Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2015, Article ID 635792, 10 pages
http://dx.doi.org/10.1155/2015/635792
Review Article

Genetic Engineering of Dystroglycan in Animal Models of Muscular Dystrophy

1Istituto di Chimica del Riconoscimento Molecolare, CNR c/o Istituto di Biochimica e Biochimica Clinica, Università Cattolica del Sacro Cuore, 00168 Roma, Italy
2School of Biochemistry, Bristol University, Bristol B58 1TD, UK
3Istituto di Biochimica e Biochimica Clinica, Università Cattolica del Sacro Cuore, Roma, Italy

Received 3 October 2014; Accepted 11 March 2015

Academic Editor: Gouri Shankar Pandey

Copyright © 2015 Francesca Sciandra et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. M. Durbeej, M. D. Henry, M. Ferletta, K. P. Campbell, and P. Ekblom, “Distribution of dystroglycan in normal adult mouse tissues,” Journal of Histochemistry and Cytochemistry, vol. 46, no. 4, pp. 449–457, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Durbeej and K. P. Campbell, “Biochemical characterization of the epithelial dystroglycan complex,” The Journal of Biological Chemistry, vol. 274, no. 37, pp. 26609–26616, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. K. Matsumura, H. Yamada, T. Shimizu, and K. P. Campbell, “Differential expression of dystrophin, utrophin and dystrophin-associated proteins in peripheral nerve,” FEBS Letters, vol. 334, no. 3, pp. 281–285, 1993. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Ibraghimov-Beskrovnaya, J. M. Ervasti, C. J. Leveille, C. A. Slaughter, S. W. Sernett, and K. P. Campbell, “Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix,” Nature, vol. 355, no. 6362, pp. 696–702, 1992. View at Publisher · View at Google Scholar · View at Scopus
  5. A. Brancaccio, T. Schulthess, M. Gesemann, and J. Engel, “Electron microscopic evidence for a mucin-like region in chick muscle α-dystroglycan,” FEBS Letters, vol. 368, no. 1, pp. 139–142, 1995. View at Publisher · View at Google Scholar · View at Scopus
  6. F. Sciandra, M. Bozzi, M. G. Bigotti, and A. Brancaccio, “The multiple affinities of α-dystroglycan,” Current Protein & Peptide Science, vol. 14, no. 7, pp. 626–634, 2013. View at Google Scholar
  7. A. Suzuki, M. Yoshida, K. Hayashi, Y. Mizuno, Y. Hagiwara, and E. Ozawa, “Molecular organization at the glycoprotein-complex-binding site of dystrophin. Three dystrophin-associated proteins bind directly to the carboxy-terminal portion of dystrophin,” European Journal of Biochemistry, vol. 220, no. 2, pp. 283–292, 1994. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Jung, B. Yang, J. Meyer, J. S. Chamberlain, and K. P. Campbell, “Identification and characterization of the dystrophin anchoring site on β-dystroglycan,” The Journal of Biological Chemistry, vol. 270, no. 45, pp. 27305–27310, 1995. View at Publisher · View at Google Scholar · View at Scopus
  9. G. Rosa, M. Ceccarini, M. Cavaldesi, M. Zini, and T. C. Petrucci, “Localization of the dystrophin binding site at the carboxyl terminus of β-dystroglycan,” Biochemical and Biophysical Research Communications, vol. 223, no. 2, pp. 272–277, 1996. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Cavaldesi, G. Macchia, S. Barca, P. Defilippi, G. Tarone, and T. C. Petrucci, “Association of the dystroglycan complex isolated from bovine brain synaptosomes with proteins involved in signal transduction,” Journal of Neurochemistry, vol. 72, no. 4, pp. 1648–1655, 1999. View at Publisher · View at Google Scholar · View at Scopus
  11. H. J. Spence, A. S. Dhillon, M. James, and S. J. Winder, “Dystroglycan, a scaffold for the ERK-MAP kinase cascade,” The EMBO Reports, vol. 5, no. 5, pp. 484–489, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. J. M. Ervasti, K. Ohlendieck, S. D. Kahl, M. G. Gaver, and K. P. Campbell, “Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle,” Nature, vol. 345, no. 6273, pp. 315–319, 1990. View at Publisher · View at Google Scholar · View at Scopus
