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Article

Myogenic Enhancers Regulate Expression of the Facioscapulohumeral Muscular Dystrophy-Associated DUX4 Gene

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Pages 1942-1955 | Received 28 Jan 2014, Accepted 11 Mar 2014, Published online: 20 Mar 2023

REFERENCES

  • Padberg GW. 1982. Facioscapulohumeral disease. Ph.D. thesis. Leiden University, Leiden, The Netherlands.
  • Tawil R, Van Der Maarel SM. 2006. Facioscapulohumeral muscular dystrophy. Muscle Nerve 34:1–15. http://dx.doi.org/10.1002/mus.20522.
  • van Deutekom JC, Wijmenga C, van Tienhoven EA, Gruter AM, Hewitt JE, Padberg GW, van Ommen GJ, Hofker MH, Frants RR. 1993. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum. Mol. Genet. 2:2037–2042. http://dx.doi.org/10.1093/hmg/2.12.2037.
  • Wijmenga C, Frants RR, Brouwer OF, Moerer P, Weber JL, Padberg GW. 1990. Location of facioscapulohumeral muscular dystrophy gene on chromosome 4. Lancet 336:651–653. http://dx.doi.org/10.1016/0140-6736(90)92148-B.
  • Wijmenga C, Sandkuijl LA, Moerer P, van der Boorn N, Bodrug SE, Ray PN, Brouwer OF, Murray JC, van Ommen GJ, Padberg GW, Frants RR. 1992. Genetic linkage map of facioscapulohumeral muscular dystrophy and five polymorphic loci on chromosome 4q35-qter. Am. J. Hum. Genet. 51:411–415.
  • Lemmers RJ, van der Vliet PJ, van der Gaag KJ, Zuniga S, Frants RR, de Knijff P, van der Maarel SM. 2010. Worldwide population analysis of the 4q and 10q subtelomeres identifies only four discrete interchromosomal sequence transfers in human evolution. Am. J. Hum. Genet. 86:364–377. http://dx.doi.org/10.1016/j.ajhg.2010.01.035.
  • Lemmers RJ, de Kievit P, Sandkuijl L, Padberg GW, van Ommen GJ, Frants RR, van der Maarel SM. 2002. Facioscapulohumeral muscular dystrophy is uniquely associated with one of the two variants of the 4q subtelomere. Nat. Genet. 32:235–236. http://dx.doi.org/10.1038/ng999.
  • Lemmers RJ, Wohlgemuth M, van der Gaag KJ, van der Vliet PJ, van Teijlingen CM, de Knijff P, Padberg GW, Frants RR, van der Maarel SM. 2007. Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 81:884–894. http://dx.doi.org/10.1086/521986.
  • Gilbert JR, Stajich JM, Wall S, Carter SC, Qiu H, Vance JM, Stewart CS, Speer MC, Pufky J, Yamaoka LH, Rozear M, Samson F, Fardeau M, Roses AD, Pericak-Vance MA. 1993. Evidence for heterogeneity in facioscapulohumeral muscular dystrophy (FSHD). Am. J. Hum. Genet. 53:401–408.
  • de Greef JC, Lemmers RJ, van Engelen BG, Sacconi S, Venance SL, Frants RR, Tawil R, van der Maarel SM. 2009. Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum. Mutat. 30:1449–1459. http://dx.doi.org/10.1002/humu.21091.
  • Lemmers RJL, de Kievit P, van Geel M, van der Wielen MJ, Bakker E, Padberg GW, Frants RR, van der Maarel SM. 2001. Complete allele information in the diagnosis of facioscapulohumeral muscular dystrophy by triple DNA analysis. Ann. Neurol. 50:816–819. http://dx.doi.org/10.1002/ana.10057.
  • van Overveld PG, Lemmers RJ, Sandkuijl LA, Enthoven L, Winokur ST, Bakels F, Padberg GW, van Ommen GJ, Frants RR, van der Maarel SM. 2003. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat. Genet. 35:315–317. http://dx.doi.org/10.1038/ng1262.
