What do mouse models of muscular dystrophy tell us about the DAPC and its components?

International Journal of Experimental Pathology

Volumn 95, Issue 6, 2014, Pages 365-377

  Whitmore, Charlotte ^a   Morgan, Jennifer ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Dystroglycan; Dystrophin; Mdx; Mouse models; Muscular dystrophy

Indexed keywords

DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; APO-DYSTROPHIN 1; DYSTROGLYCAN; DYSTROPHIN; MULTIPROTEIN COMPLEX;

DISEASE COURSE; GLYCOSYLATION; HISTOPATHOLOGY; LIFESPAN; MOUSE MODEL; MOUSE MUTANT; MUSCULAR DYSTROPHY; NONHUMAN; ONSET AGE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SYMPTOM; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE; ANIMAL; DISEASE MODEL; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; DYSTROPHIN; HUMANS; MICE, INBRED MDX; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; MUSCULAR DYSTROPHIES;

EID: 84921604348     PISSN: 09599673     EISSN: 13652613     Source Type: Journal    
DOI: 10.1111/iep.12095     Document Type: Review

References (136)

1. Ackroyd M.R., Skordis L., Kaluarachchi M. et al. (2009) Reduced expression of fukutin related protein in mice results in a model for fukutin related protein associated muscular dystrophies. Brain, 132, 439-451.
2. Adams M.E., Kramarcy N., Krall S.P. et al. (2000) Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J. Cell Biol. 150, 1385-1398.
3. Allikian M.J., Hack A.A., Mewborn S., Mayer U. & McNally E.M. (2004) Genetic compensation for sarcoglycan loss by integrin alpha7beta1 in muscle. J. Cell Sci. 117, 3821-3830.
4. Andersson D.C., Meli A.C., Reiken S. et al. (2012) Leaky ryanodine receptors in beta-sarcoglycan deficient mice: a potential common defect in muscular dystrophy. Skelet. Muscle 2, 9.
5. Araki E., Nakamura K., Nakao K. et al. (1997) Targeted disruption of exon 52 in the mouse dystrophin gene induced muscle degeneration similar to that observed in Duchenne muscular dystrophy. Biochem. Biophys. Res. Commun. 238, 492-497.
6. Assereto S., Mastrototaro M., Stringara S. et al. (2008) Aquaporin-4 expression is severely reduced in human sarcoglycanopathies and dysferlinopathies. Cell Cycle 7, 2199-2207.
7. Barton E.R. (2006) Impact of sarcoglycan complex on mechanical signal transduction in murine skeletal muscle. Am. J. Physiol. Cell Physiol. 290, C411-C419.
8. Beastrom N., Lu H., Macke A. et al. (2011) mdx((5)cv) mice manifest more severe muscle dysfunction and diaphragm force deficits than do mdx Mice. Am. J. Pathol. 179, 2464-2474.
9. Beedle A.M., Turner A.J., Saito Y. et al. (2012) Mouse fukutin deletion impairs dystroglycan processing and recapitulates muscular dystrophy. J. Clin. Investig. 122, 3330-3342.
10. Blaeser A., Keramaris E., Chan Y.M. et al. (2013) Mouse models of fukutin-related protein mutations show a wide range of disease phenotypes. Hum. Genet. 132, 923-934.
11. Brenman J.E., Chao D.S., Xia H., Aldape K. & Bredt D.S. (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82, 743-752.
12. Bridges L.R. (1986) The association of cardiac-muscle necrosis and inflammation with the degenerative and persistent myopathy of mdx mice. J. Neurol. Sci. 72, 147-157.
13. Brockington M., Yuva Y., Prandini P. et al. (2001) Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C. Hum. Mol. Genet. 10, 2851-2859.
14. Brunig I., Suter A., Knuesel I., Luscher B. & Fritschy J.M. (2002) GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J. Neurosci. 22, 4805-4813.
15. Bulfield G., Siller W.G., Wight P.A. & Moore K.J. (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl Acad. Sci. USA 81, 1189-1192.
16. Bunnell T.M., Jaeger M.A., Fitzsimons D.P., Prins K.W. & Ervasti J.M. (2008) Destabilization of the dystrophin-glycoprotein complex without functional deficits in alpha-dystrobrevin null muscle. PLoS One 3, e2604.
