Skip to main content

Advertisement

SpringerLink
Log in

Neuromuscular Disorders in Zebrafish: State of the Art and Future Perspectives

  • Original Paper
  • Published:
NeuroMolecular Medicine Aims and scope Submit manuscript

Abstract

Neuromuscular disorders are a broad group of inherited conditions affecting the structure and function of the motor system with polymorphic clinical presentation and disease severity. Although individually rare, collectively neuromuscular diseases have an incidence of 1 in 3,000 and represent a significant cause of disability of the motor system. The past decade has witnessed the identification of a large number of human genes causing muscular disorders, yet the underlying pathogenetic mechanisms remain largely unclear, limiting the developing of targeted therapeutic strategies. To overcome this barrier, model systems that replicate the different steps of human disorders are increasingly being developed. Among these, the zebrafish (Danio rerio) has emerged as an excellent organism for studying genetic disorders of the central and peripheral motor systems. In this review, we will encounter most of the available zebrafish models for childhood neuromuscular disorders, providing a brief overview of results and the techniques, mainly transgenesis and chemical biology, used for genetic manipulation. The amount of data collected in the past few years will lead zebrafish to became a common functional tool for assessing rapidly drug efficacy and off-target effects in neuromuscular diseases and, furthermore, to shed light on new etiologies emerging from large-scale massive sequencing studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adamo, C. M., Dai, D. F., Percival, J. M., Minami, E., Willis, M. S., Patrucco, E., et al. (2010). Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy. Proceedings of the National Academy of Sciences of the United States of America, 107, 19079–19083.

    Article  PubMed  Google Scholar 

  • Amato, A., & Russell, J. (2008). Neuromuscular disorders. New York: McGraw-Hill Co. Inc.

    Google Scholar 

  • Amato, V., Vina, E., Calavia, M. G., Guerriera, M. C., Laurà, R., Navarro, M., et al. (2012). TRPV4 in the sensory organs of Adult Zebrafish. Microscopy Research and Technique, 75, 89–96.

    Article  PubMed  CAS  Google Scholar 

  • Aravind, L., & Koonin, E. V. (1999). The fukutin protein family-predicted enzymes modifying cell-surface molecules. Current Biology, 9, 836–837.

    Article  Google Scholar 

  • Assereto, S., Stringara, S., Sotgia, F., Bonuccelli, G., Broccolini, A., Pedemonte, M., et al. (2006). Pharmacological rescue of the dystrophin-glycoprotein complex in Duchenne and Becker skeletal muscle explants by proteasome inhibitor treatment. American Journal of Physiology Cell Physiology, 290, C577–C582.

    Article  PubMed  CAS  Google Scholar 

  • Auer-Grumbach, M., Olschewski, A., Papic, L., Kremer, H., McEntagart, M. E., Uhrig, S., et al. (2010). Alterations in the ankyrin domain of TRPV4 cause congenital distal SMA, scapuloperoneal SMA and HMSN2C. Nature Genetics, 42, 160–164.

    Article  PubMed  CAS  Google Scholar 

  • Avşar-Ban, E., Ishikawa, H., Manya, H., Watanabe, M., Akiyama, S., Miyake, H., et al. (2010). Protein O-mannosylation is necessary for normal embryonic development in zebrafish. Glycobiology, 20, 1089–1102.

    Article  PubMed  CAS  Google Scholar 

  • Bai, X. H., Wang, D. W., Kong, L., Zhang, Y., Luan, Y., Kobayashi, T., et al. (2009). ADAMTS-7, a direct target of PTHrP, adversely regulates endochondral bone growth by associating with and inactivating GEP growth factor. Molecular and Cellular Biology, 29, 4201–4219.

    Article  PubMed  CAS  Google Scholar 

  • Bang, M. L., Centner, T., Fornoff, F., Geach, A. J., Gotthardt, M., McNabb, M., et al. (2001). The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-line to I-band linking system. Circulation Research, 89, 1065–1072.

    Article  PubMed  CAS  Google Scholar 

  • Bansal, D., Miyake, K., Vogel, S. S., Groh, S., Chen, C. C., Williamson, R., et al. (2003). Defective membrane repair in dysferlin deficient muscular dystrophy. Nature, 423, 168–172.

    Article  PubMed  CAS  Google Scholar 

  • Barišić, N., Chaouch, A., Müller, J. S., Lochmüller, H. (2011). Genetic heterogeneity and pathophysiological mechanisms in congenital myasthenic syndromes. European Journal of Paediatric Neurology, 15, 189–196

    Article  PubMed  Google Scholar 

  • Barone, R., Aiello, C., Race, V., Morava, E., Foulquier, F., Riemersma, M., et al. (2012). DPM2-CDG: a muscular dystrophy-dystroglycanopathy syndrome with severe epilepsy. Annals of Neurology, 72, 550–558.

    Article  PubMed  CAS  Google Scholar 

  • Bashir, R., Britton, S., Strachan, T., Keers, S., Vafiadaki, E., Lako, M., et al. (1998). A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nature Genetics, 20, 37–42.

