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Orphanet Journal of Rare Diseases

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Open Access 01-12-2013 | Research

miR-411 is up-regulated in FSHD myoblasts and suppresses myogenic factors

Authors: Naoe Harafuji, Peter Schneiderat, Maggie C Walter, Yi-Wen Chen

Published in: Orphanet Journal of Rare Diseases | Issue 1/2013

Abstract

Background

Facioscapulohumeral muscular dystrophy (FSHD) is an autosomal dominant muscle disorder, which is linked to the contraction of the D4Z4 array at chromosome 4q35. Recent studies suggest that this shortening of the D4Z4 array leads to aberrant expression of double homeobox protein 4 (DUX4) and causes FSHD. In addition, misregulation of microRNAs (miRNAs) has been reported in muscular dystrophies including FSHD. In this study, we identified a miRNA that is differentially expressed in FSHD myoblasts and investigated its function.

Methods

To identify misregulated miRNAs and their potential targets in FSHD myoblasts, we performed expression profiling of both miRNA and mRNA using TaqMan Human MicroRNA Arrays and Affymetrix Human Genome U133A plus 2.0 microarrays, respectively. In addition, we over-expressed miR-411 in C₂C₁₂ cells to determine the effect of miR-411 on myogenic markers.

Results

Using miRNA and mRNA expression profiling, we identified 8 miRNAs and 1,502 transcripts that were differentially expressed in FSHD myoblasts during cell proliferation. One of the 8 differentially expressed miRNAs, miR-411, was validated by quantitative RT-PCR in both primary (2.1 fold, p<0.01) and immortalized (2.7 fold, p<0.01) myoblasts. In situ hybridization showed cytoplasmic localization of miR-411 in FSHD myoblasts. By analyzing both miRNA and mRNA data using Partek Genomics Suite, we identified 4 mRNAs potentially regulated by miR-411 including YY1 associated factor 2 (YAF2). The down-regulation of YAF2 in immortalized myoblasts was validated by immunoblotting (−3.7 fold, p<0.01). C₂C₁₂ cells were transfected with miR-411 to determine whether miR-411 affects YAF2 expression in myoblasts. The results showed that over-expression of miR-411 reduced YAF2 mRNA expression. In addition, expression of myogenic markers including Myod, myogenin, and myosin heavy chain 1 (Myh1) were suppressed by miR-411.

Conclusions

The study demonstrated that miR-411 was differentially expressed in FSHD myoblasts and may play a role in regulating myogenesis.

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Padberg GW, Frants RR, Brouwer OF, Wijmenga C, Bakker E, Sandkuijl LA: Facioscapulohumeral muscular dystrophy in the Dutch population. Muscle Nerve. 1995, 2: S81-S84.CrossRef

Zatz M, Marie SK, Passos-Bueno MR, Vainzof M, Campiotto S, Cerqueira A, Wijmenga C, Padberg G, Frants R: High proportion of new mutations and possible anticipation in Brazilian facioscapulohumeral muscular dystrophy families. Am J Hum Genet. 1995, 56: 99-105.PubMedCentralPubMed

Lunt PW, Compston DA, Harper PS: Estimation of age dependent penetrance in facioscapulohumeral muscular dystrophy by minimising ascertainment bias. J Med Genet. 1989, 26: 755-760. 10.1136/jmg.26.12.755.PubMedCentralPubMedCrossRef

Tawil R, Figlewicz DA, Griggs RC, Weiffenbach B: Facioscapulohumeral dystrophy: a distinct regional myopathy with a novel molecular pathogenesis. FSH Consortium. Ann Neurol. 1998, 43: 279-282. 10.1002/ana.410430303.PubMedCrossRef

Padberg GW, Lunt PW, Koch M, Fardeau M: Diagnostic criteria for facioscapulohumeral muscular dystrophy. Neuromuscul Disord. 1991, 1: 231-234. 10.1016/0960-8966(91)90094-9.PubMedCrossRef

Wijmenga C, Hewitt JE, Sandkuijl LA, Clark LN, Wright TJ, Dauwerse HG, Gruter AM, Hofker MH, Moerer P, Williamson R: Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet. 1992, 2: 26-30. 10.1038/ng0992-26.PubMedCrossRef

Padberg GW: Facioscapulohumeral disease. University of Leiden: Doctral; 1982.

