Expression of DUX4 in zebrafish development recapitulates facioscapulohumeral muscular dystrophy

Human Molecular Genetics

Volumn 22, Issue 3, 2013, Pages 568-577

  Mitsuhashi, Hiroaki ^a,b   Mitsuhashi, Satomi ^a   Lynn jones, Taylor ^a   Kawahara, Genri ^a   Kunkel, Louis M ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b The Senator Paul D Wellstone Muscular Dystrophy Cooperative Research Center   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTIN; DUX4 PROTEIN; GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENT; EAR; EGG; EYE; FACE MUSCLE; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; FEMALE; FERTILIZATION; FIN (ORGAN); GENE EXPRESSION; MORPHOLOGY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PIGMENTATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SKELETAL MUSCLE; TRUNK; ZEBRA FISH;

ACTINS; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; OVUM; PHENOTYPE; POLYMERASE CHAIN REACTION; RNA, MESSENGER; SHOULDER; ZEBRAFISH;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 84872415036     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds467     Document Type: Article

References (40)

1. Tawil, R. and Van Der Maarel, S.M. (2006) Facioscapulohumeral muscular dystrophy. Muscle Nerve, 34, 1-15.
2. Padberg, G.W., Brouwer, O.F., de Keizer, R.J., Dijkman, G., Wijmenga, C., Grote, J.J. and Frants, R.R. (1995) On the significance of retinal vascular disease and hearing loss in facioscapulohumeral muscular dystrophy. Muscle Nerve, 2, S73-S80.
3. Wijmenga, C., Hewitt, J.E., Sandkuijl, L.A., Clark, L.N., Wright, T.J., Dauwerse, H.G., Gruter, A.M., Hofker, M.H., Moerer, P., Williamson, R. et al. (1992) Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat. Genet., 2, 26-30.
4. Tawil, R., Figlewicz, D.A., Griggs, R.C. and Weiffenbach, B. (1998) Facioscapulohumeral dystrophy: a distinct regional myopathy with a novel molecular pathogenesis. FSH Consortium. Ann. Neurol., 43, 279-282.
5. Goto, K., Lee, J.H., Matsuda, C., Hirabayashi, K., Kojo, T., Nakamura, A., Mitsunaga, Y., Furukawa, T., Sahashi, K. and Arahata, K. (1995) DNA rearrangements in Japanese facioscapulohumeral muscular dystrophy patients: clinical correlations. Neuromuscul. Disord., 5, 201-208.
6. Tupler, R., Berardinelli, A., Barbierato, L., Frants, R., Hewitt, J.E., Lanzi, G., Maraschio, P. and Tiepolo, L. (1996) Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy. J. Med. Genet., 33, 366-370.
7. Rossi, M., Ricci, E., Colantoni, L., Galluzzi, G., Frusciante, R., Tonali, P.A. and Felicetti, L. (2007) The facioscapulohumeral muscular dystrophy region on 4qter and the homologous locus on 10qter evolved independently under different evolutionary pressure. BMC Med. Genet., 8, 8.
8. Lemmers, R.J., Wohlgemuth, M., van der Gaag, K.J., van der Vliet, P.J., van Teijlingen, C.M., de Knijff, P., Padberg, G.W., Frants, R.R. and van der Maarel, S.M. (2007) Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet., 81, 884-894.
9. Snider, L., Geng, L.N., Lemmers, R.J., Kyba, M., Ware, C.B., Nelson, A.M., Tawil, R., Filippova, G.N., van der Maarel, S.M., Tapscott, S.J. et al. (2010) Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet., 6, e1001181.
10. Richards, M., Coppee, F., Thomas, N., Belayew, A. and Upadhyaya, M. (2012) Facioscapulohumeral muscular dystrophy (FSHD): an enigma unravelled? Hum. Genet., 131, 325-340.
