Staufen1s role as a splicing factor and a disease modifier in Myotonic Dystrophy Type I

References

• Micklem DR, Adams J, Grünert S, St Johnston D. Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J 2000; 19:1366-77; PMID:10716936; http://dx.doi.org/10.1093/emboj/19.6.1366
   Google Scholar
• Duchaîne TF, Hemraj I, Furic L, Deitinghoff A, Kiebler MA, DesGroseillers L. Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. J Cell Sci 2002; 115:3285-95; PMID:12140260
   Google Scholar
• Ephrussi A, Dickinson LK, Lehmann R. Oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 1991; 66:37-50; PMID:2070417; http://dx.doi.org/10.1016/0092-8674(91)90137-N
   Google Scholar
• St Johnston D, Nüsslein-Volhard C. The origin of pattern and polarity in the Drosophila embryo. Cell 1992; 68:201-19; PMID:1733499; http://dx.doi.org/10.1016/0092-8674(92)90466-P
   Google Scholar
• Wickham L, Duchaîne T, Luo M, Nabi IR, DesGroseillers L. Mammalian staufen is a double-stranded-RNA-and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol Cell Biol 1999; 19:2220-30; PMID:10022909; http://dx.doi.org/10.1128/MCB.19.3.2220
   Google Scholar
• Dugré-Brisson S, Elvira G, Boulay K, Chatel-Chaix L, Mouland AJ, DesGroseillers L. Interaction of Staufen1 with the 5′ end of mRNA facilitates translation of these RNAs. Nucleic Acids Res 2005; 33:4797-812; http://dx.doi.org/10.1093/nar/gki794
   Google Scholar
• Dubnau J, Chiang A-S, Grady L, Barditch J, Gossweiler S, McNeil J, Smith P, Buldoc F, Scott R, Certa U, et al. The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 2003; 13:286-96; PMID:12593794; http://dx.doi.org/10.1016/S0960-9822(03)00064-2
   Google Scholar
• Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, Maquat LE. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 2007; 26:2670-81; PMID:17510634; http://dx.doi.org/10.1038/sj.emboj.7601712
   Google Scholar
• Ravel-Chapuis A, Bélanger G, Yadava RS, Mahadevan MS, DesGroseillers L, Côté J, Jasmin BJ. The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing. J Cell Biol 2012; 196:699-712; PMID:22431750; http://dx.doi.org/10.1083/jcb.201108113
   Google Scholar
• Sugimoto Y, Vigilante A, Darbo E, Zirra A, Militti C, D'Ambrogio A, Luscombe NM, Ule J. hiCLIP reveals the in vivo atlas of mRNA secondary structures recognized by Staufen 1. Nature 2015; 519:491-4; PMID:25799984; http://dx.doi.org/10.1038/nature14280
   Google Scholar
• Furic L, Maher-Laporte M, DesGroseillers L. A genome-wide approach identifies distinct but overlapping subsets of cellular mRNAs associated with Staufen1-and Staufen2-containing ribonucleoprotein complexes. Rna 2008; 14:324-35; PMID:18094122; http://dx.doi.org/10.1261/rna.720308
   Google Scholar
• Laver JD, Li X, Ancevicius K, Westwood JT, Smibert CA, Morris QD, Lipshitz HD. Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity. Nucleic Acids Res 2013; 41:9438-60; PMID:23945942; http://dx.doi.org/10.1093/nar/gkt702
   Google Scholar
• Ricci EP, Kucukural A, Cenik C, Mercier BC, Singh G, Heyer EE, Ashar-Patel A, Peng L, Moore MJ. Staufen1 senses overall transcript secondary structure to regulate translation. Nat Struct Mol Biol 2014; 21:26-35; PMID:24336223; http://dx.doi.org/10.1038/nsmb.2739
   Google Scholar
• de Lucas S, Oliveros JC, Chagoyen M, Ortín J. Functional signature for the recognition of specific target mRNAs by human Staufen1 protein. Nucleic Acids Res 2014; 42:4516-26; PMID:24470147; http://dx.doi.org/10.1093/nar/gku073
   Google Scholar
