DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo

Annals of Neurology

Volumn 69, Issue 3, 2011, Pages 540-552

  Wallace, Lindsay M ^a,b   Garwick, Sara E ^b   Mei, Wenyan ^b,c   Belayew, Alexandra ^d   Coppee, Frederique ^d   Ladner, Katherine J ^a,e   Guttridge, Denis ^a,e   Yang, Jing ^b,c   Harper, Scott Q ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^c THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MONS   (Belgium)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; DNA BINDING; DUX4 GENE; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; FEMALE; GENE; GENE OVEREXPRESSION; MALE; MOUSE; MUSCLE ATROPHY; MYOPATHY; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; TRANSGENICS; TRANSPOSON; ZEBRA FISH;

ANIMALS; FEMALE; GENE TRANSFER TECHNIQUES; HAND STRENGTH; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DISEASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH;

EID: 79953292473     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.22275     Document Type: Article

References (62)

1. Flanigan KM., Facioscapulohumeral muscular dystrophy and scapuloperoneal disorders. In: Myology. 3rd ed. New York, NY: McGraw-Hill Medical Publishing Division, 2004: 1123-1133.
2. Prevalence of rare diseases: bibliographic data. Orphanet, 2008. Available at: Accessed May 2010.
3. Klinge L, Eagle M, Haggerty ID, et al. Severe phenotype in infantile facioscapulohumeral muscular dystrophy. Neuromuscul Disord 2006; 16: 553-558. (Pubitemid 44374320)
4. van Deutekom JC, Wijmenga C, van Tienhoven EA, et al. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandem repeated unit. Hum Mol Genet 1993; 2: 2037-2042. (Pubitemid 24003395)
5. Wijmenga C, Hewitt JE, Sandkuijl LA, et al. Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 1992; 2: 26-30.
6. Bakker E, Wijmenga C, Vossen RH, et al. The FSHD-linked locus D4F104S1 (p13E-11) on 4q35 has a homologue on 10qter. Muscle Nerve 1995; 2: S39-S44.
7. Lemmers RJ, van der Maarel SM, van Deutekom JC, et al. Inter- and intrachromosomal sub-telomeric rearrangements on 4q35: implications for facioscapulohumeral muscular dystrophy (FSHD) aetiology and diagnosis. Hum Mol Genet 1998; 7: 1207-1214. (Pubitemid 28383051)
8. Lemmers RJ, Wohlgemuth M, van der Gaag KJ, et al. Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am J Hum Genet 2007; 81: 884-894. (Pubitemid 47580243)
9. Thomas NS, Wiseman K, Spurlock G, et al. A large patient study confirming that facioscapulohumeral muscular dystrophy (FSHD) disease expression is almost exclusively associated with an FSHD locus located on a 4qA-defined 4qter subtelomere. J Med Genet 2007; 44: 215-218. (Pubitemid 46580532)
10. de Greef JC, Frants RR, van der Maarel SM., Epigenetic mechanisms of facioscapulohumeral muscular dystrophy. Mutat Res 2008; 647: 94-102.
11. de Greef JC, Lemmers RJ, van Engelen BG, et al. Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum Mutat 2009; 30: 1449-1459.
12. Hewitt JE, Lyle R, Clark LN, et al. Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet 1994; 3: 1287-1295. (Pubitemid 24255461)
13. Jiang G, Yang F, van Overveld PG, et al. Testing the position-effect variegation hypothesis for facioscapulohumeral muscular dystrophy by analysis of histone modification and gene expression in subtelomeric 4q. Hum Mol Genet 2003; 12: 2909-2921. (Pubitemid 37442019)
14. Lyle R, Wright TJ, Clark LN, Hewitt JE., The FSHD-associated repeat, D4Z4, is a member of a dispersed family of homeobox-containing repeats, subsets of which are clustered on the short arms of the acrocentric chromosomes. Genomics 1995; 28: 389-397.
15. van Overveld PG, Lemmers RJ, Sandkuijl LA, et al. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet 2003; 35: 315-317. (Pubitemid 37486913)
16. Zeng W, de Greef JC, Chen YY, et al. Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 2009; 5: e1000559.
17. Tupler R, Berardinelli A, Barbierato L, et al. Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy. J Med Genet 1996; 33: 366-370. (Pubitemid 26147866)