  • Yang F, Shao C, Vedanarayanan V, Ehrlich M. 2004. Cytogenetic and immuno-FISH analysis of the 4q subtelomeric region, which is associated with facioscapulohumeral muscular dystrophy. Chromosoma 112:350–359. http://dx.doi.org/10.1007/s00412-004-0280-x.
  • Jiang G, Yang F, van Overveld PG, Vedanarayanan V, van der Maarel S, Ehrlich M. 2003. Testing the position-effect variegation hypothesis for facioscapulohumeral muscular dystrophy by analysis of histone modification and gene expression in subtelomeric 4q. Hum. Mol. Genet. 12:2909–2921. http://dx.doi.org/10.1093/hmg/ddg323.
  • Zeng W, de Greef JC, Chen YY, Chien R, Kong X, Gregson HC, Winokur ST, Pyle A, Robertson KD, Schmiesing JA, Kimonis VE, Balog J, Frants RR, Ball ARJr, Lock LF, Donovan PJ, van der Maarel SM, Yokomori K. 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. http://dx.doi.org/10.1371/journal.pgen.1000559.
  • Cabianca DS, Casa V, Bodega B, Xynos A, Ginelli E, Tanaka Y, Gabellini D. 2012. A long ncRNA links copy number variation to a Polycomb/Trithorax epigenetic switch in FSHD muscular dystrophy. Cell 149:819–831. http://dx.doi.org/10.1016/j.cell.2012.03.035.
  • Hartweck LM, Anderson LJ, Lemmers RJ, Dandapat A, Toso EA, Dalton JC, Tawil R, Day JW, van der Maarel SM, Kyba M. 2013. A focal domain of extreme demethylation within D4Z4 in FSHD2. Neurology 80:392–399. http://dx.doi.org/10.1212/WNL.0b013e31827f075c.
  • Lemmers RJ, Tawil R, Petek LM, Balog J, Block GJ, Santen GW, Amell AM, van der Vliet PJ, Almomani R, Straasheijm KR, Krom YD, Klooster R, Sun Y, den Dunnen JT, Helmer Q, Donlin-Smith CM, Padberg GW, van Engelen BG, de Greef JC, Aartsma-Rus AM, Frants RR, de Visser M, Desnuelle C, Sacconi S, Filippova GN, Bakker B, Bamshad MJ, Tapscott SJ, Miller DG, van der Maarel SM. 2012. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat. Genet. 44:1370–1374. http://dx.doi.org/10.1038/ng.2454.
  • Mitsuhashi S, Boyden SE, Estrella EA, Jones TI, Rahimov F, Yu TW, Darras BT, Amato AA, Folkerth RD, Jones PL, Kunkel LM, Kang PB. 2013. Exome sequencing identifies a novel SMCHD1 mutation in facioscapulohumeral muscular dystrophy 2. Neuromuscul. Disord. 23:975–980. http://dx.doi.org/10.1016/j.nmd.2013.08.009.
  • Sacconi S, Lemmers RJ, Balog J, van der Vliet PJ, Lahaut P, van Nieuwenhuizen MP, Straasheijm KR, Debipersad RD, Vos-Versteeg M, Salviati L, Casarin A, Pegoraro E, Tawil R, Bakker E, Tapscott SJ, Desnuelle C, van der Maarel SM. 2013. The FSHD2 gene SMCHD1 is a modifier of disease severity in families affected by FSHD1. Am. J. Hum. Genet. 93:744–751. http://dx.doi.org/10.1016/j.ajhg.2013.08.004.
  • Gabellini D, Green MR, Tupler R. 2002. Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 110:339–348. http://dx.doi.org/10.1016/S0092-8674(02)00826-7.
  • Bodega B, Ramirez GD, Grasser F, Cheli S, Brunelli S, Mora M, Meneveri R, Marozzi A, Mueller S, Battaglioli E, Ginelli E. 2009. Remodeling of the chromatin structure of the facioscapulohumeral muscular dystrophy (FSHD) locus and upregulation of FSHD-related gene 1 (FRG1) expression during human myogenic differentiation. BMC Biol. 7:41. http://dx.doi.org/10.1186/1741-7007-7-41.
