Abstract
Muscular dystrophies and congenital myopathies are genetic disorders that affect skeletal muscle. Mice have been widely used as animal models of the diseases; however, the zebrafish has recently received much attention as a new model system complementary to mammalian models. The basic structure of zebrafish skeletal muscle is similar to that of humans, and approximately 70% of human genes correspond to at least one ortholog in the zebrafish genome. Furthermore, various attributes make zebrafish suited for the inherited muscular disorders, for example, ease of genetic manipulation by microinjection, rapid external development, reproducible motor behavior from 24 h postfertilization, in vivo imaging based on the transparency of embryos, and mutant resource generated by a forward genetic approach. This review highlights key studies using zebrafish as a model of inherited muscular disorders, focusing on disease mutants identified from forward genetic screening, causative gene discovery by reverse genetic approach, and drug screening to develop novel therapeutic strategies.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Ablain J, Durand EM, Yang S, Zhou Y, Zon LI (2015) A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish. Dev Cell 32:756–764. https://doi.org/10.1016/j.devcel.2015.01.032
Al-Qusairi L, Laporte J (2011) T-tubule biogenesis and triad formation in skeletal muscle and implication in human diseases. Skelet Muscle 1:26. https://doi.org/10.1186/2044-5040-1-26
Ardiccioni C, Clarke OB, Tomasek D, Issa HA, von Alpen DC, Pond HL, Banerjee S, Rajashankar KR, Liu Q, Guan Z, Li C, Kloss B, Bruni R, Kloppmann E, Rost B, Manzini MC, Shapiro L, Mancia F (2016) Structure of the polyisoprenyl-phosphate glycosyltransferase GtrB and insights into the mechanism of catalysis. Nat Commun 7:10175. https://doi.org/10.1038/ncomms10175
Auer TO, Duroure K, De Cian A, Concordet JP, Del Bene F (2014) Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair. Genome Res 24:142–153. https://doi.org/10.1101/gr.161638.113
Avsar-Ban E, Ishikawa H, Manya H, Watanabe M, Akiyama S, Miyake H, Endo T, Tamaru Y (2010) Protein O-mannosylation is necessary for normal embryonic development in zebrafish. Glycobiology 20:1089–1102. https://doi.org/10.1093/glycob/cwq069
Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP (2003) Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423:168–172. https://doi.org/10.1038/nature01573
Bassett DI, Bryson-Richardson RJ, Daggett DF, Gautier P, Keenan DG, Currie PD (2003) Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo. Development 130:5851–5860. https://doi.org/10.1242/dev.00799
Berger J, Berger S, Hall TE, Lieschke GJ, Currie PD (2010) Dystrophin-deficient zebrafish feature aspects of the Duchenne muscular dystrophy pathology. Neuromuscul Disord 20:826–832. https://doi.org/10.1016/j.nmd.2010.08.004
Berger J, Berger S, Jacoby AS, Wilton SD, Currie PD (2011) Evaluation of exon-skipping strategies for Duchenne muscular dystrophy utilizing dystrophin-deficient zebrafish. J Cell Mol Med 15:2643–2651. https://doi.org/10.1111/j.1582-4934.2011.01260.x
Berger J, Sztal T, Currie PD (2012) Quantification of birefringence readily measures the level of muscle damage in zebrafish. Biochem Biophys Res Commun 423:785–788. https://doi.org/10.1016/j.bbrc.2012.06.040
Berger J, Tarakci H, Berger S, Li M, Hall TE, Arner A, Currie PD (2014) Loss of Tropomodulin4 in the zebrafish mutant trage causes cytoplasmic rod formation and muscle weakness reminiscent of nemaline myopathy. Dis Model Mech 7:1407–1415. https://doi.org/10.1242/dmm.017376
Bonnemann CG, Modi R, Noguchi S, Mizuno Y, Yoshida M, Gussoni E, McNally EM, Duggan DJ, Angelini C, Hoffman EP (1995) Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat Genet 11:266–273. https://doi.org/10.1038/ng1195-266
Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, Simsek T, Garner HR, Agha-Mohammadi S, Tassin A, Coppee F, Belayew A, Perlingeiro RR, Kyba M (2008) An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 27:2766–2779. https://doi.org/10.1038/emboj.2008.201
Bragato C, Gaudenzi G, Blasevich F, Pavesi G, Maggi L, Giunta M, Cotelli F, Mora M (2016) Zebrafish as a model to investigate dynamin 2-related diseases. Sci Rep 6:20466. https://doi.org/10.1038/srep20466
Buysse K, Riemersma M, Powell G, van Reeuwijk J, Chitayat D, Roscioli T, Kamsteeg EJ, van den Elzen C, van Beusekom E, Blaser S, Babul-Hirji R, Halliday W, Wright GJ, Stemple DL, Lin YY, Lefeber DJ, van Bokhoven H (2013) Missense mutations in beta-1,3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome. Hum Mol Genet 22:1746–1754. https://doi.org/10.1093/hmg/ddt021
Carss KJ, Stevens E, Foley AR, Cirak S, Riemersma M, Torelli S, Hoischen A, Willer T, van Scherpenzeel M, Moore SA, Messina S, Bertini E, Bonnemann CG, Abdenur JE, Grosmann CM, Kesari A, Punetha J, Quinlivan R, Waddell LB, Young HK, Wraige E, Yau S, Brodd L, Feng L, Sewry C, MacArthur DG, North KN, Hoffman E, Stemple DL, Hurles ME, van Bokhoven H, Campbell KP, Lefeber DJ, Consortium UK, Lin YY, Muntoni F (2013) Mutations in GDP-mannose pyrophosphorylase B cause congenital and limb-girdle muscular dystrophies associated with hypoglycosylation of alpha-dystroglycan. Am J Hum Genet 93:29–41. https://doi.org/10.1016/j.ajhg.2013.05.009
Cheng L, Guo XF, Yang XY, Chong M, Cheng J, Li G, Gui YH, Lu DR (2006) Delta-sarcoglycan is necessary for early heart and muscle development in zebrafish. Biochem Biophys Res Commun 344:1290–1299. https://doi.org/10.1016/j.bbrc.2006.03.234
Cohn RD, Campbell KP (2000) Molecular basis of muscular dystrophies. Muscle Nerve 23:1456–1471
Dangain J, Vrbova G (1984) Muscle development in mdx mutant mice. Muscle Nerve 7:700–704. https://doi.org/10.1002/mus.880070903
Davidson AE, Siddiqui FM, Lopez MA, Lunt P, Carlson HA, Moore BE, Love S, Born DE, Roper H, Majumdar A, Jayadev S, Underhill HR, Smith CO, von der Hagen M, Hubner A, Jardine P, Merrison A, Curtis E, Cullup T, Jungbluth H, Cox MO, Winder TL, Abdel Salam H, Li JZ, Moore SA, Dowling JJ (2013) Novel deletion of lysine 7 expands the clinical, histopathological and genetic spectrum of TPM2-related myopathies. Brain 136:508–521. https://doi.org/10.1093/brain/aws344
de Winter JM, Ottenheijm CAC (2017) Sarcomere dysfunction in nemaline myopathy. J Neuromuscul Dis 4:99–113. https://doi.org/10.3233/JND-160200
Di Costanzo S, Balasubramanian A, Pond HL, Rozkalne A, Pantaleoni C, Saredi S, Gupta VA, Sunu CM, Yu TW, Kang PB, Salih MA, Mora M, Gussoni E, Walsh CA, Manzini MC (2014) POMK mutations disrupt muscle development leading to a spectrum of neuromuscular presentations. Hum Mol Genet 23:5781–5792. https://doi.org/10.1093/hmg/ddu296
Dong M, Noguchi S, Endo Y, Hayashi YK, Yoshida S, Nonaka I, Nishino I (2015) DAG1 mutations associated with asymptomatic hyperCKemia and hypoglycosylation of alpha-dystroglycan. Neurology 84:273–279. https://doi.org/10.1212/WNL.0000000000001162
Dowling JJ, Vreede AP, Low SE, Gibbs EM, Kuwada JY, Bonnemann CG, Feldman EL (2009) Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet 5:e1000372. https://doi.org/10.1371/journal.pgen.1000372
Dowling JJ, Arbogast S, Hur J, Nelson DD, McEvoy A, Waugh T, Marty I, Lunardi J, Brooks SV, Kuwada JY, Ferreiro A (2012) Oxidative stress and successful antioxidant treatment in models of RYR1-related myopathy. Brain 135:1115–1127. https://doi.org/10.1093/brain/aws036
Dowling JJ, Lawlor MW, Dirksen RT (2014) Triadopathies: an emerging class of skeletal muscle diseases. Neurotherapeutics 11:773–785. https://doi.org/10.1007/s13311-014-0300-3
Elworthy S, Hargrave M, Knight R, Mebus K, Ingham PW (2008) Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity. Development 135:2115–2126. https://doi.org/10.1242/dev.015719
Felsenfeld AL, Walker C, Westerfield M, Kimmel C, Streisinger G (1990) Mutations affecting skeletal muscle myofibril structure in the zebrafish. Development 108:443–459