  13. R. D. Cohn and K. P. Campbell, “Molecular basis of muscular dystrophies,” Muscle & Nerve, vol. 23, no. 10, pp. 1456–1471, 2000. View at Publisher · View at Google Scholar
  14. E. P. Hoffman, R. H. Brown Jr., and L. M. Kunkel, “Dystrophin: the protein product of the duchenne muscular dystrophy locus,” Cell, vol. 51, no. 6, pp. 919–928, 1987. View at Publisher · View at Google Scholar · View at Scopus
  15. C. G. Bonnemann, R. Modi, S. Noguchi et al., “β-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex,” Nature Genetics, vol. 11, no. 3, pp. 266–273, 1995. View at Publisher · View at Google Scholar · View at Scopus
  16. V. Nigro, E. De Sa Moreira, G. Piluso et al., “Autosomal recessive limb-girdle muscular dystrophy, LGMD2F, is caused by a mutation in the δ-sarcoglycan gene,” Nature Genetics, vol. 14, no. 2, pp. 195–198, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Noguchi, E. M. McNally, K. Ben Othmane et al., “Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy,” Science, vol. 270, no. 5237, pp. 819–822, 1995. View at Publisher · View at Google Scholar · View at Scopus
  18. S. L. Roberds, F. Leturcq, V. Allemand et al., “Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy,” Cell, vol. 78, no. 4, pp. 625–633, 1994. View at Publisher · View at Google Scholar · View at Scopus
  19. L. E. Lim, F. Duclos, O. Broux et al., “β-Sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12,” Nature Genetics, vol. 11, no. 3, pp. 257–265, 1995. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Helbling-Leclerc, X. Zhang, H. Topaloglu et al., “Mutations in the laminin α2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy,” Nature Genetics, vol. 11, no. 2, pp. 216–218, 1995. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Hara, B. Balci-Hayta, T. Yoshida-Moriguchi et al., “A dystroglycan mutation associated with limb-girdle muscular dystrophy,” The New England Journal of Medicine, vol. 364, no. 10, pp. 939–946, 2011. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Dong, S. Noguchi, Y. Endo et al., “DAG1 mutations associated with asymptomatic hyperCKemia and hypoglycosylation of α-dystroglycan,” Neurology, vol. 84, no. 3, pp. 273–279, 2015. View at Publisher · View at Google Scholar
  23. T. Geis, K. Marquard, T. Rödl et al., “Homozygous dystroglycan mutation associated with a novel muscle-eye-brain disease-like phenotype with multicystic leucodystrophy,” Neurogenetics, vol. 14, no. 3-4, pp. 205–213, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Live, L. Wells, and G.-J. Boons, “Dissecting the molecular basis of the role of the O-mannosylation pathway in disease: α-dystroglycan and forms of muscular dystrophy,” ChemBioChem, vol. 14, no. 18, pp. 2392–2402, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Wells, “The O-mannosylation pathway: glycosyltransferases and proteins implicated in congenital muscular dystrophy,” The Journal of Biological Chemistry, vol. 288, no. 10, pp. 6930–6935, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. C. di Blasi, L. Morandi, R. Barresi, F. Blasevich, F. Cornelio, and M. Mora, “Dystrophin-associated protein abnormalities in dystrophin-deficient muscle fibers from symptomatic and asymptomatic Duchenne/Becker muscular dystrophy carriers,” Acta Neuropathologica, vol. 92, no. 4, pp. 369–377, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. R. Barresi, D. E. Michele, M. Kanagawa et al., “LARGE can functionally bypass α-dystroglycan glycosylation defects in distinct congenital muscular dystrophies,” Nature Medicine, vol. 10, no. 7, pp. 696–703, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. F. Saito, M. Kanagawa, M. Ikeda et al., “Overexpression of LARGE suppresses muscle regeneration via down-regulation of insulin-like growth factor 1 and aggravates muscular dystrophy in mice,” Human Molecular Genetics, vol. 23, no. 17, pp. 4543–4558, 2014. View at Publisher · View at Google Scholar