  • Cabianca DS, Gabellini D. 2010. The cell biology of disease: FSHD: copy number variations on the theme of muscular dystrophy. J. Cell Biol. 191:1049–1060. http://dx.doi.org/10.1083/jcb.201007028.
  • Ottaviani A, Rival-Gervier S, Boussouar A, Foerster AM, Rondier D, Sacconi S, Desnuelle C, Gilson E, Magdinier F. 2009. The D4Z4 macrosatellite repeat acts as a CTCF and A-type lamins-dependent insulator in facio-scapulo-humeral dystrophy. PLoS Genet. 5:e1000394. http://dx.doi.org/10.1371/journal.pgen.1000394.
  • Petrov A, Pirozhkova I, Carnac G, Laoudj D, Lipinski M, Vassetzky YS. 2006. Chromatin loop domain organization within the 4q35 locus in facioscapulohumeral dystrophy patients versus normal human myoblasts. Proc. Natl. Acad. Sci. U. S. A. 103:6982–6987. http://dx.doi.org/10.1073/pnas.0511235103.
  • Petrov A, Allinne J, Pirozhkova I, Laoudj D, Lipinski M, Vassetzky YS. 2008. A nuclear matrix attachment site in the 4q35 locus has an enhancer-blocking activity in vivo: implications for the facio-scapulo-humeral dystrophy. Genome Res. 18:39–45.
  • Snider L, Geng LN, Lemmers RJ, Kyba M, Ware CB, Nelson AM, Tawil R, Filippova GN, van der Maarel SM, Tapscott SJ, Miller DG. 2010. Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet. 6:e1001181. http://dx.doi.org/10.1371/journal.pgen.1001181.
  • Jones TI, Chen JC, Rahimov F, Homma S, Arashiro P, Beermann ML, King OD, Miller JB, Kunkel LM, Emerson CPJr, Wagner KR, Jones PL. 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. http://dx.doi.org/10.1093/hmg/dds284.
  • Gabriels J, Beckers MC, Ding H, De Vriese A, Plaisance S, van der Maarel SM, Padberg GW, Frants RR, Hewitt JE, Collen D, Belayew A. 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. http://dx.doi.org/10.1016/S0378-1119(99)00267-X.
  • Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, Dauwerse JG, Snider L, Straasheijm KR, van Ommen GJ, Padberg GW, Miller DG, Tapscott SJ, Tawil R, Frants RR, van der Maarel SM. 2010. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329:1650–1653. http://dx.doi.org/10.1126/science.1189044.
  • Kowaljow V, Marcowycz A, Ansseau E, Conde CB, Sauvage S, Matteotti C, Arias C, Corona ED, Nunez NG, Leo O, Wattiez R, Figlewicz D, Laoudj-Chenivesse D, Belayew A, Coppee F, Rosa AL. 2007. The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul. Disord. 17:611–623. http://dx.doi.org/10.1016/j.nmd.2007.04.002.
  • Bosnakovski D, Xu Z, Gang EJ, Galindo CL, Liu M, Simsek T, Garner HR, Agha-Mohammadi S, Tassin A, Coppee F, Belayew A, Perlingeiro RR, Kyba M. 2008. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J. 27:2766–2779. http://dx.doi.org/10.1038/emboj.2008.201.
  • Bosnakovski D, Daughters RS, Xu Z, Slack JM, Kyba M. 2009. Biphasic myopathic phenotype of mouse DUX, an ORF within conserved FSHD-related repeats. PLoS One 4:e7003. http://dx.doi.org/10.1371/journal.pone.0007003.
  • Wallace LM, Garwick SE, Mei W, Belayew A, Coppee F, Ladner KJ, Guttridge D, Yang J, Harper SQ. 2011. DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy in vivo. Ann. Neurol. 69:540–552. http://dx.doi.org/10.1002/ana.22275.