Gawlik KI, Durbeej M (2011) Skeletal muscle laminin and MDC1A: pathogenesis and treatment strategies. Skelet Muscle 1:9. https://doi.org/10.1186/2044-5040-1-9
Geis T, Marquard K, Rodl T, Reihle C, Schirmer S, von Kalle T, Bornemann A, Hehr U, Blankenburg M (2013) Homozygous dystroglycan mutation associated with a novel muscle-eye-brain disease-like phenotype with multicystic leucodystrophy. Neurogenetics 14:205–213. https://doi.org/10.1007/s10048-013-0374-9
Geng LN, Yao Z, Snider L, Fong AP, Cech JN, Young JM, van der Maarel SM, Ruzzo WL, Gentleman RC, Tawil R, Tapscott SJ (2012) DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 22:38–51. https://doi.org/10.1016/j.devcel.2011.11.013
Giacomotto J, Rinkwitz S, Becker TS (2015) Effective heritable gene knockdown in zebrafish using synthetic microRNAs. Nat Commun 6:7378. https://doi.org/10.1038/ncomms8378
Goody MF, Kelly MW, Reynolds CJ, Khalil A, Crawford BD, Henry CA (2012) NAD+ biosynthesis ameliorates a zebrafish model of muscular dystrophy. PLoS Biol 10:e1001409. https://doi.org/10.1371/journal.pbio.1001409
Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Nusslein-Volhard C (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123:399–413
Gupta VA, Beggs AH (2014) Kelch proteins: emerging roles in skeletal muscle development and diseases. Skelet Muscle 4:11. https://doi.org/10.1186/2044-5040-4-11
Gupta V, Kawahara G, Gundry SR, Chen AT, Lencer WI, Zhou Y, Zon LI, Kunkel LM, Beggs AH (2011) The zebrafish dag1 mutant: a novel genetic model for dystroglycanopathies. Hum Mol Genet 20:1712–1725. https://doi.org/10.1093/hmg/ddr047
Gupta VA, Kawahara G, Myers JA, Chen AT, Hall TE, Manzini MC, Currie PD, Zhou Y, Zon LI, Kunkel LM, Beggs AH (2012) A splice site mutation in laminin-alpha2 results in a severe muscular dystrophy and growth abnormalities in zebrafish. PLoS One 7:e43794. https://doi.org/10.1371/journal.pone.0043794
Gupta VA, Ravenscroft G, Shaheen R, Todd EJ, Swanson LC, Shiina M, Ogata K, Hsu C, Clarke NF, Darras BT, Farrar MA, Hashem A, Manton ND, Muntoni F, North KN, Sandaradura SA, Nishino I, Hayashi YK, Sewry CA, Thompson EM, Yau KS, Brownstein CA, Yu TW, Allcock RJ, Davis MR, Wallgren-Pettersson C, Matsumoto N, Alkuraya FS, Laing NG, Beggs AH (2013) Identification of KLHL41 mutations implicates BTB-Kelch-mediated ubiquitination as an alternate pathway to myofibrillar disruption in nemaline myopathy. Am J Hum Genet 93:1108–1117. https://doi.org/10.1016/j.ajhg.2013.10.020
Guyon JR, Mosley AN, Zhou Y, O’Brien KF, Sheng X, Chiang K, Davidson AJ, Volinski JM, Zon LI, Kunkel LM (2003) The dystrophin associated protein complex in zebrafish. Hum Mol Genet 12:601–615. https://doi.org/10.1093/hmg/ddg071
Guyon JR, Mosley AN, Jun SJ, Montanaro F, Steffen LS, Zhou Y, Nigro V, Zon LI, Kunkel LM (2005) Delta-sarcoglycan is required for early zebrafish muscle organization. Exp Cell Res 304:105–115. https://doi.org/10.1016/j.yexcr.2004.10.032
Guyon JR, Goswami J, Jun SJ, Thorne M, Howell M, Pusack T, Kawahara G, Steffen LS, Galdzicki M, Kunkel LM (2009) Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin. Hum Mol Genet 18:202–211. https://doi.org/10.1093/hmg/ddn337
Hall TE, Bryson-Richardson RJ, Berger S, Jacoby AS, Cole NJ, Hollway GE, Berger J, Currie PD (2007) The zebrafish candyfloss mutant implicates extracellular matrix adhesion failure in laminin alpha2-deficient congenital muscular dystrophy. Proc Natl Acad Sci USA 104:7092–7097. https://doi.org/10.1073/pnas.0700942104
Hara Y, Balci-Hayta B, Yoshida-Moriguchi T, Kanagawa M, Beltran-Valero de Bernabe D, Gundesli H, Willer T, Satz JS, Crawford RW, Burden SJ, Kunz S, Oldstone MB, Accardi A, Talim B, Muntoni F, Topaloglu H, Dincer P, Campbell KP (2011) A dystroglycan mutation associated with limb-girdle muscular dystrophy. N Engl J Med 364:939–946. https://doi.org/10.1056/NEJMoa1006939
