Spectrum of muscular dystrophies associated with sarcolemmal-protein genetic defects

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1852, Issue 4, 2015, Pages 585-

  Nigro, Vincenzo ^a,b   Piluso, Giulio ^a,b  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

Author keywords

Duchenne muscular dystrophy; Dysferlin; Dystroglycan; Dystrophin; Limb girdle muscular dystrophy; Sarcoglycan

Indexed keywords

DYSTROPHIN; MUSCLE PROTEIN; SARCOLEMMAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; BECKER MUSCULAR DYSTROPHY; DUCHENNE MUSCULAR DYSTROPHY; DYSFERLINOPATHY; DYSTROGLYCANOPATHY; GENE MUTATION; GENETIC SCREENING; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; MOLECULAR GENETICS; MUSCULAR DYSTROPHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SARCOGLYCANOPATHY; SARCOLEMMA; ANIMAL; GENETIC DISORDER; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; GENETIC DISEASES, INBORN; HUMANS; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES; SARCOLEMMA;

EID: 84941746700     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.07.023     Document Type: Article

References (155)

1. Tyler F.H., Stephens F.E. Studies in disorders of muscle. IV. The clinical manifestations and inheritance of childhood progressive muscular dystrophy. Ann. Intern. Med. 1951, 35:169-185.
2. Tyler F.H., Stephens F.E. Studies in disorders of muscle. II Clinical manifestations and inheritance of facioscapulohumeral dystrophy in a large family. Ann. Intern. Med. 1950, 32:640-660.
3. Bach J.R. The Duchenne de Boulogne-Meryon controversy and pseudohypertrophic muscular dystrophy. J. Hist. Med. Allied Sci. 2000, 55:158-178.
4. Emery A. Duchenne muscular dystrophy or Meryon's disease. Lancet 2001, 357:1529.
5. Nigro G. One-hundred-seventy-five years of Neapolitan contributions to the fight against the muscular diseases. Acta Myol. 2010, 29:369-391.
6. Monaco A.P., Bertelson C.J., Middlesworth W., Colletti C.A., Aldridge J., Fischbeck K.H., Bartlett R., Pericak-Vance M.A., Roses A.D., Kunkel L.M. Detection of deletions spanning the Duchenne muscular dystrophy locus using a tightly linked DNA segment. Nature 1985, 316:842-845.
7. Rowland L.P. Dystrophin: a triumph of reverse genetics and the end of the beginning. N. Engl. J. Med. 1988, 318:1392-1394.
8. Hoffman E.P., Brown R.H., Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 1987, 51:919-928.
9. Zubrzycka-Gaarn E.E., Bulman D.E., Karpati G., Burghes A.H., Belfall B., Klamut H.J., Talbot J., Hodges R.S., Ray P.N., Worton R.G. The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature 1988, 333:466-469.
10. Ervasti J.M., Campbell K.P. Membrane organization of the dystrophin-glycoprotein complex. Cell 1991, 66:1121-1131.
11. Ozawa E. Our trails and trials in the subsarcolemmal cytoskeleton network and muscular dystrophy researches in the dystrophin era. Proc. Jpn. Acad. 2010, 86:798-821.
12. Ehmsen J., Poon E., Davies K. The dystrophin-associated protein complex. J. Cell Sci. 2002, 115:2801-2803.
13. Bonnemann C.G., Modi R., Noguchi S., Mizuno Y., Yoshida M., Gussoni E., McNally E.M., Duggan D.J., Angelini C., Hoffman E.P. Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat. Genet. 1995, 11:266-273.
14. Nigro V., de Sa Moreira E., Piluso G., Vainzof M., Belsito A., Politano L., Puca A.A., Passos-Bueno M.R., Zatz M. Autosomal recessive limb-girdle muscular dystrophy, LGMD2F, is caused by a mutation in the delta-sarcoglycan gene. Nat. Genet. 1996, 14:195-198.
15. Noguchi S., McNally E.M., Ben Othmane K., Hagiwara Y., Mizuno Y., Yoshida M., Yamamoto H., Bonnemann C.G., Gussoni E., Denton P.H., Kyriakides T., Middleton L., Hentati F., Ben Hamida M., Nonaka I., Vance J.M., Kunkel L.M., Ozawa E. Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science (New York, N.Y.) 1995, 270:819-822.
16. Roberds S.L., Leturcq F., Allamand V., Piccolo F., Jeanpierre M., Anderson R.D., Lim L.E., Lee J.C., Tome F.M., Romero N.B., et al. Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell 1994, 78:625-633.
17. Lim L.E., Duclos F., Broux O., Bourg N., Sunada Y., Allamand V., Meyer J., Richard I., Moomaw C., Slaughter C., et al. Beta-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12. Nat. Genet. 1995, 11:257-265.
18. Helbling-Leclerc A., Zhang X., Topaloglu H., Cruaud C., Tesson F., Weissenbach J., Tome F.M., Schwartz K., Fardeau M., Tryggvason K., et al. Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat. Genet. 1995, 11:216-218.
19. Muntoni F., Torelli S., Wells D.J., Brown S.C. Muscular dystrophies due to glycosylation defects: diagnosis and therapeutic strategies. Curr. Opin. Neurol. 2011, 24:437-442.
20. Wells L. The o-mannosylation pathway: glycosyltransferases and proteins implicated in congenital muscular dystrophy. J. Biol. Chem. 2013, 288:6930-6935.
