Molecular-targeted therapy for duchenne muscular dystrophy: Progress and potential

Molecular Diagnosis and Therapy

Volumn 12, Issue 2, 2008, Pages 99-108

  Scimè, Anthony ^a   Rudnicki, Michael A ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Antisense oligonucleotides, therapeutic use; Duchenne muscular dystrophy; Gene therapies, therapeutic use; Genetic variation targets

Indexed keywords

ALENDRONIC ACID; ANGIOTENSIN 2 RECEPTOR ANTAGONIST; ANTISENSE OLIGONUCLEOTIDE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM CARBONATE; COPOLYMER; COPOLYMER F127; CORTICOSTEROID; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DYSTROPHIN; GENTAMICIN; INTEGRASE; MORPHOLINO ANTISENSE OLIGONUCLEOTIDE; NAKED DNA; PARVOVIRUS VECTOR; PLASMID DNA; PTC 124; UNCLASSIFIED DRUG; VIRUS VECTOR; VITAMIN D;

ABSENCE OF SIDE EFFECTS; ANTISENSE THERAPY; BECKER MUSCULAR DYSTROPHY; CARDIOMYOPATHY; CATARACT; CLINICAL FEATURE; CLINICAL TRIAL; DIZZINESS; DNA REPAIR; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DRUG TOLERABILITY; DRUG UPTAKE; DUCHENNE MUSCULAR DYSTROPHY; EXON; GASTROINTESTINAL SYMPTOM; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENETIC TRANSCRIPTION; HEADACHE; HEART ARRHYTHMIA; HUMAN; HYPERGLYCEMIA; HYPERTENSION; LOW DRUG DOSE; NONHUMAN; NONVIRAL GENE THERAPY; OSTEOPOROSIS; POINT MUTATION; PRIORITY JOURNAL; PROGNOSIS; QUALITY OF LIFE; RESPIRATORY TRACT DISEASE; REVIEW; RNA SPLICING; SHORT STATURE; SIDE EFFECT; STOP CODON; VENTILATOR; VIRAL GENE THERAPY; WEIGHT GAIN;

ADENO-ASSOCIATED VIRUS;

EID: 42449086920     PISSN: 11771062     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF03256275     Document Type: Review

References (94)

