Jensen CJ, Fischer MD, Hansen-Schwartz J, Javazon EH et al. (2004). Heregulin ameliorates the dystrophic phenotype in mdx mice. Proc Natl Acad Sci USA 101, 13856-13860.
34. Le Hir M, Goyenvalle A, Peccate C, Précigout G, Davies KE, Voit T et al. (2013). AAV genome loss from dystrophic mouse muscles during AAV-U7 snRNA-mediated exon-skipping therapy. Mol Ther 21, 1551-1558.
35. Li D, Bareja A, Judge L, Yue Y, Lai Y, Fairclough R et al. (2010). Sarcolemmal nNOS anchoring reveals a qualitative difference between dystrophin and utrophin. J Cell Sci 123, 2008-2013.
36. Li HL, Fujimoto N, Sasakawa N, Shirai S, Ohkame T, Sakuma T et al. (2015). Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Reports 4, 143-154.
37. Long C, McAnally JR, Shelton JM, Mireault AA, Bassel-Duby R & Olson EN (2014). Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA. Science 345, 1184-1188.
38. Love DR, Hill DF, Dickson G, Spurr NK, Byth BC, Marsden RF et al. (1989). An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339, 55-58.
39. Malik V, Rodino-Klapac LR, Viollet L, Wall C, King W, Al-Dahhak R et al. (2010). Gentamicin-induced readthrough of stop codons in Duchenne muscular dystrophy. Ann Neurol 67, 771-780.
40. Mendell JR, Campbell K, Rodino-Klapac L, Sahenk Z, Shilling C, Lewis S et al. (2010). Dystrophin immunity in Duchenne's muscular dystrophy. N Engl J Med 363, 1429-1437.
41. Mendell JR, Rodino-Klapac LR, Sahenk Z, Roush K, Bird L, Lowes LP et al. (2013). Eteplirsen for the treatment of Duchenne muscular dystrophy. Ann Neurol 74, 637-647.
42. Mendell JR, Shilling C, Leslie ND, Flanigan KM, al-Dahhak R, Gastier-Foster J et al. (2012). Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann Neurol 71, 304-313.
43. Monaco AP, Neve RL, Colletti-Feener C, Bertelson CJ, Kurnit DM & Kunkel LM (1986). Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 323, 646-650.
44. Nguyen TM, Ellis JM, Love DR, Davies KE, Gatter KC, Dickson G et al. (1991). Localization of the DMDL gene-encoded dystrophin-related protein using a panel of nineteen monoclonal antibodies: presence at neuromuscular junctions, in the sarcolemma of dystrophic skeletal muscle, in vascular and other smooth muscles, and in proliferating brain cell lines. J Cell Biol 115, 1695-1700.
45. Ousterout DG, Kabadi AM, Thakore PI, Majoros WH, Reddy TE & Gersbach CA (2015). Multiplex CRISPR/Cas9-based genome editing for correction of dystrophin mutations that cause Duchenne muscular dystrophy. Nat Commun 6, 6244.
46. Ramachandran J, Schneider JS, Crassous PA, Zheng R, Gonzalez JP, Xie LH et al. (2013). Nitric oxide signalling pathway in Duchenne muscular dystrophy mice: up-regulation of L-arginine transporters. Biochem J 449, 133-142.
47. Schofield J, Houzelstein D, Davies K, Buckingham M & Edwards YH (1993). Expression of the dystrophin-related protein (utrophin) gene during mouse embryogenesis. Dev Dyn 198, 254-264.
48. Sharp NJ, Kornegay JN, Van Camp SD, Herbstreith MH, Secore SL, Kettle S 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.
49. Sonnemann KJ, Heun-Johnson H, Turner AJ, Baltgalvis KA, Lowe DA & Ervasti JM (2009). Functional substitution by TAT-utrophin in dystrophin-deficient mice. PLoS Med 6, e1000083.
50. Squire S, Raymackers JM, Vandebrouck C, Potter A, Tinsley J, Fisher R et al. (2002). Prevention of pathology in mdx mice by expression of utrophin: analysis using an inducible transgenic expression system. Hum Mol Genet 11, 3333-3344.
51. Strimpakos G, Corbi N, Pisani C, Di Certo MG, Onori A, Luvisetto S et al. (2014). Novel adeno-associated viral vector delivering the utrophin gene regulator jazz counteracts dystrophic pathology in mdx mice. J Cell Physiol 229, 1283-1291.
52. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM et al. (1998). Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4, 1441-1444.
53. Tinsley J, Robinson N & Davies KE (2015). Safety, tolerability, and pharmacokinetics of SMT C1100, a 2-arylbenzoxazole utrophin modulator, following single- and multiple-dose administration to healthy male adult volunteers. J Clin Pharmacol 55, 698-707.
54. Tinsley JM, Fairclough RJ, Storer R, Wilkes FJ, Potter AC, Squire SE et al. (2011). Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the dystrophic symptoms in the mdx mouse. PLoS ONE 6, e19189.
55. Vainzof M, Passos-Bueno MR, Man N & Zatz M (1995). Absence of correlation between utrophin localization and quantity and the clinical severity in Duchenne/Becker dystrophies. Am J Med Genet 58, 305-309.
56. van den Bergen JC, Schade van Westrum SM, Dekker L, van der Kooi AJ, de Visser M, Wokke BH et al. (2014). Clinical characterisation of Becker muscular dystrophy patients predicts favourable outcome in exon-skipping therapy. J Neurol Neurosurg Psychiatry 85, 92-98.
57. van Deutekom JC, Bremmer-Bout M, Janson AA, Ginjaar IB, Baas F, den Dunnen JT et al. (2001). Antisense-induced exon skipping restores dystrophin expression in DMD patient derived muscle cells. Hum Mol Genet 10, 1547-1554.
58. 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.
59. Voit T, Topaloglu H, Straub V, Muntoni F, Deconinck N, Campion G et al. (2014). Safety and efficacy of drisapersen for the treatment of Duchenne muscular dystrophy (DEMAND II): an exploratory, randomised, placebo-controlled phase 2 study. Lancet Neurol 13, 987-996.
60. Voit T et al., Safety and efficacy of drisapersen for the treatment of Duchenne muscular dystrophy (DEMAND II): an exploratory, randomised, placebo-controlled phase 2 study. Lancet Neurol. 2014 Oct;13(10):987-96.
61. Wang Z, Kuhr CS, Allen JM, Blankinship M, Gregorevic P, Chamberlain JS et al. (2007). Sustained AAV-mediated dystrophin expression in a canine model of Duchenne muscular dystrophy with a brief course of immunosuppression. Mol Ther 15, 1160-1166.
62. Weir AP, Burton EA, Harrod G & Davies KE (2002). A- and B-utrophin have different expression patterns and are differentially up-regulated in mdx muscle. J Biol Chem 277, 45285-45290.