    Article  PubMed  CAS  Google Scholar 

  • Bassett, D. I., Bryson-Richardson, R. J., Daggett, D. F., Gautier, P., Keenan, D. G., & Currie, P. D. (2003). Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development, 130, 5851–5860.

    Article  PubMed  CAS  Google Scholar 

  • Bassett, D., & Currie, P. D. (2004). Identification of a zebrafish model of muscular dystrophy. Clinical and Experimental Pharmacology and Physiology, 31, 537–540.

    Article  PubMed  CAS  Google Scholar 

  • Bateman, A., & Bennett, H. P. (2009). The granulin gene family: From cancer to dementia. BioEssays, 31, 1245–1254.

    Article  PubMed  CAS  Google Scholar 

  • Beattie, C. E., Carrel, T. L., & McWhorter, M. L. (2007). Fishing for a mechanism: Using zebrafish to understand spinal muscular atrophy. Journal of Child Neurology, 22, 995–1003.

    Article  PubMed  Google Scholar 

  • Belkin, A. M., & Stepp, M. A. (2000). Integrins as receptor for laminins. Microscopy Research and Technique, 51(3), 280–301.

    Article  PubMed  CAS  Google Scholar 

  • Bello, L., Melacini, P., Pezzani, R., D’Amico, A., Piva, L., Leopardi, E., et al. (2012). Cardiomyopathy in patients with POMT1-related congenital and limb-girdle muscular dystrophy. European Journal of Human Genetics, 20, 1234–1239.

    Article  PubMed  CAS  Google Scholar 

  • Beltran-Valero de Bernabé, D., Currier, S., Steinbrecher, A., Celli, J., van Beusekom, E., van der Zwaag, B., et al. (2002). Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker–Warburg syndrome. American Journal of Human Genetics, 7, 1033–1043.

    Article  Google Scholar 

  • Bhandari, V., Palfree, R. G., & Bateman, A. (1992). Isolation and sequence of the granulin precursor cDNA from human bone marrow reveals tandem cysteine-rich granulin domains. Proceedings of the National Academy of Sciences of the United States of America, 89, 1715–1719.

    Article  PubMed  CAS  Google Scholar 

  • Biancheri, R., Falace, A., Tessa, A., Pedemonte, M., Scapolan, S., Cassandrini, D., et al. (2007). POMT2 gene mutation in limb-girdle muscular dystrophy with inflammatory changes. Biochemical and Biophysical Research Communications, 363, 1033–1037.

    Article  PubMed  CAS  Google Scholar 

  • Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., et al. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science, 326, 1509–1512.

    Article  PubMed  CAS  Google Scholar 

  • Bolanos-Jimenez, F., Bordais, A., Behra, M., Strahle, U., Mornet, D., Sahel, J., et al. (2001). Molecular cloning and characterization of dystrophin and Dp71, two products of the Duchenne Muscular Dystrophy gene, in zebrafish. Gene, 274, 217–226.

    Article  PubMed  CAS  Google Scholar 

  • Bonuccelli, G., Sotgia, F., Schubert, W., Park, D. S., Frank, P. G., Woodman, S. E., et al. (2003). Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. American Journal of Pathology, 163, 1663–1675.

    Article  PubMed  CAS  Google Scholar 

  • Boon, K. L., Xiao, S., McWhorter, M. L., Donn, T., Wolf-Saxon, E., Bohnsack, M. T., et al. (2009). Zebrafish survival motor neuron mutants exhibit presynaptic neuromuscular junction defects. Human Molecular Genetics, 18, 3615–3625.

    Article  PubMed  CAS  Google Scholar 

  • Brockington, M., Yuva, Y., Prandini, P., Brown, S. C., Torelli, S., Benson, M. A., 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. Human Molecular Genetics, 10, 2851–2859.

    Article  PubMed  CAS  Google Scholar 

  • Brown, S. C., & Winder, S. J. (2012). Dystroglycan and dystroglycanopathies: report of the 187th ENMC Workshop 11–13 November 2011, Naarden, The Netherlands. Neuromuscular Disorders, 22, 659–668.

    Article  PubMed  Google Scholar 

  • Brzustowicz, L. M., Lehner, T., Castilla, L. H., Penchaszadeh, G. K., Wilhelmsen, K. C., Daniels, R., et al. (1990). Genetic mapping of chronic childhood onset spinal muscular atrophy to chromosome 5q11.2-13.3. Nature, 344, 540–541.

    Article  PubMed  CAS  Google Scholar 

  • Cade, L., Reyon, D., Hwang, W. Y., Tsai, S. Q., Patel, S., Khayter, C., et al. (2012). Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Research, 40, 8001–8010.

    Article  PubMed  CAS  Google Scholar 

  • Carrel, T. L., McWhorter, M. L., Workman, E., Zhang, H., Wolstencroft, E. C., Lorson, C., et al. (2006). Survival motor neuron function in motor axons is independent of functions required for small nuclear ribonucleoprotein biogenesis. J of Neuroscience, 26, 11014–11022.