Helbling-Leclerc A, Zhang X, Topaloglu H, Cruaud C, Tesson F, Weissenbach J, Tome FM, Schwartz K, Fardeau M, Tryggvason K et al (1995) Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat Genet 11:216–218. https://doi.org/10.1038/ng1095-216
Higashijima S, Okamoto H, Ueno N, Hotta Y, Eguchi G (1997) High-frequency generation of transgenic zebrafish which reliably express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev Biol 192:289–299
Hirata H, Watanabe T, Hatakeyama J, Sprague SM, Saint-Amant L, Nagashima A, Cui WW, Zhou W, Kuwada JY (2007) Zebrafish relatively relaxed mutants have a ryanodine receptor defect, show slow swimming and provide a model of multi-minicore disease. Development 134:2771–2781. https://doi.org/10.1242/dev.004531
Hisano Y, Sakuma T, Nakade S, Ohga R, Ota S, Okamoto H, Yamamoto T, Kawahara A (2015) Precise in-frame integration of exogenous DNA mediated by CRISPR/Cas9 system in zebrafish. Sci Rep 5:8841. https://doi.org/10.1038/srep08841
Horstick EJ, Linsley JW, Dowling JJ, Hauser MA, McDonald KK, Ashley-Koch A, Saint-Amant L, Satish A, Cui WW, Zhou W, Sprague SM, Stamm DS, Powell CM, Speer MC, Franzini-Armstrong C, Hirata H, Kuwada JY (2013) Stac3 is a component of the excitation-contraction coupling machinery and mutated in Native American myopathy. Nat Commun 4:1952. https://doi.org/10.1038/ncomms2952
Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch GJ, White S, Chow W, Kilian B, Quintais LT, Guerra-Assuncao JA, Zhou Y, Gu Y, Yen J, Vogel JH, Eyre T, Redmond S, Banerjee R, Chi J, Fu B, Langley E, Maguire SF, Laird GK, Lloyd D, Kenyon E, Donaldson S, Sehra H, Almeida-King J, Loveland J, Trevanion S, Jones M, Quail M, Willey D, Hunt A, Burton J, Sims S, McLay K, Plumb B, Davis J, Clee C, Oliver K, Clark R, Riddle C, Elliot D, Threadgold G, Harden G, Ware D, Begum S, Mortimore B, Kerry G, Heath P, Phillimore B, Tracey A, Corby N, Dunn M, Johnson C, Wood J, Clark S, Pelan S, Griffiths G, Smith M, Glithero R, Howden P, Barker N, Lloyd C, Stevens C, Harley J, Holt K, Panagiotidis G, Lovell J, Beasley H, Henderson C, Gordon D, Auger K, Wright D, Collins J, Raisen C, Dyer L, Leung K, Robertson L, Ambridge K, Leongamornlert D, McGuire S, Gilderthorp R, Griffiths C, Manthravadi D, Nichol S, Barker G et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503. https://doi.org/10.1038/nature12111
Hwang JH, Zorzato F, Clarke NF, Treves S (2012) Mapping domains and mutations on the skeletal muscle ryanodine receptor channel. Trends Mol Med 18:644–657. https://doi.org/10.1016/j.molmed.2012.09.006
Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31:227–229. https://doi.org/10.1038/nbt.2501
Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696–702. https://doi.org/10.1038/355696a0
Jurynec MJ, Xia R, Mackrill JJ, Gunther D, Crawford T, Flanigan KM, Abramson JJ, Howard MT, Grunwald DJ (2008) Selenoprotein N is required for ryanodine receptor calcium release channel activity in human and zebrafish muscle. Proc Natl Acad Sci USA 105:12485–12490. https://doi.org/10.1073/pnas.0806015105
Kaplan JC, Hamroun D (2015) The 2016 version of the gene table of monogenic neuromuscular disorders (nuclear genome). Neuromuscul Disord 25:991–1020. https://doi.org/10.1016/j.nmd.2015.10.010
Kawahara G, Guyon JR, Nakamura Y, Kunkel LM (2010) Zebrafish models for human FKRP muscular dystrophies. Hum Mol Genet 19:623–633. https://doi.org/10.1093/hmg/ddp528
Kawahara G, Karpf JA, Myers JA, Alexander MS, Guyon JR, Kunkel LM (2011a) Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 108:5331–5336. https://doi.org/10.1073/pnas.1102116108
Kawahara G, Serafini PR, Myers JA, Alexander MS, Kunkel LM (2011b) Characterization of zebrafish dysferlin by morpholino knockdown. Biochem Biophys Res Commun 413:358–363. https://doi.org/10.1016/j.bbrc.2011.08.105
Kimura Y, Hisano Y, Kawahara A, Higashijima S (2014) Efficient generation of knock-in transgenic zebrafish carrying reporter/driver genes by CRISPR/Cas9-mediated genome engineering. Sci Rep 4:6545. https://doi.org/10.1038/srep06545