17. Burkin D.J., Wallace G.Q., Nicol K.J., Kaufman D.J. & Kaufman S.J. (2001) Enhanced expression of the alpha 7 beta 1 integrin reduces muscular dystrophy and restores viability in dystrophic mice. J. Cell Biol. 152, 1207-1218.
18. Cai B., Spencer M.J., Nakamura G., Tseng-Ong L. & Tidball J.G. (2000) Eosinophilia of dystrophin-deficient muscle is promoted by perforin-mediated cytotoxicity by T cell effectors. Am. J. Pathol. 156, 1789-1796.
19. Carnwath J.W. & Shotton D.M. (1987) Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J. Neurol. Sci. 80, 39-54.
20. Chamberlain J.S., Phelps S.F., Cox G.A., Maichele A.J. & Greenwood A.D. (1993) PCR analysis of muscular dystrophy in mdx mice. Mol. Cell Biol. Hum. Dis. Ser. 3, 167-189.
21. Chamberlain J.S., Metzger J., Reyes M., Townsend D.W. & Faulkner J.A. (2007) Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 21, 2195-2204.
22. Chan Y.M., Bonnemann C.G., Lidov H.G. & Kunkel L.M. (1998) Molecular organization of sarcoglycan complex in mouse myotubes in culture. J. Cell Biol. 143, 2033-2044.
23. Chan Y.M., Keramaris-Vrantsis E., Lidov H.G. et al. (2010) Fukutin-related protein is essential for mouse muscle, brain and eye development and mutation recapitulates the wide clinical spectrums of dystroglycanopathies. Hum. Mol. Genet. 19, 3995-4006.
24. Chandrasekharan K., Yoon J.H., Xu Y. et al. (2010) A human-specific deletion in mouse Cmah increases disease severity in the mdx model of Duchenne muscular dystrophy. Sci. Transl. Med., 2, 42ra54.
25. Chapman V.M., Miller D.R., Armstrong D. & Caskey C.T. (1989) Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc. Natl Acad. Sci. USA 86, 1292-1296.
26. Chou H.H., Takematsu H., Diaz S. et al. (1998) A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl Acad. Sci. USA 95, 11751-11756.
27. Cohn R.D., Henry M.D., Michele D.E. et al. (2002) Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration. Cell 110, 639-648.
28. Connolly A.M., Keeling R.M., Mehta S., Pestronk A. & Sanes J.R. (2001) Three mouse models of muscular dystrophy: the natural history of strength and fatigue in dystrophin-, dystrophin/utrophin-, and laminin alpha2-deficient mice. Neuromuscul. Disord. 11, 703-712.
29. Consolino C.M., Duclos F., Lee J., Williamson R.A., Campbell K.P. & Brooks S.V. (2005) Muscles of mice deficient in alpha-sarcoglycan maintain large masses and near control force values throughout the life span. Physiol. Genomics 22, 244-256.
30. Constantin B. (2014) Dystrophin complex functions as a scaffold for signalling proteins. Biochim. Biophys. Acta 1838, 635-642.
31. Coral-Vazquez R., Cohn R.D., Moore S.A. et al. (1999) Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: a novel mechanism for cardiomyopathy and muscular dystrophy. Cell 98, 465-474.
32. Cote P.D., Moukhles H., Lindenbaum M. & Carbonetto S. (1999) Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses. Nat. Genet. 23, 338-342.
33. Coulton G.R., Morgan J.E., Partridge T.A. & Sloper J.C. (1988) The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol. Appl. Neurobiol. 14, 53-70.
34. Cox G.A., Cole N.M., Matsumura K. et al. (1993a) Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature 364, 725-729.
35. Cox G.A., Phelps S.F., Chapman V.M. & Chamberlain J.S. (1993b) New mdx mutation disrupts expression of muscle and nonmuscle isoforms of dystrophin. Nat. Genet. 4, 87-93.
36. Danko I., Chapman V. & Wolff J.A. (1992) The frequency of revertants in mdx mouse genetic models for Duchenne muscular dystrophy. Pediatr. Res. 32, 128-131.
