The FSHD atrophic myotube phenotype is caused by DUX4 expression

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Vanderplanck, Céline ^a   Ansseau, Eugénie ^a   Charron, Sébastien ^a   Stricwant, Nadia ^a   Tassin, Alexandra ^a   Laoudj Chenivesse, Dalila ^b   Wilton, Steve D ^c   Coppée, Frédérique ^a   Belayew, Alexandra ^a  

^a UNIVERSITY OF MONS   (Belgium)

^b MONTPELLIER UNIVERSITY HOSPITAL   (France)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ATROGIN 1; BIOLOGICAL MARKER; CELL PROTEIN; CRYSTALLIN; DOUBLE HOMEOBOX 4 PROTEIN; MESSENGER RNA; MU CRYSTALLIN; MUSCLE RING FINGER 1 PROTEIN; PROTEIN P53; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DUX4 PROTEIN, HUMAN; FBXO32 PROTEIN, HUMAN; HOMEODOMAIN PROTEIN; MUSCLE PROTEIN; TRIM63 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DISEASE MARKER; DOWN REGULATION; DUX4 GENE; ENZYME INDUCTION; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; MOUSE; MUSCLE ATROPHY; MUSCLE BIOPSY; MUSCLE FIBER CULTURE; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHENOTYPE; POLYADENYLATION; PROMOTER REGION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; RNA SPLICING; SKELETAL MUSCLE;

ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; DOWN-REGULATION; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; HUMANS; MICE; MODELS, BIOLOGICAL; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR ATROPHY; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; OLIGONUCLEOTIDES, ANTISENSE; PHENOTYPE; RNA INTERFERENCE; RNA SPLICING; RNA, MESSENGER; RNA, SMALL INTERFERING; SKP CULLIN F-BOX PROTEIN LIGASES; TRANSFECTION; UBIQUITIN-PROTEIN LIGASES;

EID: 80055040201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026820     Document Type: Article

References (49)

