Preventing phosphorylation of dystroglycan ameliorates the dystrophic phenotype in mdx mouse

Human Molecular Genetics

Volumn 21, Issue 20, 2012, Pages 4508-4520

  Miller, Gaynor ^a   Moore, Chris J ^a   Terry, Rebecca ^b   La riviere, Tracy ^a   Mitchell, Andrew ^a   Piggott, Robert ^a   Dear, T Neil ^a,c   Wells, Dominic J ^b   Winder, Steve J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DYSTROGLYCAN; ALPHA SARCOGLYCAN; BETA DYSTROGLYCAN; DYSTROGLYCAN; DYSTROPHIN; EVANS BLUE; PHENYLALANINE; PLECTIN; TYROSINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CREATINE KINASE BLOOD LEVEL; DUCHENNE MUSCULAR DYSTROPHY; ECCENTRIC MUSCLE CONTRACTION; MALE; MOUSE; MUSCLE INJURY; MUSCULAR DYSTROPHY; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SARCOLEMMA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; MICE; MICE, INBRED MDX; MUSCULAR DYSTROPHY, ANIMAL; PHENOTYPE; PHOSPHORYLATION;

MUS;

EID: 84867123429     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds293     Document Type: Article

References (47)

1. Ervasti, J.M. and Campbell, K.P. (1993) A role for the dystrophin glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell. Biol., 112, 809-823.
2. Ervasti, J.M. (2003) Costameres: the Achilles' heel of Herculean muscle. J. Biol. Chem., 278, 13591-13594.
3. Winder, S.J. (2001) The complexities of dystroglycan. Trends Biochem. Sci., 26, 118-124.
4. Moore, C. and Winder, S.J. (2010) Dystroglycan versatility in cell adhesion: a tale of multiple motifs. Cell Commun. Signal., 8, 3.
5. Ilsley, J.L., Sudol, M. and Winder, S.J. (2001) The interaction of dystrophin with b-dystroglycan is regulated by tyrosine phosphorylation. Cell Signal., 13, 625-632.
6. James, M., Nuttall, A., Ilsley, J.L., Ottersbach, K., Tinsley, J.N., Sudol, M. and Winder, S.J. (2000) Adhesion-dependent tyrosine phosphorylation of b-dystroglycan regulates its interaction with utrophin. J. Cell Sci., 113, 1717-1726.
7. Sotgia, F., Bonuccelli, G., Bedford, M., Brancaccio, A., Mayer, U., Wilson, M.T., Campos-Gonzalez, R., Brooks, J.W., Sudol, M. and Lisanti, M.P. (2003) Localization of phospho-b-dystroglycan (pY892) to an intracellular vesicular compartment in cultured cells and skeletal muscle fibers in vivo. Biochemistry, 42, 7110-7123.
8. Bonuccelli, G., Sotgia, F., Schubert, W., Park, D.S., Frank, P.G., Woodman, S.E., Insabato, L., Cammer, M., Minetti, C. and Lisanti, M.P. (2003) Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. Am. J. Pathol., 163, 1663-1675.
9. Assereto, S., Stringara, S., Sotgia, F., Bonuccelli, G., Broccolini, A., Pedemonte, M., Traverso, M., Biancheri, R., Zara, F., Bruno, C. et al. (2006) Pharmacological rescue of the dystrophin complex in Duchenne and Becker skeletal muscle explants by proteasomal inhibitor treatment. Am. J. Physiol. Cell Physiol., 290, C577-582.
10. Cox, G.A., Sunada, Y., Campbell, K.P. and Chamberlain, J.S. (1994) Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nat. Genet., 8, 333-339.
11. Greenberg, D.S., Sunada, Y., Campbell, K.P., Yaffe, D. and Nudel, U. (1994) Exogenous Dp71 restores the levels of dystrophin-associated proteins but does not alleviate muscle damage in mdx mice. Nat. Genet., 8, 340-344.
12. Hoyte, K., Jayasinha, V., Xia, B. and Martin, P.T. (2004) Transgenic overexpression of dystroglycan does not inhibit muscular dystrophy in mdx mice. Am. J. Pathol., 164, 711-718.
13. Ervasti, J.M., Ohlendieck, K., Kahl, S.D., Gaver, M.G. and Campbell, K.P. (1990) Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature, 345, 315-319.
14. Batchelor, C. and Winder, S. (2006) Sparks, signals and shock absorbers: how dystrophin loss causes muscular dystrophy. Trends Cell Biol., 16, 198-205.