21. Nigro V., Savarese M. Genetic basis of limb-girdle muscular dystrophies: the 2014 update. Acta Myol. 2014, 33:1-12.
22. Mendell J.R., Shilling C., Leslie N.D., Flanigan K.M., al-Dahhak R., Gastier-Foster J., Kneile K., Dunn D.M., Duval B., Aoyagi A., Hamil C., Mahmoud M., Roush K., Bird L., Rankin C., Lilly H., Street N., Chandrasekar R., Weiss R.B. Evidence-based path to newborn screening for Duchenne muscular dystrophy. Ann. Neurol. 2012, 71:304-313.
23. Ellis J.A., Vroom E., Muntoni F. 195th ENMC International Workshop: Newborn screening for Duchenne muscular dystrophy 14-16th December, 2012, Naarden, The Netherlands. Neuromuscul. Disord. 2013, 23:682-689.
24. Mazzone E., Vasco G., Sormani M.P., Torrente Y., Berardinelli A., Messina S., D'Amico A., Doglio L., Politano L., Cavallaro F., Frosini S., Bello L., Bonfiglio S., Zucchini E., De Sanctis R., Scutifero M., Bianco F., Rossi F., Motta M.C., Sacco A., Donati M.A., Mongini T., Pini A., Battini R., Pegoraro E., Pane M., Gasperini S., Previtali S., Napolitano S., Martinelli D., Bruno C., Vita G., Comi G., Bertini E., Mercuri E. Functional changes in Duchenne muscular dystrophy: a 12-month longitudinal cohort study. Neurology 2011, 77:250-256.
25. Nigro G., Comi L.I., Limongelli F.M., Giugliano M.A., Politano L., Petretta V., Passamano L., Stefanelli S. Prospective study of X-linked progressive muscular dystrophy in Campania. Muscle Nerve 1983, 6:253-262.
26. Spurney C., Shimizu R., Hache L.P., Kolski H., Gordish-Dressman H., Clemens P.R. CINRG Duchenne Natural History Study demonstrates insufficient diagnosis and treatment of cardiomyopathy in Duchenne muscular dystrophy. Muscle Nerve 2014, 50:250-256.
27. Kieny P., Chollet S., Delalande P., Le Fort M., Magot A., Pereon Y., Perrouin Verbe B. Evolution of life expectancy of patients with Duchenne muscular dystrophy at AFM Yolaine de Kepper centre between 1981 and 2011. Ann. Phys. Rehabil. Med. 2013, 56:443-454.
28. Passamano L., Taglia A., Palladino A., Viggiano E., D'Ambrosio P., Scutifero M., Cecio M.R., Torre V., De Luca F., Picillo E., Paciello O., Piluso G., Nigro G., Politano L. Improvement of survival in Duchenne Muscular Dystrophy: retrospective analysis of 835 patients. Acta Myol. 2012, 31:121-125.
29. Nigro V. Improving the course of muscular dystrophy?. Acta Myol. 2012, 31:109.
30. Ferlini A., Sewry C., Melis M.A., Mateddu A., Muntoni F. X-linked dilated cardiomyopathy and the dystrophin gene. Neuromuscul. Disord. 1999, 9:339-346.
31. Abbs S., Roberts R.G., Mathew C.G., Bentley D.R., Bobrow M. Accurate assessment of intragenic recombination frequency within the Duchenne muscular dystrophy gene. Genomics 1990, 7:602-606.
32. Tennyson C.N., Klamut H.J., Worton R.G. The human dystrophin gene requires 16hours to be transcribed and is cotranscriptionally spliced. Nat. Genet. 1995, 9:184-190.
33. Surono A., Takeshima Y., Wibawa T., Ikezawa M., Nonaka I., Matsuo M. Circular dystrophin RNAs consisting of exons that were skipped by alternative splicing. Hum. Mol. Genet. 1999, 8:493-500.
34. Bovolenta M., Erriquez D., Valli E., Brioschi S., Scotton C., Neri M., Falzarano M.S., Gherardi S., Fabris M., Rimessi P., Gualandi F., Perini G., Ferlini A. The DMD locus harbours multiple long non-coding RNAs which orchestrate and control transcription of muscle dystrophin mRNA isoforms. PLoS One 2012, 7:e45328.
35. Muntoni F., Torelli S., Ferlini A. Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2003, 2:731-740.
36. Neri M., Torelli S., Brown S., Ugo I., Sabatelli P., Merlini L., Spitali P., Rimessi P., Gualandi F., Sewry C., Ferlini A., Muntoni F. Dystrophin levels as low as 30% are sufficient to avoid muscular dystrophy in the human. Neuromuscul. Disord. 2007, 17:913-918.
37. Schwartz M., Duno M., Palle A.L., Krag T., Vissing J. Deletion of exon 16 of the dystrophin gene is not associated with disease. Hum. Mutat. 2007, 28:205.
38. Aartsma-Rus A., Van Deutekom J.C., Fokkema I.F., Van Ommen G.J., Den Dunnen J.T. 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 2006, 34:135-144.
39. Torella A., Trimarco A., Blanco Fdel V., Cuomo A., Aurino S., Piluso G., Minetti C., Politano L., Nigro V. One hundred twenty-one dystrophin point mutations detected from stored DNA samples by combinatorial denaturing high-performance liquid chromatography. J. Mol. Diagn. 2010, 12:65-73.
