Swimming into prominence: The zebrafish as a valuable tool for studying human myopathies and muscular dystrophies

FEBS Journal

Volumn 280, Issue 17, 2013, Pages 4187-4197

  Gibbs, Elizabeth M ^a   Horstick, Eric J ^a   Dowling, James J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

birefringence; drug discovery; muscular dystrophy; myopathy; zebrafish

Indexed keywords

ACETYLCYSTEINE; ACTININ; ALPHA DYSTROGLYCAN; ALPHA DYSTROGLYCAN 1; ALPHA6 INTEGRIN; ALPHA7 INTEGRIN; BIOLOGICAL MARKER; CAPPED RNA; CONNECTIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; LAMININ ALPHA2; MORPHOLINO OLIGONUCLEOTIDE; NEBULIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; NICOTINIC ACID; PHOSPHODIESTERASE INHIBITOR; RYANODINE RECEPTOR 1; UNCLASSIFIED DRUG; VITAMIN; ZINC FINGER NUCLEASE;

ANTIOXIDANT ACTIVITY; B3GNT1 GENE; BIREFRINGENCE; CALCIUM TRANSPORT; CCDC78 GENE; DISEASE MODEL; DNA BINDING; DRUG SCREENING; DRUG TARGETING; DUCHENNE MUSCULAR DYSTROPHY; EMBRYO DEVELOPMENT; EXCITATION CONTRACTION COUPLING; EXOME; EXON; GENE; GENE CONTROL; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE INSERTION; GENE SEQUENCE; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC MANIPULATION; GENETIC MODEL; GENOME; GLYCOSYLATION; GTDC2 GENE; HUMAN; INTRON; ISPD GENE; LIMB GIRDLE MUSCULAR DYSTROPHY; MUSCLE FATIGUE; MUSCLE RELAXATION; MUSCULAR DYSTROPHY; MUTAGENESIS; MUTATIONAL ANALYSIS; NEMALINE MYOPATHY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA SPLICING; SARCOMERE; SEQUENCE ANALYSIS; SWIMMING; UPREGULATION; WALKER WARBURG SYNDROME; ZEBRA FISH;

BIREFRINGENCE; DRUG DISCOVERY; MUSCULAR DYSTROPHY; MYOPATHY; ZEBRAFISH;

ANIMALS; BIOMEDICAL RESEARCH; DISEASE MODELS, ANIMAL; HUMANS; MUSCULAR DISEASES; MUSCULAR DYSTROPHIES; ZEBRAFISH;

DANIO RERIO;

EID: 84882655566     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12412     Document Type: Review

References (75)

