Dystrophin-Deficient Cardiomyopathy

Journal of the American College of Cardiology

Volumn 67, Issue 21, 2016, Pages 2533-2546

  Kamdar, Forum ^a   Garry, Daniel J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Becker muscular dystrophy cardiomyopathy; Duchenne muscular dystrophy cardiomyopathy; muscular dystrophy cardiomyopathy

Indexed keywords

ANGIOTENSIN RECEPTOR ANTAGONIST; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CORTICOSTEROID; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; DRISAPERSEN; DYSTROGLYCAN; DYSTROPHIN; MINERALOCORTICOID ANTAGONIST; GLUCOCORTICOID;

BECKER MUSCULAR DYSTROPHY; CARDIAC IMAGING; CARDIOMYOPATHY; CELL THERAPY; CLINICAL FEATURE; CONGESTIVE CARDIOMYOPATHY; DRUG RESPONSE; DUCHENNE MUSCULAR DYSTROPHY; DYSTROPHIN GENE; EXON SKIPPING; GENE EDITING; GENE THERAPY; GENETIC PROCEDURES; HEART ARRHYTHMIA; HEART FAILURE; HEART TRANSPLANTATION; HUMAN; INHERITANCE; LEFT VENTRICULAR ASSIST DEVICE; MOLECULAR PATHOLOGY; NONHUMAN; PATIENT CARE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SURVIVAL RATE; TREATMENT OUTCOME; AGING; ARRHYTHMIAS, CARDIAC; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; CINE MAGNETIC RESONANCE IMAGING; DISEASE COURSE; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; GENETICS; HEART ASSIST DEVICE; HETEROZYGOTE; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION;

ADRENERGIC BETA-ANTAGONISTS; AGING; ANGIOTENSIN RECEPTOR ANTAGONISTS; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ARRHYTHMIAS, CARDIAC; CARDIOMYOPATHIES; CARDIOMYOPATHY, DILATED; DISEASE PROGRESSION; DYSTROPHIN; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; GENE EDITING; GENETIC THERAPY; GLUCOCORTICOIDS; HEART TRANSPLANTATION; HEART-ASSIST DEVICES; HETEROZYGOTE; HUMANS; MAGNETIC RESONANCE IMAGING, CINE; MINERALOCORTICOID RECEPTOR ANTAGONISTS; MUSCULAR DYSTROPHY, DUCHENNE; MUTATION;

EID: 84969951603     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2016.02.081     Document Type: Review

References (118)

1. E. Meryon On granular and fatty degeneration of the voluntary muscles Medico-Chirugical Trans 35 1852 73 74
2. G.B.A. Duchenne Recherches sur la paralysie musculaire pseudo-hypertrophique ou paralysie myo-sclerosique Arch Gen Med 11 1868 5 25
3. W.R. Gowers A manual of disease of the nervous system 1 1886 Churchill London, UK 391 394
4. A.P. Monaco, R.L. Neve, C. Colletti-Feener, and et al. Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene Nature 323 1986 646 650
5. E.P. Hoffman, R.H. Brown Jr., and L.M. Kunkel Dystrophin: the protein product of the Duchenne muscular dystrophy locus Cell 51 1987 919 928
6. A.E. Emery The muscular dystrophies Lancet 359 2002 687 695
7. G.F. Cox, and L.M. Kunkel Dystrophies and heart disease Curr Opin Cardiol 12 1997 329 343
8. J.R. Mendell, C. Shilling, N.D. Leslie, and et al. Evidence-based path to newborn screening for Duchenne muscular dystrophy Ann Neurol 71 2012 304 313
9. M. Koenig, E.P. Hoffman, C.J. Bertelson, and et al. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals Cell 50 1987 509 517
10. A.H. Ahn, and L.M. Kunkel The structural and functional diversity of dystrophin Nat Genet 3 1993 283 291
11. K.M. Dent, D.M. Dunn, A.C. von Niederhausern, and et al. Improved molecular diagnosis of dystrophinopathies in an unselected clinical cohort Am J Med Genet A 134 2005 295 298
12. I.N. Rybakova, J.R. Patel, and J.M. Ervasti The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin J Cell Biol 150 2000 1209 1214
13. J.M. Ervasti, and K.P. Campbell A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin J Cell Biol 122 1993 809 823
14. R.D. Cohn, and K.P. Campbell Molecular basis of muscular dystrophies Muscle Nerve 23 2000 1456 1471