40. Flanigan K.M., Dunn D.M., von Niederhausern A., Soltanzadeh P., Gappmaier E., Howard M.T., Sampson J.B., Mendell J.R., Wall C., King W.M., Pestronk A., Florence J.M., Connolly A.M., Mathews K.D., Stephan C.M., Laubenthal K.S., Wong B.L., Morehart P.J., Meyer A., Finkel R.S., Bonnemann C.G., Medne L., Day J.W., Dalton J.C., Margolis M.K., Hinton V.J., Weiss R.B. Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum. Mutat. 2009, 30:1657-1666.
41. Nigro V., Politano L., Nigro G., Romano S.C., Molinari A.M., Puca G.A. Detection of a nonsense mutation in the dystrophin gene by multiple SSCP. Hum. Mol. Genet. 1992, 1:517-520.
42. Flanigan K.M., Dunn D.M., von Niederhausern A., Soltanzadeh P., Howard M.T., Sampson J.B., Swoboda K.J., Bromberg M.B., Mendell J.R., Taylor L.E., Anderson C.B., Pestronk A., Florence J.M., Connolly A.M., Mathews K.D., Wong B., Finkel R.S., Bonnemann C.G., Day J.W., McDonald C., Weiss R.B. Nonsense mutation-associated Becker muscular dystrophy: interplay between exon definition and splicing regulatory elements within the DMD gene. Hum. Mutat. 2011, 32:299-308.
43. Vulin A., Wein N., Strandjord D.M., Johnson E.K., Findlay A.R., Maiti B., Howard M.T., Kaminoh Y.J., Taylor L.E., Simmons T.R., Ray W.C., Montanaro F., Ervasti J.M., Flanigan K.M. The ZZ domain of dystrophin in DMD: making sense of missense mutations. Hum. Mutat. 2014, 35:257-264.
44. Trimarco A., Torella A., Piluso G., Maria Ventriglia V., Politano L., Nigro V. Log-PCR: a new tool for immediate and cost-effective diagnosis of up to 85% of dystrophin gene mutations. Clin. Chem. 2008, 54:973-981.
45. Schouten J.P., McElgunn C.J., Waaijer R., Zwijnenburg D., Diepvens F., Pals G. Relative quantification of 40 nucleic acid sequences by multiplex ligation-dependent probe amplification. Nucleic Acids Res. 2002, 30:e57.
46. Lalic T., Vossen R.H., Coffa J., Schouten J.P., Guc-Scekic M., Radivojevic D., Djurisic M., Breuning M.H., White S.J., den Dunnen J.T. Deletion and duplication screening in the DMD gene using MLPA. Eur. J. Hum. Genet. 2005, 13:1231-1234.
47. Hegde M.R., Chin E.L., Mulle J.G., Okou D.T., Warren S.T., Zwick M.E. Microarray-based mutation detection in the dystrophin gene. Hum. Mutat. 2008, 29:1091-1099.
48. Saillour Y., Cossee M., Leturcq F., Vasson A., Beugnet C., Poirier K., Commere V., Sublemontier S., Viel M., Letourneur F., Barbot J.C., Deburgrave N., Chelly J., Bienvenu T. Detection of exonic copy-number changes using a highly efficient oligonucleotide-based comparative genomic hybridization-array method. Hum. Mutat. 2008, 29:1083-1090.
49. del Gaudio D., Yang Y., Boggs B.A., Schmitt E.S., Lee J.A., Sahoo T., Pham H.T., Wiszniewska J., Chinault A.C., Beaudet A.L., Eng C.M. Molecular diagnosis of Duchenne/Becker muscular dystrophy: enhanced detection of dystrophin gene rearrangements by oligonucleotide array-comparative genomic hybridization. Hum. Mutat. 2008, 29:1100-1107.
50. Piluso G., Dionisi M., Del Vecchio Blanco F., Torella A., Aurino S., Savarese M., Giugliano T., Bertini E., Terracciano A., Vainzof M., Criscuolo C., Politano L., Casali C., Santorelli F.M., Nigro V. Motor chip: a comparative genomic hybridization microarray for copy-number mutations in 245 neuromuscular disorders. Clin. Chem. 2011, 57:1584-1596.
51. Nigro V., Piluso G. Next generation sequencing (NGS) strategies for the genetic testing of myopathies. Acta Myol. 2012, 31:196-200.
52. Monaco A.P., Bertelson C.J., Liechti-Gallati S., Moser H., Kunkel L.M. An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 1988, 2:90-95.
53. Politano L., Nigro V., Nigro G., Petretta V.R., Passamano L., Papparella S., Di Somma S., Comi L.I. Development of cardiomyopathy in female carriers of Duchenne and Becker muscular dystrophies. JAMA 1996, 275:1335-1338.
54. Brown K.J., Marathi R., Fiorillo A.A., Ciccimaro E.F., Sharma S., Rowlands D.S., Rayavarapu S., Nagaraju K., Hoffman E.P., Hathout Y. Accurate Quantitation of Dystrophin Protein in Human Skeletal Muscle Using Mass Spectrometry. J. Bioanal. Biomed. 2012, (Suppl. 7).
55. Rybakova I.N., Patel J.R., Ervasti J.M. The dystrophin complex forms a mechanically strong link between the sarcolemma and costameric actin. J. Cell Biol. 2000, 150:1209-1214.
56. Prins K.W., Humston J.L., Mehta A., Tate V., Ralston E., Ervasti J.M. Dystrophin is a microtubule-associated protein. J. Cell Biol. 2009, 186:363-369.