    Article  CAS  Google Scholar 

  • Chambers, S. P., Dodd, A., Overall, R., Sirey, T., Lam, L. T., Morris, G. E., et al. (2001). Dystrophin in adult zebrafish muscle. Biochemical and Biophysical Research Communications, 286, 478–483.

    Article  PubMed  CAS  Google Scholar 

  • Cheng, L., Guo, X., Yang, X., Chong, M., Cheng, J., Li, G., et al. (2006). Delta-sarcoglycan is necessary for early heart and muscle development in zebrafish. Biochemical and Biophysical Research Communications, 344, 1290–1299.

    Article  PubMed  CAS  Google Scholar 

  • Chitramuthu, B. P., Baranowski, D. C., Kay, D. G., Bateman, A., & Bennett, H. P. J. (2010). Progranulin modulates zebrafish motoneuron development in vivo and rescues truncation defects associated with knockdown of Survival motor neuron 1. Molecular Neurodegeneration, 5, 41.

    Article  PubMed  CAS  Google Scholar 

  • Clark, K. J., Voytas, D. F., & Ekker, S. C. (2011). A TALE of two nucleases: Gene targeting for the masses? Zebrafish, 8, 147–149.

    Article  PubMed  CAS  Google Scholar 

  • Damann, N., Voets, T., & Nilius, B. (2008). TRPs in our senses. Current Biology, 18, R880–R889.

    Article  PubMed  CAS  Google Scholar 

  • Daniel, R., Daniels, E., He, Z., & Bateman, A. (2003). Progranulin (acrogranin/PC cell-derived growth factor/granulin-epithelin precursor) is expressed in the placenta, epidermis, microvasculature, and brain during murine development. Developmental Dynamics, 227, 593–599.

    Article  PubMed  CAS  Google Scholar 

  • Desmarais, J. A., Cao, M., Bateman, A., & Murphy, B. D. (2008). Spatiotemporal expression pattern of progranulin in embryo implantation and placenta formation suggests a role in cell proliferation, remodeling, and angiogenesis. Reproduction, 136, 247–257.

    Article  PubMed  CAS  Google Scholar 

  • Detrich, H. W., 3rd, Westerfield, M., & Zon, L. I. (2011). The zebrafish. Preface. Methods Cell Biology, 105, 3–5.

    Google Scholar 

  • Diaz-Cueto, L., & Gerton, G. L. (2001). The influence of growth factors on the development of preimplantation mammalian embryos. Archives of Medical Research, 32, 619–626.

    Article  PubMed  CAS  Google Scholar 

  • Durbeej, M., & Campbell, K. P. (2002). Muscular dystrophies involving the dystrophin–glycoprotein complex: An overview of current mouse models. Current Opinion in Genetics and Development, 12, 349–361.

    Article  PubMed  CAS  Google Scholar 

  • Emery, A. E. (1991). Population frequencies of inherited neuromuscular diseases: A world survey. Neuromuscular Disorders, 1, 19–29.

    Article  PubMed  CAS  Google Scholar 

  • Engel, A. G. (2012). Congenital myasthenic syndromes in 2012. Current Neurology and Neuroscience Reports, 12, 92–101.

    Article  PubMed  Google Scholar 

  • Engel, A. G., & Sine, S. M. (2005). Current understanding of congenital myasthenic syndromes. Current Opinion in Pharmacology, 5, 308–321.

    Article  PubMed  CAS  Google Scholar 

  • Esapa, C. T., Benson, M. A., Schroder, J. E., Martin-Rendon, E., Brockington, M., Brown, S. C., et al. (2002). Functional requirements for fukutin related protein in the Golgi apparatus. Human Molecular Genetics, 11, 3319–3331.

    Article  PubMed  CAS  Google Scholar 

  • Finlayson, S., Beeson, D., & Palace, J. (2013). Congenital myasthenic syndromes: An update. Practical Neurology, 13, 80–91.

    Article  PubMed  Google Scholar 

  • Fiorillo, C., Moro, F., Brisca, G., Astrea, G., Nesti, C., Bálint, Z., et al. (2012). TRPV4 mutations in children with congenital distal spinal muscular atrophy. Neurogenetics, 13(3), 195–203.

    Article  PubMed  CAS  Google Scholar 

  • Froehner, S. C., Gulbrandsen, V., Hyman, C., Jeng, A. Y., Neubig, R. R., & Cohen, J. B. (1981). Immunofluorescence localization at the mammalian neuromuscular junction of the Mr 43,000 protein of Torpedo postsynaptic membranes. Proceedings of the National Academy of Sciences of the United States of America, 78, 5230–5234.

    Article  PubMed  CAS  Google Scholar 

  • Gautam, M., Noakes, P. G., Mudd, J., Nichol, M., Chu, G. C., Sanes, J. R., et al. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature, 377, 232–236.

    Article  PubMed  CAS  Google Scholar 

  • Godfrey, C., Escolar, D., Brockington, M., Clement, E. M., Mein, R., Jimenez-Mallebrera, C., et al. (2006). Fukutin gene mutations in steroid-responsive limb girdle muscular dystrophy. Annals of Neurology, 60, 603–610.