  29. C. H. Vannoy, L. Xu, E. Keramaris, P. Lu, X. Xiao, and Q. L. Lu, “Adeno-associated virus-mediated overexpression of LARGE rescues α-dystroglycan function in dystrophic mice with mutations in the fukutin-related protein,” Human Gene Therapy Methods, vol. 25, no. 3, pp. 187–196, 2014. View at Publisher · View at Google Scholar
  30. C. Whitmore, M. Fernandez-Fuente, H. Booler et al., “The transgenic expression of LARGE exacerbates the muscle phenotype of dystroglycanopathy mice,” Human Molecular Genetics, vol. 23, no. 7, pp. 1842–1855, 2014. View at Publisher · View at Google Scholar
  31. R. A. Williamson, M. D. Henry, K. J. Daniels et al., “Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice,” Human Molecular Genetics, vol. 6, no. 6, pp. 831–841, 1997. View at Publisher · View at Google Scholar · View at Scopus
  32. M. D. Henry and K. P. Campbell, “A role for dystroglycan in basement membrane assembly,” Cell, vol. 95, no. 6, pp. 859–870, 1998. View at Publisher · View at Google Scholar · View at Scopus
  33. A. R. Frost, S. V. Böhm, R. N. Sewduth et al., “Heterozygous deletion of a 2-Mb region including the dystroglycan gene in a patient with mild myopathy, facial hypotonia, oral-motor dyspraxia and white matter abnormalities,” European Journal of Human Genetics, vol. 18, no. 7, pp. 852–855, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. P. D. Côté, H. Moukhles, M. Lindenbaum, and S. Carbonetto, “Chimaeric mice deficient in dystroglycans develop muscular dystrophy and have disrupted myoneural synapses,” Nature Genetics, vol. 23, no. 3, pp. 338–342, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. A. E. Deconinck, J. A. Rafael, J. A. Skinner et al., “Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy,” Cell, vol. 90, no. 4, pp. 717–727, 1997. View at Publisher · View at Google Scholar · View at Scopus
  36. F. Montanaro, S. H. Gee, C. Jacobson, M. H. Lindenbaum, S. C. Froehner, and S. Carbonetto, “Laminin and α-dystroglycan mediate acetylcholine receptor aggregation via a MuSK-independent pathway,” Journal of Neuroscience, vol. 18, no. 4, pp. 1250–1260, 1998. View at Google Scholar · View at Scopus
  37. U. Mayer, “Integrins: redundant or important players in skeletal muscle?” The Journal of Biological Chemistry, vol. 278, no. 17, pp. 14587–14590, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. R. D. Cohn, M. D. Henry, D. E. Michele et al., “Disruption of DAG1 in differentiated skeletal muscle reveals a role for dystroglycan in muscle regeneration,” Cell, vol. 110, no. 5, pp. 639–648, 2002. View at Publisher · View at Google Scholar · View at Scopus
  39. J. S. Satz, R. Barresi, M. Durbeej et al., “Brain and eye malformations resembling Walker-Warburg syndrome are recapitulated in mice by dystroglycan deletion in the epiblast,” The Journal of Neuroscience, vol. 28, no. 42, pp. 10567–10575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Hoyte, V. Jayasinha, B. Xia, and P. T. Martin, “Transgenic overexpression of dystroglycan does not inhibit muscular dystrophy in mdx mice,” The American Journal of Pathology, vol. 164, no. 2, pp. 711–718, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Fukuyama, M. Osawa, and H. Suzuki, “Congenital progressive muscular dystrophy of the Fukuyama type—clinical, genetic and pathological considerations,” Brain & Development, vol. 3, no. 1, pp. 1–29, 1981. View at Google Scholar