Padberg GW: Facioscapulohumeral Muscular Dystrophy: a Clinician's Experience. Facioscapulohumeral muscular dystrophy. Edited by: Upadhyaya D, Cooper DN. Clinical Medicine and Molecular Cell Biology, Garland Science/BIOS Scientific Publishers; 2004:41-54.

Arahata K, Ishihara T, Fukunaga H, Orimo S, Lee JH, Goto K, Nonaka I: Inflammatory response in facioscapulohumeral muscular dystrophy (FSHD): immunocytochemical and genetic analyses. Muscle Nerve. 1995, 2: S56-S66.CrossRef

10.

Padberg G, Adams C: Facioscapulohumeral muscular dystrophy. Neurogenetics. Edited by: Pulst S-M. Oxford, UK: Oxford University Press; 2000:105-116.

11.

Padberg GW, Brouwer OF, de Keizer RJ, Dijkman G, Wijmenga C, Grote JJ, Frants RR: On the significance of retinal vascular disease and hearing loss in facioscapulohumeral muscular dystrophy. Muscle Nerve. 1995, 2: S73-S80.CrossRef

12.

Tupler R, Berardinelli A, Barbierato L, Frants R, Hewitt JE, Lanzi G, Maraschio P, Tiepolo L: Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy. J Med Genet. 1996, 33: 366-370. 10.1136/jmg.33.5.366.PubMedCentralPubMedCrossRef

13.

van der Maarel SM, Frants RR, Padberg GW: Facioscapulohumeral muscular dystrophy. Biochim Biophys Acta. 2007, 1772: 186-194. 10.1016/j.bbadis.2006.05.009.PubMedCrossRef

14.

van Deutekom JC, Wijmenga C, van Tienhoven EA, Gruter AM, Hewitt JE, Padberg GW, van Ommen GJ, Hofker MH, Frants RR: FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum Mol Genet. 1993, 2: 2037-2042. 10.1093/hmg/2.12.2037.PubMedCrossRef

15.

Bengtsson U, Altherr MR, Wasmuth JJ, Winokur ST: High resolution fluorescence in situ hybridization to linearly extended DNA visually maps a tandem repeat associated with facioscapulohumeral muscular dystrophy immediately adjacent to the telomere of 4q. Hum Mol Genet. 1994, 3: 1801-1805. 10.1093/hmg/3.10.1801.PubMedCrossRef

16.

Hewitt JE, Lyle R, Clark LN, Valleley EM, Wright TJ, Wijmenga C, van Deutekom JC, Francis F, Sharpe PT, Hofker M: Analysis of the tandem repeat locus D4Z4 associated with facioscapulohumeral muscular dystrophy. Hum Mol Genet. 1994, 3: 1287-1295. 10.1093/hmg/3.8.1287.PubMedCrossRef

17.

Dixit M, Ansseau E, Tassin A, Winokur S, Shi R, Qian H, Sauvage S, Matteotti C, van Acker AM, Leo O: 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. 10.1073/pnas.0708659104.PubMedCentralPubMedCrossRef

18.

Snider L, Geng LN, Lemmers RJ, Kyba M, Ware CB, Nelson AM, Tawil R, Filippova GN, van der Maarel SM, Tapscott SJ, Miller DG: Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet. 2010, 6: e1001181-10.1371/journal.pgen.1001181.PubMedCentralPubMedCrossRef

19.

Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, Maves L, Miller DG, Lemmers RJ, Winokur ST, Tawil R: 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. 10.1093/hmg/ddp180.PubMedCentralPubMedCrossRef

20.

Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, Simsek T, Garner HR, Agha-Mohammadi S, Tassin A, Coppee F: An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J. 2008, 27: 2766-2779. 10.1038/emboj.2008.201.PubMedCentralPubMedCrossRef

21.

Kowaljow V, Marcowycz A, Ansseau E, Conde CB, Sauvage S, Matteotti C, Arias C, Corona ED, Nunez NG, Leo O: The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul Disord. 2007, 17: 611-623. 10.1016/j.nmd.2007.04.002.PubMedCrossRef

22.