37. Deconinck A.E., Rafael J.A., Skinner J.A. et al. (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90, 717-727.
38. Dellorusso C., Crawford R.W., Chamberlain J.S. & Brooks S.V. (2001) Tibialis anterior muscles in mdx mice are highly susceptible to contraction-induced injury. J. Muscle Res. Cell Motil. 22, 467-475.
39. Dowling P., Culligan K. & Ohlendieck K. (2002) Distal mdx muscle groups exhibiting up-regulation of utrophin and rescue of dystrophin-associated glycoproteins exemplify a protected phenotype in muscular dystrophy. Naturwissenschaften 89, 75-78.
40. Duclos F., Straub V., Moore S.A. et al. (1998) Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice. J. Cell Biol. 142, 1461-1471.
41. Durbeej M., Cohn R.D., Hrstka R.F. et al. (2000) Disruption of the beta-sarcoglycan gene reveals pathogenetic complexity of limb-girdle muscular dystrophy type 2E. Mol. Cell 5, 141-151.
42. Echigoya Y., Lee J., Rodrigues M. et al. (2013) Mutation types and aging differently affect revertant fiber expansion in dystrophic mdx and mdx52 mice. PLoS One 8, e69194.
43. Evans N.P., Misyak S.A., Robertson J.L., Bassaganya-Riera J. & Grange R.W. (2009) Immune-mediated mechanisms potentially regulate the disease time-course of Duchenne muscular dystrophy and provide targets for therapeutic intervention. PM R 1, 755-768.
44. Fan Z., Wang J., Ahn M. et al. (2014) Characteristics of magnetic resonance imaging biomarkers in a natural history study of golden retriever muscular dystrophy. Neuromuscul. Disord., 24, 178-191.
45. Farini A., Meregalli M., Belicchi M. et al. (2007) T and B lymphocyte depletion has a marked effect on the fibrosis of dystrophic skeletal muscles in the scid/mdx mouse. J. Pathol. 213, 229-238.
46. Fukada S., Morikawa D., Yamamoto Y. et al. (2010) Genetic background affects properties of satellite cells and mdx phenotypes. Am. J. Pathol. 176, 2414-2424.
47. Godfrey C., Foley A.R., Clement E. & Muntoni F. (2011) Dystroglycanopathies: coming into focus. Curr. Opin. Genet. Dev. 21, 278-285.
48. Grady R.M., Grange R.W., Lau K.S. et al. (1999) Role for alpha-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat. Cell Biol. 1, 215-220.
49. Gregorevic P., Blankinship M.J., Allen J.M. et al. (2004) Systemic delivery of genes to striated muscles using adeno-associated viral vectors. Nat. Med. 10, 828-834.
50. Grewal P.K., McLaughlan J.M., Moore C.J., Browning C.A. & Hewitt J.E. (2005) Characterization of the LARGE family of putative glycosyltransferases associated with dystroglycanopathies. Glycobiology 15, 912-923.
51. Gumerson J.D., Davis C.S., Kabaeva Z.T., Hayes J.M., Brooks S.V. & Michele D.E. (2013) Muscle-specific expression of LARGE restores neuromuscular transmission deficits in dystrophic LARGE(myd) mice. Hum. Mol. Genet. 22, 757-768.
52. Hack A.A., Ly C.T., Jiang F. et al. (1998) Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol. 142, 1279-1287.
53. Hack A.A., Cordier L., Shoturma D.I., Lam M.Y., Sweeney H.L. & McNally E.M. (1999) Muscle degeneration without mechanical injury in sarcoglycan deficiency. Proc. Natl Acad. Sci. USA 96, 10723-10728.
54. Hack A.A., Lam M.Y., Cordier L. et al. (2000) Differential requirement for individual sarcoglycans and dystrophin in the assembly and function of the dystrophin-glycoprotein complex. J. Cell Sci. 113(Pt 14), 2535-2544.
55. Hamer P.W., McGeachie J.M., Davies M.J. & Grounds M.D. (2002) Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J. Anat. 200, 69-79.
56. Han R., Rader E.P., Levy J.R., Bansal D. & Campbell K.P. (2011) Dystrophin deficiency exacerbates skeletal muscle pathology in dysferlin-null mice. Skelet. Muscle 1, 35.