1. Emery AE. Muscular dystrophy into the new millennium. Neuromuscul Disord 2002 May; 12 (4): 343-9
2. Rando TA. Non-viral gene therapy for Duchenne muscular dystrophy: progress and challenges. Biochim Biophys Acta 2007 Feb; 1772 (2): 263-71
3. Peault B, Rudnicki M, Torrente Y, et al. Stem and progenitor cells in skeletal muscle development, maintenance, and therapy. Mol Ther 2007 May; 15 (5): 867-77
4. Blankinship MJ, Gregorevic P, Chamberlain JS. Gene therapy strategies for Duchenne muscular dystrophy utilizing recombinant adeno-associated virus vectors. Mol Ther 2006 Feb; 13 (2): 241-9
5. Arahata K, Engel AG. Monoclonal antibody analysis of mononuclear cells in myopathies: I. Quantitation of subsets according to diagnosis and sites of accumulation and demonstration and counts of muscle fibers invaded by T cells. Ann Neurol 1984 Aug; 16 (2): 193-208
6. Griggs RC, Moxley RT, Mendell JR, et al. Prednisone in Duchenne dystrophy: a randomized, controlled trial defining the time course and dose response. Clinical Investigation of Duchenne Dystrophy Group. Arch Neurol 1991 Apr; 48 (4): 383-8
7. Mendell JR, Moxley RT, Griggs RC, et al. Randomized, double-blind six-month trial of prednisone in Duchenne's muscular dystrophy. N Engl J Med 1989 Jun 15; 320 (24): 1592-7
8. Moxley RT, Ashwal S, Pandya S, et al. Practice parameter: corticosteroid treatment of Duchenne dystrophy: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology 2005 Jan 11; 64 (1): 13-20
9. Balaban B, Matthews DJ, Clayton GH, et al. Corticosteroid treatment and functional improvement in Duchenne muscular dystrophy: long-term effect. Am J Phys Med Rehabil 2005 Nov; 84 (11): 843-50
10. Kinali M, Mercuri E, Main M, et al. An effective, low-dosage, intermittent schedule of prednisolone in the long-term treatment of early cases of Duchenne dystrophy. Neuromuscul Disord 2002 Oct; 12 Suppl. 1: S169-74
11. Wagner KR, Lechtzin N, Judge DP. Current treatment of adult Duchenne muscular dystrophy. Biochim Biophys Acta 2007 Feb; 1772 (2): 229-37
12. McDonald DG, Kinali M, Gallagher AC, et al. Fracture prevalence in Duchenne muscular dystrophy. Dev Med Child Neurol 2002 Oct; 44 (10): 695-8
13. Simonds AK. Respiratory complications of the muscular dystrophies. Semin Respir Crit Care Med 2002 Jun; 23 (3): 231-8
14. Mohr CH, Hill NS. Long-term follow-up of nocturnal ventilatory assistance in patients with respiratory failure due to Duchenne-type muscular dystrophy. Chest 1990 Jan; 97 (1): 91-6
15. Simonds AK, Muntoni F, Heather S, et al. Impact of nasal ventilation on survival in hypercapnic Duchenne muscular dystrophy. Thorax 1998 Nov; 53 (11): 949-52
16. Vianello A, Bevilacqua M, Salvador V, et al. Long-term nasal intermittent positive pressure ventilation in advanced Duchenne's muscular dystrophy. Chest 1994 Feb; 105 (2): 445-8
17. Finder JD, Birnkrant D, Carl J, et al. Respiratory care of the patient with Duchenne muscular dystrophy: ATS consensus statement. Am J Respir Crit Care Med 2004 Aug 15; 170 (4): 456-65
18. Bach JR, Ishikawa Y, Kim H. Prevention of pulmonary morbidity for patients with Duchenne muscular dystrophy. Chest 1997 Oct; 112 (4): 1024-8
19. Nigro G, Comi LI, Politano L, et al. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 1990 Mar; 26 (3): 271-7
20. Nohria A, Lewis E, Stevenson LW. Medical management of advanced heart failure. JAMA 2002 Feb 6; 287 (5): 628-40
21. Pfeffer MA, Braunwald E, Moye LA, et al. Effect of captopril on mortality and morbidity in patients with left ventricular dysfunction after myocardial infarction: results of the survival and ventricular enlargement trial. The SAVE Investigators. N Engl J Med 1992 Sep 3; 327 (10): 669-77
22. Pitt B, Poole-Wilson PA, Segal R, et al. Effect of losartan compared with captopril on mortality in patients with symptomatic heart failure: randomised trial - the Losartan Heart Failure Survival Study ELITE II. Lancet 2000 May 6; 355 (9215): 1582-7
23. Alton E. Progress and prospects: gene therapy clinical trials (part 1). Gene Ther 2007 Oct; 14 (20): 1439-47
24. Duboc D, Meune C, Pierre B, et al. Perindopril preventive treatment on mortality in Duchenne muscular dystrophy: 10 years' follow-up. Am Heart J 2007 Sep; 154 (3): 596-602