57. Rybakova I.N., Amann K.J., Ervasti J.M. A new model for the interaction of dystrophin with F-actin. J. Cell Biol. 1996, 135:661-672.
58. Lai Y., Thomas G.D., Yue Y., Yang H.T., Li D., Long C., Judge L., Bostick B., Chamberlain J.S., Terjung R.L., Duan D. 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. 2009, 119:624-635.
59. Lai Y., Zhao J., Yue Y., Duan D. alpha2 and alpha3 helices of dystrophin R16 and R17 frame a microdomain in the alpha1 helix of dystrophin R17 for neuronal NOS binding. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:525-530.
60. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santillano D.R., Wu Z., Huang F., Xia H., Peters M.F., Froehner S.C., Bredt D.S. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 1996, 84:757-767.
61. Kameya S., Miyagoe Y., Nonaka I., Ikemoto T., Endo M., Hanaoka K., Nabeshima Y., Takeda S. alpha1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration. J. Biol. Chem. 1999, 274:2193-2200.
62. Holmberg J., Durbeej M. Laminin-211 in skeletal muscle function. Cell Adhes. Migr. 2013, 7:111-121.
63. Sandona D., Betto R. Sarcoglycanopathies: molecular pathogenesis and therapeutic prospects. Expert Rev. Mol. Med. 2009, 11:e28.
64. Nigro V., Piluso G., Belsito A., Politano L., Puca A.A., Papparella S., Rossi E., Viglietto G., Esposito M.G., Abbondanza C., Medici N., Molinari A.M., Nigro G., Puca G.A. Identification of a novel sarcoglycan gene at 5q33 encoding a sarcolemmal 35kDa glycoprotein. Hum. Mol. Genet. 1996, 5:1179-1186.
65. Zimprich A., Grabowski M., Asmus F., Naumann M., Berg D., Bertram M., Scheidtmann K., Kern P., Winkelmann J., Muller-Myhsok B., Riedel L., Bauer M., Muller T., Castro M., Meitinger T., Strom T.M., Gasser T. Mutations in the gene encoding epsilon-sarcoglycan cause myoclonus-dystonia syndrome. Nat. Genet. 2001, 29:66-69.
66. Wheeler M.T., Zarnegar S., McNally E.M. Zeta-sarcoglycan, a novel component of the sarcoglycan complex, is reduced in muscular dystrophy. Hum. Mol. Genet. 2002, 11:2147-2154.
67. Allikian M.J., McNally E.M. Processing and assembly of the dystrophin glycoprotein complex. Traffic 2007, 8:177-183.
68. Draviam R.A., Wang B., Shand S.H., Xiao X., Watkins S.C. Alpha-sarcoglycan is recycled from the plasma membrane in the absence of sarcoglycan complex assembly. Traffic 2006, 7:793-810.
69. Bianchini E., Fanin M., Mamchaoui K., Betto R., Sandona D. Unveiling the degradative route of the V247M alpha-sarcoglycan mutant responsible for LGMD-2D. Hum. Mol. Genet. 2014, 23:3746-3758.
70. Lancioni A., Rotundo I.L., Kobayashi Y.M., D'Orsi L., Aurino S., Nigro G., Piluso G., Acampora D., Cacciottolo M., Campbell K.P., Nigro V. Combined deficiency of alpha and epsilon sarcoglycan disrupts the cardiac dystrophin complex. Hum. Mol. Genet. 2011, 20:4644-4654.
71. Fanin M., Nascimbeni A.C., Aurino S., Tasca E., Pegoraro E., Nigro V., Angelini C. Frequency of LGMD gene mutations in Italian patients with distinct clinical phenotypes. Neurology 2009, 72:1432-1435.
72. Nigro V. Molecular bases of autosomal recessive limb-girdle muscular dystrophies. Acta Myol. 2003, 22:35-42.
73. Vainzof M., Passos-Bueno M.R., Pavanello R.C., Marie S.K., Oliveira A.S., Zatz M. Sarcoglycanopathies are responsible for 68% of severe autosomal recessive limb-girdle muscular dystrophy in the Brazilian population. J. Neurol. Sci. 1999, 164:44-49.
74. Khadilkar S.V., Singh R.K., Hegde M., Urtizberea A., Love D.R., Chong B. Spectrum of mutations in sarcoglycan genes in the Mumbai region of western India: high prevalence of 525del T. Neurol. India 2009, 57:406-410.
75. Piccolo F., Jeanpierre M., Leturcq F., Dode C., Azibi K., Toutain A., Merlini L., Jarre L., Navarro C., Krishnamoorthy R., Tome F.M., Urtizberea J.A., Beckmann J.S., Campbell K.P., Kaplan J.C. A founder mutation in the gamma-sarcoglycan gene of gypsies possibly predating their migration out of India. Hum. Mol. Genet. 1996, 5:2019-2022.
76. McNally E.M., Passos-Bueno M.R., Bonnemann C.G., Vainzof M., de Sa Moreira E., Lidov H.G., Othmane K.B., Denton P.H., Vance J.M., Zatz M., Kunkel L.M. Mild and severe muscular dystrophy caused by a single gamma-sarcoglycan mutation. Am. J. Hum. Genet. 1996, 59:1040-1047.
77. Fanin M., Melacini P., Boito C., Pegoraro E., Angelini C. LGMD2E patients risk developing dilated cardiomyopathy. Neuromuscul. Disord. 2003, 13:303-309.