15. R. Klietsch, J.M. Ervasti, W. Arnold, and et al. Dystrophin-glycoprotein complex and laminin colocalize to the sarcolemma and transverse tubules of cardiac muscle Circ Res 72 1993 349 360
16. E.K. Johnson, L. Zhang, M.E. Adams, and et al. Proteomic analysis reveals new cardiac-specific dystrophin-associated proteins PloS One 7 2012 e43515
17. G.A. Cox, N.M. Cole, K. Matsumura, and et al. Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity Nature 364 1993 725 729
18. B.J. Petrof, J.B. Shrager, H.H. Stedman, and et al. Dystrophin protects the sarcolemma from stresses developed during muscle contraction Proc Natl Acad Sci U S A 90 1993 3710 3714
19. S. Yasuda, D. Townsend, D.E. Michele, and et al. Dystrophic heart failure blocked by membrane sealant poloxamer Nature 436 2005 1025 1029
20. M. Konagaya, and T. Takayanagi Regularity in the change of serum creatine kinase level in Duchenne muscular dystrophy. A study with long-term follow-up cases Jpn J Med 25 1986 2 8
21. M. Eagle, S.V. Baudouin, C. Chandler, and et al. Survival in Duchenne muscular dystrophy: improvements in life expectancy since 1967 and the impact of home nocturnal ventilation Neuromuscul Disord 12 2002 926 929
22. G. Nigro, L.I. Comi, L. Politano, and et al. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy Int J Cardiol 26 1990 271 277
23. C. Angelini The role of corticosteroids in muscular dystrophy: a critical appraisal Muscle Nerve 36 2007 424 435
24. K. Bushby, R. Finkel, D.J. Birnkrant, et al. for the DMD Care Considerations Working Group Diagnosis and management of Duchenne muscular dystrophy, part 1: diagnosis, and pharmacological and psychosocial management Lancet Neurol 9 2010 77 93
25. A.Y. Manzur, T. Kuntzer, M. Pike, and et al. Glucocorticoid corticosteroids for Duchenne muscular dystrophy Cochrane Database Syst Rev 2008 CD003725
26. M.D. Bonifati, G. Ruzza, P. Bonometto, and et al. A multicenter, double-blind, randomized trial of deflazacort versus prednisone in Duchenne muscular dystrophy Muscle Nerve 23 2000 1344 1347
27. K. Bushby, R. Finkel, D.J. Birnkrant, et al. for the DMD Care Considerations Working Group Diagnosis and management of Duchenne muscular dystrophy, part 2: implementation of multidisciplinary care Lancet Neurol 9 2010 177 189
28. D. Gozal Pulmonary manifestations of neuromuscular disease with special reference to Duchenne muscular dystrophy and spinal muscular atrophy Pediatr Pulmonol 29 2000 141 150
29. M. Eagle, J. Bourke, R. Bullock, and et al. Managing Duchenne muscular dystrophy - the additive effect of spinal surgery and home nocturnal ventilation in improving survival Neuromuscul Disord 17 2007 470 475
30. J.D. Finder, D. Birnkrant, J. Carl, and et al. Respiratory care of the patient with Duchenne muscular dystrophy: ATS consensus statement Am J Respir Crit Care Med 170 2004 456 465
31. American Academy of Pediatrics Section on Cardiology and Cardiac Surgery Cardiovascular health supervision for individuals affected by Duchenne or Becker muscular dystrophy Pediatrics 116 2005 1569 1573
32. L.W. Markham, R.L. Spicer, P.R. Khoury, and et al. Steroid therapy and cardiac function in Duchenne muscular dystrophy Pediatr Cardiol 26 2005 768 771
33. J.L. Jefferies, B.W. Eidem, J.W. Belmont, and et al. Genetic predictors and remodeling of dilated cardiomyopathy in muscular dystrophy Circulation 112 2005 2799 2804
34. A. Romfh, and E.M. McNally Cardiac assessment in Duchenne and Becker muscular dystrophies Curr Heart Fail Rep 7 2010 212 218
35. P.T. Thrush, H.D. Allen, L. Viollet, and et al. Re-examination of the electrocardiogram in boys with Duchenne muscular dystrophy and correlation with its dilated cardiomyopathy Am J Cardiol 103 2009 262 265