Kobayashi I, Kobayashi-Sun J, Kim AD, Pouget C, Fujita N, Suda T, Traver D (2014) Jam1a-Jam2a interactions regulate haematopoietic stem cell fate through Notch signalling. Nature 512:319–323. https://doi.org/10.1038/nature13623
Koenig M, Hoffman EP, Bertelson CJ, Monaco AP, Feener C, Kunkel LM (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50:509–517
Koshimizu E, Imamura S, Qi J, Toure J, Valdez DM Jr, Carr CE, Hanai J, Kishi S (2011) Embryonic senescence and laminopathies in a progeroid zebrafish model. PLoS One 6:e17688. https://doi.org/10.1371/journal.pone.0017688
Kowaljow V, Marcowycz A, Ansseau E, Conde CB, Sauvage S, Matteotti C, Arias C, Corona ED, Nunez NG, Leo O, Wattiez R, Figlewicz D, Laoudj-Chenivesse D, Belayew A, Coppee F, Rosa AL (2007) The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul Disord 17:611–623. https://doi.org/10.1016/j.nmd.2007.04.002
Li M, Arner A (2015) Immobilization of Dystrophin and Laminin alpha2-Chain Deficient Zebrafish Larvae In Vivo Prevents the Development of Muscular Dystrophy. PLoS One 10:e0139483. https://doi.org/10.1371/journal.pone.0139483
Li M, Andersson-Lendahl M, Sejersen T, Arner A (2013) Knockdown of desmin in zebrafish larvae affects interfilament spacing and mechanical properties of skeletal muscle. J Gen Physiol 141:335–345. https://doi.org/10.1085/jgp.201210915
Li M, Andersson-Lendahl M, Sejersen T, Arner A (2014) Muscle dysfunction and structural defects of dystrophin-null sapje mutant zebrafish larvae are rescued by ataluren treatment. FASEB J 28:1593–1599. https://doi.org/10.1096/fj.13-240044
Lim LE, Duclos F, Broux O, Bourg N, Sunada Y, Allamand V, Meyer J, Richard I, Moomaw C, Slaughter C et al (1995) Beta-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12. Nat Genet 11:257–265. https://doi.org/10.1038/ng1195-257
Lin YY, White RJ, Torelli S, Cirak S, Muntoni F, Stemple DL (2011) Zebrafish Fukutin family proteins link the unfolded protein response with dystroglycanopathies. Hum Mol Genet 20:1763–1775. https://doi.org/10.1093/hmg/ddr059
Lipscomb L, Piggott RW, Emmerson T, Winder SJ (2016) Dasatinib as a treatment for Duchenne muscular dystrophy. Hum Mol Genet 25:266–274. https://doi.org/10.1093/hmg/ddv469
Lo HP, Nixon SJ, Hall TE, Cowling BS, Ferguson C, Morgan GP, Schieber NL, Fernandez-Rojo MA, Bastiani M, Floetenmeyer M, Martel N, Laporte J, Pilch PF, Parton RG (2015) The caveolin-cavin system plays a conserved and critical role in mechanoprotection of skeletal muscle. J Cell Biol 210:833–849. https://doi.org/10.1083/jcb.201501046
Manzini MC, Tambunan DE, Hill RS, Yu TW, Maynard TM, Heinzen EL, Shianna KV, Stevens CR, Partlow JN, Barry BJ, Rodriguez J, Gupta VA, Al-Qudah AK, Eyaid WM, Friedman JM, Salih MA, Clark R, Moroni I, Mora M, Beggs AH, Gabriel SB, Walsh CA (2012) Exome sequencing and functional validation in zebrafish identify GTDC2 mutations as a cause of Walker-Warburg syndrome. Am J Hum Genet 91:541–547. https://doi.org/10.1016/j.ajhg.2012.07.009
Marchese M, Pappalardo A, Baldacci J, Verri T, Doccini S, Cassandrini D, Bruno C, Fiorillo C, Garcia-Gil M, Bertini E, Pitto L, Santorelli FM (2016) Dolichol-phosphate mannose synthase depletion in zebrafish leads to dystrophic muscle with hypoglycosylated alpha-dystroglycan. Biochem Biophys Res Commun 477:137–143. https://doi.org/10.1016/j.bbrc.2016.06.033
Mitsuhashi H, Mitsuhashi S, Lynn-Jones T, Kawahara G, Kunkel LM (2013) Expression of DUX4 in zebrafish development recapitulates facioscapulohumeral muscular dystrophy. Hum Mol Genet 22:568–577. https://doi.org/10.1093/hmg/dds467
Miyagoe Y, Hanaoka K, Nonaka I, Hayasaka M, Nabeshima Y, Arahata K, Nabeshima Y, Takeda S (1997) Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett 415:33–39
Nam TS, Li W, Heo SH, Lee KH, Cho A, Shin JH, Kim YO, Chae JH, Kim DS, Kim MK, Choi SY (2015) A novel mutation in DNAJB6, p.(Phe91Leu), in childhood-onset LGMD1D with a severe phenotype. Neuromuscul Disord 25:843–851. https://doi.org/10.1016/j.nmd.2015.08.002