25. Duboc D, Meune C, Lerebours G, et al. Effect of perindopril on the onset and progression of left ventricular dysfunction in Duchenne muscular dystrophy. J Am Coll Cardiol 2005 Mar 15; 45 (6): 855-7
26. Gradaus R, Wollmann C, Kobe J, et al. Potential benefit from implantable cardioverter-defibrillator therapy in children and young adolescents. Heart 2004 Mar; 90 (3): 328-9
27. Gao G, Vandenberghe LH, Wilson JM. New recombinant serotypes of AAV vectors. Curr Gene Ther 2005 Jun; 5 (3): 285-97
28. Gregorevic P, Blankinship MJ, Allen JM, et al. Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat Med 2004 Aug; 10 (8): 828-34
29. Wang Z, Zhu T, Qiao C, et al. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 2005 Mar; 23 (3): 321-8
30. Gregorevic P, Allen JM, Minami E, et al. rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice. Nat Med 2006 Jul; 12 (7): 787-9
31. Harper SQ, Hauser MA, DelloRusso C, et al. Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 2002 Mar; 8 (3): 253-61
32. England SB, Nicholson LV, Johnson MA, et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 1990 Jan 11; 343 (6254): 180-2
33. Mirabella M, Galluzzi G, Manfredi G, et al. Giant dystrophin deletion associated with congenital cataract and mild muscular dystrophy. Neurology 1998 Aug; 51 (2): 592-5
34. Liu M, Yue Y, Harper SQ, et al. Adeno-associated virus-mediated microdystrophin expression protects young mdx muscle from contraction-induced injury. Mol Ther 2005 Feb; 11 (2): 245-56
35. Yoshimura M, Sakamoto M, Ikemoto M, et al. AAV vector-mediated microdystrophin expression in a relatively small percentage of mdx myofibers improved the mdx phenotype. Mol Ther 2004 Nov; 10 (5): 821-8
36. Watchko J, O'Day T, Wang B, et al. Adeno-associated virus vector-mediated minidystrophin gene therapy improves dystrophic muscle contractile function in mdx mice. Hum Gene Ther 2002 Aug 10; 13 (12): 1451-60
37. Ghosh A, Yue Y, Duan D. Viral serotype and the transgene sequence influence overlapping adeno-associated viral (AAV) vector-mediated gene transfer in skeletal muscle. J Gene Med 2006 Mar; 8 (3): 298-305
38. Ghosh A, Yue Y, Long C, et al. Efficient whole-body transduction with transsplicing adeno-associated viral vectors. Mol Ther 2007 Apr; 15 (4): 750-5
39. Lai Y, Yue Y, Liu M, et al. Efficient in vivo gene expression by trans-splicing adeno-associated viral vectors. Nat Biotechnol 2005 Nov; 23 (11): 1435-9
40. McCarty DM, Young Jr SM, Samulski RJ. Integration of adeno-associated virus (AAV) and recombinant AAV vectors. Annu Rev Genet 2004; 38: 819-45
41. Louboutin JP, Wang L, Wilson JM. Gene transfer into skeletal muscle using novel AAV serotypes. J Gene Med 2005 Apr; 7 (4): 442-51
42. Schmidt M, Katano H, Bossis I, et al. Cloning and characterization of a bovine adeno-associated virus. J Virol 2004 Jun; 78 (12): 6509-16
43. Blouin V, Brument N, Toublanc E, et al. Improving rAAV production and purification: towards the definition of a scaleable process. J Gene Med 2004 Feb; 6 Suppl. 1: S223-8
44. University of North Carolina at Chapel Hill, Gene Therapy Center. Clinical trials: Duchenne muscular dystrophy clinical trial [online]. Available from URL: http://genetherapy.unc.edu/clinical.htm [Accessed 2008 Feb 28]
45. Safety study of mini-dystrophin gene to treat Duchenne muscular dystrophy. Trial identifier: NCT00428935 [online]. Available from URL: http://clinicaltrials.gov/ct2/show/NCT00428935 [Accessed 2008 Feb 28]
46. Wolff JA, Malone RW, Williams P, et al. Direct gene transfer into mouse muscle in vivo. Science 1990 Mar 23; 247: 1465-8
47. Bartlett RJ, Secore SL, Singer JT, et al. Long-term expression of a fluorescent reporter gene via direct injection of plasmid vector into mouse skeletal muscle: comparison of human creatine kinase and CMV promoter expression levels in vivo. Cell Transplant 1996 May-Jun; 5 (3): 411-9
48. Wells DJ, Maule J, McMahon J, et al. Evaluation of plasmid DNA for in vivo gene therapy: factors affecting the number of transfected fibers. J Pharm Sci 1998 Jun; 87 (6): 763-8