1. Wijmenga C, Hewitt JE, Sandkuijl LA, Clark LN, Wright TJ, et al. (1992) Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 2: 26-30.
2. Hewitt JE, Lyle R, Clark LN, Valleley EM, Wright TJ, et al. (1994) Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet 3: 1287-1295.
3. van der Maarel SM, Frants RR, Padberg GW, (2007) Facioscapulohumeral muscular dystrophy. Biochim Biophys Acta 1772: 186-194.
4. de Greef JC, Lemmers RJLF, van Engelen BGM, Sacconi S, Venance SL, et al. (2009) Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum Mutat 30: 1449-1459.
5. de Greef JC, Lemmers RJLF, Camano P, Day JW, Sacconi S, et al. (2010) Clinical features of facioscapulohumeral muscular dystrophy 2. Neurology 75: 1548-1554.
6. Ding H, Beckers M, Plaisance S, Marynen P, Collen D, et al. (1998) Characterization of a double homeodomain protein (DUX1) encoded by a cDNA homologous to 3.3 kb dispersed repeated elements. Hum Mol Genet 7: 1681-1694.
7. Gabriëls J, Beckers MC, Ding H, De Vriese A, Plaisance S, 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.
8. Dixit M, Ansseau E, Tassin A, Winokur S, Shi R, et al. (2007) DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc Natl Acad Sci U S A 104: 18157-18162.
9. Lemmers RJLF, van der Vliet PJ, Klooster R, Sacconi S, Camano P, et al. (2010) A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329: 1650-1653.
10. Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, 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.
11. Snider L, Geng LN, Lemmers RJLF, Kyba M, Ware CB, et al. (2010) Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet 6: e1001181.
12. Kawamura-Saito M, Yamazaki Y, Kaneko K, Kawaguchi N, Kanda 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.
13. Kowaljow V, Marcowycz A, Ansseau E, Conde CB, Sauvage S, et al. (2007) The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul Disord 17: 611-623.
14. Richards M, Coppée F, Thomas N, Belayew A, Upadhyaya M, (2011) Facioscapulohumeral muscular dystrophy (FSHD): an enigma unravelled? Human Genetics in press.
15. Lanctôt C, Moreau A, Chamberland M, Tremblay ML, (1999) Hindlimb patterning and mandible development require the Ptx1 gene. Development 126: 1805-1810.
16. Dixit M, Shi R, Sutherland M, Munger S, Chen Y-W, (2007) Characterization of a tet-repressible muscle-specific Pitx1 transgenic mouse model as an animal model of FSHD. FASEB Journal 21: 870-878.
17. Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, et al. (2008) An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J 27: 2766-2779.
18. Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, et al. (2010) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol 69: 540-552.
19. Liu DX, Lobie PE, (2007) Transcriptional activation of p53 by Pitx1. Cell Death Differ 14: 1893-1907.
20. Ansseau E, Laoudj-Chenivesse D, Marcowycz A, Tassin A, Vanderplanck C, et al. (2009) DUX4c is up-regulated in FSHD. It induces the MYF5 protein and human myoblast proliferation. PLoS ONE 4: e7482.
21. Masny PS, Chan OY, de Greef JC, Bengtsson U, Ehrlich M, et al. (2010) Analysis of allele-specific RNA transcription in FSHD by RNA-DNA FISH in single myonuclei. Eur J Hum Genet 18: 448-456.
22. Gabellini D, D'Antona G, Moggio M, Prelle A, Zecca C, et al. (2006) Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 439: 973-977.
23. Barro M, Carnac G, Flavier S, Mercier J, Vassetzky Y, et al. (2008) Myoblasts from affected and non-affected FSHD muscles exhibit morphological differentiation defects. J Cell Mol Med 14: 275-289.
24. de Palma L, Marinelli M, Pavan M, Orazi A, (2008) Ubiquitin ligases MuRF1 and MAFbx in human skeletal muscle atrophy. Joint Bone Spine 75: 53-57.
25. Lagirand-Cantaloube J, Cornille K, Csibi A, Batonnet-Pichon S, Leibovitch MP, et al. (2009) Inhibition of atrogin-1/MAFbx mediated MyoD proteolysis prevents skeletal muscle atrophy in vivo. PLoS ONE 4: e4973.
26. Reed PW, Corse AM, Porter NC, Flanigan KM, Bloch RJ, (2007) Abnormal expression of mu-crystallin in facioscapulohumeral muscular dystrophy. Exp Neurol 205: 583-586.
27. Wilton SD, Fall AM, Harding PL, McClorey G, Coleman C, et al. (2007) Antisense oligonucleotide-induced exon skipping across the human dystrophin gene transcript. Mol Ther 15: 1288-1296.
28. Fletcher S, Adams AM, Johnsen RD, Greer K, Moulton HM, et al. (2010) Dystrophin isoform induction in vivo by antisense-mediated alternative splicing. Mol Ther 18: 1218-1223.
29. Wilton SD, Lloyd F, Carville K, Fletcher S, Honeyman K, et al. (1999) Specific removal of the nonsense mutation from the mdx dystrophin mRNA using antisense oligonucleotides. Neuromuscular Disorders 9: 330-338.
30. Errington SJ, Mann CJ, Fletcher S, Wilton SD, (2003) Target selection for antisense oligonucleotide induced exon skipping in the dystrophin gene. J Gene Med 5: 518-527.
31. Klooster R, Straasheijm K, Shah B, Sowden J, Frants R, et al. (2009) Comprehensive expression analysis of FSHD candidate genes at the mRNA and protein level. Eur J Hum Genet 17: 1615-1624.
32. Vie MP, Evrard C, Osty J, Breton-gilet A, Blanchet P, et al. (1997) Purification, molecular cloning, and functional expression of the human nicodinamide-adenine dinucleotide phosphate-regulated thyroid hormone-binding protein. Mol Endocrinol 11.
33. Muscat GE, Downes M, Dowhan DH, (1995) Regulation of vertebrate muscle differentiation by thyroid hormone: the role of the myoD gene family. BioEssays 17: 211-218.
34. Tawil R, van der Maarel SM, (2006) Facioscapulohumeral muscular dystrophy. Muscle Nerve 34: 1-15.
35. Winokur ST, Barrett K, Martin JH, Forrester JR, Simon M, et al. (2003) Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress. Neuromuscul Disord 13: 322-333.
36. Casas F, Pessemesse L, Grandemange S, Seyer P, Baris O, et al. (2009) Overexpression of the mitochondrial T3 receptor induces skeletal muscle atrophy during aging. Plos One 5.
37. Kim RY, Gasser R, Wistow GJ, (1992) mu-Crystallin is a mammalian homologue of Agrobacterium ornithine cyclodeaminase and is expressed in human retina. Proc Natl Acad Sci U S A 89: 9292-9296.
38. Umeda S, Suzuki MT, Okamoto H, Ono F, Mizota A, et al. (2005) Molecular composition of drusen and possible involvement of anti-retinal autoimmunity in two different forms of macular degeneration in cynomolgus monkey (Macaca fascicularis). FASEB J 19: 1683-1685.
39. Oshima A, Suzuki S, Takumi Y, Hashizume K, Abe S, et al. (2006) CRYM mutations cause deafness through thyroid hormone binding properties in the fibrocytes of the cochlea. J Med Genet 43: e25.
40. Padberg GW, Brouwer OF, de Keizer RJ, Dijkman G, Wijmenga C, et al. (1995) On the significance of retinal vascular disease and hearing loss in facioscapulohumeral muscular dystrophy. Muscle Nerve 2: S73-S80.
41. Brooks CL, Gu W, (2006) p53 ubiquitination: Mdm2 and beyond. Mol Cell 21: 307-315.
42. Maddocks ODK, Vousden KH, (2011) Metabolic regulation by p53. J Mol Med 89: 237-245.
43. Braasch DA, Jensen S, Liu Y, Kaur K, Arar K, et al. (2003) RNA interference in mammalian cells by chemically-modified RNA. Biochem 42: 7967-7975.
44. Amantana A, Iversen PL, (2005) Pharmacokinetics and biodistribution of phosphorodiamidate morpholino antisense oligomers. Curr Opin Pharmacol 5: 550-555.
45. Deas TS, Binduga-Gajewska I, Tilgner M, Ren P, Stein DA, et al. (2005) Inhibition of flavivirus infections by antisense oligomers specifically suppressing viral translation and RNA replication. J Virol 79: 4599-4609.
46. Vickers TA, Wyatt JR, Burckin T, Bennett CF, Freier SM, (2001) Fully modified 2′MOE oligonucleotides redirect polyadenylation. Nucleic Acids Res 29: 1293-1299.
47. Lemmers RJFL, Wohlgemuth M, Frants RR, Padberg GW, Morava E, (2004) Contractions of D4Z4 on 4qB subtelomeres do not cause Facioscapulohumeral Muscular Dystrophy. Am J Hum Genet 75: 1124-1130.
48. Zhu CH, Mouly V, Cooper RN, Mamchaoui K, Bigot A, et al. (2007) Cellular senescence in human myoblasts is overcome by human telomerase reverse transcriptase and cyclin-dependent kinase 4: consequences in aging muscle and therapeutic strategies for muscular dystrophies. Aging Cell 6: 515-523.
49. Mann CJ, Honeyman K, McClorey G, Fletcher S, Wilton SD, (2002) Improved antisense oligonucleotide induced exon skipping in the mdx mouse model of muscular dystrophy. J Gene Med 4: 644-654.