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.PubMedCentralPubMed

23.

Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, Ladner KJ, Guttridge D, Yang J, Harper SQ: DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann Neurol. 2010

24.

Vanderplanck C, Ansseau E, Charron S, Stricwant N, Tassin A, Laoudj-Chenivesse D, Wilton SD, Coppee F, Belayew A: The FSHD atrophic myotube phenotype is caused by DUX4 expression. PLoS One. 2011, 6: e26820-10.1371/journal.pone.0026820.PubMedCentralPubMedCrossRef

25.

Pandey SN, Cabotage J, Shi R, Dixit M, Sutherland M, Liu J, Muger S, Harper SQ, Nagaraju K, Chen YW: Conditional over-expression of PITX1 causes skeletal muscle dystrophy in mice. Biol Open. 2012, 1: 629-639. 10.1242/bio.20121305.PubMedCentralPubMedCrossRef

26.

van Overveld PG, Lemmers RJ, Sandkuijl LA, Enthoven L, Winokur ST, Bakels F, Padberg GW, van Ommen GJ, Frants RR, van der Maarel SM: Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat Genet. 2003, 35: 315-317. 10.1038/ng1262.PubMedCrossRef

27.

Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, Dauwerse JG, Snider L, Straasheijm KR, Jan Van Ommen G, Padberg GW: A Unifying Genetic Model for Facioscapulohumeral Muscular Dystrophy. Science. 2010, 329: 1650-1653. 10.1126/science.1189044.PubMedCentralPubMedCrossRef

28.

Tsumagari K, Chang SC, Lacey M, Baribault C, Chittur SV, Sowden J, Tawil R, Crawford GE, Ehrlich M: Gene expression during normal and FSHD myogenesis. BMC Med Genomics. 2011, 4: 67-10.1186/1755-8794-4-67.PubMedCentralPubMedCrossRef

29.

Winokur ST, Chen YW, Masny PS, Martin JH, Ehmsen JT, Tapscott SJ, van der Maarel SM, Hayashi Y, Flanigan KM: Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum Mol Genet. 2003, 12: 2895-2907. 10.1093/hmg/ddg327.PubMedCrossRef

30.

Celegato B, Capitanio D, Pescatori M, Romualdi C, Pacchioni B, Cagnin S, Vigano A, Colantoni L, Begum S, Ricci E: 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. 10.1002/pmic.200600056.PubMedCrossRef

31.

Cheli S, Francois S, Bodega B, Ferrari F, Tenedini E, Roncaglia E, Ferrari S, Ginelli E, Meneveri R: Expression profiling of FSHD-1 and FSHD-2 cells during myogenic differentiation evidences common and distinctive gene dysregulation patterns. PLoS One. 2011, 6: e20966-10.1371/journal.pone.0020966.PubMedCentralPubMedCrossRef

32.

Winokur ST, Barrett K, Martin JH, Forrester JR, Simon M, Tawil R, Chung SA, Masny PS, Figlewicz DA: Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress. Neuromuscul Disord. 2003, 13: 322-333. 10.1016/S0960-8966(02)00284-5.PubMedCrossRef

33.

Barro M, Carnac G, Flavier S, Mercier J, Vassetzky Y, Laoudj-Chenivesse D: Myoblasts from affected and non-affected FSHD muscles exhibit morphological differentiation defects. J Cell Mol Med. 2010, 14: 275-289. 10.1111/j.1582-4934.2008.00368.x.PubMedCentralPubMedCrossRef

34.

Tawil R: Facioscapulohumeral muscular dystrophy. Neurotherapeutics. 2008, 5: 601-606. 10.1016/j.nurt.2008.07.005.PubMedCentralPubMedCrossRef

35.

Sayed D, Abdellatif M: MicroRNAs in development and disease. Physiol Rev. 2011, 91: 827-887. 10.1152/physrev.00006.2010.PubMedCrossRef

36.

Winter J, Jung S, Keller S, Gregory RI, Diederichs S: Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol. 2009, 11: 228-234. 10.1038/ncb0309-228.PubMedCrossRef

37.

Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim VN: The nuclear RNase III Drosha initiates microRNA processing. Nature. 2003, 425: 415-419. 10.1038/nature01957.PubMedCrossRef

38.