36. J.K. Perloff, W.C. Roberts, A.C. de Leon Jr., and et al. The distinctive electrocardiogram of Duchenne's progressive muscular dystrophy. An electrocardiographic-pathologic correlative study Am J Med 42 1967 179 188
37. S.K. Sanyal, W.W. Johnson, M.K. Thapar, and et al. An ultrastructural basis for electrocardiographic alterations associated with Duchenne's progressive muscular dystrophy Circulation 57 1978 1122 1129
38. K.A. Frankel, and R.J. Rosser The pathology of the heart in progressive muscular dystrophy: epimyocardial fibrosis Human Pathol 7 1976 375 386
39. L.W. Markham, E.C. Michelfelder, W.L. Border, and et al. Abnormalities of diastolic function precede dilated cardiomyopathy associated with Duchenne muscular dystrophy J Am Soc Echocardiogr 19 2006 865 871
40. E.P. Boas, and H. Lowenburg The heart rate in progressive muscular dystrophy Arch Intern Med 47 1931 376 383
41. C.W. Fitch, and L.E. Ainger The Frank vectorcardiogram and the electrocardiogram in Duchenne progressive muscular dystrophy Circulation 35 1967 1124 1140
42. R.B. Kovick, A.M. Fogelman, A.D. Abbasi, and et al. Echocardiographic evaluation of posterior left ventricular wall motion in muscular dystrophy Circulation 52 1975 447 454
43. H. Nomura, and K. Hizawa Histopathological study of the conduction system of the heart in Duchenne progressive muscular dystrophy Acta Pathol Jpn 32 1982 1027 1033
44. M. Yotsukura, K. Sasaki, E. Kachi, and et al. Circadian rhythm and variability of heart rate in Duchenne-type progressive muscular dystrophy Am J Cardiol 76 1995 947 951
45. M. Yotsukura, K. Fujii, A. Katayama, and et al. Nine-year follow-up study of heart rate variability in patients with Duchenne-type progressive muscular dystrophy Am Heart J 136 1998 289 296
46. T.O. Thomas, T.M. Morgan, W.B. Burnette, and et al. Correlation of heart rate and cardiac dysfunction in Duchenne muscular dystrophy Pediatr Cardiol 33 2012 1175 1179
47. Y. Dalmaz, L. Peyrin, J.C. Mamelle, and et al. The pattern of urinary catecholamines and their metabolites in Duchenne myopathy, in relation to disease evolution J Neural Transm 46 1979 17 34
48. C.R. Villa, R.J. Czosek, H. Ahmed, and et al. Ambulatory monitoring and arrhythmic outcomes in pediatric and adolescent patients with Duchenne muscular dystrophy J Am Heart Assoc 5 2015 e002620
49. G. Corrado, A. Lissoni, S. Beretta, and et al. Prognostic value of electrocardiograms, ventricular late potentials, ventricular arrhythmias, and left ventricular systolic dysfunction in patients with Duchenne muscular dystrophy Am J Cardiol 89 2002 838 841
50. M. Yotsukura, A. Yamamoto, T. Kajiwara, and et al. QT dispersion in patients with Duchenne-type progressive muscular dystrophy Am Heart J 137 1999 672 677
51. C.W. Yancy, M. Jessup, B. Bozkurt, and et al. 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines J Am Coll Cardiol 62 2013 e147 e239
52. C. Rapezzi, O. Leone, E. Biagini, and et al. Echocardiographic clues to diagnosis of dystrophin related dilated cardiomyopathy Heart 93 2007 10
53. L.W. Markham, K. Kinnett, B.L. Wong, and et al. Corticosteroid treatment retards development of ventricular dysfunction in Duchenne muscular dystrophy Neuromuscul Disord 18 2008 365 370
54. M.C. Silva, Z.M. Meira, J. Gurgel Giannetti, and et al. Myocardial delayed enhancement by magnetic resonance imaging in patients with muscular dystrophy J Am Coll Cardiol 49 2007 1874 1879
55. S.C. Hagenbuch, W.M. Gottliebson, J. Wansapura, and et al. Detection of progressive cardiac dysfunction by serial evaluation of circumferential strain in patients with Duchenne muscular dystrophy Am J Cardiol 105 2010 1451 1455