57. Harper S.Q., Hauser M.A., Dellorusso C. et al. (2002) Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat. Med. 8, 253-261.
58. Heydemann A., Huber J.M., Demonbreun A., Hadhazy M. & McNally E.M. (2005) Genetic background influences muscular dystrophy. Neuromuscul. Disord. 15, 601-609.
59. Hoffman E.P., Brown R.H. Jr, Kunkel L.M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell, 51, 919-928.
60. Hoffman E.P., Morgan J.E., Watkins S.C. & Partridge T.A. (1990) Somatic reversion/suppression of the mouse mdx phenotype in vivo. J. Neurol. Sci. 99, 9-25.
61. Hu H., Li J., Gagen C.S. et al. (2011) Conditional knockout of protein O-mannosyltransferase 2 reveals tissue-specific roles of O-mannosyl glycosylation in brain development. J. Comp. Neurol. 519, 1320-1337.
62. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H. & Fishman M.C. (1993) Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75, 1273-1286.
63. Im W.B., Phelps S.F., Copen E.H., Adams E.G., Slightom J.L. & Chamberlain J.S. (1996) Differential expression of dystrophin isoforms in strains of mdx mice with different mutations. Hum. Mol. Genet. 5, 1149-1153.
64. Irie A., Koyama S., Kozutsumi Y., Kawasaki T. & Suzuki A. (1998) The molecular basis for the absence of N-glycolylneuraminic acid in humans. J. Biol. Chem. 273, 15866-15871.
65. Jakubiec-Puka A., Biral D., Krawczyk K. & Betto R. (2005) Ultrastructure of diaphragm from dystrophic alpha-sarcoglycan-null mice. Acta Biochim. Pol. 52, 453-460.
66. Johnson E.K., Li B., Yoon J.H. et al. (2013) Identification of new dystroglycan complexes in skeletal muscle. PLoS One 8, e73224.
67. Kanagawa M., Nishimoto A., Chiyonobu T. et al. (2009) Residual laminin-binding activity and enhanced dystroglycan glycosylation by LARGE in novel model mice to dystroglycanopathy. Hum. Mol. Genet. 18, 621-631.
68. Kelly D., Chancellor K., Milatovich A., Francke U., Suzuki K. & Popko B. (1994) Autosomal recessive neuromuscular disorder in a transgenic line of mice. J. Neurosci. 14, 198-207.
69. Kobuke K., Piccolo F., Garringer K.W. et al. (2008) A common disease-associated missense mutation in alpha-sarcoglycan fails to cause muscular dystrophy in mice. Hum. Mol. Genet. 17, 1201-1213.
70. Konieczny P., Swiderski K. & Chamberlain J.S. (2013) Gene and cell-mediated therapies for muscular dystrophy. Muscle Nerve 47, 649-663.
71. Kudoh H., Ikeda H., Kakitani M. et al. (2005) A new model mouse for Duchenne muscular dystrophy produced by 2.4 Mb deletion of dystrophin gene using Cre-loxP recombination system. Biochem. Biophys. Res. Commun. 328, 507-516.
72. Kurahashi H., Taniguchi M., Meno C. et al. (2005) Basement membrane fragility underlies embryonic lethality in fukutin-null mice. Neurobiol. Dis. 19, 208-217.
73. Lancioni A., Rotundo I.L., Kobayashi Y.M. et al. (2011) Combined deficiency of alpha and epsilon sarcoglycan disrupts the cardiac dystrophin complex. Hum. Mol. Genet. 20, 4644-4654.
74. Lane P.W., Beamer T.C. & Myers D.D. (1976) Myodystrophy, a new myopathy on chromosome 8 of the mouse. J. Hered. 67, 135-138.
75. Langenbach K.J. & Rando T.A. (2002) Inhibition of dystroglycan binding to laminin disrupts the PI3K/AKT pathway and survival signaling in muscle cells. Muscle Nerve 26, 644-653.
76. Laws N., Hoey A. (2004) Progression of kyphosis in mdx mice. J. Appl. Physiol. (1985), 97, 1970-1977.
77. Lebakken C.S., Venzke D.P., Hrstka R.F. et al. (2000) Sarcospan-deficient mice maintain normal muscle function. Mol. Cell. Biol. 20, 1669-1677.