18. Celegato B, Capitanio D, Pescatori M, et al. Parallel protein and transcript profiles of FSHD patient muscles correlate to the D4Z4 arrangement and reveal a common impairment of slow to fast fibre differentiation and a general deregulation of MyoD-dependent genes. Proteomics 2006; 6: 5303-5321. (Pubitemid 44547168)
19. Clapp J, Mitchell LM, Bolland DJ, et al. Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am J Hum Genet 2007; 81: 264-279. (Pubitemid 47236075)
20. Dixit M, Ansseau E, Tassin A, et al. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc Natl Acad Sci U S A 2007; 104: 18157-18162. (Pubitemid 350210837)
21. Eisenberg I, Eran A, Nishino I, et al. Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A 2007; 104: 17016-17021. (Pubitemid 350210983)
22. Gabellini D, D'Antona G, Moggio M, et al. Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 2006; 439: 973-977. (Pubitemid 43292415)
23. Gabellini D, Green MR, Tupler R., Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 2002; 110: 339-348.
24. Gabriels J, Beckers MC, Ding H, et al. Nucleotide sequence of the partially deleted D4Z4 locus in a patient with FSHD identifies a putative gene within each 3.3 kb element. Gene 1999; 236: 25-32. (Pubitemid 29347656)
25. Kowaljow V, Marcowycz A, Ansseau E, et al. The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul Disord 2007; 17: 611-623. (Pubitemid 47030917)
26. Laoudj-Chenivesse D, Carnac G, Bisbal C, et al. Increased levels of adenine nucleotide translocator 1 protein and response to oxidative stress are early events in facioscapulohumeral muscular dystrophy muscle. J Mol Med 2005; 83: 216-224. (Pubitemid 40487410)
27. Osborne RJ, Welle S, Venance SL, et al. Expression profile of FSHD supports a link between retinal vasculopathy and muscular dystrophy. Neurology 2007; 68: 569-577.
28. Reed PW, Corse AM, Porter NC, et al. Abnormal expression of mu-crystallin in facioscapulohumeral muscular dystrophy. Exp Neurol 2007; 205: 583-586. (Pubitemid 46755775)
29. Snider L, Asawachaicharn A, Tyler AE, et al. RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum Mol Genet 2009; 18: 2414-2430.
30. Winokur ST, Chen YW, Masny PS, et al. Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum Mol Genet 2003; 12: 2895-2907. (Pubitemid 37442018)
31. Bosnakovski D, Xu Z, Gang EJ, et al. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 2008; 27: 2766-2779.
32. Wuebbles RD, Long SW, Hanel ML, Jones PL., Testing the effects of FSHD candidate gene expression in vertebrate muscle development. Int J Clin Exp Pathol 2010; 3: 386-400.
33. Lemmers RJ, van der Vliet PJ, Klooster R, et al. A Unifying Genetic Model for Facioscapulohumeral Muscular Dystrophy. Science 2010; 329: 1650-1653.
34. Sandri M, El Meslemani AH, Sandri C, et al. Caspase 3 expression correlates with skeletal muscle apoptosis in Duchenne and facioscapulo human muscular dystrophy. A potential target for pharmacological treatment? J Neuropathol Exp Neurol 2001; 60: 302-312. (Pubitemid 32209649)
35. Ostlund C, Garcia-Carrasquillo RM, Belayew A, Worman HJ., Intracellular trafficking and dynamics of double homeodomain proteins. Biochemistry 2005; 44: 2378-2384. (Pubitemid 40279542)
36. Kawakami K, Takeda H, Kawakami N, et al. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 2004; 7: 133-144. (Pubitemid 39172695)
37. Harper SQ, Hauser MA, DelloRusso C, et al. Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 2002; 8: 253-261. (Pubitemid 34250103)
38. Thornhill P, Bassett D, Lochmuller H, et al. Developmental defects in a zebrafish model for muscular dystrophies associated with the loss of fukutin-related protein (FKRP). Brain 2008; 131: 1551-1561. (Pubitemid 351806461)
39. Salva MZ, Himeda CL, Tai PW, et al. Design of tissue-specific regulatory cassettes for high-level rAAV-mediated expression in skeletal and cardiac muscle. Mol Ther 2007; 15: 320-329. (Pubitemid 46111882)