  42. M. Haltia, I. Leivo, H. Somer et al., “Muscle-eye-brain disease: a neuropathological study,” Annals of Neurology, vol. 41, no. 2, pp. 173–180, 1997. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Cormand, H. Pihko, M. Bayés et al., “Clinical and genetic distinction between Walker-Warburg syndrome and muscle-eye-brain disease,” Neurology, vol. 56, no. 8, pp. 1059–1069, 2001. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Godfrey, E. Clement, R. Mein et al., “Refining genotype-phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan,” Brain, vol. 130, no. 10, pp. 2725–2735, 2007. View at Publisher · View at Google Scholar · View at Scopus
  45. S. A. Moore, F. Saito, J. Chen et al., “Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy,” Nature, vol. 418, no. 6896, pp. 422–425, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Noell, K. Wolburg-Buchholz, A. F. Mack et al., “Evidence for a role of dystroglycan regulating the membrane architecture of astroglial endfeet,” European Journal of Neuroscience, vol. 33, no. 12, pp. 2179–2186, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. J. S. Satz, A. R. Philp, H. Nguyen et al., “Visual impairment in the absence of dystroglycan,” Journal of Neuroscience, vol. 29, no. 42, pp. 13136–13146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. J. S. Satz, A. P. Ostendorf, S. Hou et al., “Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain,” The Journal of Neuroscience, vol. 30, no. 43, pp. 14560–14572, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. T. D. Myshrall, S. A. Moore, A. P. Ostendorf et al., “Dystroglycan on radial glia end feet is required for pial basement membrane integrity and columnar organization of the developing cerebral cortex,” Journal of Neuropathology and Experimental Neurology, vol. 71, no. 12, pp. 1047–1063, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Omori, F. Araki, T. Chaya et al., “Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells,” The Journal of Neuroscience, vol. 32, no. 18, pp. 6126–6137, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. V. Nigro and M. Savarese, “Genetic basis of limb-girdle muscular dystrophies: the 2014 update,” Acta Myologica, vol. 33, no. 1, pp. 1–12, 2014. View at Google Scholar · View at Scopus
  52. D. Bozic, F. Sciandra, D. Lamba, and A. Brancaccio, “The structure of the N-terminal region of murine skeletal muscle α-dystroglycan discloses a modular architecture,” Journal of Biological Chemistry, vol. 279, no. 43, pp. 44812–44816, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Kanagawa, F. Saito, S. Kunz et al., “Molecular recognition by LARGE is essential for expression of functional dystroglycan,” Cell, vol. 117, no. 7, pp. 953–964, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. N. Watanabe, T. Sasaoka, S. Noguchi, I. Nishino, and T. Tanaka, “Cys669-Cys713 disulfide bridge formation is a key to dystroglycan cleavage and subunit association,” Genes to Cells, vol. 12, no. 1, pp. 75–88, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. F. Sciandra, M. Bozzi, S. Morlacchi, A. Galtieri, B. Giardina, and A. Brancaccio, “Mutagenesis at the α-β Interface impairs the cleavage of the dystroglycan precursor,” FEBS Journal, vol. 276, no. 17, pp. 4933–4945, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Miller, C. J. Moore, R. Terry et al., “Preventing phosphorylation of dystroglycan ameliorates the dystrophic phenotype in mdx mouse,” Human Molecular Genetics, vol. 21, no. 20, Article ID dds293, pp. 4508–4520, 2012. View at Publisher · View at Google Scholar · View at Scopus
  57. M. James, A. Nuttall, J. L. Ilsley et al., “Adhesion-dependent tyrosine phosphorylation of β-dystroglycan regulates its interaction with utrophin,” Journal of Cell Science, vol. 113, no. 10, pp. 1717–1726, 2000. View at Google Scholar · View at Scopus