78. Politano L., Nigro V., Passamano L., Petretta V., Comi L.I., Papparella S., Nigro G., Rambaldi P.F., Raia P., Pini A., Mora M., Giugliano M.A., Esposito M.G., Nigro G. Evaluation of cardiac and respiratory involvement in sarcoglycanopathies. Neuromuscul. Disord. 2001, 11:178-185.
79. Nigro V., Okazaki Y., Belsito A., Piluso G., Matsuda Y., Politano L., Nigro G., Ventura C., Abbondanza C., Molinari A.M., Acampora D., Nishimura M., Hayashizaki Y., Puca G.A. Identification of the Syrian hamster cardiomyopathy gene. Hum. Mol. Genet. 1997, 6:601-607.
80. Cheng L., Guo X.F., Yang X.Y., Chong M., Cheng J., Li G., Gui Y.H., Lu D.R. Delta-sarcoglycan is necessary for early heart and muscle development in zebrafish. Biochem. Biophys. Res. Commun. 2006, 344:1290-1299.
81. Warner L.E., DelloRusso C., Crawford R.W., Rybakova I.N., Patel J.R., Ervasti J.M., Chamberlain J.S. Expression of Dp260 in muscle tethers the actin cytoskeleton to the dystrophin-glycoprotein complex and partially prevents dystrophy. Hum. Mol. Genet. 2002, 11:1095-1105.
82. Judge L.M., Arnett A.L., Banks G.B., Chamberlain J.S. Expression of the dystrophin isoform Dp116 preserves functional muscle mass and extends lifespan without preventing dystrophy in severely dystrophic mice. Hum. Mol. Genet. 2011, 20:4978-4990.
83. Johnson E.K., Li B., Yoon J.H., Flanigan K.M., Martin P.T., Ervasti J., Montanaro F. Identification of new dystroglycan complexes in skeletal muscle. PLoS One 2013, 8:e73224.
84. Williamson R.A., Henry M.D., Daniels K.J., Hrstka R.F., Lee J.C., Sunada Y., Ibraghimov-Beskrovnaya O., Campbell K.P. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 1997, 6:831-841.
85. Barresi R., Campbell K.P. Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 2006, 119:199-207.
86. Hara Y., Balci-Hayta B., Yoshida-Moriguchi T., Kanagawa M., Beltran-Valero de Bernabe D., Gundesli H., Willer T., Satz J.S., Crawford R.W., Burden S.J., Kunz S., Oldstone M.B., Accardi A., Talim B., Muntoni F., Topaloglu H., Dincer P., Campbell K.P. A dystroglycan mutation associated with limb-girdle muscular dystrophy. N. Engl. J. Med. 2011, 364:939-946.
87. Nigro V., Aurino S., Piluso G. Limb girdle muscular dystrophies: update on genetic diagnosis and therapeutic approaches. Curr. Opin. Neurol. 2011, 24:429-436.
88. Yang A.C., Ng B.G., Moore S.A., Rush J., Waechter C.J., Raymond K.M., Willer T., Campbell K.P., Freeze H.H., Mehta L. Congenital disorder of glycosylation due to DPM1 mutations presenting with dystroglycanopathy-type congenital muscular dystrophy. Mol. Genet. Metab. 2013, 110:345-351.
89. Barone R., Aiello C., Race V., Morava E., Foulquier F., Riemersma M., Passarelli C., Concolino D., Carella M., Santorelli F., Vleugels W., Mercuri E., Garozzo D., Sturiale L., Messina S., Jaeken J., Fiumara A., Wevers R.A., Bertini E., Matthijs G., Lefeber D.J. DPM2-CDG: a muscular dystrophy-dystroglycanopathy syndrome with severe epilepsy. Ann. Neurol. 2012, 72:550-558.
90. Lefeber D.J., Schonberger J., Morava E., Guillard M., Huyben K.M., Verrijp K., Grafakou O., Evangeliou A., Preijers F.W., Manta P., Yildiz J., Grunewald S., Spilioti M., van den Elzen C., Klein D., Hess D., Ashida H., Hofsteenge J., Maeda Y., van den Heuvel L., Lammens M., Lehle L., Wevers R.A. Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am. J. Hum. Genet. 2009, 85:76-86.
91. Lefeber D.J., de Brouwer A.P., Morava E., Riemersma M., Schuurs-Hoeijmakers J.H., Absmanner B., Verrijp K., van den Akker W.M., Huijben K., Steenbergen G., van Reeuwijk J., Jozwiak A., Zucker N., Lorber A., Lammens M., Knopf C., van Bokhoven H., Grunewald S., Lehle L., Kapusta L., Mandel H., Wevers R.A. Autosomal recessive dilated cardiomyopathy due to DOLK mutations results from abnormal dystroglycan O-mannosylation. PLoS Genet. 2011, 7:e1002427.
92. Goddeeris M.M., Wu B., Venzke D., Yoshida-Moriguchi T., Saito F., Matsumura K., Moore S.A., Campbell K.P. LARGE glycans on dystroglycan function as a tunable matrix scaffold to prevent dystrophy. Nature 2013, 503:136-140.
93. Barresi R., Michele D.E., Kanagawa M., Harper H.A., Dovico S.A., Satz J.S., Moore S.A., Zhang W., Schachter H., Dumanski J.P., Cohn R.D., Nishino I., Campbell K.P. LARGE can functionally bypass alpha-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat. Med. 2004, 10:696-703.