78. Lee Y., Kameya S., Cox G.A. et al. (2005) Ocular abnormalities in Large(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol. Cell. Neurosci. 30, 160-172.
79. Levedakou E.N., Chen X.J., Soliven B. & Popko B. (2005) Disruption of the mouse Large gene in the enr and myd mutants results in nerve, muscle, and neuromuscular junction defects. Mol. Cell. Neurosci. 28, 757-769.
80. Li D.J., Long C., Yue Y.P. & Duan D.S. (2009) Sub-physiological sarcoglycan expression contributes to compensatory muscle protection in mdx mice. Hum. Mol. Genet. 18, 1209-1220.
81. Liu J., Ball S.L., Yang Y. et al. (2006) A genetic model for muscle-eye-brain disease in mice lacking protein O-mannose 1, 2-N-acetylglucosaminyltransferase (POMGnT1). Mech. Dev. 123, 228-240.
82. Lu Q.L., Morris G.E., Wilton S.D. et al. (2000) Massive idiosyncratic exon skipping corrects the nonsense mutation in dystrophic mouse muscle and produces functional revertant fibers by clonal expansion. J. Cell Biol. 148, 985-996.
83. Lynch G.S., Hinkle R.T., Chamberlain J.S., Brooks S.V. & Faulkner J.A. (2001) Force and power output of fast and slow skeletal muscles from mdx mice 6-28 months old. J. Physiol. 535, 591-600.
84. Macpherson P.C., Schork M.A. & Faulkner J.A. (1996) Contraction-induced injury to single fiber segments from fast and slow muscles of rats by single stretches. Am. J. Physiol. 271, C1438-C1446.
85. Mann C.J., Perdiguero E., Kharraz Y. et al. (2011) Aberrant repair and fibrosis development in skeletal muscle. Skelet. Muscle 1, 21.
86. Marques M.J., Ferretti R., Vomero V.U., Minatel E. & Neto H.S. (2007) Intrinsic laryngeal muscles are spared from myonecrosis in the mdx mouse model of Duchenne muscular dystrophy. Muscle Nerve 35, 349-353.
87. Martin P.T., Xu R., Rodino-Klapac L.R. et al. (2009) Overexpression of Galgt2 in skeletal muscle prevents injury resulting from eccentric contractions in both mdx and wild-type mice. Am. J. Physiol. Cell Physiol. 296, C476-C488.
88. Martin P.T., Camboni M., Xu R. et al. (2013) N-Glycolylneuraminic acid deficiency worsens cardiac and skeletal muscle pathophysiology in alpha-sarcoglycan-deficient mice. Glycobiology 23, 833-843.
89. Martins P.C., Ayub-Guerrieri D., Martins-Bach A.B. et al. (2013) Dmdmdx/Largemyd: a new mouse model of neuromuscular diseases useful for studying physiopathological mechanisms and testing therapies. Dis. Models Mech. 6, 1167-1174.
90. Mathews K.D., Mills K.A., Bailey H.L., Schelper R.L., Murray J.C. (1995) Mouse myodystrophy (myd) mutation: refined mapping in an interval flanked by homology with distal human 4q. Muscle Nerve Suppl., 9, 8-102.
91. Matsuda R., Nishikawa A. & Tanaka H. (1995) Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem. 118, 959-964.
92. Michele D.E. & Campbell K.P. (2003) Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J. Biol. Chem. 278, 15457-15460.
93. Millay D.P., Maillet M., Roche J.A. et al. (2009) Genetic manipulation of dysferlin expression in skeletal muscle: novel insights into muscular dystrophy. Am. J. Pathol. 175, 1817-1823.
94. Milner D.J. & Kaufman S.J. (2007) Alpha7beta1 integrin does not alleviate disease in a mouse model of limb girdle muscular dystrophy type 2F. Am. J. Pathol. 170, 609-619.
95. Miyagoe-Suzuki Y., Masubuchi N., Miyamoto K. et al. (2009) Reduced proliferative activity of primary POMGnT1-null myoblasts in vitro. Mech. Dev. 126, 107-116.