    Article  PubMed  CAS  Google Scholar 

  • Godfrey, C., Foley, A. R., Clement, E., & Muntoni, F. (2011). Dystroglycanopathies: Coming into focus. Current Opinion in Genetics and Development, 21, 278–285.

    Article  PubMed  CAS  Google Scholar 

  • Granato, M., van Eeden, J. M. F., Schach, U., Trowe, T., Brand, M., Furutani-Seiki, M., et al. (1996). Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development, 123, 399–413.

    PubMed  CAS  Google Scholar 

  • Grewal, P. K., & Hewitt, J. E. (2002). Mutation of large, which encodes a putative glycosyltransferase, in an animal model of muscular dystrophy. Biochimica et Biophysica Acta, 1573, 216–224.

    Article  PubMed  CAS  Google Scholar 

  • Grewal, P. K., Holzfeind, P. J., Bittner, R. E., & Hewitt, J. E. (2001). Mutant glycosyltransferase and altered glycosylation of α-dystroglycan in the myodystrophy mouse. Nature Genetics, 28, 151–154.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Grounds, M., Sorokin, L., & White, J. (2005). Strength at the extracellular matrix-muscle interface. Scandinavian Journal of Medicine and Science in Sports, 15(6), 381–391.

    Article  PubMed  CAS  Google Scholar 

  • Gupta, V., Kawahara, G., Gundry, S. R., Chen, A. T., Lencer, W. I., Zhou, Y., et al. (2011). The zebrafish dag1 mutant: A novel genetic model for dystroglycanopathies. Human Molecular Genetics, 20, 1712–1725.

    Article  PubMed  CAS  Google Scholar 

  • Guyon, J. R., Goswami, J., Jun, S. J., Thorne, M., Howell, M., Pusack, T., et al. (2009). Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin. Human Molecular Genetics, 18, 202–211.

    Article  PubMed  CAS  Google Scholar 

  • Guyon, J. R., Mosley, A. N., Jun, S. J., Montanaro, F., Steffen, L. S., Zhou, Y., et al. (2005). Delta-sarcoglycan is required for early zebrafish muscle organization. Experimental Cell Research, 304, 105–115.

    Article  PubMed  CAS  Google Scholar 

  • Guyon, J. R., Mosley, A. N., Zhou, Y., Davidson, A. J., Sheng, X., Chiang, K., et al. (2003). The dystrophin associated protein complex in zebrafish. Human Molecular Genetics, 12, 601–615.

    Article  PubMed  CAS  Google Scholar 

  • Hackman, P., Vihola, A., Haravuori, H., Marchand, S., Sarparanta, J., De Seze, J., et al. (2002). Tibial muscular dystrophy is a titinopathy caused by mutations in TTN, the gene encoding the giant skeletal-muscle protein titin. American Journal of Human Genetics, 71, 492–500.

    Article  PubMed  CAS  Google Scholar 

  • Hall, T. E., Bryson-Richardson, R. J., Berger, S., Jacoby, A. S., Cole, N. J., Hollway, G. E., et al. (2007). The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin alpha2-deficient congenital muscular dystrophy. Proceedings of the National Academy of Sciences of the United States of America, 104, 7092–7097.

    Article  PubMed  CAS  Google Scholar 

  • Hans, S., Freudenreich, D., Geffarth, M., Kaslin, J., Machate, A., & Brand, M. (2011). Generation of a non-leaky heat shock-inducible Cre line for conditional Cre/lox strategies in zebrafish. Developmental Dynamics, 240, 108–115.

    Article  PubMed  CAS  Google Scholar 

  • Hao, L. T., Burghes, A. H. M., & Beattie, E. C. (2011). Generation and characterization of a genetic zebrafish model of SMA carrying the human SMN2 gene. Molecular Neurodegeneration, 6, 24.

    Article  CAS  Google Scholar 

  • Hao, L. T., Wolman, M., Granato, M., & Beattie, C. E. (2012). Survival Motor Neuron affects Plastin 3 protein levels leading to motor defects. Journal of Neuroscience, 32, 5074–5084.

    Article  CAS  Google Scholar 

  • Haravuori, H., Vihola, A., Straub, V., Auranen, M., Richard, I., Marchand, S., et al. (2001). Secondary calpain3 deficiency in 2q-linked muscular dystrophy: Titin is the candidate gene. Neurology, 56, 869–877.

    Article  PubMed  CAS  Google Scholar 

  • Harvey, A. R., & Fletcher-Holmes, D. W. (2004). Birefringent Fourier-transform imaging spectrometer. Optics Express, 12, 5368–5374.

    Article  PubMed  Google Scholar 

  • He, Z., Ong, C. H., Halper, J., & Bateman, A. (2003). Progranulin is a mediator of the wound response. Nature Medicine, 9, 225–229.

    Article  PubMed  CAS  Google Scholar 

  • Helbling-Leclerc, A., Zhang, X., Topaloglu, H., Cruaud, C., Tesson, F., Weissenbach, J., et al. (1995). Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nature Genetics, 11, 216–218.