94. Saito F., Kanagawa M., Ikeda M., Hagiwara H., Masaki T., Ohkuma H., Shimizu T., Sonoo M., Toda T., Matsumura K. Overexpression of LARGE suppresses muscle regeneration via down-regulation of insulin-like growth factor 1 and aggravates muscular dystrophy in mice. Hum. Mol. Genet. 2014, 23:4543-4558.
95. Whitmore C., Fernandez-Fuente M., Booler H., Parr C., Kavishwar M., Ashraf A., Lacey E., Kim J., Terry R., Ackroyd M.R., Wells K.E., Muntoni F., Wells D.J., Brown S.C. The transgenic expression of LARGE exacerbates the muscle phenotype of dystroglycanopathy mice. Hum. Mol. Genet. 2014, 23:1842-1855.
96. Nalini A., Gayathri N. Dysferlinopathy: a clinical and histopathological study of 28 patients from India. Neurol. India 2008, 56:379-385. (discussion 386-377).
97. Guglieri M., Magri F., D'Angelo M.G., Prelle A., Morandi L., Rodolico C., Cagliani R., Mora M., Fortunato F., Bordoni A., Del Bo R., Ghezzi S., Pagliarani S., Lucchiari S., Salani S., Zecca C., Lamperti C., Ronchi D., Aguennouz M., Ciscato P., Di Blasi C., Ruggieri A., Moroni I., Turconi A., Toscano A., Moggio M., Bresolin N., Comi G.P. Clinical, molecular, and protein correlations in a large sample of genetically diagnosed Italian limb girdle muscular dystrophy patients. Hum. Mutat. 2008, 29:258-266.
98. Lo H.P., Cooper S.T., Evesson F.J., Seto J.T., Chiotis M., Tay V., Compton A.G., Cairns A.G., Corbett A., MacArthur D.G., Yang N., Reardon K., North K.N. Limb-girdle muscular dystrophy: diagnostic evaluation, frequency and clues to pathogenesis. Neuromuscul. Disord. 2008, 18:34-44.
99. van der Kooi A.J., Frankhuizen W.S., Barth P.G., Howeler C.J., Padberg G.W., Spaans F., Wintzen A.R., Wokke J.H., van Ommen G.J., de Visser M., Bakker E., Ginjaar H.B. Limb-girdle muscular dystrophy in the Netherlands: gene defect identified in half the families. Neurology 2007, 68:2125-2128.
100. Bansal D., Miyake K., Vogel S.S., Groh S., Chen C.C., Williamson R., McNeil P.L., Campbell K.P. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 2003, 423:168-172.
101. de Morree A., Flix B., Bagaric I., Wang J., van den Boogaard M., Grand Moursel L., Frants R.R., Illa I., Gallardo E., Toes R., van der Maarel S.M. Dysferlin regulates cell adhesion in human monocytes. J. Biol. Chem. 2013, 288:14147-14157.
102. Rosales X.Q., Gastier-Foster J.M., Lewis S., Vinod M., Thrush D.L., Astbury C., Pyatt R., Reshmi S., Sahenk Z., Mendell J.R. Novel diagnostic features of dysferlinopathies. Muscle Nerve 2010, 42:14-21.
103. Klinge L., Dean A.F., Kress W., Dixon P., Charlton R., Muller J.S., Anderson L.V., Straub V., Barresi R., Lochmuller H., Bushby K. Late onset in dysferlinopathy widens the clinical spectrum. Neuromuscul. Disord. 2008, 18:288-290.
104. Nguyen K., Bassez G., Krahn M., Bernard R., Laforet P., Labelle V., Urtizberea J.A., Figarella-Branger D., Romero N., Attarian S., Leturcq F., Pouget J., Levy N., Eymard B. Phenotypic study in 40 patients with dysferlin gene mutations: high frequency of atypical phenotypes. Arch. Neurol. 2007, 64:1176-1182.
105. Weiler T., Bashir R., Anderson L.V., Davison K., Moss J.A., Britton S., Nylen E., Keers S., Vafiadaki E., Greenberg C.R., Bushby C.R., Wrogemann K. Identical mutation in patients with limb girdle muscular dystrophy type 2B or Miyoshi myopathy suggests a role for modifier gene(s). Hum. Mol. Genet. 1999, 8:871-877.
106. Paradas C., Llauger J., Diaz-Manera J., Rojas-Garcia R., De Luna N., Iturriaga C., Marquez C., Uson M., Hankiewicz K., Gallardo E., Illa I. Redefining dysferlinopathy phenotypes based on clinical findings and muscle imaging studies. Neurology 2010, 75:316-323.
107. Klinge L., Aboumousa A., Eagle M., Hudson J., Sarkozy A., Vita G., Charlton R., Roberts M., Straub V., Barresi R., Lochmuller H., Bushby K. New aspects on patients affected by dysferlin deficient muscular dystrophy. J. Neurol. Neurosurg. Psychiatry 2010, 81:946-953.
108. Chiu Y.H., Hornsey M.A., Klinge L., Jorgensen L.H., Laval S.H., Charlton R., Barresi R., Straub V., Lochmuller H., Bushby K. Attenuated muscle regeneration is a key factor in dysferlin-deficient muscular dystrophy. Hum. Mol. Genet. 2009, 18:1976-1989.