96. Moat S.J., Bradley D.M., Salmon R., Clarke A. & Hartley L. (2013) Newborn bloodspot screening for Duchenne muscular dystrophy: 21 years experience in Wales (UK). Eur. J. Hum. Genet. 21, 1049-1053.
97. Morrison J., Lu Q.L., Pastoret C., Partridge T. & Bou-Gharios G. (2000) T-cell-dependent fibrosis in the mdx dystrophic mouse. Lab. Invest. 80, 881-891.
98. Muntoni F., Torelli S. & Ferlini A. (2003) Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2, 731-740.
99. Nahirney P.C., Dow P.R. & Ovalle W.K. (1997) Quantitative morphology of mast cells in skeletal muscle of normal and genetically dystrophic mice. Anat. Rec. 247, 341-349.
100. Pagel C.N. & Partridge T.A. (1999) Covert persistence of mdx mouse myopathy is revealed by acute and chronic effects of irradiation. J. Neurol. Sci. 164, 103-116.
101. Parames S.F., Coletta-Yudice E.D., Nogueira F.M. et al. (2014) Altered acetylcholine release in the hippocampus of dystrophin-deficient mice. Neuroscience, 269, 173-183.
102. Partridge T.A. (2013) The mdx mouse model as a surrogate for Duchenne muscular dystrophy. FEBS J. 280, 4177-4186.
103. Partridge T.A., Morgan J.E., Coulton G.R., Hoffman E.P. & Kunkel L.M. (1989) Conversion of mdx myofibres from dystrophin-negative to -positive by injection of normal myoblasts. Nature 337, 176-179.
104. Patel N.D., Jannapureddy S.R., Hwang W., Chaudhry I., Boriek A.M. (2003) Altered muscle force and stiffness of skeletal muscles in alpha-sarcoglycan-deficient mice. Am. J. Physiol.Cell Physiol., 284, C962-C968.
105. Peter A.K. & Crosbie R.H. (2006) Hypertrophic response of Duchenne and limb-girdle muscular dystrophies is associated with activation of Akt pathway. Exp. Cell Res. 312, 2580-2591.
106. Porter J.D., Rafael J.A., Ragusa R.J., Brueckner J.K., Trickett J.I. & Davies K.E. (1998) The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J. Cell Sci. 111(Pt 13), 1801-1811.
107. Reimers C.D., Schlotter B., Eicke B.M. & Witt T.N. (1996) Calf enlargement in neuromuscular diseases: a quantitative ultrasound study in 350 patients and review of the literature. J. Neurol. Sci. 143, 46-56.
108. Roberts T.C., Blomberg K.E., McClorey G. et al. (2012) Expression analysis in multiple muscle groups and serum reveals complexity in the microRNA transcriptome of the mdx mouse with implications for therapy. Mol. Ther. Nucleic Acids 1, e39.
109. Roberts T.C., Godfrey C., McClorey G. et al. (2013) Extracellular microRNAs are dynamic non-vesicular biomarkers of muscle turnover. Nucleic Acids Res. 41, 9500-9513.
110. Rooney J.E., Welser J.V., Dechert M.A., Flintoff-Dye N.L., Kaufman S.J. & Burkin D.J. (2006) Severe muscular dystrophy in mice that lack dystrophin and alpha7 integrin. J. Cell Sci. 119, 2185-2195.
111. Sasaoka T., Imamura M., Araishi K. et al. (2003) Pathological analysis of muscle hypertrophy and degeneration in muscular dystrophy in gamma-sarcoglycan-deficient mice. Neuromuscul. Disord. 13, 193-206.
112. Satz J.S., Barresi R., Durbeej M. et al. (2008) Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast. J. Neurosci. 28, 10567-10575.
113. Schiaffino S. & Mammucari C. (2011) Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet. Muscle 1, 4.
114. Sharp P.S., Bye-A-jee H. & Wells D.J. (2011) Physiological characterization of muscle strength with variable levels of dystrophin restoration in mdx mice following local antisense therapy. Mol. Ther. 19, 165-171.
115. Sicinski P., Geng Y., Ryder-Cook A.S., Barnard E.A., Darlison M.G. & Barnard P.J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244, 1578-1580.
116. Spurney C.F., Gordish-Dressman H., Guerron A.D. et al. (2009) Preclinical drug trials in the mdx mouse: assessment of reliable and sensitive outcome measures. Muscle Nerve 39, 591-602.