    Article  PubMed  CAS  Google Scholar 

  • Hewitt, J. E. (2009). Abnormal glycosylation of dystroglycan in human genetic disease. Biochimica et Biophysica Acta, 1792, 853–861.

    Article  PubMed  CAS  Google Scholar 

  • Holt, K. H., Crosbie, R. H., Venzke, D. P., & Campbell, K. P. (2000). Biosynthesis of dystroglycan: Processing of a precursor propeptide. FEBS Letters, 468, 79–83.

    Article  PubMed  CAS  Google Scholar 

  • Illa, I., Serrano-Munuera, C., Gallardo, E., Lasa, A., Rojas-García, R., Palmer, J., et al. (2001). Distal anterior compartment myopathy: A dysferlin mutation causing a new muscular dystrophy phenotype. Annals of Neurology, 49, 130–134.

    Article  PubMed  CAS  Google Scholar 

  • Joung, J. K., & Sander, J. D. (2013). TALENs: A widely applicable technology for targeted genome editing. Nature Reviews, 14, 49–55.

    PubMed  CAS  Google Scholar 

  • Kabashi, E., Brustein, E., Champagne, N., & Drapeau, P. (2011). Zebrafish models for the functional genomics of neurogenetic disorders. Biochimica et Biophysica Acta, 1812, 335–345.

    Article  PubMed  CAS  Google Scholar 

  • Kabashi, E., Champagne, N., Brustein, E., & Drapeau, P. (2010). In the swim of things: Recent insights to neurogenetic disorders from zebrafish. Trends in Genetics, 26, 373–381.

    Article  PubMed  CAS  Google Scholar 

  • Kaplan, J. C., & Hamroun, D. (2012). The 2013 version of the gene table of monogenic neuromuscular disorders (nuclear genome). Neuromuscular Disorders, 22(12), 1108–1135.

    Article  Google Scholar 

  • Kawahara, G., Guyon, J. R., Nakamura, Y., & Kunkel, L. M. (2010). Zebrafish models for human FKRP muscular dystrophies. Human Molecular Genetics, 19, 623–633.

    Article  PubMed  CAS  Google Scholar 

  • Kawahara, G., Karpf, J. A., Myers, J. A., Alexander, M. S., Guyon, J. R., & Kunkel, L. M. (2011a). Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proceedings of the National Academy of Sciences of the United States of America, 108, 5331–5336.

    Article  PubMed  CAS  Google Scholar 

  • Kawahara, G., Serafini, P. R., Myers, J. A., Alexander, M. S., & Kunkel, L. M. (2011b). Characterization of zebrafish dysferlin by morpholino knockdown. Biochemical and Biophysical Research Communications, 413, 358–363.

    Article  PubMed  CAS  Google Scholar 

  • Kessenbrock, K., Frohlich, L., Sixt, M., Lammermann, T., Pfister, H., Bateman, A., et al. (2008). Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. Journal of Clinical Investigation, 118, 2438–2447.

    PubMed  CAS  Google Scholar 

  • Kliegman, R. M., Behrman, R. E., Jenson, H. B., & Stanton, B. F. (2007) Muscular dystrophies. In: Nelson textbook of pediatrics (18th Ed). Philadelphia: Saunders Elsevier, Chap. 608.

  • Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura, K., Kondo-Iida, E., Nomura, Y., et al. (1998). An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature, 394, 388–392.

    Article  PubMed  CAS  Google Scholar 

  • LaRochelle, W. J., & Froehner, S. C. (1986). Determination of the tissue distributions and relative concentrations of the postsynaptic 43 kDa protein and the acetylcholine receptor in Torpedo. Journal of Biological Chemistry, 261, 5270–5274.

    PubMed  CAS  Google Scholar 

  • Lefeber, D. J., Schönberger, J., Morava, E., Guillard, M., Huyben, K. M., Verrijp, K., et al. (2011). Zebrafish Fukutin family proteins link the unfolded protein response with dystroglycanopathies. Human Molecular Genetics, 20, 1763–1775.

    Article  CAS  Google Scholar 

  • Leong, I. U., Lai, D., Lan, C. C., Johnson, R., Love, D. R., Johnson, R., et al. (2011). Targeted mutagenesis of zebrafish: use of zinc finger nucleases. Birth Defects Research. Part C, Embryo Today, 93, 249–255.

    Article  CAS  Google Scholar 

  • Lin, Y. Y. (2012). Muscle diseases in the zebrafish. Neuromuscular Disorders, 22, 673–684.

    Article  PubMed  Google Scholar 

  • Liu, J., Aoki, M., Illa, I., Wu, C., Fardeau, M., Angelini, C., et al. (1998). Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nature Genetics, 20, 31–36.

    Article  PubMed  CAS  Google Scholar 

  • Longman, C., Brockington, M., Torelli, S., Jimenez-Mallebrera, C., Kennedy, C., Khalil, N., et al. (2003). Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of alpha-dystroglycan. Human Molecular Genetics, 12, 2853–2861.

    Article  PubMed  CAS  Google Scholar 

  • Maeda, Y., van den Heuve, L., Lammens, M., Lehle, L., & Wevers, R. A. (2009). Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. American Journal of Human Genetics, 85, 76–86.