  • 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.
  • Geng LN, Yao Z, Snider L, Fong AP, Cech JN, Young JM, van der Maarel SM, Ruzzo WL, Gentleman RC, Tawil R, Tapscott SJ. 2012. DUX4 activates germline genes, retroelements, and immune mediators: implications for facioscapulohumeral dystrophy. Dev. Cell 22:38–51. http://dx.doi.org/10.1016/j.devcel.2011.11.013.
  • Miller JB, Crow MT, Stockdale FE. 1985. Slow and fast myosin heavy chain content defines three types of myotubes in early muscle cell cultures. J. Cell Biol. 101:1643–1650. http://dx.doi.org/10.1083/jcb.101.5.1643.
  • Nelson JD, Denisenko O, Bomsztyk K. 2006. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 1:179–185. http://dx.doi.org/10.1038/nprot.2006.27.
  • Taberlay PC, Kelly TK, Liu CC, You JS, De Carvalho DD, Miranda TB, Zhou XJ, Liang G, Jones PA. 2011. Polycomb-repressed genes have permissive enhancers that initiate reprogramming. Cell 147:1283–1294. http://dx.doi.org/10.1016/j.cell.2011.10.040.
  • Naumova N, Smith EM, Zhan Y, Dekker J. 2012. Analysis of long-range chromatin interactions using chromosome conformation capture. Methods 58:192–203. http://dx.doi.org/10.1016/j.ymeth.2012.07.022.
  • van Geel M, Heather LJ, Lyle R, Hewitt JE, Frants RR, de Jong PJ. 1999. The FSHD region on human chromosome 4q35 contains potential coding regions among pseudogenes and a high density of repeat elements. Genomics 61:55–65. http://dx.doi.org/10.1006/geno.1999.5942.
  • Homma S, Chen JC, Rahimov F, Beermann ML, Hanger K, Bibat GM, Wagner KR, Kunkel LM, Emerson CPJr, Miller JB. 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. http://dx.doi.org/10.1038/ejhg.2011.213.
  • Geng LN, Tyler AE, Tapscott SJ. 2011. Immunodetection of human double homeobox 4. Hybridoma (Larchmt.) 30:125–130. http://dx.doi.org/10.1089/hyb.2010.0094.
  • Bader D, Masaki T, Fischman DA. 1982. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95:763–770. http://dx.doi.org/10.1083/jcb.95.3.763.
  • Broucqsault N, Morere J, Gaillard MC, Dumonceaux J, Torrents J, Salort-Campana E, Maues de Paula A, Bartoli M, Fernandez C, Chesnais AL, Ferreboeuf M, Sarda L, Dufour H, Desnuelle C, Attarian S, Levy N, Nguyen K, Magdinier F, Roche S. 2013. Dysregulation of 4q35- and muscle-specific genes in fetuses with a short D4Z4 array linked to facio-scapulo-humeral dystrophy. Hum. Mol. Genet. 22:4206–4214. http://dx.doi.org/10.1093/hmg/ddt272.
  • Rahimov F, King OD, Leung DG, Bibat GM, Emerson CPJr, Kunkel LM, Wagner KR. 2012. Transcriptional profiling in facioscapulohumeral muscular dystrophy to identify candidate biomarkers. Proc. Natl. Acad. Sci. U. S. A. 109:16234–16239. http://dx.doi.org/10.1073/pnas.1209508109.
  • Pirozhkova I, Petrov A, Dmitriev P, Laoudj D, Lipinski M, Vassetzky Y. 2008. A functional role for 4qA/B in the structural rearrangement of the 4q35 region and in the regulation of FRG1 and ANT1 in facioscapulohumeral dystrophy. PLoS One 3:e3389. http://dx.doi.org/10.1371/journal.pone.0003389.
  • Natoli G, Andrau JC. 2012. Noncoding transcription at enhancers: general principles and functional models. Annu. Rev. Genet. 46:1–19. http://dx.doi.org/10.1146/annurev-genet-110711-155459.