1. Lieschke GJ, &, Currie PD, (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8, 353-367.
2. Santoriello C, &, Zon LI, (2012) Hooked! Modeling human disease in zebrafish. J Clin Invest 122, 2337-2343.
3. Parsons MJ, Campos I, Hirst EM, &, Stemple DL, (2002) Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development 129, 3505-3512.
4. 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.
5. 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.
6. Dou Y, Andersson-Lendahl M, &, Arner A, (2008) Structure and function of skeletal muscle in zebrafish early larvae. J Gen Physiol 131, 445-453.
7. 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.
8. 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.
9. Telfer WR, Busta AS, Bonnemann CG, Feldman EL, &, Dowling JJ, (2010) Zebrafish models of collagen VI-related myopathies. Hum Mol Genet 19, 2433-2444.
10. Berger J, &, Currie PD, (2012) Zebrafish models flex their muscles to shed light on muscular dystrophies. Dis Model Mech 5, 726-732.
11. 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.
12. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, &, Barnard PJ, (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244, 1578-1580.
13. 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.
14. Granato M, van Eeden FJ, Schach U, Trowe T, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, et al,. (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development 123, 399-413.
15. Haffter P, Granato M, Brand M, Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, van Eeden FJ, Jiang YJ, Heisenberg CP, et al,. (1996) The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1-36.
16. 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.
17. Gupta VA, Kawahara G, Myers JA, Chen AT, Hall TE, Manzini MC, Currie PD, Zhou Y, Zon LI, Kunkel LM, et al,. (2012) A splice site mutation in laminin-alpha2 results in a severe muscular dystrophy and growth abnormalities in zebrafish. PLoS One 7, e43794.
18. Hirata H, Wen H, Kawakami Y, Naganawa Y, Ogino K, Yamada K, Saint-Amant L, Low SE, Cui WW, Zhou W, et al,. (2012) Connexin 39.9 protein is necessary for coordinated activation of slow-twitch muscle and normal behavior in zebrafish. J Biol Chem 287, 1080-1089.
19. Saint-Amant L, Sprague SM, Hirata H, Li Q, Cui WW, Zhou W, Poudou O, Hume RI, &, Kuwada JY, (2008) The zebrafish ennui behavioral mutation disrupts acetylcholine receptor localization and motor axon stability. Dev Neurobiol 68, 45-61.
20. 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.
21. 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.
22. Ekker SC, (2008) Zinc finger-based knockout punches for zebrafish genes. Zebrafish 5, 121-123.
23. Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, &, Yeh JR, (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29, 697-698.
24. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG II, Tan W, Penheiter SG, Ma AC, Leung AY, et al,. (2012) In vivo genome editing using a high-efficiency TALEN system. Nature 491, 114-118.
25. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, et al,. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
26. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, &, Church GM, (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826.
27. 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.
28. Chang N, Sun C, Gao L, Zhu D, Xu X, Zhu X, Xiong JW, &, Xi JJ, (2013) Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res 23, 465-472.
29. Saint-Amant L, &, Drapeau P, (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37, 622-632.
30. 2+ pump SERCA1. Development 131, 5457-5468.
31. Buss RR, &, Drapeau P, (2000) Physiological properties of zebrafish embryonic red and white muscle fibers during early development. J Neurophysiol 84, 1545-1557.
32. Roostalu U, &, Strahle U, (2012) In vivo imaging of molecular interactions at damaged sarcolemma. Dev Cell 22, 515-529.
33. 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.
34. 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.
35. Horstick EJ, Gibbs EM, Li X, Davidson AE, and, Dowling JJ, (2013). Analysis of Embryonic and Larval Zebrafish Skeletal Myofibers from Dissociated Preparations. Journal of Visualized Experiments. In press.
36. Lin YY, (2012) Muscle diseases in the zebrafish. Neuromuscul Disord 22, 673-684.
37. Majczenko K, Davidson AE, Camelo-Piragua S, Agrawal PB, Manfready RA, Li X, Joshi S, Xu J, Peng W, Beggs AH, et al,. (2012) Dominant mutation of CCDC78 in a unique congenital myopathy with prominent internal nuclei and atypical cores. Am J Hum Genet 91, 365-371.
38. 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.
39. Willer T, Prados B, Falcon-Perez JM, Renner-Muller I, Przemeck GK, Lommel M, Coloma A, Valero MC, de Angelis MH, Tanner W, et al,. (2004) Targeted disruption of the Walker-Warburg syndrome gene Pomt1 in mouse results in embryonic lethality. Proc Natl Acad Sci USA 101, 14126-14131.
40. Kurahashi H, Taniguchi M, Meno C, Taniguchi Y, Takeda S, Horie M, Otani H, &, Toda T, (2005) Basement membrane fragility underlies embryonic lethality in fukutin-null mice. Neurobiol Dis 19, 208-217.