40. Huang WY, Aramburu J, Douglas PS, Izumo S., Transgenic expression of green fluorescent protein can cause dilated cardiomyopathy. Nat Med 2000; 6: 482-483. (Pubitemid 30305874)
41. Franich NR, Fitzsimons HL, Fong DM, et al. AAV vector-mediated RNAi of mutant huntingtin expression is neuroprotective in a novel genetic rat model of Huntington's disease. Mol Ther 2008; 16: 947-956. (Pubitemid 351587106)
42. Wang F, Rendahl KG, Manning WC, et al. AAV-mediated expression of vascular endothelial growth factor induces choroidal neovascularization in rat. Invest Ophthalmol Vis Sci 2003; 44: 781-790. (Pubitemid 36159730)
43. Blankinship MJ, Gregorevic P, Allen JM, et al. Efficient transduction of skeletal muscle using vectors based on adeno-associated virus serotype 6. Mol Ther 2004; 10: 671-678. (Pubitemid 39272856)
44. Wang Z, Zhu T, Qiao C, et al. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 2005; 23: 321-328. (Pubitemid 41094420)
45. Chipuk JE, Kuwana T, Bouchier-Hayes L, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004; 303: 1010-1014. (Pubitemid 38209704)
46. Degli Esposti M, Dive C., Mitochondrial membrane permeabilisation by Bax/Bak. Biochem Biophys Res Commun 2003; 304: 455-461. (Pubitemid 36506517)
47. Gupta S, Radha V, Furukawa Y, Swarup G., Direct transcriptional activation of human caspase-1 by tumor suppressor p53. J Biol Chem 2001; 276: 10585-10588. (Pubitemid 38089225)
48. Sadasivam S, Gupta S, Radha V, et al. Caspase-1 activator Ipaf is a p53-inducible gene involved in apoptosis. Oncogene 2005; 24: 627-636. (Pubitemid 40188567)
49. Thalappilly S, Sadasivam S, Radha V, Swarup G., Involvement of caspase 1 and its activator Ipaf upstream of mitochondrial events in apoptosis. FEBS J 2006; 273: 2766-2778.
50. Jacks T, Remington L, Williams BO, et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol 1994; 4: 1-7.
51. de Greef JC, Wohlgemuth M, Chan OA, et al. Hypomethylation is restricted to the D4Z4 repeat array in phenotypic FSHD. Neurology 2007; 69: 1018-1026. (Pubitemid 47366056)
52. Flanigan KM, Coffeen CM, Sexton L, et al. Genetic characterization of a large, historically significant Utah kindred with facioscapulohumeral dystrophy. Neuromuscul Disord 2001; 11: 525-529. (Pubitemid 32761794)
53. Arashiro P, Eisenberg I, Kho AT, et al. Transcriptional regulation differs in affected facioscapulohumeral muscular dystrophy patients compared to asymptomatic related carriers. Proc Natl Acad Sci U S A 2009; 106: 6220-6225.
54. Masny PS, Chan OY, de Greef JC, et al. Analysis of allele-specific RNA transcription in FSHD by RNA-DNA FISH in single myonuclei. Eur J Hum Genet 2010; 18: 448-456.
55. Rijkers T, Deidda G, van Koningsbruggen S, et al. FRG2, an FSHD candidate gene, is transcriptionally upregulated in differentiating primary myoblast cultures of FSHD patients. J Med Genet 2004; 41: 826-836. (Pubitemid 39524309)
56. van Deutekom JC, Lemmers RJ, Grewal PK, et al. Identification of the first gene (FRG1) from the FSHD region on human chromosome 4q35. Hum Mol Genet 1996; 5: 581-590. (Pubitemid 26141270)
57. Winokur ST, Barrett K, Martin JH, et al. Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress. Neuromuscul Disord 2003; 13: 322-333. (Pubitemid 36966161)
58. Xia SJ, Pressey JG, Barr FG., Molecular pathogenesis of rhabdomyosarcoma. Cancer Biol Ther 2002; 1: 97-104.
59. Heng MY, Detloff PJ, Albin RL., Rodent genetic models of Huntington disease. Neurobiol Dis 2008; 32: 1-9.
60. Liu DX, Lobie PE., Transcriptional activation of p53 by Pitx1. Cell Death Differ 2007; 14: 1893-1907. (Pubitemid 350011665)
61. Fernando P, Kelly JF, Balazsi K, et al. Caspase 3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci U S A 2002; 99: 11025-11030. (Pubitemid 34920873)
62. Larsen BD, Rampalli S, Burns LE, et al. Caspase 3/caspase-activated DNase promote cell differentiation by inducing DNA strand breaks. Proc Natl Acad Sci U S A 2010; 107: 4230-4235.