  58. J. L. Ilsley, M. Sudol, and S. J. Winder, “The interaction of dystrophin with β-dystroglycan is regulated by tyrosine phosphorylation,” Cellular Signalling, vol. 13, no. 9, pp. 625–632, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Sotgia, G. Bonuccelli, M. Bedford et al., “Localization of phospho-β-dystroglycan (pY892) to an intracellular vesicular compartment in cultured cells and skeletal muscle fibers in vivo,” Biochemistry, vol. 42, no. 23, pp. 7110–7123, 2003. View at Publisher · View at Google Scholar · View at Scopus
  60. G. A. Rezniczek, P. Konieczny, B. Nikolic et al., “Plectin 1f scaffolding at the sarcolemma of dystrophic (mdx) muscle fibers through multiple interactions with β-dystroglycan,” The Journal of Cell Biology, vol. 176, no. 7, pp. 965–977, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Bonuccelli, F. Sotgia, F. Capozza, E. Gazzerro, C. Minetti, and M. P. Lisanti, “Localized treatment with a novel FDA-approved proteasome inhibitor blocks the degradation of dystrophin and dystrophin-associated proteins in mdx mice,” Cell Cycle, vol. 6, no. 10, pp. 1242–1248, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. V. Carmignac, R. Quéré, and M. Durbeej, “Proteasome inhibition improves the muscle of laminin α2 chain-deficient mice,” Human Molecular Genetics, vol. 20, no. 3, pp. 541–552, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. V. Jayasinha, H. H. Nguyen, B. Xia, A. Kammesheidt, K. Hoyte, and P. T. Martin, “Inhibition of dystroglycan cleavage causes muscular dystrophy in transgenic mice,” Neuromuscular Disorders, vol. 13, no. 5, pp. 365–375, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. G. Jarad, J. W. Pippin, S. J. Shankland, J. A. Kreidberg, and J. H. Miner, “Dystroglycan does not contribute significantly to kidney development or function, in health or after injury,” The American Journal of Physiology—Renal Physiology, vol. 300, no. 3, pp. F811–F820, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Kojima, H. Nosaka, Y. Kishimoto et al., “Defective glycosylation of α-dystroglycan contributes to podocyte flattening,” Kidney International, vol. 79, no. 3, pp. 311–316, 2011. View at Publisher · View at Google Scholar · View at Scopus
  66. F. Saito, S. A. Moore, R. Barresi et al., “Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization,” Neuron, vol. 38, no. 5, pp. 747–758, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Occhi, D. Zambroni, U. del Carro et al., “Both laminin and Schwann cell dystroglycan are necessary for proper clustering of sodium channels at nodes of Ranvier,” The Journal of Neuroscience, vol. 25, no. 41, pp. 9418–9427, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. R. P. Johnson, S. H. Kang, and J. M. Kramer, “C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin,” Development, vol. 133, no. 10, pp. 1911–1921, 2006. View at Publisher · View at Google Scholar · View at Scopus
  69. T. E. Lloyd and J. P. Taylor, “Flightless flies: Drosophila models of neuromuscular disease,” Annals of the New York Academy of Sciences, vol. 1184, pp. e1–e20, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. M. J. Greener and R. G. Roberts, “Conservation of components of the dystrophin complex in Drosophila,” FEBS Letters, vol. 482, no. 1-2, pp. 13–18, 2000. View at Publisher · View at Google Scholar · View at Scopus
  71. M. Schneider, A. A. Khalil, J. Poulton et al., “Perlecan and dystroglycan act at the basal side of the Drosophila follicular epithelium to maintain epithelial organization,” Development, vol. 133, no. 19, pp. 3805–3815, 2006. View at Publisher · View at Google Scholar · View at Scopus