    Article  PubMed  CAS  Google Scholar 

  • Manya, H., Chiba, A., Yoshida, A., Wang, X., Chiba, Y., Jigami, Y., et al. (2004). Demonstration of mammalian protein O-mannosyltransferase activity: Coexpression of POMT1 and POMT2 required for enzymatic activity. Proceedings of the National Academy of Sciences of the United States of America, 101, 500–505.

    Article  PubMed  CAS  Google Scholar 

  • Manzini, M. C., Gleason, D., Chang, B. S., Hill, R. S., Barry, B. J., Partlow, J. N., et al. (2008). Ethnically diverse causes of Walker–Warburg syndrome (WWS): FCMD mutations are a more common cause of WW outside of the Middle East. Human Mutation, 29, E231–E241.

    Article  PubMed  Google Scholar 

  • Manzini, M. C., Tambunan, D. E., Hill, R. S., Yu, T. W., Maynard, T. M., Heinzen, E. L., et al. (2012). Exome sequencing and functional validation in zebrafish identify GTDC2 mutations as a cause of Walker–Warburg Syndrome. American Journal of Human Genetics, 91, 541–547.

    Article  PubMed  CAS  Google Scholar 

  • McWhorter, M. L., Monani, U. R., Burghes, A. H., & Beattie, C. E. (2003). Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding. Journal of Cell Biology, 162, 919–931.

    Article  PubMed  CAS  Google Scholar 

  • Milone, M., Wang, H. L., Ohno, K., Fukudome, T., Pruitt, J. N., Bren, N., et al. (1997). Slow-channel myasthenic syndrome caused by enhanced activation, desensitization, and agonist binding affinity attributable to mutation in the M2 domain of the acetylcholine receptor alpha subunit. Journal of Neuroscience, 17, 5651–5665.

    PubMed  CAS  Google Scholar 

  • Miner, J. H., & Yurchenco, P. D. (2004). Laminin functions in tissue morphogenesis. Annual Review of Cell and Developmental Biology, 20, 255–284.

    Article  PubMed  CAS  Google Scholar 

  • Moore, C. J., Tse Goh, H., & Hewitt, J. E. (2008). Genes required for functional glycosylation of dystroglycan are conserved in zebrafish. Genomics, 92, 159–167.

    Article  PubMed  CAS  Google Scholar 

  • Moscou, M. J., & Bogdanove, A. J. (2009). A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501.

    Article  PubMed  CAS  Google Scholar 

  • Müller, J. S., Herczegfalvi, A., Vilchez, J. J., Colomer, J., Bachinski, L. L., Mihaylova, V., et al. (2007). Phenotypical spectrum of DOK7 mutations in congenital myasthenic syndromes. Brain, 130, 1497–1506.

    Article  PubMed  Google Scholar 

  • Müller, J. S., Jepson, C. D., Laval, S. H., Bushby, K., Straub, V., & Lochmüller, H. (2010). Dok-7 promotes slow muscle integrity as well as neuromuscular junction formation in a zebrafish model of congenital myasthenic syndromes. Human Molecular Genetics, 19, 1726–1740.

    Article  PubMed  CAS  Google Scholar 

  • Neubig, R. R., Krodel, E. K., Boyd, N. D., & Cohen, J. B. (1979). Acetylcholine and local anesthetic binding to Torpedo nicotinic postsynaptic membranes after removal of nonreceptor peptides. Proceedings of the National Academy of Sciences of the United States of America, 76, 690–694.

    Article  PubMed  CAS  Google Scholar 

  • Neuromuscular disorders: Gene location. (2006). Neuromuscular Disorders, 16, 64–90.

  • Ng, S. B., Buckingham, K. J., Lee, C., Bigham, A. W., Tabor, H. K., Dent, K. M., et al. (2010). Exome sequencing identifies the cause of a Mendelian disorder. Nature Genetics, 42, 30–35.

    Article  PubMed  CAS  Google Scholar 

  • Nigro, V., Aurino, S., & Piluso, G. (2011). Limb girdle muscular dystrophies: Update on genetic diagnosis and therapeutic approaches. Current Opinion in Neurology, 5, 429–436.

    Article  CAS  Google Scholar 

  • Nigro, V., Moreira, E.d. S., Piluso, G., Vainzof, M., Belsito, A., Politano, L., et al. (1996). Autosomal recessive limb girdle muscular dystrophy (LGMD2F) is caused by a mutation in the delta-sarcoglycan gene. Nature Genetics, 14, 195–198.

    Article  PubMed  CAS  Google Scholar 

  • Noakes, P. G., Phillips, W. D., Hanley, T. A., Sanes, J. R., & Merlie, J. P. (1993). 43 K protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Developmental Biology, 155, 275–280.

    Article  PubMed  CAS  Google Scholar 

  • Norwood, F. L., Harling, C., Chinnery, P. F., Eagle, M., Bushby, K., & Straub, V. (2009). Prevalence of genetic muscle disease in Northern England: In-depth analysis of a muscle clinic population. Brain, 132, 3175–3186.