56. K.N. Hor, J. Wansapura, L.W. Markham, and et al. Circumferential strain analysis identifies strata of cardiomyopathy in Duchenne muscular dystrophy: a cardiac magnetic resonance tagging study J Am Coll Cardiol 53 2009 1204 1210
57. M.D. Puchalski, R.V. Williams, B. Askovich, and et al. Late gadolinium enhancement: precursor to cardiomyopathy in Duchenne muscular dystrophy? Int J Cardiovasc Imaging 25 2009 57 63
58. D. Verhaert, K. Richards, J.A. Rafael-Fortney, and et al. Cardiac involvement in patients with muscular dystrophies: magnetic resonance imaging phenotype and genotypic considerations Circ Cardiovasc Imaging 4 2011 67 76
59. K.N. Hor, M.D. Taylor, H.R. Al-Khalidi, and et al. Prevalence and distribution of late gadolinium enhancement in a large population of patients with Duchenne muscular dystrophy: effect of age and left ventricular systolic function J Cardiovasc Magn Reson 15 2013 107
60. A. Tandon, C.R. Villa, K.N. Hor, and et al. Myocardial fibrosis burden predicts left ventricular ejection fraction and is associated with age and steroid treatment duration in Duchenne muscular dystrophy J Am Heart Assoc 4 2015 e001338
61. G.W. Dec Steroid therapy effectively delays Duchenne's cardiomyopathy J Am Coll Cardiol 61 2013 955 956
62. C.K. Silversides, G.D. Webb, V.A. Harris, and et al. Effects of deflazacort on left ventricular function in patients with Duchenne muscular dystrophy Am J Cardiol 91 2003 769 772
63. S. Mavrogeni, A. Papavasiliou, M. Douskou, and et al. Effect of deflazacort on cardiac and sternocleidomastoid muscles in Duchenne muscular dystrophy: a magnetic resonance imaging study Eur J Paediatr Neurol 13 2009 34 40
64. B.J. Barber, J.G. Andrews, Z. Lu, and et al. Oral corticosteroids and onset of cardiomyopathy in Duchenne muscular dystrophy J Pediatr 163 2013 1080 1084.e1
65. G. Schram, A. Fournier, H. Leduc, and et al. All-cause mortality and cardiovascular outcomes with prophylactic steroid therapy in Duchenne muscular dystrophy J Am Coll Cardiol 61 2013 948 954
66. D. Duboc, C. Meune, G. Lerebours, and et al. Effect of perindopril on the onset and progression of left ventricular dysfunction in Duchenne muscular dystrophy J Am Coll Cardiol 45 2005 855 857
67. D. Duboc, C. Meune, B. Pierre, and et al. Perindopril preventive treatment on mortality in Duchenne muscular dystrophy: 10 years' follow-up Am Heart J 154 2007 596 602
68. H.D. Allen, K.M. Flanigan, P.T. Thrush, and et al. A randomized, double-blind trial of lisinopril and losartan for the treatment of cardiomyopathy in Duchenne muscular dystrophy [published correction appears in PLoS Curr 2015;7] PLoS Curr 5 2013
69. T. Saito, T. Matsumura, I. Miyai, S. Nozaki, and S. Shinno [Carvedilol effectiveness for left ventricular-insufficient patients with Duchenne muscular dystrophy] Rinsho Shinkeigaku 41 2001 691 694
70. J. Rhodes, R. Margossian, B.T. Darras, and et al. Safety and efficacy of carvedilol therapy for patients with dilated cardiomyopathy secondary to muscular dystrophy Pediatr Cardiol 29 2008 343 351
71. H. Kajimoto, K. Ishigaki, K. Okumura, and et al. Beta-blocker therapy for cardiac dysfunction in patients with muscular dystrophy Circ J 70 2006 991 994
72. L. Viollet, P.T. Thrush, K.M. Flanigan, and et al. Effects of angiotensin-converting enzyme inhibitors and/or beta blockers on the cardiomyopathy in Duchenne muscular dystrophy Am J Cardiol 110 2012 98 102
73. S.V. Raman, K.N. Hor, W. Mazur, and et al. Eplerenone for early cardiomyopathy in Duchenne muscular dystrophy: a randomised, double-blind, placebo-controlled trial Lancet Neurol 14 2015 153 161