41. 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.
42. Kawahara G, Guyon JR, Nakamura Y, &, Kunkel LM, (2010) Zebrafish models for human FKRP muscular dystrophies. Hum Mol Genet 19, 623-633.
43. Moore CJ, Goh HT, &, Hewitt JE, (2008) Genes required for functional glycosylation of dystroglycan are conserved in zebrafish. Genomics 92, 159-167.
44. 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.
45. Manzini MC, Tambunan DE, Hill RS, Yu TW, Maynard TM, Heinzen EL, Shianna KV, Stevens CR, Partlow JN, Barry BJ, et al,. (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.
46. Buysse K, Riemersma M, Powell G, van Reeuwijk J, Chitayat D, Roscioli T, Kamsteeg EJ, van den Elzen C, van Beusekom E, Blaser S, et al,. (2013) Missense mutations in beta-1,3-N-acetylglucosaminyltransferase 1 (B3GNT1) cause Walker-Warburg syndrome. Hum Mol Genet 22, 1746-1754.
47. Roscioli T, Kamsteeg EJ, Buysse K, Maystadt I, van Reeuwijk J, van den Elzen C, van Beusekom E, Riemersma M, Pfundt R, &, Vissers LE, et al,. (2012) Mutations in ISPD cause Walker-Warburg syndrome and defective glycosylation of alpha-dystroglycan. Nat Genet 44, 581-585.
48. + biosynthesis ameliorates a zebrafish model of muscular dystrophy. PLoS Biol 10, e1001409.
49. Zhang Y, Chen HS, Khanna VK, De Leon S, Phillips MS, Schappert K, Britt BA, Browell AK, &, MacLennan DH, (1993) A mutation in the human ryanodine receptor gene associated with central core disease. Nat Genet 5, 46-50.
50. Jungbluth H, Zhou H, Sewry CA, Robb S, Treves S, Bitoun M, Guicheney P, Buj-Bello A, Bonnemann C, &, Muntoni F, (2007) Centronuclear myopathy due to a de novo dominant mutation in the skeletal muscle ryanodine receptor (RYR1) gene. Neuromuscul Disord 17, 338-345.
51. Wilmshurst JM, Lillis S, Zhou H, Pillay K, Henderson H, Kress W, Muller CR, Ndondo A, Cloke V, Cullup T, et al,. (2010) RYR1 mutations are a common cause of congenital myopathies with central nuclei. Ann Neurol 68, 717-726.
52. Bevilacqua JA, Monnier N, Bitoun M, Eymard B, Ferreiro A, Monges S, Lubieniecki F, Taratuto AL, Laquerriere A, Claeys KG, et al,. (2011) Recessive RYR1 mutations cause unusual congenital myopathy with prominent nuclear internalization and large areas of myofibrillar disorganization. Neuropathol Appl Neurobiol 37, 271-284.
53. Dowling JJ, Lillis S, Amburgey K, Zhou H, Al-Sarraj S, Buk SJ, Wraige E, Chow G, Abbs S, Leber S, et al,. (2011) King-Denborough syndrome with and without mutations in the skeletal muscle ryanodine receptor (RYR1) gene. Neuromuscul Disord 21, 420-427.
54. Monnier N, Ferreiro A, Marty I, Labarre-Vila A, Mezin P, &, Lunardi J, (2003) A homozygous splicing mutation causing a depletion of skeletal muscle RYR1 is associated with multi-minicore disease congenital myopathy with ophthalmoplegia. Hum Mol Genet 12, 1171-1178.
55. Dowling JJ, Arbogast S, Hur J, Nelson DD, McEvoy A, Waugh T, Marty I, Lunardi J, Brooks SV, Kuwada JY, et al,. (2012) Oxidative stress and successful antioxidant treatment in models of RYR1-related myopathy. Brain 135, 1115-1127.
56. White RM, Cech J, Ratanasirintrawoot S, Lin CY, Rahl PB, Burke CJ, Langdon E, Tomlinson ML, Mosher J, Kaufman C, et al,. (2011) DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 471, 518-522.
57. Kawahara G, Karpf JA, Myers JA, Alexander MS, Guyon JR, &, Kunkel LM, (2011) Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 108, 5331-5336.
58. Adamo CM, Dai DF, Percival JM, Minami E, Willis MS, Patrucco E, Froehner SC, &, Beavo JA, (2010) Sildenafil reverses cardiac dysfunction in the mdx mouse model of Duchenne muscular dystrophy. Proc Natl Acad Sci USA 107, 19079-19083.
59. Percival JM, Whitehead NP, Adams ME, Adamo CM, Beavo JA, &, Froehner SC, (2012) Sildenafil reduces respiratory muscle weakness and fibrosis in the mdx mouse model of Duchenne muscular dystrophy. J Pathol 228, 77-87.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. Sarparanta J, Jonson PH, Golzio C, Sandell S, Luque H, Screen M, McDonald K, Stajich JM, Mahjneh I, Vihola A, et al,. (2012) Mutations affecting the cytoplasmic functions of the co-chaperone DNAJB6 cause limb-girdle muscular dystrophy. Nat Genet 44, 450-455, S1-2.
67. 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.
68. 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.
69. 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.
70. Wood AJ, Müller JS, Jepson CD, Laval SH, Lochmüller 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.
71. Gibbs EM, Clarke NF, Rose K, Oates EC, Webster R, Feldman EL, &, Dowling JJ, (2013) Neuromuscular junction abnormalities in DNM2-related centronuclear myopathy. J Mol Med (Berl) 91, 727-737.
72. Deniziak M, Thisse C, Rederstorff M, Hindelang C, Thisse B, &, Lescure A, (2007) Loss of selenoprotein N function causes disruption of muscle architecture in the zebrafish embryo. Exp Cell Res 313, 156-167.
73. 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.
74. 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.
75. Nixon SJ, Wegner J, Ferguson C, Méry 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.