Lund E, Guttinger S, Calado A, Dahlberg JE, Kutay U: Nuclear export of microRNA precursors. Science. 2004, 303: 95-98. 10.1126/science.1090599.PubMedCrossRef

39.

Schwarz DS, Hutvagner G, Haley B, Zamore PD: Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol Cell. 2002, 10: 537-548. 10.1016/S1097-2765(02)00651-2.PubMedCrossRef

40.

Guller I, Russell AP: MicroRNAs in skeletal muscle: their role and regulation in development, disease and function. J Physiol. 588: 4075-4087.

41.

Bartel DP: MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004, 116: 281-297. 10.1016/S0092-8674(04)00045-5.PubMedCrossRef

42.

Stefani G, Slack FJ: Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol. 2008, 9: 219-230. 10.1038/nrm2347.PubMedCrossRef

43.

Valencia-Sanchez MA, Liu J, Hannon GJ, Parker R: Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 2006, 20: 515-524. 10.1101/gad.1399806.PubMedCrossRef

44.

Cardinali B, Castellani L, Fasanaro P, Basso A, Alema S, Martelli F, Falcone G: Microrna-221 and microrna-222 modulate differentiation and maturation of skeletal muscle cells. PLoS One. 2009, 4: e7607-10.1371/journal.pone.0007607.PubMedCentralPubMedCrossRef

45.

Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF: Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci U S A. 2006, 103: 8721-8726. 10.1073/pnas.0602831103.PubMedCentralPubMedCrossRef

46.

Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ: The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet. 2006, 38: 228-233. 10.1038/ng1725.PubMedCentralPubMedCrossRef

47.

Chen JF, Tao Y, Li J, Deng Z, Yan Z, Xiao X, Wang DZ: microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol. 2010, 190: 867-879. 10.1083/jcb.200911036.PubMedCentralPubMedCrossRef

48.

Naguibneva I, Ameyar-Zazoua M, Polesskaya A, Ait-Si-Ali S, Groisman R, Souidi M, Cuvellier S, Harel-Bellan A: The microRNA miR-181 targets the homeobox protein Hox-A11 during mammalian myoblast differentiation. Nat Cell Biol. 2006, 8: 278-284. 10.1038/ncb1373.PubMedCrossRef

49.

Liu J, Luo XJ, Xiong AW, Zhang ZD, Yue S, Zhu MS, Cheng SY: MicroRNA-214 promotes myogenic differentiation by facilitating exit from mitosis via down-regulation of proto-oncogene N-ras. J Biol Chem. 285: 26599-26607.

50.

Sun Q, Zhang Y, Yang G, Chen X, Cao G, Wang J, Sun Y, Zhang P, Fan M, Shao N, Yang X: Transforming growth factor-beta-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res. 2008, 36: 2690-2699. 10.1093/nar/gkn032.PubMedCentralPubMedCrossRef

51.

Flynt AS, Li N, Thatcher EJ, Solnica-Krezel L, Patton JG: Zebrafish miR-214 modulates Hedgehog signaling to specify muscle cell fate. Nat Genet. 2007, 39: 259-263. 10.1038/ng1953.PubMedCentralPubMedCrossRef

52.

McCarthy JJ, Esser KA, Andrade FH: MicroRNA-206 is overexpressed in the diaphragm but not the hindlimb muscle of mdx mouse. Am J Physiol Cell Physiol. 2007, 293: C451-457. 10.1152/ajpcell.00077.2007.PubMedCrossRef

53.

Gambardella S, Rinaldi F, Lepore SM, Viola A, Loro E, Angelini C, Vergani L, Novelli G, Botta A: Overexpression of microRNA-206 in the skeletal muscle from myotonic dystrophy type 1 patients. J Transl Med. 8: 48.

54.

Cacchiarelli D, Martone J, Girardi E, Cesana M, Incitti T, Morlando M, Nicoletti C, Santini T, Sthandier O, Barberi L: MicroRNAs involved in molecular circuitries relevant for the Duchenne muscular dystrophy pathogenesis are controlled by the dystrophin/nNOS pathway. Cell Metab. 2010, 12: 341-351. 10.1016/j.cmet.2010.07.008.PubMedCrossRef

55.