74. W. Rees, S. Schüler, M. Hummel, and et al. Heart transplantation in patients with muscular dystrophy associated with end-stage cardiomyopathy J Heart Lung Transplant 12 1993 804 807
75. M.J. Ruiz-Cano, J.F. Delgado, C. Jiménez, and et al. Successful heart transplantation in patients with inherited myopathies associated with end-stage cardiomyopathy Transplant Proc 35 2003 1513 1515
76. F. Patanè, E. Zingarelli, M. Attisani, and et al. Successful heart transplantation in Becker's muscular dystrophy Eur J Cardiothorac Surg 29 2006 250
77. R.S. Wu, S. Gupta, R.N. Brown, and et al. Clinical outcomes after cardiac transplantation in muscular dystrophy patients J Heart Lung Transplant 29 2010 432 438
78. E.A. Rose, A.C. Gelijns, A.J. Moskowitz, et al. for the Randomized Evaluation of Mechanical Assistance for the Treatment of Congestive Heart Failure (REMATCH) Study Group Long-term use of a left ventricular assist device for end-stage heart failure N Engl J Med 345 2001 1435 1443
79. M.S. Slaughter, J.G. Rogers, C.A. Milano, et al. for the HeartMate II Investigators Advanced heart failure treated with continuous-flow left ventricular assist device N Engl J Med 361 2009 2241 2251
80. A. Amodeo, and R. Adorisio Left ventricular assist device in Duchenne cardiomyopathy: can we change the natural history of cardiac disease? Int J Cardiol 161 2012 e43
81. T.D. Ryan, J.L. Jefferies, H. Sawnani, and et al. Implantation of the HeartMate II and HeartWare left ventricular assist devices in patients with Duchenne muscular dystrophy: lessons learned from the first applications ASAIO J 60 2014 246 248
82. P.E. Becker, and F. Kiener [A new x-chromosomal muscular dystrophy] Archiv Psychiatr Nervenkr Z Gesamte Neurol Psychiatr 193 1955 427 448
83. P.E. Becker Two families of benign sex-linked recessive muscular dystrophy Rev Can Biol 21 1962 551 566
84. H.M. Kingston, M. Sarfarazi, N.S. Thomas, and et al. Localisation of the Becker muscular dystrophy gene on the short arm of the X chromosome by linkage to cloned DNA sequences Hum Genet 67 1984 6 17
85. M. Koenig, A.H. Beggs, M. Moyer, and et al. The molecular basis for Duchenne versus Becker muscular dystrophy: correlation of severity with type of deletion Am J Hum Genet 45 1989 498 506
86. R. Worton Muscular dystrophies: diseases of the dystrophin-glycoprotein complex Science 270 1995 755 756
87. A.P. Monaco, C.J. Bertelson, S. Liechti-Gallati, and et al. An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus Genomics 2 1988 90 95
88. W.G. Bradley, M.Z. Jones, J.M. Mussini, and P.R. Fawcett Becker-type muscular dystrophy Muscle Nerve 1 1978 111 132
89. P. Melacini, M. Fanin, G.A. Danieli, and et al. Myocardial involvement is very frequent among patients affected with subclinical Becker's muscular dystrophy Circulation 94 1996 3168 3175
90. J. Finsterer, and C. Stöllberger Cardiac involvement in Becker muscular dystrophy Can J Cardiol 24 2008 786 792
91. E.M. Hoogerwaard, W.G. de Voogt, A.A. Wilde, and et al. Evolution of cardiac abnormalities in Becker muscular dystrophy over a 13-year period J Neurol 244 1997 657 663
92. G. Nigro, L. Politano, V. Nigro, and et al. Mutation of dystrophin gene and cardiomyopathy Neuromusc Disord 4 1994 371 379
93. A. Yilmaz, H.J. Gdynia, H. Baccouche, and et al. Cardiac involvement in patients with Becker muscular dystrophy: new diagnostic and pathophysiological insights by a CMR approach J Cardiovasc Magn Reson 10 2008 50
94. A. Norman, and P. Harper A survey of manifesting carriers of Duchenne and Becker muscular dystrophy in Wales Clin Genet 36 1989 31 37
95. L.I. Comi, G. Nigro, L. Politano, and et al. The cardiomyopathy of Duchenne/Becker consultands Int J Cardiol 34 1992 297 305