15. Nguyen, T., Ellis, J.M., Love, D.R., Davies, K.E., Gatter, K.C., Dickson, G. and Morris, G.E. (1991) Localization of the DMDL gene-encoded dystrophin-related protein using a panel of nineteen monoclonal antibodies: presence at neuromuscular junctions, in the sarcolemma of dystrophic skeletal muscle in vascular and other smooth muscles, and in proliferating brain cell lines. J. Cell Biol., 115, 1695-1700.
16. Matsumura, K., Ervasti, J.M., Ohlendieck, K., Kahl, S. and Campbell, K. (1992) Association of dystrophin-related protein with dystrophin-associated protein in mdx mouse muscle. Nature, 360, 588-591.
17. Cluchague, N., Moreau, C., Rocher, C., Pottier, S., Leray, G., Cherel, Y. and Le Rumeur, E. (2004) beta-Dystroglycan can be revealed in microsomes from mdx mouse muscle by detergent treatment. FEBS Lett., 572, 216-220.
18. Morgan, J.E., Beauchamp, J.R., Pagel, C.N., Peckham, M., Ataliotis, P., Jat, P.S., Noble, M.D., Farmer, K. and Partridge, T.A. (1994) Myogenic cell lines derived from transgenic mice carrying a thermolabile T antigen: a model system for the derivation of tissue-specific and mutation-specific cell lines. Dev. Biol., 162, 486-498.
19. Pereboev, A., Ahmed, N., Man, Nt. and Morris, G. (2001) Epitopes in the interacting regions of beta-dystroglycan (PPxY motif) and dystrophin (WW domain). Biochim. Biophys. Acta, 1527, 54-60.
20. Sharp, P.S., Bye-a-Jee, H. and 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.
21. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Trickett, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
22. Rezniczek, G.A., Konieczny, P., Nikolic, B., Reipert, S., Schneller, D., Abrahamsberg, C., Davies, K.E., Winder, S.J. and Wiche, G. (2007) Plectin 1f scaffolding at the sarcolemma of dystrophic (mdx) muscle fibers through multiple interactions with b-dystroglycan. J. Cell Biol., 176, 965-977.
23. Konieczny, P., Fuchs, P., Reipert, S., Kunz, W.S., Zeold, A., Fischer, I., Paulin, D., Schroder, R. and Wiche, G. (2008) Myofiber integrity depends on desmin network targeting to Z-disks and costameres via distinct plectin isoforms. J. Cell Biol., 181, 667-681.
24. Goyenvalle, A., Seto, J.T., Davies, K.E. and Chamberlain, J. (2011) Therapeutic approaches to muscular dystrophy. Hum. Mol. Genet., 20, R69-R78.
25. Pichavant, C., Aartsma-Rus, A., Clemens, P.R., Davies, K.E., Dickson, G., Takeda, S.I., Wilton, S.D., Wolff, J.A., Wooddell, C.I., Xiao, X. et al. (2011) Current status of pharmaceutical and genetic therapeutic approaches to treat DMD. Mol. Ther., 19, 830-840.
26. Deconinck, A.E., Rafael, J.A., Skinner, J.A., Brown, S.C., Potter, A.C., Metzinger, L., Watt, D.J., Dickson, J.G., Tinsley, J.M. and Davies, K.E. (1997) Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell, 90, 717-727.
27. Grady, R.M., Teng, H., Nicholl, M.C., Cunningham, J.C., Wilkinson, R.S. and Sanes, J.R. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell, 90, 729-738.
28. Sotgia, F., Lee, H., Bedford, M., Petrucci, T.C., Sudol, M. and Lisanti, M.P. (2001) Tyrosine phosphorylation of b-dystroglycan at its WW domain binding motif, PPxY, recruits SH2 domain containing proteins. Biochemistry, 40, 14585-14592.
29. Bonuccelli, G., Sotgia, F., Capozza, F., Gazzerro, E., Minetti, C. and Lisanti, M.P. (2007) Localized treatment with a novel FDA-approved proteasome inhibitor blocks the degradation of dystrophin and dystrophin-associated proteins in mdx mice. Cell Cycle, 6, 1242-1248.
30. Gazzerro, E., Assereto, S., Bonetto, A., Sotgia, F., ScarfÏ, S., Pistorio, A., Bonuccelli, G., Cilli, M., Bruno, C., Zara, F. et al. (2010) Therapeutic potential of proteasome inhibition in Duchenne and Becker muscular dystrophies. Am. J. Pathol., 176, 1863-1877.
31. Lipscomb, L., Parkin, C.A., Juusola, M.I. and Winder, S.J. (2011) The proteasomal inhibitor MG132 prevents muscular dystrophy in zebrafish. PLoS Curr., 3, RRN1286.
32. Karpati, G., Carpenter, S., Morris, G.E., Davies, K.E., Guerin, C. and Holland, P. (1993) Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J. Neuropathol. Exp. Neurol., 52, 119-128.