117. Stillwell E., Vitale J., Zhao Q. et al. (2009) Blastocyst injection of wild type embryonic stem cells induces global corrections in mdx mice. PLoS One 4, e4759.
118. Takeda S., Kondo M., Sasaki J. et al. (2003) Fukutin is required for maintenance of muscle integrity, cortical histiogenesis and normal eye development. Hum. Mol. Genet. 12, 1449-1459.
119. Torres L.F., Duchen L.W. (1987) The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain, 110(Pt 2), 269-299.
120. Tozawa T., Itoh K., Yaoi T. et al. (2012) The shortest isoform of dystrophin (Dp40) interacts with a group of presynaptic proteins to form a presumptive novel complex in the mouse brain. Mol. Neurobiol. 45, 287-297.
121. Varki A. (2010) Colloquium paper: uniquely human evolution of sialic acid genetics and biology. Proc. Natl Acad. Sci. USA 107(Suppl 2), 8939-8946.
122. Vignier N., Amor F., Fogel P. et al. (2013) Distinctive serum miRNA profile in mouse models of striated muscular pathologies. PLoS One 8, e55281.
123. Villalta S.A., Nguyen H.X., Deng B., Gotoh T. & Tidball J.G. (2009) Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet. 18, 482-496.
124. Vitale J.M., Schneider J.S., Beck A.J. et al. (2012) Dystrophin-compromised sarcoglycan-delta-knockout diaphragm requires full wild-type embryonic stem cell reconstitution for correction. J. Cell Sci. 125, 1807-1813.
125. Waite A., Tinsley C.L., Locke M. & Blake D.J. (2009) The neurobiology of the dystrophin-associated glycoprotein complex. Ann. Med. 41, 344-359.
126. Wang B., Li J. & Xiao X. (2000) Adeno-associated virus vector carrying human minidystrophin genes effectively ameliorates muscular dystrophy in mdx mouse model. Proc. Natl Acad. Sci. USA 97, 13714-13719.
127. Wansapura J.P., Millay D.P., Dunn R.S., Molkentin J.D. & Benson D.W. (2011) Magnetic resonance imaging assessment of cardiac dysfunction in delta-sarcoglycan null mice. Neuromusc. Disord. 21, 68-73.
128. Wertz K. & Fuchtbauer E.M. (1998) Dmd(mdx-beta geo): a new allele for the mouse dystrophin gene. Dev. Dyn. 212, 229-241.
129. Whitehead N.P., Yeung E.W. & Allen D.G. (2006) Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin. Exp. Pharmacol. Physiol. 33, 657-662.
130. Whitmore C., Fernandez-Fuente M., Booler H. et al. (2014) The transgenic expression of LARGE exacerbates the muscle phenotype of dystroglycanopathy mice. Hum. Mol. Genet. 23, 1842-1855.
131. Willer T., Prados B., Falcon-Perez J.M. et al. (2004) Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc. Natl Acad. Sci. USA 101, 14126-14131.
132. Williamson R.A., Henry M.D., Daniels K.J. et al. (1997) Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6, 831-841.
133. Willmann R., Possekel S., Dubach-Powell J., Meier T. & Ruegg M.A. (2009) Mammalian animal models for Duchenne muscular dystrophy. Neuromuscul. Disord. 19, 241-249.
134. Xu R., Devries S., Camboni M. & Martin P.T. (2009) Overexpression of Galgt2 reduces dystrophic pathology in the skeletal muscles of alpha sarcoglycan-deficient mice. Am. J. Pathol. 175, 235-247.
135. Yoon J.H., Johnson E., Xu R., Martin L.T., Martin P.T. & Montanaro F. (2012) Comparative proteomic profiling of dystroglycan-associated proteins in wild type, mdx, and Galgt2 transgenic mouse skeletal muscle. J. Proteome Res. 11, 4413-4424.
136. Zhu X., Hadhazy M., Groh M.E., Wheeler M.T., Wollmann R. & McNally E.M. (2001) Overexpression of gamma-sarcoglycan induces severe muscular dystrophy. Implications for the regulation of Sarcoglycan assembly. J. Biol. Chem. 276, 21785-21790.