96. E.M. Hoogerwaard, P.A. van der Wouw, A.A. Wilde, and et al. Cardiac involvement in carriers of Duchenne and Becker muscular dystrophy Neuromusc Disord 9 1999 347 351
97. E.M. Hoogerwaard, E. Bakker, P.F. Ippel, and et al. Signs and symptoms of Duchenne muscular dystrophy and Becker muscular dystrophy among carriers in The Netherlands: a cohort study Lancet 353 1999 2116 2119
98. S.M. Schade van Westrum, E.M. Hoogerwaard, L. Dekker, and et al. Cardiac abnormalities in a follow-up study on carriers of Duchenne and Becker muscular dystrophy Neurology 77 2011 62 66
99. J. Schelhorn, A. Schoenecker, U. Neudorf, and et al. Cardiac pathologies in female carriers of Duchenne muscular dystrophy assessed by cardiovascular magnetic resonance imaging Eur Radiol 25 2015 3066 3072
100. S.M. Lang, S. Shugh, W. Mazur, and et al. Myocardial fibrosis and left ventricular dysfunction in Duchenne muscular dystrophy carriers using cardiac magnetic resonance imaging Pediatr Cardiol 36 2015 1495 1501
101. B.A. Berko, and M. Swift X-linked dilated cardiomyopathy N Engl J Med 316 1987 1186 1191
102. F. Muntoni, M. Cau, A. Ganau, and et al. Brief report: deletion of the dystrophin muscle-promoter region associated with X-linked dilated cardiomyopathy N Engl J Med 329 1993 921 925
103. J.A. Towbin, J.F. Hejtmancik, P. Brink, and et al. X-linked dilated cardiomyopathy. Molecular genetic evidence of linkage to the Duchenne muscular dystrophy (dystrophin) gene at the Xp21 locus Circulation 87 1993 1854 1865
104. A. Aartsma-Rus, I. Fokkema, J. Verschuuren, and et al. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations Hum Mutat 30 2009 293 299
105. N.M. Goemans, M. Tulinius, J.T. van den Akker, and et al. Systemic administration of PRO051 in Duchenne's muscular dystrophy N Engl J Med 364 2011 1513 1522
106. S. Cirak, V. Arechavala-Gomeza, M. Guglieri, and et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study Lancet 378 2011 595 605
107. C. Pichavant, A. Aartsma-Rus, P.R. Clemens, and et al. Current status of pharmaceutical and genetic therapeutic approaches to treat DMD Mol Ther 19 2011 830 840
108. S.B. England, L.V. Nicholson, M.A. Johnson, and et al. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin Nature 343 1990 180 182
109. S.Q. Harper, M.A. Hauser, C. DelloRusso, and et al. Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy Nat Med 8 2002 253 261
110. P. Gregorevic, J.M. Allen, E. Minami, and et al. rAAV6-microdystrophin preserves muscle function and extends lifespan in severely dystrophic mice Nat Med 12 2006 787 789
111. G.B. Banks, J.S. Chamberlain, and S.C. Froehner Truncated dystrophins can influence neuromuscular synapse structure Mol Cell Neurosci 40 2009 433 441
112. J.R. Mendell, K. Campbell, L. Rodino-Klapac, and et al. Dystrophin immunity in Duchenne's muscular dystrophy N Engl J Med 363 2010 1429 1437
113. D.E. Bowles, S.W. McPhee, C. Li, and et al. Phase 1 gene therapy for Duchenne muscular dystrophy using a translational optimized AAV vector Mol Ther 20 2012 443 455
114. M. Jinek, K. Chylinski, I. Fonfara, and et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity Science 337 2012 816 821
115. L. Cong, F.A. Ran, D. Cox, and et al. Multiplex genome engineering using CRISPR/Cas systems Science 339 2013 819 823
116. C. Long, J.R. McAnally, J.M. Shelton, and et al. Prevention of muscular dystrophy in mice by CRISPR/Cas9-mediated editing of germline DNA Science 345 2014 1184 1188
117. C. Long, L. Amoasii, A.A. Mireault, and et al. Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy Science 351 2016 400 403
118. C.E. Nelson, C.H. Hakim, D.G. Ousterout, and et al. In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy Science 351 2016 403 407