33. Clerk, A., Morris, G.E., Dubowitz, V., Davies, K.E. and Sewry, C.A. (1993) Dystrophin-related protein, utrophin in normal and dystrophic human fetal skeletal muscle. Histochem. J., 25, 554-561.
34. Tinsley, J.M., Fairclough, R.J., Storer, R., Wilkes, F.J., Potter, A.C., Squire, S.E., Powell, D.S., Cozzoli, A., Capogrosso, R.F., Lambert, A. et al. (2011) Daily treatment with SMTC1100, a novel small molecule utrophin upregulator, dramatically reduces the Dystrophic symptoms in the mdx mouse. PLoS One, 6, e19189.
35. Smith, F.J.D., Eady, R.A.J., Leigh, I.M., McMillan, J.R., Rugg, E.L., Kelsell, D.P., Bryant, S.P., Spurr, N.K., Geddes, J.F., Kirtschig, G. et al. (1996) Plectin deficiency results in muscular dystrophy with epidermolysis bullosa. Nat. Genet., 13, 450-457.
36. Andrä, K., Lassmann, H., Bittner, R., Shorny, S., Fässler, R., Propst, F. and Wiche, G. (1997) Targeted inactivation of plectin reveals essential function in maintaining the integrity of skin, muscle, and heart cytoarchitecture. Genes Dev., 11, 3143-3156.
37. Pulkkinen, L., Smith, F.J.D., Shimizu, H., Murata, S., Yaoita, H., Hachisuka, H., Nishikawa, T., McLean, W.H.I. and Uitto, J. (1996) Homozygous deletion mutations in the plectin gene (PLEC1) in patients with epidermolysis bullosa simplex associated with late-onset muscular dystrophy. Hum. Mol. Genet., 5, 1539-1546.
38. Schröder, R., Mundegar, R., Treusch, M., Schlegel, U., Blümcke, I., Owaribe, K. and Magin, T. (1997) Altered distribution of plectin/HD1 in dystrophinopathies. Eur. J. Cell Biol., 74, 165-171.
39. Gundesli, H., Talim, B., Korkusuz, P., Balci-Hayta, B., Cirak, S., Akarsu, N.A., Topaloglu, H. and Dincer, P. (2010) Mutation in exon 1f of PLEC, leading to disruption of plectin isoform 1f, causes autosomal-recessive limb-girdle muscular dystrophy. Am. J. Hum. Genet., 87, 834-841.
40. Hu, H., Columbus, J., Zhang, Y., Wu, D., Lian, L., Yang, S., Goodwin, J., Luczak, C., Carter, M., Chen, L. et al. (2004) A map of WW domain family interactions. PROTEOMICS, 4, 643-655.
41. Otte, L., Wiedemann, U., Schlegel, B., Pires, J.R., Beyermann, M., Schmieder, P., Krause, G., Volkmer-Engert, R., Schneider-Mergener, J. and Oschkinat, H. (2003) WW domain sequence activity relationships identified using ligand recognition propensities of 42 WW domains. Protein Sci., 12, 491-500.
42. McArthur, T. and Ohtoshi, A. (2007) A brain-specific homeobox gene, Bsx, is essential for proper postnatal growth and nursing. Mol. Cell. Biol., 27, 5120-5127.
43. Miller, G., Peter, A., Espinoza, E., Heighway, J. and Crosbie, R. (2006) Over-expression of Microspan, a novel component of the sarcoplasmic reticulum, causes severe muscle pathology with triad abnormalities. J. Muscle Res. Cell Motil., 27, 545-558.
44. Judge, L.M., Arnett, A.L.H., Banks, G.B. and Chamberlain, J.S. (2011) Expression of the dystrophin isoform Dp116 preserves functional muscle mass and extends lifespan without preventing dystrophy in severely dystrophic mice. Hum. Mol. Genet., 20, 4978-4990.
45. Foster, H., Sharp, P.S., Athanasopoulos, T., Trollet, C., Graham, I.R., Foster, K., Wells, D.J. and Dickson, G. (2008) Codon and mRNA sequence optimization of microdystrophin transgenes improves expression and physiological outcome in dystrophic mdx mice following AAV2/8 gene transfer. Mol. Ther., 16, 1825-1832.
46. Thompson, O., Kleino, I., Crimaldi, L., Gimona, M., Saksela, K. and Winder, S.J. (2008) Dystroglycan, Tks5 and Src mediated assembly of podosomes in myoblasts. PLoS One, 3, e3638.
47. Thompson, O., Moore, C.J., Hussain, S.-A., Kleino, I., Peckham, M., Hohenester, E., Ayscough, K.R., Saksela, K. and Winder, S.J. (2010) Modulation of cell spreading and cell-substrate adhesion dynamics by dystroglycan. J. Cell Sci., 123, 118-127.