    Article  PubMed  Google Scholar 

  • Ohno, K. (2013) Glycosylation defects as an emerging novel cause leading to a limb-girdle type of congenital myasthenic syndromes. Journal of Neurology, Neurosurgery, and Psychiatry, [Epub ahead of print], PMID: 23457230.

  • Okada, K., Inoue, A., Okada, M., Murata, Y., Kakuta, S., Jigami, T., et al. (2006). The muscle protein Dok-7 is essential for neuromuscular synaptogenesis. Science, 312, 1802–1805.

    Article  PubMed  CAS  Google Scholar 

  • Ono, F., Shcherbatko, A., Higashijima, S. I., Mandel, G., & Brehm, P. (2002). The zebrafish motility mutant twitch once reveals new roles for rapsyn in synaptic function. Journal of Neuroscience, 22, 6491–6498.

    PubMed  CAS  Google Scholar 

  • Oprea, G. E., Krober, S., McWhorter, M. L., Rossoll, W., Muller, S., Krawczak, M., et al. (2008). Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science, 320, 524–527.

    Article  PubMed  CAS  Google Scholar 

  • Qin, J., Diaz-Cueto, L., Schwarze, J. E., Takahashi, Y., Imai, M., Isuzugawa, K., et al. (2005). Effects of progranulin on blastocyst hatching and subsequent adhesion and outgrowth in the mouse. Biology of Reproduction, 73, 434–442.

    Article  PubMed  CAS  Google Scholar 

  • Ramesh, T., Lyon, A. N., Pineda, R. H., Wang, C., Janssen, P. M. L., Canan, B. D., et al. (2010). A genetic model of amyotrophic lateral sclerosis in zebrafish displays phenotypic hallmarks of motoneuron disease. Disease Models and Mechanisms, 3, 652–662.

    Article  PubMed  CAS  Google Scholar 

  • Reyon, D., Tsai, S. Q., Khayter, C., Foden, J. A., Sander, J. D., & Joung, J. K. (2012). FLASH assembly of TALENs for high throughput genome editing. Nature Biotechnology, 30, 460–465.

    Article  PubMed  CAS  Google Scholar 

  • Rochette, C. F., Gilbert, N., & Simard, L. R. (2001). SMN gene duplication and the emergence of the SMN2 gene occurred in distinct hominids: SMN2 is unique to Homo sapiens. Human Genetics, 108, 255–266.

    Article  PubMed  CAS  Google Scholar 

  • Roostalu, U., & Strähle, U. (2012). In vivo imaging of molecular interactions at damaged sarcolemma. Developmental Cell, 22, 515–529.

    Article  PubMed  CAS  Google Scholar 

  • Roscioli, T., Kamsteeg, E. J., Buysse, K., Maystadt, I., van Reeuwijk, J., van den Elzen, C., et al. (2012). Mutations in ISPD cause Walker–Warburg syndrome and defective glycosylation of α-dystroglycan. Nature Genetics, 44, 581–585.

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Ramos, C., Guerrera, M. C., Bonnin-Arias, C., Calavia, M. G., Laurà, R., Germanà, A., et al. (2012). Expression of TRPV4 in the zebrafish retina during development. Microscopy Research and Technique, 75, 743–748.

    Article  PubMed  CAS  Google Scholar 

  • Sander, J. D., Cade, L., Khayter, C., Reyon, D., Peterson, R. T., Joung, J. K., et al. (2011). Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nature Biotechnology, 29, 697–698.

    Article  PubMed  CAS  Google Scholar 

  • Santoriello, C., & Zon, L. I. (2012). Hooked! Modeling human disease in zebrafish. Journal of Clinical Investigation, 122, 2337–2343.

    Article  PubMed  CAS  Google Scholar 

  • Sewry, C. A. (2010). Muscular dystrophies: An update on pathology and diagnosis. Acta Neuropathologica, 120, 343–358.

    Article  PubMed  CAS  Google Scholar 

  • Sobel, A., Weber, M., & Changeux, J. P. (1977). Large-scale purification of the acetylcholine-receptor protein in its membrane-bound and detergent extracted forms from Torpedo marmorata electric organ. European Journal of Biochemistry, 80, 215–224.

    Article  PubMed  CAS  Google Scholar 

  • Steffen, L. S., Guyon, J. R., Vogel, E. D., Beltre, R., Pusack, T. J., Zhou, Y., et al. (2007). Zebrafish orthologs of human muscular dystrophy genes. BMC Genomics, 20, 8–79.

    Google Scholar 

  • Tan, E., Topaloglu, H., Sewry, C., Zorlu, Y., Naom, I., Erdem, S., et al. (1997). Late onset muscular dystrophy with cerebral white matter changes due to partial merosin deficiency. Neuromuscular Disorders, 7, 85–89.

    Article  PubMed  CAS  Google Scholar 

  • Tesson, L., Usal, C., Ménoret, S., Leung, E., Niles, B. J., Remy, S., et al. (2011). Knockout rats generated by embryo microinjection of TALENs. Nature Biotechnology, 29, 695–696.