Eisenberg I, Eran A, Nishino I, Moggio M, Lamperti C, Amato AA, Lidov HG, Kang PB, North KN, Mitrani-Rosenbaum S: Distinctive patterns of microRNA expression in primary muscular disorders. Proc Natl Acad Sci U S A. 2007, 104: 17016-17021. 10.1073/pnas.0708115104.PubMedCentralPubMedCrossRef

56.

Glazov EA, McWilliam S, Barris WC, Dalrymple BP: Origin, evolution, and biological role of miRNA cluster in DLK-DIO3 genomic region in placental mammals. Mol Biol Evol. 2008, 25: 939-948. 10.1093/molbev/msn045.PubMedCrossRef

57.

Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G: Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 2009, 28: 697-710. 10.1038/emboj.2009.10.PubMedCentralPubMedCrossRef

58.

Stadler G, Chen JC, Wagner K, Robin JD, Shay JW, Emerson CP, Wright WE: Establishment of clonal myogenic cell lines from severely affected dystrophic muscles - CDK4 maintains the myogenic population. Skelet Muscle. 2011, 1: 12-10.1186/2044-5040-1-12.PubMedCentralPubMedCrossRef

59.

Homma S, Chen JC, Rahimov F, Beermann ML, Hanger K, Bibat GM, Wagner KR, Kunkel LM, Emerson CP, Miller JB: A unique library of myogenic cells from facioscapulohumeral muscular dystrophy subjects and unaffected relatives: family, disease and cell function. Eur J Hum Genet. 2012, 20: 404-410. 10.1038/ejhg.2011.213.PubMedCentralPubMedCrossRef

60.

Chen YW, Nader GA, Baar KR, Fedele MJ, Hoffman EP, Esser KA: Response of rat muscle to acute resistance exercise defined by transcriptional and translational profiling. J Physiol. 2002, 545: 27-41. 10.1113/jphysiol.2002.021220.PubMedCentralPubMedCrossRef

61.

Chen YW, Zhao P, Borup R, Hoffman EP: Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J Cell Biol. 2000, 151: 1321-1336. 10.1083/jcb.151.6.1321.PubMedCentralPubMedCrossRef

62.

Thompson WA: The Problem of Negative Estimates of Variance Components. Ann Math Statist. 1962, 33: 273-289. 10.1214/aoms/1177704731.CrossRef

63.

Bookout AL, Mangelsdorf DJ: Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl Recept Signal. 2003, 1: e012.PubMedCentralPubMedCrossRef

64.

Guide to Performing Relative Quantitation of Gene Expression Using Real-Time Quantitative PCR Applied Biosystems:

65.

Chen YW, Hubal MJ, Hoffman EP, Thompson PD, Clarkson PM: Molecular responses of human muscle to eccentric exercise. J Appl Physiol. 2003, 95: 2485-2494.PubMedCrossRef

66.

Duddy WJ, Cohen T, Duguez S, Partridge TA: The isolated muscle fibre as a model of disuse atrophy: characterization using PhAct, a method to quantify f-actin. Exp Cell Res. 2011, 317: 1979-1993. 10.1016/j.yexcr.2011.05.013.PubMedCentralPubMedCrossRef

67.

Wilkinson DG: in situ hybridization: a practical approach. Oxford University Press; 1992.

68.

Schneider CA, Rasband WS, Eliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012, 9: 671-675. 10.1038/nmeth.2089.PubMedCrossRef

69.

Rijkers T, Deidda G, van Koningsbruggen S, van Geel M, Lemmers RJ, van Deutekom JC, Figlewicz D, Hewitt JE, Padberg GW, Frants RR, van der Maarel SM: FRG2, an FSHD candidate gene, is transcriptionally upregulated in differentiating primary myoblast cultures of FSHD patients. J Med Genet. 2004, 41: 826-836. 10.1136/jmg.2004.019364.PubMedCentralPubMedCrossRef

70.

Kalenik JL, Chen D, Bradley ME, Chen SJ, Lee TC: Yeast two-hybrid cloning of a novel zinc finger protein that interacts with the multifunctional transcription factor YY1. Nucleic Acids Res. 1997, 25: 843-849. 10.1093/nar/25.4.843.PubMedCentralPubMedCrossRef

71.