  • Ong CT, Corces VG. 2012. Enhancers: emerging roles in cell fate specification. EMBO Rep. 13:423–430. http://dx.doi.org/10.1038/embor.2012.52.
  • Andreu-Vieyra C, Lai J, Berman BP, Frenkel B, Jia L, Jones PA, Coetzee GA. 2011. Dynamic nucleosome-depleted regions at androgen receptor enhancers in the absence of ligand in prostate cancer cells. Mol. Cell. Biol. 31:4648–4662. http://dx.doi.org/10.1128/MCB.05934-11.
  • You JS, Kelly TK, De Carvalho DD, Taberlay PC, Liang G, Jones PA. 2011. OCT4 establishes and maintains nucleosome-depleted regions that provide additional layers of epigenetic regulation of its target genes. Proc. Natl. Acad. Sci. U. S. A. 108:14497–14502. http://dx.doi.org/10.1073/pnas.1111309108.
  • Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA. 2012. Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res. 22:2497–2506. http://dx.doi.org/10.1101/gr.143008.112.
  • Wolff EM, Byun HM, Han HF, Sharma S, Nichols PW, Siegmund KD, Yang AS, Jones PA, Liang G. 2010. Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer. PLoS Genet. 6:e1000917. http://dx.doi.org/10.1371/journal.pgen.1000917.
  • Bakshi R, Hassan MQ, Pratap J, Lian JB, Montecino MA, van Wijnen AJ, Stein JL, Imbalzano AN, Stein GS. 2010. The human SWI/SNF complex associates with RUNX1 to control transcription of hematopoietic target genes. J. Cell. Physiol. 225:569–576. http://dx.doi.org/10.1002/jcp.22240.
  • de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, Tapscott SJ, Imbalzano AN. 2005. MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol. Cell. Biol. 25:3997–4009. http://dx.doi.org/10.1128/MCB.25.10.3997-4009.2005.
  • Leidenroth A, Clapp J, Mitchell LM, Coneyworth D, Dearden FL, Iannuzzi L, Hewitt JE. 2012. Evolution of DUX gene macrosatellites in placental mammals. Chromosoma 121:489–497. http://dx.doi.org/10.1007/s00412-012-0380-y.
  • Clapp J, Mitchell LM, Bolland DJ, Fantes J, Corcoran AE, Scotting PJ, Armour JA, Hewitt JE. 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. http://dx.doi.org/10.1086/519311.
  • Soleimani VD, Yin H, Jahani-Asl A, Ming H, Kockx CE, van Ijcken WF, Grosveld F, Rudnicki MA. 2012. Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis. Mol. Cell 47:457–468. http://dx.doi.org/10.1016/j.molcel.2012.05.046.
  • Blackwell TK, Weintraub H. 1990. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250:1104–1110. http://dx.doi.org/10.1126/science.2174572.
  • Wright WE, Binder M, Funk W. 1991. Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site. Mol. Cell. Biol. 11:4104–4110.
  • Buskin JN, Hauschka SD. 1989. Identification of a myocyte nuclear factor that binds to the muscle-specific enhancer of the mouse muscle creatine kinase gene. Mol. Cell. Biol. 9:2627–2640.
  • Kophengnavong T, Michnowicz JE, Blackwell TK. 2000. Establishment of distinct MyoD, E2A, and twist DNA binding specificities by different basic region-DNA conformations. Mol. Cell. Biol. 20:261–272. http://dx.doi.org/10.1128/MCB.20.1.261-272.2000.
  • Molkentin JD, Black BL, Martin JF, Olson EN. 1995. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell 83:1125–1136. http://dx.doi.org/10.1016/0092-8674(95)90139-6.
  • Maeda T, Chapman DL, Stewart AF. 2002. Mammalian vestigial-like 2, a cofactor of TEF-1 and MEF2 transcription factors that promotes skeletal muscle differentiation. J. Biol. Chem. 277:48889–48898. http://dx.doi.org/10.1074/jbc.M206858200.