11. Hewitt, J.E., Lyle, R., Clark, L.N., Valleley, E.M., Wright, T.J., Wijmenga, C., van Deutekom, J.C., Francis, F., Sharpe, P.T., Hofker, M. et al. (1994) Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum. Mol. Genet., 3, 1287-1295.
12. Gabriels, J., Beckers, M.C., Ding, H., De Vriese, A., Plaisance, S., van der Maarel, S.M., Padberg, G.W., Frants, R.R., Hewitt, J.E., Collen, D. et al. (1999) Nucleotide sequence of the partially deleted D4Z4 locus in a patient with FSHD identifies a putative gene within each 3.3 kb element. Gene, 236, 25-32.
13. Lemmers, R.J., van der Vliet, P.J., Klooster, R., Sacconi, S., Camano, P., Dauwerse, J.G., Snider, L., Straasheijm, K.R., van Ommen, G.J., Padberg, G.W. et al. (2010) A unifying genetic model for facioscapulohumeral muscular dystrophy. Science, 329, 1650-1653.
14. Dixit, M., Ansseau, E., Tassin, A., Winokur, S., Shi, R., Qian, H., Sauvage, S., Matteotti, C., van Acker, A.M., Leo, O. et al. (2007) DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc. Natl. Acad. Sci. USA., 104, 18157-18162.
15. Bosnakovski, D., Xu, Z., Gang, E.J., Galindo, C.L., Liu, M., Simsek, T., Garner, H.R., Agha-Mohammadi, S., Tassin, A., Coppee, F. et al. (2008) An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J., 27, 2766-2779.
16. Vanderplanck, C., Ansseau, E., Charron, S., Stricwant, N., Tassin, A., Laoudj-Chenivesse, D., Wilton, S.D., Coppee, F. and Belayew, A. (2011) The FSHD atrophic myotube phenotype is caused by DUX4 expression. PLoS One, 6, e26820.
17. Geng, L.N., Yao, Z., Snider, L., Fong, A.P., Cech, J.N., Young, J.M., van der Maarel, S.M., Ruzzo, W.L., Gentleman, R.C., Tawil, R. et al. (2012) DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev. Cell, 22, 38-51.
18. Kowaljow, V., Marcowycz, A., Ansseau, E., Conde, C.B., Sauvage, S., Matteotti, C., Arias, C., Corona, E.D., Nunez, N.G., Leo, O. et al. (2007) The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul. Disord., 17, 611-623.
19. Wuebbles, R.D., Long, S.W., Hanel, M.L. and Jones, P.L. (2010) Testing the effects of FSHD candidate gene expression in vertebrate muscle development. Int. J. Clin. Exp. Pathol., 3, 386-400.
20. Wallace, L.M., Garwick, S.E., Mei, W., Belayew, A., Coppee, F., Ladner, K.J., Guttridge, D., Yang, J. and Harper, S.Q. (2011) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann. Neurol., 69, 540-552.
21. Jones, T.I., Chen, J.C.J., Rahimov, F., Homma, S., Arashiro, P., Beermann, M.L., King, O.D., Miller, J.B., Kunkel, L.M., Charles, P. et al. (2012) Facioscapulohumeral muscular dystrophy family studies of DUX4 expression: evidence for disease modifiers and a quantitative model of pathogenesis. Hum. Mol. Genet., 21, 4419-4430.
22. Geng, L.N., Tyler, A.E. and Tapscott, S.J. (2011) Immunodetection of human double homeobox 4. Hybridoma (Larchmt), 30, 125-130.
23. Granato, M., van Eeden, F.J., Schach, U., Trowe, T., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C.P., Jiang, Y.J. et al. (1996) Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva. Development, 123, 399-413.
24. Parsons, M.J., Campos, I., Hirst, E.M. and Stemple, D.L. (2002) Removal of dystroglycan causes severe muscular dystrophy in zebrafish embryos. Development, 129, 3505-3512.