Gualberto A, LePage D, Pons G, Mader SL, Park K, Atchison ML, Walsh K: Functional antagonism between YY1 and the serum response factor. Mol Cell Biol. 1992, 12: 4209-4214.PubMedCentralPubMedCrossRef

72.

Lee TC, Chow KL, Fang P, Schwartz RJ: Activation of skeletal alpha-actin gene transcription: the cooperative formation of serum response factor-binding complexes over positive cis-acting promoter serum response elements displaces a negative-acting nuclear factor enriched in replicating myoblasts and nonmyogenic cells. Mol Cell Biol. 1991, 11: 5090-5100.PubMedCentralPubMedCrossRef

73.

Kaneko T, Miyagishima H, Hasegawa T, Mizutani-Koseki Y, Isono K, Koseki H: The mouse YAF2 gene generates two distinct transcripts and is expressed in pre-and postimplantation embryos. Gene. 2003, 315: 183-192.PubMedCrossRef

74.

Sawa C, Yoshikawa T, Matsuda-Suzuki F, Delehouzee S, Goto M, Watanabe H, Sawada J, Kataoka K, Handa H: YEAF1/RYBP and YAF-2 are functionally distinct members of a cofactor family for the YY1 and E4TF1/hGABP transcription factors. J Biol Chem. 2002, 277: 22484-22490. 10.1074/jbc.M203060200.PubMedCrossRef

75.

Sparmann A, van Lohuizen M: Polycomb silencers control cell fate, development and cancer. Nat Rev Cancer. 2006, 6: 846-856. 10.1038/nrc1991.PubMedCrossRef

76.

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. 10.1016/S0092-8674(02)00826-7.PubMedCrossRef

77.

Delehouzee S, Yoshikawa T, Sawa C, Sawada J, Ito T, Omori M, Wada T, Yamaguchi Y, Kabe Y, Handa H: GABP, HCF-1 and YY1 are involved in Rb gene expression during myogenesis. Genes Cells. 2005, 10: 717-731. 10.1111/j.1365-2443.2005.00873.x.PubMedCrossRef

78.

Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS: NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell. 2008, 14: 369-381. 10.1016/j.ccr.2008.10.006.PubMedCrossRef

79.

L'Honore A, Lamb NJ, Vandromme M, Turowski P, Carnac G, Fernandez A: MyoD distal regulatory region contains an SRF binding CArG element required for MyoD expression in skeletal myoblasts and during muscle regeneration. Mol Biol Cell. 2003, 14: 2151-2162. 10.1091/mbc.E02-07-0451.PubMedCentralPubMedCrossRef

80.

Treisman R: The serum response element. Trends Biochem Sci. 1992, 17: 423-426. 10.1016/0968-0004(92)90013-Y.PubMedCrossRef

81.

Vandromme M, Gauthier-Rouviere C, Carnac G, Lamb N, Fernandez A: Serum response factor p67SRF is expressed and required during myogenic differentiation of both mouse C2 and rat L6 muscle cell lines. J Cell Biol. 1992, 118: 1489-1500. 10.1083/jcb.118.6.1489.PubMedCrossRef

82.

Gauthier-Rouviere C, Vandromme M, Tuil D, Lautredou N, Morris M, Soulez M, Kahn A, Fernandez A, Lamb N: Expression and activity of serum response factor is required for expression of the muscle-determining factor MyoD in both dividing and differentiating mouse C2C12 myoblasts. Mol Biol Cell. 1996, 7: 719-729.PubMedCentralPubMedCrossRef

83.

Soulez M, Rouviere CG, Chafey P, Hentzen D, Vandromme M, Lautredou N, Lamb N, Kahn A, Tuil D: Growth and differentiation of C2 myogenic cells are dependent on serum response factor. Mol Cell Biol. 1996, 16: 6065-6074.PubMedCentralPubMedCrossRef

84.