    Article  PubMed  CAS  Google Scholar 

  • Thornhill, P., Bassett, D., Lochmüller, H., Bushby, K., & Straub, V. (2008). Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin-related protein (FKRP). Brain, 131, 1551–1561.

    Article  PubMed  Google Scholar 

  • Tunggal, P., Smyth, N., Paulsson, M., & Ott, M. C. (2000). Laminins: Structure and genetic regulation. Microscopy Research and Technique, 51, 214–227.

    Article  PubMed  CAS  Google Scholar 

  • van Reeuwijk, J., van den Janssen, M., Elzen, C., Beltran-Valero de Bernabé, D., Sabatelli, P., Merlini, L., et al. (2005). POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker–Warburg syndrome. Journal of Medical Genetics, 42, 907–912.

    Article  PubMed  CAS  Google Scholar 

  • Vasli, N., Böhm, J., Le Gras, S., Muller, J., Pizot, C., Jost, B., et al. (2012). Next generation sequencing for molecular diagnosis of neuromuscular diseases. Acta Neuropathologica, 124, 273–283.

    Article  PubMed  CAS  Google Scholar 

  • Verhaert, D., Richards, K., Rafael-Fortney, J. A., & Raman, S. V. (2011). Cardiac involvement in patients with muscular dystrophies: Magnetic resonance imaging phenotype and genotypic considerations. Circulation. Cardiovascular Imaging, 4, 67–76.

    Article  PubMed  Google Scholar 

  • Verma, P., Kumar, A., & Goswami, C. (2010). TRPV4-mediated channelopathies. Channels, 4, 319–328.

    Article  PubMed  CAS  Google Scholar 

  • Walogorsky, M., Mongeon, R., Wen, H., Mandel, G., & Brehm, P. (2012a). Acetylcholine receptor gating in a zebrafish model for slow-channel syndrome. Journal of Neuroscience, 32, 7941–7948.

    Article  PubMed  CAS  Google Scholar 

  • Walogorsky, M., Mongeon, R., Wen, H., Nelson, N. R., Urban, J. M., Ono, F., et al. (2012b). Zebrafish model for congenital myasthenic syndrome reveals mechanisms causal to developmental recovery. Proceedings of the National Academy of Sciences of the United States of America, 109, 17711–17716.

    Article  PubMed  CAS  Google Scholar 

  • Walton, J. N. (1981). Disorders of voluntary muscle (4th ed.). Churchill Livingston: New York.

    Google Scholar 

  • Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., et al. (2001). Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Developmental Cell, 1, 717–724.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, R., Yang, J., Zhu, J., & Xu, X. (2009). Depletion of zebrafish Tcap leads to muscular dystrophy via disrupting sarcomere–membrane interaction, not sarcomere assembly. Human Molecular Genetics, 18, 4130–4140.

    Article  PubMed  CAS  Google Scholar 

  • Zhou, J., Tawk, M., Tiziano, F. D., Veillet, J., Bayes, M., Nolent, F., et al. (2012). Spinal muscular atrophy associated with progressive myoclonic epilepsy is caused by mutations in ASAH1. American Journal of Human Genetics, 91, 5–14.

    Article  PubMed  CAS  Google Scholar 

  • Zhu, J., Nathan, C., Jin, W., Sim, D., Ashcroft, G. S., Wahl, S. M., et al. (2002). Conversion of proepithelin to epithelins: Roles of SLPI and elastase in host defense and wound repair. Cell, 111, 867–878.

    Article  PubMed  CAS  Google Scholar 

  • Zon, L. I., & Peterson, R. T. (2005). In vivo drug discovery in the zebrafish. Nature Reviews. Drug Discovery, 4, 35–44.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported in part by the Italian Ministry of Health, Regione Toscana (RR5/09-RT, to C.B. and A.D.) and Fondazione Telethon (Grant GUP11001D to F.M.S., GUP11001E to C.B.). The authors thank Dr. Catherine J. Wrenn for her editorial assistance.

Author information

Authors and Affiliations

  1. Molecular Medicine, and Neuromuscular Lab, IRCCS Stella Maris, Via dei Giacinti 2, 56128, Pisa, Italy

    Andrea Pappalardo, Chiara Fiorillo & Filippo M. Santorelli

  2. Institute of Clinical Physiology, CNR, Pisa, Italy

    Letizia Pitto

  3. AOU Meyer Hospital, Florence, Italy

    M. Alice Donati

  4. Pediatric Neurology Unit, Department of Neuroscience and Rehabilitation, Center of Myology, IRCCS G. Gaslini, Genoa, Italy

    Claudio Bruno

Authors
  1. Andrea Pappalardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Letizia Pitto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chiara Fiorillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Alice Donati
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Claudio Bruno
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Filippo M. Santorelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Filippo M. Santorelli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pappalardo, A., Pitto, L., Fiorillo, C. et al. Neuromuscular Disorders in Zebrafish: State of the Art and Future Perspectives. Neuromol Med 15, 405–419 (2013). https://doi.org/10.1007/s12017-013-8228-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12017-013-8228-z

Keywords

Search

Navigation