Nance JR, Dowling JJ, Gibbs EM, Bonnemann CG (2012) Congenital myopathies: an update. Curr Neurol Neurosci Rep 12:165–174. https://doi.org/10.1007/s11910-012-0255-x
Nigro V, de Sa ME, Piluso G, Vainzof M, Belsito A, Politano L, Puca AA, Passos-Bueno MR, Zatz M (1996) Autosomal recessive limb-girdle muscular dystrophy, LGMD2F, is caused by a mutation in the delta-sarcoglycan gene. Nat Genet 14:195–198. https://doi.org/10.1038/ng1096-195
Nishikawa A, Mitsuhashi S, Miyata N, Nishino I (2017) Targeted massively parallel sequencing and histological assessment of skeletal muscles for the molecular diagnosis of inherited muscle disorders. J Med Genet 54:104–110. https://doi.org/10.1136/jmedgenet-2016-104073
Nixon SJ, Wegner J, Ferguson C, Mery PF, Hancock JF, Currie PD, Key B, Westerfield M, Parton RG (2005) Zebrafish as a model for caveolin-associated muscle disease; caveolin-3 is required for myofibril organization and muscle cell patterning. Hum Mol Genet 14:1727–1743. https://doi.org/10.1093/hmg/ddi179
Noguchi S, McNally EM, Ben Othmane K, Hagiwara Y, Mizuno Y, Yoshida M, Yamamoto H, Bonnemann CG, Gussoni E, Denton PH, Kyriakides T, Middleton L, Hentati F, Ben Hamida M, Nonaka I, Vance JM, Kunkel LM, Ozawa E (1995) Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science 270:819–822
Nowak KJ, Davies KE (2004) Duchenne muscular dystrophy and dystrophin: pathogenesis and opportunities for treatment. EMBO Rep 5:872–876. https://doi.org/10.1038/sj.embor.7400221
Ozawa E, Yoshida M, Suzuki A, Mizuno Y, Hagiwara Y, Noguchi S (1995) Dystrophin-associated proteins in muscular dystrophy. Hum Mol Genet 4:1711–1716
Parsons MJ, Campos I, Hirst EM, Stemple DL (2002) Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development 129:3505–3512
Postel R, Vakeel P, Topczewski J, Knoll R, Bakkers J (2008) Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin-ECM adhesion complex. Dev Biol 318:92–101. https://doi.org/10.1016/j.ydbio.2008.03.024
Praissman JL, Willer T, Sheikh MO, Toi A, Chitayat D, Lin YY, Lee H, Stalnaker SH, Wang S, Prabhakar PK, Nelson SF, Stemple DL, Moore SA, Moremen KW, Campbell KP, Wells L (2016) The functional O-mannose glycan on alpha-dystroglycan contains a phospho-ribitol primed for matriglycan addition. Elife:5. https://doi.org/10.7554/eLife.14473
Radev Z, Hermel JM, Elipot Y, Bretaud S, Arnould S, Duchateau P, Ruggiero F, Joly JS, Sohm F (2015) A TALEN-Exon Skipping Design for a Bethlem Myopathy Model in Zebrafish. PLoS One 10:e0133986. https://doi.org/10.1371/journal.pone.0133986
Rahimov F, Kunkel LM (2013) The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy. J Cell Biol 201:499–510. https://doi.org/10.1083/jcb.201212142
Ravenscroft G, Miyatake S, Lehtokari VL, Todd EJ, Vornanen P, Yau KS, Hayashi YK, Miyake N, Tsurusaki Y, Doi H, Saitsu H, Osaka H, Yamashita S, Ohya T, Sakamoto Y, Koshimizu E, Imamura S, Yamashita M, Ogata K, Shiina M, Bryson-Richardson RJ, Vaz R, Ceyhan O, Brownstein CA, Swanson LC, Monnot S, Romero NB, Amthor H, Kresoje N, Sivadorai P, Kiraly-Borri C, Haliloglu G, Talim B, Orhan D, Kale G, Charles AK, Fabian VA, Davis MR, Lammens M, Sewry CA, Manzur A, Muntoni F, Clarke NF, North KN, Bertini E, Nevo Y, Willichowski E, Silberg IE, Topaloglu H, Beggs AH, Allcock RJ, Nishino I, Wallgren-Pettersson C, Matsumoto N, Laing NG (2013) Mutations in KLHL40 are a frequent cause of severe autosomal-recessive nemaline myopathy. Am J Hum Genet 93:6–18. https://doi.org/10.1016/j.ajhg.2013.05.004
Roberds SL, Leturcq F, Allamand V, Piccolo F, Jeanpierre M, Anderson RD, Lim LE, Lee JC, Tome FM, Romero NB et al (1994) Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell 78:625–633
Roostalu U, Strähle U (2012) In vivo imaging of molecular interactions at damaged sarcolemma. Dev Cell 22:515–529. https://doi.org/10.1016/j.devcel.2011.12.008