Wang H, Hertlein E, Bakkar N, Sun H, Acharyya S, Wang J, Carathers M, Davuluri R, Guttridge DC: NF-kappaB regulation of YY1 inhibits skeletal myogenesis through transcriptional silencing of myofibrillar genes. Mol Cell Biol. 2007, 27: 4374-4387. 10.1128/MCB.02020-06.PubMedCentralPubMedCrossRef

85.

Geng LN, Yao Z, Snider L, Fong AP, Cech JN, Young JM, van der Maarel SM, Ruzzo WL, Gentleman RC, Tawil R, Tapscott SJ: DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev Cell. 2012, 22: 38-51. 10.1016/j.devcel.2011.11.013.PubMedCentralPubMedCrossRef

86.

Vilquin JT, Marolleau JP, Sacconi S, Garcin I, Lacassagne MN, Robert I, Ternaux B, Bouazza B, Larghero J, Desnuelle C: Normal growth and regenerating ability of myoblasts from unaffected muscles of facioscapulohumeral muscular dystrophy patients. Gene Ther. 2005, 12: 1651-1662. 10.1038/sj.gt.3302565.PubMedCrossRef

87.

Morosetti R, Mirabella M, Gliubizzi C, Broccolini A, Sancricca C, Pescatori M, Gidaro T, Tasca G, Frusciante R, Tonali PA: Isolation and characterization of mesoangioblasts from facioscapulohumeral muscular dystrophy muscle biopsies. Stem Cells. 2007, 25: 3173-3182. 10.1634/stemcells.2007-0465.PubMedCrossRef

88.

Aziz A, Liu QC, Dilworth FJ: Regulating a master regulator: establishing tissue-specific gene expression in skeletal muscle. Epigenetics. 2010, 5: 691-695. 10.4161/epi.5.8.13045.PubMedCentralPubMedCrossRef

89.

Rudnicki MA, Schnegelsberg PN, Stead RH, Braun T, Arnold HH, Jaenisch R: MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993, 75: 1351-1359. 10.1016/0092-8674(93)90621-V.PubMedCrossRef

90.

Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, Parker MH, MacQuarrie KL, Davison J, Morgan MT, Ruzzo WL: Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell. 2010, 18: 662-674. 10.1016/j.devcel.2010.02.014.PubMedCentralPubMedCrossRef

91.

Bergstrom DA, Penn BH, Strand A, Perry RL, Rudnicki MA, Tapscott SJ: Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression. Mol Cell. 2002, 9: 587-600. 10.1016/S1097-2765(02)00481-1.PubMedCrossRef

92.

Martelli F, Cenciarelli C, Santarelli G, Polikar B, Felsani A, Caruso M: MyoD induces retinoblastoma gene expression during myogenic differentiation. Oncogene. 1994, 9: 3579-3590.PubMed

93.

Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB: Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science. 1995, 267: 1018-1021. 10.1126/science.7863327.PubMedCrossRef

94.

Lassar AB, Paterson BM, Weintraub H: Transfection of a DNA locus that mediates the conversion of 10T1/2 fibroblasts to myoblasts. Cell. 1986, 47: 649-656. 10.1016/0092-8674(86)90507-6.PubMedCrossRef

95.

Davis RL, Weintraub H, Lassar AB: Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell. 1987, 51: 987-1000. 10.1016/0092-8674(87)90585-X.PubMedCrossRef

96.

Krom YD, Dumonceaux J, Mamchaoui K, den Hamer B, Mariot V, Negroni E, Geng LN, Martin N, Tawil R, Tapscott SJ: Generation of isogenic D4Z4 contracted and noncontracted immortal muscle cell clones from a mosaic patient: a cellular model for FSHD. Am J Pathol. 2012, 181: 1387-1401. 10.1016/j.ajpath.2012.07.007.PubMedCentralPubMedCrossRef

Title: miR-411 is up-regulated in FSHD myoblasts and suppresses myogenic factors
Authors: Naoe Harafuji
Peter Schneiderat
Maggie C Walter
Yi-Wen Chen
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: Orphanet Journal of Rare Diseases / Issue 1/2013
Electronic ISSN: 1750-1172
DOI: https://doi.org/10.1186/1750-1172-8-55

Keynote webinar | Spotlight on medication adherence

Springer Medicine

miR-411 is up-regulated in FSHD myoblasts and suppresses myogenic factors

Abstract

Background

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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