DUX4 Differentially Regulates Transcriptomes of Human Rhabdomyosarcoma and Mouse C2C12 Cells

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Sharma, Vishakha ^a   Harafuji, Naoe ^b   Belayew, Alexandra ^c   Chen, Yi Wen ^b,d  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^c UNIVERSITY OF MONS   (Belgium)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DOUBLE HOMEOBOX 4 PROTEIN; HOMEODOMAIN PROTEIN; MYOD PROTEIN; MYOGENIN; PROTEIN P53; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL ENERGY; CELL IMMORTALIZATION; CELL LINE; CELL METABOLISM; CELL STRAIN C2C12; CONTROLLED STUDY; DUX4 GENE; ENERGY METABOLISM; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE INDUCTION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC TRANSFECTION; GERM LINE; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; MYOBLAST; MYOD GENE; MYOG GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; SIGNAL TRANSDUCTION; UPREGULATION; UTS2 GENE; VALIDATION PROCESS; ZSCAN4 GENE;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL LINE, TUMOR; DNA PRIMERS; HOMEODOMAIN PROTEINS; HUMANS; MICE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA; TRANSCRIPTOME;

EID: 84878055077     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064691     Document Type: Article

References (66)

1. Emery AE, (1991) Population frequencies of inherited neuromuscular diseases-a world survey. Neuromuscul Disord 1: 19-29.
2. van der Maarel SM, Frants RR, (2005) The D4Z4 repeat-mediated pathogenesis of facioscapulohumeral muscular dystrophy. Am J Hum Genet 76: 375-386.
3. Wijmenga C, Frants RR, Brouwer OF, Moerer P, Weber JL, et al. (1990) Location of facioscapulohumeral muscular dystrophy gene on chromosome 4. Lancet 336: 651-653.
4. 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.
5. Lemmers RJ, Tawil R, Petek LM, Balog J, Block GJ, et al. (2012) Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat Genet 44: 1370-1374.
6. 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.
7. Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, et al. (2012) A long ncRNA links copy number variation to a polycomb/trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149: 819-831.
8. Clapp J, Mitchell LM, Bolland DJ, Fantes J, Corcoran AE, et al. (2007) Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am J Hum Genet 81: 264-279.
9. Gabriels 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.
10. Jones TI, Chen JC, Rahimov F, Homma S, Arashiro 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.
11. Lemmers RJ, 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.
12. 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.
13. Snider L, Geng LN, Lemmers RJ, Kyba M, Ware CB, et al. (2010) Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet 6: e1001181.
14. Zeng W, de Greef JC, Chen YY, Chien R, Kong X, et al. (2009) Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet 5: e1000559.
15. 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.
16. Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, et al. (2011) DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol 69: 540-552.
17. Barro M, Carnac G, Flavier S, Mercier J, Vassetzky Y, et al. (2010) Myoblasts from affected and non-affected FSHD muscles exhibit morphological differentiation defects. J Cell Mol Med 14: 275-289.
18. Celegato B, Capitanio D, Pescatori M, Romualdi C, Pacchioni B, et al. (2006) 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 6: 5303-5321.
19. Cheli S, Francois S, Bodega B, Ferrari F, Tenedini E, et al. (2011) Expression profiling of FSHD-1 and FSHD-2 cells during myogenic differentiation evidences common and distinctive gene dysregulation patterns. PLoS One 6: e20966.
20. Geng LN, Yao Z, Snider L, Fong AP, Cech JN, et al. (2012) DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell 22: 38-51.
21. Krom YD, Dumonceaux J, Mamchaoui K, den Hamer B, Mariot V, et al. (2012) Generation of isogenic D4Z4 contracted and noncontracted immortal muscle cell clones from a mosaic patient: a cellular model for FSHD. Am J Pathol 181: 1387-1401.
22. Sandri M, El Meslemani AH, Sandri C, Schjerling P, Vissing K, et al. (2001) 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 60: 302-312.
23. Tsumagari K, Chang SC, Lacey M, Baribault C, Chittur SV, et al. (2011) Gene expression during normal and FSHD myogenesis. BMC Med Genomics 4: 67.
24. Vanderplanck C, Ansseau E, Charron S, Stricwant N, Tassin A, et al. (2011) The FSHD atrophic myotube phenotype is caused by DUX4 expression. PLoS One 6: e26820.