25. Hsiao, C.D., Hsieh, F.J. and Tsai, H.J. (2001) Enhanced expression and stable transmission of transgenes flanked by inverted terminal repeats from adeno-associated virus in zebrafish. Dev. Dyn., 220, 323-336.
26. Devoto, S.H., Melancon, E., Eisen, J.S. and Westerfield, M. (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development, 122, 3371-3380.
27. Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y. and 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.
28. Brouwer, O.F., Padberg, G.W., Bakker, E., Wijmenga, C. and Frants, R.R. (1995) Early onset facioscapulohumeral muscular dystrophy. Muscle Nerve, 2, S67-S72.
29. Snider, L., Asawachaicharn, A., Tyler, A.E., Geng, L.N., Petek, L.M., Maves, L., Miller, D.G., Lemmers, R.J., Winokur, S.T., Tawil, R. et al. (2009) RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum. Mol. Genet., 18, 2414-2430.
30. Cabianca, D.S., Casa, V., Bodega, B., Xynos, A., Ginelli, E., Tanaka, Y. and Gabellini, D. (2012) A long ncRNA links copy number variation to a Polycomb/Trithorax epigenetic switch in FSHD muscular dystrophy. Cell, 149, 819-831.
31. Daston, G., Lamar, E., Olivier, M. and Goulding, M. (1996) Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development, 122, 1017-1027.
32. Kawamura-Saito, M., Yamazaki, Y., Kaneko, K., Kawaguchi, N., Kanda, H., Mukai, H., Gotoh, T., Motoi, T., Fukayama, M., Aburatani, H. et al. (2006) Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation. Hum. Mol. Genet., 15, 2125-2137.
33. Pramono, Z.A., Takeshima, Y., Alimsardjono, H., Ishii, A., Takeda, S. and Matsuo, M. (1996) Induction of exon skipping of the dystrophin transcript in lymphoblastoid cells by transfecting an antisense oligodeoxynucleotide complementary to an exon recognition sequence. Biochem. Biophys. Res. Commun., 226, 445-449.
34. Lu, Q.L., Mann, C.J., Lou, F., Bou-Gharios, G., Morris, G.E., Xue, S.A., Fletcher, S., Partridge, T.A. and Wilton, S.D. (2003) Functional amounts of dystrophin produced by skipping the mutated exon in the mdx dystrophic mouse. Nat. Med., 9, 1009-1014.
35. Goemans, N.M., Tulinius, M., van den Akker, J.T., Burm, B.E., Ekhart, P.F., Heuvelmans, N., Holling, T., Janson, A.A., Platenburg, G.J., Sipkens, J.A. et al. (2011) Systemic administration of PRO051 in Duchenne's muscular dystrophy. N. Engl. J. Med., 364, 1513-1522.
36. Wheeler, T.M., Lueck, J.D., Swanson, M.S., Dirksen, R.T. and Thornton, C.A. (2007) Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J. Clin. Invest., 117, 3952-3957.
37. Taniguchi-Ikeda, M., Kobayashi, K., Kanagawa, M., Yu, C.C., Mori, K., Oda, T., Kuga, A., Kurahashi, H., Akman, H.O., DiMauro, S. et al. (2011) Pathogenic exon-trapping by SVA retrotransposon and rescue in Fukuyama muscular dystrophy. Nature, 478, 127-131.
38. Nüsslein-Volhard, C. and Dahm, R. (2002) Zebrafish: A Practical Approach. New York, USA: Oxford University press.
39. Kawahara, G., Guyon, J.R., Nakamura, Y. and Kunkel, L.M. (2010) Zebrafish models for human FKRP muscular dystrophies. Hum. Mol. Genet., 19, 623-633.
40. Fujita, M., Mitsuhashi, H., Isogai, S., Nakata, T., Kawakami, A., Nonaka, I., Noguchi, S., Hayashi, Y.K., Nishino, I. and Kudo, A. (2012) Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev. Biol., 361, 79-89.