  • Maeda T, Gupta MP, Stewart AF. 2002. TEF-1 and MEF2 transcription factors interact to regulate muscle-specific promoters. Biochem. Biophys. Res. Commun. 294:791–797. http://dx.doi.org/10.1016/S0006-291X(02)00556-9.
  • Groisman R, Masutani H, Leibovitch MP, Robin P, Soudant I, Trouche D, Harel-Bellan A. 1996. Physical interaction between the mitogen-responsive serum response factor and myogenic basic-helix-loop-helix proteins. J. Biol. Chem. 271:5258–5264. http://dx.doi.org/10.1074/jbc.271.9.5258.
  • Gupta M, Kogut P, Davis FJ, Belaguli NS, Schwartz RJ, Gupta MP. 2001. Physical interaction between the MADS box of serum response factor and the TEA/ATTS DNA-binding domain of transcription enhancer factor-1. J. Biol. Chem. 276:10413–10422. http://dx.doi.org/10.1074/jbc.M008625200.
  • Delgado-Olguin P, Brand-Arzamendi K, Scott IC, Jungblut B, Stainier DY, Bruneau BG, Recillas-Targa F. 2011. CTCF promotes muscle differentiation by modulating the activity of myogenic regulatory factors. J. Biol. Chem. 286:12483–12494. http://dx.doi.org/10.1074/jbc.M110.164574.
  • 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. 2004. FRG2, an FSHD candidate gene, is transcriptionally upregulated in differentiating primary myoblast cultures of FSHD patients. J. Med. Genet. 41:826–836. http://dx.doi.org/10.1136/jmg.2004.019364.
  • Dmitriev P, Petrov A, Ansseau E, Stankevicins L, Charron S, Kim E, Bos TJ, Robert T, Turki A, Coppee F, Belayew A, Lazar V, Carnac G, Laoudj D, Lipinski M, Vassetzky YS. 2011. The Kruppel-like factor 15 as a molecular link between myogenic factors and a chromosome 4q transcriptional enhancer implicated in facioscapulohumeral dystrophy. J. Biol. Chem. 286:44620–44631. http://dx.doi.org/10.1074/jbc.M111.254052.
  • Caruso N, Herberth B, Bartoli M, Puppo F, Dumonceaux J, Zimmermann A, Denadai S, Lebosse M, Roche S, Geng L, Magdinier F, Attarian S, Bernard R, Maina F, Levy N, Helmbacher F. 2013. Deregulation of the protocadherin gene FAT1 alters muscle shapes: implications for the pathogenesis of facioscapulohumeral dystrophy. PLoS Genet. 9:e1003550. http://dx.doi.org/10.1371/journal.pgen.1003550.
  • Lang D, Powell SK, Plummer RS, Young KP, Ruggeri BA. 2007. PAX genes: roles in development, pathophysiology, and cancer. Biochem. Pharmacol. 73:1–14. http://dx.doi.org/10.1016/j.bcp.2006.06.024.
  • Wang YX, Rudnicki MA. 2012. Satellite cells, the engines of muscle repair. Nat. Rev. Mol. Cell Biol. 13:127–133.
  • Sanyal A, Lajoie BR, Jain G, Dekker J. 2012. The long-range interaction landscape of gene promoters. Nature 489:109–113. http://dx.doi.org/10.1038/nature11279.
  • Lemmers RJ, Osborn M, Haaf T, Rogers M, Frants RR, Padberg GW, Cooper DN, van der Maarel SM, Upadhyaya M. 2003. D4F104S1 deletion in facioscapulohumeral muscular dystrophy: phenotype, size, and detection. Neurology 61:178–183. http://dx.doi.org/10.1212/01.WNL.0000078889.51444.81.
  • Hou C, Corces VG. 2012. Throwing transcription for a loop: expression of the genome in the 3D nucleus. Chromosoma 121:107–116. http://dx.doi.org/10.1007/s00412-011-0352-7.