109. Han R. Muscle membrane repair and inflammatory attack in dysferlinopathy. Skelet. Muscle 2011, 1:10.
110. Weisleder N., Takizawa N., Lin P., Wang X., Cao C., Zhang Y., Tan T., Ferrante C., Zhu H., Chen P.J., Yan R., Sterling M., Zhao X., Hwang M., Takeshima M., Cai C., Cheng H., Takeshima H., Xiao R.P., Ma J. Recombinant MG53 protein modulates therapeutic cell membrane repair in treatment of muscular dystrophy. Sci. Transl. Med. 2012, 4:139ra185.
111. Puttini S., Lekka M., Dorchies O.M., Saugy D., Incitti T., Ruegg U.T., Bozzoni I., Kulik A.J., Mermod N. Gene-mediated restoration of normal myofiber elasticity in dystrophic muscles. Mol. Ther. 2009, 17:19-25.
112. Hakim C.H., Grange R.W., Duan D. The passive mechanical properties of the extensor digitorum longus muscle are compromised in 2- to 20-mo-old mdx mice. J. Appl. Physiol. (1985) 2011, 110:1656-1663.
113. Allen D.G. Eccentric muscle damage: mechanisms of early reduction of force. Acta Physiol. Scand. 2001, 171:311-319.
114. Cheung K., Hume P., Maxwell L. Delayed onset muscle soreness: treatment strategies and performance factors. Sports Med. 2003, 33:145-164.
115. Iwata Y., Katanosaka Y., Arai Y., Komamura K., Miyatake K., Shigekawa M. A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. J. Cell Biol. 2003, 161:957-967.
116. Allen D.G., Gervasio O.L., Yeung E.W., Whitehead N.P. Calcium and the damage pathways in muscular dystrophy. Can. J. Physiol. Pharmacol. 2010, 88:83-91.
117. Millay D.P., Goonasekera S.A., Sargent M.A., Maillet M., Aronow B.J., Molkentin J.D. Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19023-19028.
118. Spencer M.J., Mellgren R.L. Overexpression of a calpastatin transgene in mdx muscle reduces dystrophic pathology. Hum. Mol. Genet. 2002, 11:2645-2655.
119. Stupka N., Gregorevic P., Plant D.R., Lynch G.S. The calcineurin signal transduction pathway is essential for successful muscle regeneration in mdx dystrophic mice. Acta Neuropathol. 2004, 107:299-310.
120. Sundaram J.S., Rao V.M., Meena A.K., Anandaraj M.P. Decreased calcineurin activity in circulation of Duchenne muscular dystrophy. Clin. Biochem. 2007, 40:443-446.
121. Fadic R. Cell surface and gene expression regulation molecules in dystrophinopathy: mdx vs. Duchenne. Biol. Res. 2005, 38:375-380.
122. Constantin B. Dystrophin complex functions as a scaffold for signalling proteins. Biochim. Biophys. Acta 2014, 1838:635-642.
123. Bhatnagar S., Kumar A. Therapeutic targeting of signaling pathways in muscular dystrophy. J. Mol. Med. 2010, 88:155-166.
124. Stamler J.S., Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol. Rev. 2001, 81:209-237.
125. Brenman J.E., Chao D.S., Xia H., Aldape K., Bredt D.S. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995, 82:743-752.
126. Chang W.J., Iannaccone S.T., Lau K.S., Masters B.S., McCabe T.J., McMillan K., Padre R.C., Spencer M.J., Tidball J.G., Stull J.T. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9142-9147.
127. Crosbie R.H., Barresi R., Campbell K.P. Loss of sarcolemma nNOS in sarcoglycan-deficient muscle. FASEB J. 2002, 16:1786-1791.
128. Chao D.S., Gorospe J.R., Brenman J.E., Rafael J.A., Peters M.F., Froehner S.C., Hoffman E.P., Chamberlain J.S., Bredt D.S. Selective loss of sarcolemmal nitric oxide synthase in Becker muscular dystrophy. J. Exp. Med. 1996, 184:609-618.
129. Gentil C., Leturcq F., Ben Yaou R., Kaplan J.C., Laforet P., Penisson-Besnier I., Espil-Taris C., Voit T., Garcia L., Pietri-Rouxel F. Variable phenotype of del45-55 Becker patients correlated with nNOSmu mislocalization and RYR1 hypernitrosylation. Hum. Mol. Genet. 2012, 21:3449-3460.
130. Torelli S., Brown S.C., Jimenez-Mallebrera C., Feng L., Muntoni F., Sewry C.A. 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. 2004, 30:540-545.
131. Thomas G.D., Sander M., Lau K.S., Huang P.L., Stull J.T., Victor R.G. Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15090-15095.
132. Sander M., Chavoshan B., Harris S.A., Iannaccone S.T., Stull J.T., Thomas G.D., Victor R.G. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13818-13823.
133. Zhang Y., Yue Y., Li L., Hakim C.H., Zhang K., Thomas G.D., Duan D. Dual AAV therapy ameliorates exercise-induced muscle injury and functional ischemia in murine models of Duchenne muscular dystrophy. Hum. Mol. Genet. 2013, 22:3720-3729.
134. Lawler J.M. Exacerbation of pathology by oxidative stress in respiratory and locomotor muscles with Duchenne muscular dystrophy. J. Physiol. 2011, 589:2161-2170.
135. Rando T.A. Role of nitric oxide in the pathogenesis of muscular dystrophies: a "two hit" hypothesis of the cause of muscle necrosis. Microsc. Res. Tech. 2001, 55:223-235.