25. 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.
26. Winokur ST, Chen YW, Masny PS, Martin JH, Ehmsen JT, et al. (2003) Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum Mol Genet 12: 2895-2907.
27. Yaffe D, Saxel O, (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
28. McAllister RM, Melnyk J, Finkelstein JZ, Adams EC Jr, Gardner MB, (1969) Cultivation in vitro of cells derived from a human rhabdomyosarcoma. Cancer 24: 520-526.
29. Xu Q, Wu Z, (2000) The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J Biol Chem 275: 36750-36757.
30. Yang Z, MacQuarrie KL, Analau E, Tyler AE, Dilworth FJ, et al. (2009) MyoD and E-protein heterodimers switch rhabdomyosarcoma cells from an arrested myoblast phase to a differentiated state. Genes Dev 23: 694-707.
31. Homma S, Chen JC, Rahimov F, Beermann ML, Hanger K, et al. (2012) A unique library of myogenic cells from facioscapulohumeral muscular dystrophy subjects and unaffected relatives: family, disease and cell function. Eur J Hum Genet 20: 404-410.
32. Stadler G, Chen JC, Wagner K, Robin JD, Shay JW, et al. (2011) Establishment of clonal myogenic cell lines from severely affected dystrophic muscles- CDK4 maintains the myogenic population. Skelet Muscle 1: 12.
33. Chen YW, Hubal MJ, Hoffman EP, Thompson PD, Clarkson PM, (2003) Molecular responses of human muscle to eccentric exercise. J Appl Physiol 95: 2485-2494.
34. Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, et al. (2002) Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell 9: 587-600.
35. Tasca G, Pescatori M, Monforte M, Mirabella M, Iannaccone E, et al. (2012) Different molecular signatures in magnetic resonance imaging-staged facioscapulohumeral muscular dystrophy muscles. PLoS One 7: e38779.
36. Rahimov F, King OD, Leung DG, Bibat GM, Emerson CP Jr, et al. (2012) Transcriptional profiling in facioscapulohumeral muscular dystrophy to identify candidate biomarkers. Proc Natl Acad Sci U S A 109: 16234-16239.
37. Tapscott SJ, Davis RL, Thayer MJ, Cheng PF, Weintraub H, et al. (1988) MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242: 405-411.
38. Schuster-Gossler K, Cordes R, Gossler A, (2007) Premature myogenic differentiation and depletion of progenitor cells cause severe muscle hypotrophy in Delta1 mutants. Proc Natl Acad Sci U S A 104: 537-542.
39. Hasty P, Bradley A, Morris JH, Edmondson DG, Venuti JM, et al. (1993) Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364: 501-506.
40. Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, et al. (1993) MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75: 1351-1359.
41. Bosnakovski D, Lamb S, Simsek T, Xu Z, Belayew A, et al. (2008) DUX4c, an FSHD candidate gene, interferes with myogenic regulators and abolishes myoblast differentiation. Exp Neurol 214: 87-96.
42. Ono Y, Calhabeu F, Morgan JE, Katagiri T, Amthor H, et al. (2011) BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ 18: 222-234.
43. Chaussabel D, Semnani RT, McDowell MA, Sacks D, Sher A, et al. (2003) Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102: 672-681.
44. Nau GJ, Richmond JF, Schlesinger A, Jennings EG, Lander ES, et al. (2002) Human macrophage activation programs induced by bacterial pathogens. Proc Natl Acad Sci U S A 99: 1503-1508.
45. Sen M, Lauterbach K, El-Gabalawy H, Firestein GS, Corr M, et al. (2000) Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci U S A 97: 2791-2796.
46. Ghosh MC, Collins GD, Vandanmagsar B, Patel K, Brill M, et al. (2009) Activation of Wnt5A signaling is required for CXC chemokine ligand 12-mediated T-cell migration. Blood 114: 1366-1373.
47. Rauner M, Stein N, Winzer M, Goettsch C, Zwerina J, et al. (2012) WNT5A is induced by inflammatory mediators in bone marrow stromal cells and regulates cytokine and chemokine production. J Bone Miner Res 27: 575-585.