  • Mousavi K, Zare H, Dell'orso S, Grontved L, Gutierrez-Cruz G, Derfoul A, Hager GL, Sartorelli V. 2013. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell 51:606–617. http://dx.doi.org/10.1016/j.molcel.2013.07.022.
  • Sanchez A, Golding I. 2013. Genetic determinants and cellular constraints in noisy gene expression. Science 342:1188–1193. http://dx.doi.org/10.1126/science.1242975.
  • Carvajal JJ, Keith A, Rigby PW. 2008. Global transcriptional regulation of the locus encoding the skeletal muscle determination genes Mrf4 and Myf5. Genes Dev. 22:265–276. http://dx.doi.org/10.1101/gad.442408.
  • Krom YD, Thijssen PE, Young JM, den Hamer B, Balog J, Yao Z, Maves L, Snider L, Knopp P, Zammit PS, Rijkers T, van Engelen BG, Padberg GW, Frants RR, Tawil R, Tapscott SJ, van der Maarel SM. 2013. Intrinsic epigenetic regulation of the D4Z4 macrosatellite repeat in a transgenic mouse model for FSHD. PLoS Genet. 9:e1003415. http://dx.doi.org/10.1371/journal.pgen.1003415.
  • Funakoshi M, Goto K, Arahata K. 1998. Epilepsy and mental retardation in a subset of early onset 4q35-facioscapulohumeral muscular dystrophy. Neurology 50:1791–1794. http://dx.doi.org/10.1212/WNL.50.6.1791.
  • Padberg GW, Brouwer OF, de Keizer RJ, Dijkman G, Wijmenga C, Grote JJ, Frants RR. 1995. On the significance of retinal vascular disease and hearing loss in facioscapulohumeral muscular dystrophy. Muscle Nerve 2:S73–S80.
  • Fitzsimons RB, Gurwin EB, Bird AC. 1987. Retinal vascular abnormalities in facioscapulohumeral muscular dystrophy. A general association with genetic and therapeutic implications. Brain 110:631–648.
  • Block GJ, Narayanan D, Amell AM, Petek LM, Davidson KC, Bird TD, Tawil R, Moon RT, Miller DG. 2013. Wnt/beta-catenin signaling suppresses DUX4 expression and prevents apoptosis of FSHD muscle cells. Hum. Mol. Genet. 22:4661–4672. http://dx.doi.org/10.1093/hmg/ddt314.
  • Atcha FA, Syed A, Wu B, Hoverter NP, Yokoyama NN, Ting JH, Munguia JE, Mangalam HJ, Marsh JL, Waterman ML. 2007. A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol. Cell. Biol. 27:8352–8363. http://dx.doi.org/10.1128/MCB.02132-06.
  • Block GJ, Petek LM, Narayanan D, Amell AM, Moore JM, Rabaia NA, Tyler A, van der Maarel SM, Tawil R, Filippova GN, Miller DG. 2012. Asymmetric bidirectional transcription from the FSHD-Causing D4Z4 array modulates DUX4 production. PLoS One 7:e35532. http://dx.doi.org/10.1371/journal.pone.0035532.
  • Maurano MT, Humbert R, Rynes E, Thurman RE, Haugen E, Wang H, Reynolds AP, Sandstrom R, Qu H, Brody J, Shafer A, Neri F, Lee K, Kutyavin T, Stehling-Sun S, Johnson AK, Canfield TK, Giste E, Diegel M, Bates D, Hansen RS, Neph S, Sabo PJ, Heimfeld S, Raubitschek A, Ziegler S, Cotsapas C, Sotoodehnia N, Glass I, Sunyaev SR, Kaul R, Stamatoyannopoulos JA. 2012. Systematic localization of common disease-associated variation in regulatory DNA. Science 337:1190–1195. http://dx.doi.org/10.1126/science.1222794.
  • Goldhamer DJ, Brunk BP, Faerman A, King A, Shani M, Emerson CPJr. 1995. Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121:637–649.

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