49. Acsadi G, Dickson G, Love DR, et al. Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature 1991 Aug 29; 352 (6338): 815-8
50. Romero NB, Braun S, Benveniste O, et al. Phase I study of dystrophin plasmid-based gene therapy in Duchenne/Becker muscular dystrophy. Hum Gene Ther 2004 Nov; 15 (11): 1065-76
51. Taniyama Y, Tachibana K, Hiraoka K, et al. Development of safe and efficient novel nonviral gene transfer using ultrasound: enhancement of transfection efficiency of naked plasmid DNA in skeletal muscle. Gene Ther 2002 Mar; 9 (6): 372-80
52. Danialou G, Comtois AS, Dudley RW, et al. Ultrasound increases plasmid-mediated gene transfer to dystrophic muscles without collateral damage. Mol Ther 2002 Nov; 6 (5): 687-93
53. Lu QL, Liang HD, Partridge T, et al. Microbubble ultrasound improves the efficiency of gene transduction in skeletal muscle in vivo with reduced tissue damage. Gene Ther 2003 Mar; 10 (5): 396-405
54. Bekeredjian R, Chen S, Frenkel PA, et al. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation 2003 Aug 26; 108 (8): 1022-6
55. Mir LM, Bureau MF, Gehl J, et al. High-efficiency gene transfer into skeletal muscle mediated by electric pulses. Proc Natl Acad Sci U S A 1999 Apr 13; 96 (8): 4262-7
56. Aihara H, Miyazaki J. Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 1998 Sep; 16 (9): 867-70
57. Andre F, Mir LM. DNA electrotransfer: its principles and an updated review of its therapeutic applications. Gene Ther 2004 Oct; 11 Suppl. 1: S33-42
58. Wong SH, Lowes KN, Quigley AF, et al. DNA electroporation in vivo targets mature fibres in dystrophic mdx muscle. Neuromuscul Disord 2005 Oct; 15 (9-10): 630-41
59. Murakami T, Nishi T, Kimura E, et al. Full-length dystrophin cDNA transfer into skeletal muscle of adult mdx mice by electroporation. Muscle Nerve 2003 Feb; 27 (2): 237-41
60. Ferrer A, Foster H, Wells KE, et al. Long-term expression of full-length human dystrophin in transgenic mdx mice expressing internally deleted human dystrophins. Gene Ther 2004 Jun; 11 (11): 884-93
61. Lefesvre P, Attema J, van Bekkum D. A comparison of efficacy and toxicity between electroporation and adenoviral gene transfer. BMC Mol Biol 2002 Aug 13; 3: 12
62. Schertzer JD, Plant DR, Lynch GS. Optimizing plasmid-based gene transfer for investigating skeletal muscle structure and function. Mol Ther 2006 Apr; 13 (4): 795-803
63. Molnar MJ, Gilbert R, Lu Y, et al. Factors influencing the efficacy, longevity, and safety of electroporation-assisted plasmid-based gene transfer into mouse muscles. Mol Ther 2004 Sep; 10 (3): 447-55
64. Mennuni C, Calvaruso F, Zampaglione I, et al. Hyaluronidase increases electrogene transfer efficiency in skeletal muscle. Hum Gene Ther 2002 Feb 10; 13 (3): 355-65
65. McMahon JM, Signori E, Wells KE, et al. Optimisation of electrotransfer of plasmid into skeletal muscle by pretreatment with hyaluronidase: increased expression with reduced muscle damage. Gene Ther 2001 Aug; 8 (16): 1264-70
66. Danialou G, Comtois AS, Matecki S, et al. Optimization of regional intraarterial naked DNA-mediated transgene delivery to skeletal muscles in a large animal model. Mol Ther 2005 Feb; 11 (2): 257-66
67. Liang KW, Nishikawa M, Liu F, et al. Restoration of dystrophin expression in mdx mice by intravascular injection of naked DNA containing full-length dystrophin cDNA. Gene Ther 2004 Jun; 11 (11): 901-8
68. Zhang G, Ludtke JJ, Thioudellet C, et al. Intraarterial delivery of naked plasmid DNA expressing full-length mouse dystrophin in the mdx mouse model of duchenne muscular dystrophy. Hum Gene Ther 2004 Aug; 15 (8): 770-82
69. Hagstrom JE, Hegge J, Zhang G, et al. A facile nonviral method for delivering genes and siRNAs to skeletal muscle of mammalian limbs. Mol Ther 2004 Aug; 10 (2): 386-98
70. Bertoni C, Jarrahian S, Wheeler TM, et al. Enhancement of plasmid-mediated gene therapy for muscular dystrophy by directed plasmid integration. Proc Natl Acad Sci U S A 2006 Jan 10; 103 (2): 419-24
71. Prior TW, Bridgeman SJ. Experience and strategy for the molecular testing of Duchenne muscular dystrophy. J Mol Diagn 2005 Aug; 7 (3): 317-26