  72. W.-M. Deng, M. Schneider, R. Frock et al., “Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila,” Development, vol. 130, no. 1, pp. 173–184, 2003. View at Publisher · View at Google Scholar · View at Scopus
  73. H. R. Shcherbata, A. S. Yatsenko, L. Patterson et al., “Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy,” The EMBO Journal, vol. 26, no. 2, pp. 481–493, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. N. Haines, S. Seabrooke, and B. A. Stewart, “Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles,” Molecular Biology of the Cell, vol. 18, no. 12, pp. 4721–4730, 2007. View at Publisher · View at Google Scholar · View at Scopus
  75. M. M. Kucherenko, M. Pantoja, A. S. Yatsenko et al., “Genetic modifier screens reveal new components that interact with the Drosophila dystroglycan-dystrophin complex,” PLoS ONE, vol. 3, no. 6, Article ID e2418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  76. A. S. Yatsenko, A. K. Marrone, and H. R. Shcherbata, “miRNA-based buffering of the cobblestone-lissencephaly-associated extracellular matrix receptor dystroglycan via its alternative 3′-UTR,” Nature Communications, vol. 5, article 4906, 2014. View at Publisher · View at Google Scholar
  77. L. S. Steffen, J. R. Guyon, E. D. Vogel et al., “Zebrafish orthologs of human muscular dystrophy genes,” BMC Genomics, vol. 8, article 79, 2007. View at Publisher · View at Google Scholar · View at Scopus
  78. M. J. Parsons, I. Campos, E. M. A. Hirst, and D. L. Stemple, “Removal of dystroglycan causes severe muscular dystrophy in Zebrafish embryos,” Development, vol. 129, no. 14, pp. 3505–3512, 2002. View at Google Scholar · View at Scopus
  79. V. Gupta, G. Kawahara, S. R. Gundry et al., “The zebrafish dag1 mutant: a novel genetic model for dystroglycanopathies,” Human Molecular Genetics, vol. 20, no. 9, Article ID ddr047, pp. 1712–1725, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. D. Pirolli, F. Sciandra, M. Bozzi et al., “Insights from molecular dynamics simulations: structural basis for the V567D mutation-induced instability of zebrafish α-dystroglycan and comparison with the murine model,” PLoS ONE, vol. 9, no. 7, Article ID e103866, 2014. View at Publisher · View at Google Scholar
  81. Y.-Y. Lin, R. J. White, S. Torelli, S. Cirak, F. Muntoni, and D. L. Stemple, “Zebrafish fukutin family proteins link the unfolded protein response with dystroglycanopathies,” Human Molecular Genetics, vol. 20, no. 9, pp. 1763–1775, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Hidalgo, C. Sirour, V. Bello, N. Moreau, M. Beaudry, and T. Darribère, “In vivo analyzes of dystroglycan function during somitogenesis in Xenopus laevis,” Developmental Dynamics, vol. 238, no. 6, pp. 1332–1345, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. C. Sirour, M. Hidalgo, V. Bello, N. Buisson, T. Darribère, and N. Moreau, “Dystroglycan is involved in skin morphogenesis downstream of the Notch signaling pathway,” Molecular Biology of the Cell, vol. 22, no. 16, pp. 2957–2969, 2011. View at Publisher · View at Google Scholar · View at Scopus
  84. A. Lunardi, F. Cremisi, and L. Dente, “Dystroglycan is required for proper retinal layering,” Developmental Biology, vol. 290, no. 2, pp. 411–420, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. V. Bello, C. Sirour, N. Moreau, E. Denker, and T. Darribère, “A function for dystroglycan in pronephros development in Xenopus laevis,” Developmental Biology, vol. 317, no. 1, pp. 106–120, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. R. D. Heathcote, J. M. Ekman, K. P. Campbell, and E. W. Godfrey, “Dystroglycan overexpression in vivo alters acetylcholine receptor aggregation at the neuromuscular junction,” Developmental Biology, vol. 227, no. 2, pp. 595–605, 2000. View at Publisher · View at Google Scholar · View at Scopus