136. Tidball J.G., Villalta S.A. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. 2010, 298:R1173-R1187.
137. Deng B., Wehling-Henricks M., Villalta S.A., Wang Y., Tidball J.G. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration. J. Immunol. 2012, 189:3669-3680.
138. Villalta S.A., Rinaldi C., Deng B., Liu G., Fedor B., Tidball J.G. Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Hum. Mol. Genet. 2011, 20:790-805.
139. Nitahara-Kasahara Y., Hayashita-Kinoh H., Chiyo T., Nishiyama A., Okada H., Takeda S., Okada T. Dystrophic mdx mice develop severe cardiac and respiratory dysfunction following genetic ablation of the anti-inflammatory cytokine IL-10. Hum. Mol. Genet. 2014, 23:3990-4000.
140. Manzur A.Y., Kuntzer T., Pike M., Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst. Rev. 2008, CD003725.
141. Henricson E.K., Abresch R.T., Cnaan A., Hu F., Duong T., Arrieta A., Han J., Escolar D.M., Florence J.M., Clemens P.R., Hoffman E.P., McDonald C.M. The cooperative international neuromuscular research group Duchenne natural history study: glucocorticoid treatment preserves clinically meaningful functional milestones and reduces rate of disease progression as measured by manual muscle testing and other commonly used clinical trial outcome measures. Muscle Nerve 2013, 48:55-67.
142. Tamma R., Annese T., Capogrosso R.F., Cozzoli A., Benagiano V., Sblendorio V., Ruggieri S., Crivellato E., Specchia G., Ribatti D., De Luca A., Nico B. Effects of prednisolone on the dystrophin-associated proteins in the blood-brain barrier and skeletal muscle of dystrophic mdx mice. Lab. Investig. 2013, 93:592-610.
143. Wuebbles R.D., Sarathy A., Kornegay J.N., Burkin D.J. Levels of alpha7 integrin and laminin-alpha2 are increased following prednisone treatment in the mdx mouse and GRMD dog models of Duchenne muscular dystrophy. Dis. Model. Mech. 2013, 6:1175-1184.
144. Kirschner J., Schessl J., Schara U., Reitter B., Stettner G.M., Hobbiebrunken E., Wilichowski E., Bernert G., Weiss S., Stehling F., Wiegand G., Muller-Felber W., Thiele S., Grieben U., von der Hagen M., Lutschg J., Schmoor C., Ihorst G., Korinthenberg R. Treatment of Duchenne muscular dystrophy with ciclosporin A: a randomised, double-blind, placebo-controlled multicentre trial. Lancet Neurol. 2010, 9:1053-1059.
145. Griggs R.C. Duchenne muscular dystrophy: an important negative trial. Lancet Neurol. 2010, 9:1038-1039.
146. Burks T.N., Cohn R.D. Role of TGF-beta signaling in inherited and acquired myopathies. Skelet. Muscle 2011, 1:19.
147. Akhurst R.J., Hata A. Targeting the TGFbeta signalling pathway in disease. Nat. Rev. 2012, 11:790-811.
148. Flanigan K.M., Ceco E., Lamar K.M., Kaminoh Y., Dunn D.M., Mendell J.R., King W.M., Pestronk A., Florence J.M., Mathews K.D., Finkel R.S., Swoboda K.J., Gappmaier E., Howard M.T., Day J.W., McDonald C., McNally E.M., Weiss R.B. LTBP4 genotype predicts age of ambulatory loss in Duchenne muscular dystrophy. Ann. Neurol. 2013, 73:481-488.
149. Saccone V., Consalvi S., Giordani L., Mozzetta C., Barozzi I., Sandona M., Ryan T., Rojas-Munoz A., Madaro L., Fasanaro P., Borsellino G., De Bardi M., Frige G., Termanini A., Sun X., Rossant J., Bruneau B.G., Mercola M., Minucci S., Puri P.L. HDAC-regulated myomiRs control BAF60 variant exchange and direct the functional phenotype of fibro-adipogenic progenitors in dystrophic muscles. Genes Dev. 2014, 28:841-857.
150. Goyenvalle A., Seto J.T., Davies K.E., Chamberlain J. Therapeutic approaches to muscular dystrophy. Hum. Mol. Genet. 2011, 20:R69-R78.
151. Durbeej M., Campbell K.P. Muscular dystrophies involving the dystrophin-glycoprotein complex: an overview of current mouse models. Curr. Opin. Genet. Dev. 2002, 12:349-361.
152. Shin J.H., Pan X., Hakim C.H., Yang H.T., Yue Y., Zhang K., Terjung R.L., Duan D. Microdystrophin ameliorates muscular dystrophy in the canine model of duchenne muscular dystrophy. Mol. Ther. 2013, 21:750-757.
153. van Deutekom J.C., Janson A.A., Ginjaar I.B., Frankhuizen W.S., Aartsma-Rus A., Bremmer-Bout M., den Dunnen J.T., Koop K., van der Kooi A.J., Goemans N.M., de Kimpe S.J., Ekhart P.F., Venneker E.H., Platenburg G.J., Verschuuren J.J., van Ommen G.J. Local dystrophin restoration with antisense oligonucleotide PRO051. N. Engl. J. Med. 2007, 357:2677-2686.
154. Leung D.G., Wagner K.R. Therapeutic advances in muscular dystrophy. Ann. Neurol. 2013, 74:404-411.
155. Spitali P., Aartsma-Rus A. Splice modulating therapies for human disease. Cell 2012, 148:1085-1088.