Roscioli T, Kamsteeg EJ, Buysse K, Maystadt I, van Reeuwijk J, van den Elzen C, van Beusekom E, Riemersma M, Pfundt R, Vissers LE, Schraders M, Altunoglu U, Buckley MF, Brunner HG, Grisart B, Zhou H, Veltman JA, Gilissen C, Mancini GM, Delree P, Willemsen MA, Ramadza DP, Chitayat D, Bennett C, Sheridan E, Peeters EA, Tan-Sindhunata GM, de Die-Smulders CE, Devriendt K, Kayserili H, El-Hashash OA, Stemple DL, Lefeber DJ, Lin YY, van Bokhoven H (2012) Mutations in ISPD cause Walker-Warburg syndrome and defective glycosylation of alpha-dystroglycan. Nat Genet 44:581–585. https://doi.org/10.1038/ng.2253
Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37:622–632
Sarparanta J, Jonson PH, Golzio C, Sandell S, Luque H, Screen M, McDonald K, Stajich JM, Mahjneh I, Vihola A, Raheem O, Penttila S, Lehtinen S, Huovinen S, Palmio J, Tasca G, Ricci E, Hackman P, Hauser M, Katsanis N, Udd B (2012) Mutations affecting the cytoplasmic functions of the co-chaperone DNAJB6 cause limb-girdle muscular dystrophy. Nat Genet 44(450-5):S1–S2. https://doi.org/10.1038/ng.1103
Schindler RF, Scotton C, Zhang J, Passarelli C, Ortiz-Bonnin B, Simrick S, Schwerte T, Poon KL, Fang M, Rinne S, Froese A, Nikolaev VO, Grunert C, Muller T, Tasca G, Sarathchandra P, Drago F, Dallapiccola B, Rapezzi C, Arbustini E, Di Raimo FR, Neri M, Selvatici R, Gualandi F, Fattori F, Pietrangelo A, Li W, Jiang H, Xu X, Bertini E, Decher N, Wang J, Brand T, Ferlini A (2016) POPDC1(S201F) causes muscular dystrophy and arrhythmia by affecting protein trafficking. J Clin Invest 126:239–253. https://doi.org/10.1172/JCI79562
Seger C, Hargrave M, Wang X, Chai RJ, Elworthy S, Ingham PW (2011) Analysis of Pax7 expressing myogenic cells in zebrafish muscle development, injury, and models of disease. Dev Dyn 240:2440–2451. https://doi.org/10.1002/dvdy.22745
Sewry CA, Jimenez-Mallebrera C, Muntoni F (2008) Congenital myopathies. Curr Opin Neurol 21:569–575. https://doi.org/10.1097/WCO.0b013e32830f93c7
Shih YH, Dvornikov AV, Zhu P, Ma X, Kim M, Ding Y, Xu X (2016) Exon- and contraction-dependent functions of titin in sarcomere assembly. Development 143:4713–4722. https://doi.org/10.1242/dev.139246
Smith LL, Gupta VA, Beggs AH (2014) Bridging integrator 1 (Bin1) deficiency in zebrafish results in centronuclear myopathy. Hum Mol Genet 23:3566–3578. https://doi.org/10.1093/hmg/ddu067
Smith SJ, Wang JC, Gupta VA, Dowling JJ (2017) A novel early onset phenotype in a zebrafish model of merosin deficient congenital muscular dystrophy. PLoS One 12:e0172648. https://doi.org/10.1371/journal.pone.0172648
Steffen LS, Guyon JR, Vogel ED, Howell MH, Zhou Y, Weber GJ, Zon LI, Kunkel LM (2007) The zebrafish runzel muscular dystrophy is linked to the titin gene. Dev Biol 309:180–192. https://doi.org/10.1016/j.ydbio.2007.06.015
Stevens E, Carss KJ, Cirak S, Foley AR, Torelli S, Willer T, Tambunan DE, Yau S, Brodd L, Sewry CA, Feng L, Haliloglu G, Orhan D, Dobyns WB, Enns GM, Manning M, Krause A, Salih MA, Walsh CA, Hurles M, Campbell KP, Manzini MC, Consortium UK, Stemple D, Lin YY, Muntoni F (2013) Mutations in B3GALNT2 cause congenital muscular dystrophy and hypoglycosylation of alpha-dystroglycan. Am J Hum Genet 92:354–365. https://doi.org/10.1016/j.ajhg.2013.01.016
Sztal TE, Zhao M, Williams C, Oorschot V, Parslow AC, Giousoh A, Yuen M, Hall TE, Costin A, Ramm G, Bird PI, Busch-Nentwich EM, Stemple DL, Currie PD, Cooper ST, Laing NG, Nowak KJ, Bryson-Richardson RJ (2015) Zebrafish models for nemaline myopathy reveal a spectrum of nemaline bodies contributing to reduced muscle function. Acta Neuropathol 130:389–406. https://doi.org/10.1007/s00401-015-1430-3
Telfer WR, Busta AS, Bonnemann CG, Feldman EL, Dowling JJ (2010) Zebrafish models of collagen VI-related myopathies. Hum Mol Genet 19:2433–2444. https://doi.org/10.1093/hmg/ddq126
Telfer WR, Nelson DD, Waugh T, Brooks SV, Dowling JJ (2012) Neb: a zebrafish model of nemaline myopathy due to nebulin mutation. Dis Model Mech 5:389–396. https://doi.org/10.1242/dmm.008631