72. Bertoni C, Rando TA. Dystrophin gene repair in mdx muscle precursor cells in vitro and in vivo mediated by RNA-DNA chimeric oligonucleotides. Hum Gene Ther 2002 Apr 10; 13 (6): 707-18
73. Bertoni C, Morris GE, Rando TA. Strand bias in oligonucleotide-mediated dystrophin gene editing. Hum Mol Genet 2005 Jan 15; 14 (2): 221-33
74. Rando TA, Disatnik MH, Zhou LZ. Rescue of dystrophin expression in mdx mouse muscle by RNA/DNA oligonucleotides. Proc Natl Acad Sci U S A 2000 May 9; 97 (10): 5363-8
75. Bertoni C, Lau C, Rando TA. Restoration of dystrophin expression in mdx muscle cells by chimeraplast-mediated exon skipping. Hum Mol Genet 2003 May 15; 12 (10): 1087-99
76. Mann CJ, Honeyman K, Cheng AJ, et al. Antisense-induced exon skipping and synthesis of dystrophin in the mdx mouse. Proc Natl Acad Sci U S A 2001 Jan 2; 98 (1): 42-7
77. Lu QL, Mann CJ, Lou F, et al. Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat Med 2003 Aug; 9 (8): 1009-14
78. Alter J, Lou F, Rabinowitz A, et al. Systemic delivery of morpholino oligonucleotide restores dystrophin expression bodywide and improves dystrophic pathology. Nat Med 2006 Feb; 12 (2): 175-7
79. Fletcher S, Honeyman K, Fall AM, et al. Dystrophin expression in the mdx mouse after localised and systemic administration of a morpholino antisense oligonucleotide. J Gene Med 2006 Feb; 8 (2): 207-16
80. Fletcher S, Honeyman K, Fall AM, et al. Morpholino oligomer-mediated exon skipping averts the onset of dystrophic pathology in the mdx mouse. Mol Ther 2007 Sep; 15 (9): 1587-92
81. Aartsma-Rus A, Bremmer-Bout M, Janson AA, et al. Targeted exon skipping as a potential gene correction therapy for Duchenne muscular dystrophy. Neuromuscul Disord 2002 Oct; 12 Suppl. 1: S71-7
82. Wilton SD, Fall AM, Harding PL, et al. Antisense oligonucleotide-induced exon skipping across the human dystrophin gene transcript. Mol Ther 2007 Jul; 15 (7): 1288-96
83. Aartsma-Rus A, Janson AA, Kaman WE, et al. Therapeutic antisense-induced exon skipping in cultured muscle cells from six different DMD patients. Hum Mol Genet 2003 Apr 15; 12 (8): 907-14
84. Aartsma-Rus A, Janson AA, Kaman WE, et al. Antisense-induced multiexon skipping for Duchenne muscular dystrophy makes more sense. Am J Hum Genet 2004 Jan; 74 (1): 83-92
85. Aartsma-Rus A, Janson AA, van Ommen GJ, et al. Antisense-induced exon skipping for duplications in Duchenne muscular dystrophy. BMC Med Genet 2007; 8: 43
86. Arechavala-Gomeza V, Graham IR, Popplewell LJ, et al. Comparative analysis of antisense oligonucleotide sequences for targeted skipping of exon 51 during dystrophin pre-mRNA splicing in human muscle. Hum Gene Ther 2007 Sep; 18 (9): 798-810
87. van Deutekom JC, Janson AA, Ginjaar IB, et al. Local dystrophin restoration with antisense oligonucleotide PRO051. N Engl J Med 2007 Dec 27; 357 (26): 2677-86
88. Takeshima Y, Yagi M, Wada H, et al. Intravenous infusion of an antisense oligonucleotide results in exon skipping in muscle dystrophin mRNA of Duchenne muscular dystrophy. Pediatr Res 2006 May; 59 (5): 690-4
89. Howard M, Frizzell RA, Bedwell DM. Aminoglycoside antibiotics restore CFTR function by overcoming premature stop mutations. Nat Med 1996 Apr; 2 (4): 467-9
90. Barton-Davis ER, Cordier L, Shoturma DI, et al. Aminoglycoside antibiotics restore dystrophin function to skeletal muscles of mdx mice. J Clin Invest 1999 Aug; 104 (4): 375-81
91. Wagner KR, Hamed S, Hadley DW, et al. Gentamicin treatment of Duchenne and Becker muscular dystrophy due to nonsense mutations. Ann Neurol 2001 Jun; 49 (6): 706-11
92. Welch EM, Barton ER, Zhuo J, et al. PTC124 targets genetic disorders caused by nonsense mutations. Nature 2007 May 3; 447 (7140): 87-91
93. Hirawat S, Welch EM, Elfring GL, et al. Safety, tolerability, and pharmacokinetics of PTC124, a nonaminoglycoside nonsense mutation suppressor, following single- and multiple-dose administration to healthy male and female adult volunteers. J Clin Pharmacol 2007 Apr; 47 (4): 430-44
94. Safety and efficacy study of PTC124 in Duchenne muscular dystrophy. Trial identifier: NCT00264888 [online]. Available from URL: http://clinicaltrials. gov/ct2/show/NCT00264888 [Accessed 2008 Feb 28]