48. Frisullo G, Frusciante R, Nociti V, Tasca G, Renna R, et al. (2011) CD8(+) T cells in facioscapulohumeral muscular dystrophy patients with inflammatory features at muscle MRI. J Clin Immunol 31: 155-166.
49. Otto A, Schmidt C, Luke G, Allen S, Valasek P, et al. (2008) Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J Cell Sci 121: 2939-2950.
50. Wuebbles RD, Long SW, Hanel ML, Jones PL, (2010) Testing the effects of FSHD candidate gene expression in vertebrate muscle development. Int J Clin Exp Pathol 3: 386-400.
51. Felix CA, Kappel CC, Mitsudomi T, Nau MM, Tsokos M, et al. (1992) Frequency and diversity of p53 mutations in childhood rhabdomyosarcoma. Cancer Res 52: 2243-2247.
52. Taylor AC, Shu L, Danks MK, Poquette CA, Shetty S, et al. (2000) P53 mutation and MDM2 amplification frequency in pediatric rhabdomyosarcoma tumors and cell lines. Med Pediatr Oncol 35: 96-103.
53. Miyachi M, Kakazu N, Yagyu S, Katsumi Y, Tsubai-Shimizu S, et al. (2009) Restoration of p53 pathway by nutlin-3 induces cell cycle arrest and apoptosis in human rhabdomyosarcoma cells. Clin Cancer Res 15: 4077-4084.
54. Turki A, Hayot M, Carnac G, Pillard F, Passerieux E, et al. (2012) Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 53: 1068-1079.
55. Gendron G, Simard B, Gobeil F Jr, Sirois P, D'Orleans-Juste P, et al. (2004) Human urotensin-II enhances plasma extravasation in specific vascular districts in Wistar rats. Can J Physiol Pharmacol 82: 16-21.
56. Matsusaka S, Wakabayashi I, (2006) Enhancement of vascular smooth muscle cell migration by urotensin II. Naunyn Schmiedebergs Arch Pharmacol 373: 381-386.
57. Shi L, Ding W, Li D, Wang Z, Jiang H, et al. (2006) Proliferation and anti-apoptotic effects of human urotensin II on human endothelial cells. Atherosclerosis 188: 260-264.
58. Spinazzi R, Albertin G, Nico B, Guidolin D, Di Liddo R, et al. (2006) Urotensin-II and its receptor (UT-R) are expressed in rat brain endothelial cells, and urotensin-II via UT-R stimulates angiogenesis in vivo and in vitro. Int J Mol Med 18: 1107-1112.
59. Xu S, Wen H, Jiang H, (2012) Urotensin II promotes the proliferation of endothelial progenitor cells through p38 and p44/42 MAPK activation. Mol Med Report 6: 197-200.
60. Suguro T, Watanabe T, Kodate S, Xu G, Hirano T, et al. (2008) Increased plasma urotensin-II levels are associated with diabetic retinopathy and carotid atherosclerosis in Type 2 diabetes. Clin Sci (Lond) 115: 327-334.
61. Fitzsimons RB, Gurwin EB, Bird AC, (1987) Retinal vascular abnormalities in facioscapulohumeral muscular dystrophy. A general association with genetic and therapeutic implications. Brain 110 (Pt 3) (): 631-648.
62. 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: S73-80.
63. Batuwangala MS, Calo G, Guerrini R, Ng LL, McDonald J, et al. (2009) Desensitisation of native and recombinant human urotensin-II receptors. Naunyn Schmiedebergs Arch Pharmacol 380: 451-457.
64. Birker-Robaczewska M, Boukhadra C, Studer R, Mueller C, Binkert C, et al. (2003) The expression of urotensin II receptor (U2R) is up-regulated by interferon-gamma. J Recept Signal Transduct Res 23: 289-305.
65. Douglas SA, Behm DJ, Aiyar NV, Naselsky D, Disa J, et al. (2005) Nonpeptidic urotensin-II receptor antagonists I: in vitro pharmacological characterization of SB-706375. Br J Pharmacol 145: 620-635.
66. Douglas SA, Naselsky D, Ao Z, Disa J, Herold CL, et al. (2004) Identification and pharmacological characterization of native, functional human urotensin-II receptors in rhabdomyosarcoma cell lines. Br J Pharmacol 142: 921-932.