Thornhill P, Bassett D, Lochmuller 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. https://doi.org/10.1093/brain/awn078
Turk R, Sterrenburg E, de Meijer EJ, van Ommen GJ, den Dunnen JT, t Hoen PA (2005) Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genomics 6:98. https://doi.org/10.1186/1471-2164-6-98
Vieira NM, Naslavsky MS, Licinio L, Kok F, Schlesinger D, Vainzof M, Sanchez N, Kitajima JP, Gal L, Cavacana N, Serafini PR, Chuartzman S, Vasquez C, Mimbacas A, Nigro V, Pavanello RC, Schuldiner M, Kunkel LM, Zatz M (2014) A defect in the RNA-processing protein HNRPDL causes limb-girdle muscular dystrophy 1G (LGMD1G). Hum Mol Genet 23:4103–4110. https://doi.org/10.1093/hmg/ddu127
Vogel B, Meder B, Just S, Laufer C, Berger I, Weber S, Katus HA, Rottbauer W (2009) In-vivo characterization of human dilated cardiomyopathy genes in zebrafish. Biochem Biophys Res Commun 390:516–522. https://doi.org/10.1016/j.bbrc.2009.09.129
Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, Ladner KJ, Guttridge D, Yang J, Harper SQ (2011) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol 69:540–552. https://doi.org/10.1002/ana.22275
Waugh TA, Horstick E, Hur J, Jackson SW, Davidson AE, Li X, Dowling JJ (2014) Fluoxetine prevents dystrophic changes in a zebrafish model of Duchenne muscular dystrophy. Hum Mol Genet 23:4651–4662. https://doi.org/10.1093/hmg/ddu185
Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, Campbell KP (1997) Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum Mol Genet 6:831–841
Winder SJ, Lipscomb L, Angela Parkin C, Juusola M (2011) The proteasomal inhibitor MG132 prevents muscular dystrophy in zebrafish. PLoS Curr 3:RRN1286. https://doi.org/10.1371/currents.RRN1286
Wood AJ, Muller JS, Jepson CD, Laval SH, Lochmuller H, Bushby K, Barresi R, Straub V (2011) Abnormal vascular development in zebrafish models for fukutin and FKRP deficiency. Hum Mol Genet 20:4879–4890. https://doi.org/10.1093/hmg/ddr426
Xu C, Tabebordbar M, Iovino S, Ciarlo C, Liu J, Castiglioni A, Price E, Liu M, Barton ER, Kahn CR, Wagers AJ, Zon LI (2013) A zebrafish embryo culture system defines factors that promote vertebrate myogenesis across species. Cell 155:909–921. https://doi.org/10.1016/j.cell.2013.10.023
Yoshida-Moriguchi T, Campbell KP (2015) Matriglycan: a novel polysaccharide that links dystroglycan to the basement membrane. Glycobiology 25:702–713. https://doi.org/10.1093/glycob/cwv021
Yuen M, Sandaradura SA, Dowling JJ, Kostyukova AS, Moroz N, Quinlan KG, Lehtokari VL, Ravenscroft G, Todd EJ, Ceyhan-Birsoy O, Gokhin DS, Maluenda J, Lek M, Nolent F, Pappas CT, Novak SM, D'Amico A, Malfatti E, Thomas BP, Gabriel SB, Gupta N, Daly MJ, Ilkovski B, Houweling PJ, Davidson AE, Swanson LC, Brownstein CA, Gupta VA, Medne L, Shannon P, Martin N, Bick DP, Flisberg A, Holmberg E, Van den Bergh P, Lapunzina P, Waddell LB, Sloboda DD, Bertini E, Chitayat D, Telfer WR, Laquerriere A, Gregorio CC, Ottenheijm CA, Bonnemann CG, Pelin K, Beggs AH, Hayashi YK, Romero NB, Laing NG, Nishino I, Wallgren-Pettersson C, Melki J, Fowler VM, MacArthur DG, North KN, Clarke NF (2014) Leiomodin-3 dysfunction results in thin filament disorganization and nemaline myopathy. J Clin Invest 124:4693–4708. https://doi.org/10.1172/JCI75199
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. Hum Mol Genet 18:4130–4140. https://doi.org/10.1093/hmg/ddp362
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Mitsuhashi, H. (2018). Zebrafish Models of Muscular Dystrophies and Congenital Myopathies. In: Hirata, H., Iida, A. (eds) Zebrafish, Medaka, and Other Small Fishes. Springer, Singapore. https://doi.org/10.1007/978-981-13-1879-5_10
Download citation
DOI: https://doi.org/10.1007/978-981-13-1879-5_10
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-13-1878-8
Online ISBN: 978-981-13-1879-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)