• Elbarbary RA, Li W, Tian B, Maquat LE. STAU1 binding 3′ UTR IRAlus complements nuclear retention to protect cells from PKR-mediated translational shutdown. Genes Dev 2013; 27:1495-510; PMID:23824540; http://dx.doi.org/10.1101/gad.220962.113
   Google Scholar
• Gong C, Maquat LE. lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3 [prime] UTRs via Alu elements. Nature 2011; 470:284-8; PMID:21307942
   Google Scholar
• Lee J-H, Oh J-Y, Pascua PNQ, Kim E-G, Choi Y-K, Kim HK. Impairment of the Staufen1-NS1 interaction reduces influenza viral replication. Biochem Biophys Res Commun 2011; 414:153-8; PMID:21945618; http://dx.doi.org/10.1016/j.bbrc.2011.09.042
   Google Scholar
• Gautrey H, McConnell J, Lako M, Hall J, Hesketh J. Staufen1 is expressed in preimplantation mouse embryos and is required for embryonic stem cell differentiation. Biochim Biophys Acta 2008; 1783:1935-42; PMID:18585410; http://dx.doi.org/10.1016/j.bbamcr.2008.05.017
   Google Scholar
• Martel C, Macchi P, Furic L, Kiebler M, Desgroseillers L. Staufen1 is imported into the nucleolus via a bipartite nuclear localization signal and several modulatory determinants. Biochem J 2006; 393:245-54; PMID:16162096; http://dx.doi.org/10.1042/BJ20050694
   Google Scholar
• Milev MP, Ravichandran M, Khan MF, Schriemer DC, Mouland AJ. Characterization of staufen1 ribonucleoproteins by mass spectrometry and biochemical analyses reveal the presence of diverse host proteins associated with human immunodeficiency virus type 1. Front Microbiol 2012; 3:367; PMID:23125841; http://dx.doi.org/10.3389/fmicb.2012.00367
   Google Scholar
• Heraud-Farlow JE, Sharangdhar T, Li X, Pfeifer P, Tauber S, Orozco D, Hörmann A, Thomas S, Bakosova A, Farlow AR, et al. Staufen2 regulates neuronal target RNAs. Cell Rep 2013; 5:1511-8; PMID:24360961; http://dx.doi.org/10.1016/j.celrep.2013.11.039
   Google Scholar
• Kosaki A, Nelson J, Webster NJ. Identification of intron and exon sequences involved in alternative splicing of insulin receptor pre-mRNA. J Biol Chem 1998; 273:10331-7; PMID:9553088; http://dx.doi.org/10.1074/jbc.273.17.10331
   Google Scholar
• Zarnack K, König J, Tajnik M, Martincorena I, Eustermann S, Stévant I, Reyes A, Anders S, Luscombe NM, Ule J. Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements. Cell 2013; 152:453-66; PMID:23374342; http://dx.doi.org/10.1016/j.cell.2012.12.023
   Google Scholar
• Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Hudson T, et al. Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 1992; 68:799-808; PMID:1310900; http://dx.doi.org/10.1016/0092-8674(92)90154-5
   Google Scholar
• Napierala M, Krzyzosiak WJ. CUG repeats present in myotonin kinase RNA form metastable “slippery” hairpins. J Biol Chem 1997; 272:31079-85; PMID:9388259; http://dx.doi.org/10.1074/jbc.272.49.31079
   Google Scholar
• Gauthier M, Marteyn A, Denis JA, Cailleret M, Giraud-Triboult K, Aubert S, Lecuyer C, Marie J, Furling D, Vernet R, et al. A defective Krab-domain zinc-finger transcription factor contributes to altered myogenesis in myotonic dystrophy type 1. Hum Mol Genet 2013; 22:5188-98; PMID:23922231; http://dx.doi.org/10.1093/hmg/ddt373
   Google Scholar
• Lee KY, Li M, Manchanda M, Batra R, Charizanis K, Mohan A, Warren SA, Chamberlain CM, Finn D, Hong H, et al. Compound loss of muscleblind-like function in myotonic dystrophy. EMBO Mol Med 2013; 5:1887-900; PMID:24293317; http://dx.doi.org/10.1002/emmm.201303275
   Google Scholar
• Philips AV, Timchenko LT, Cooper TA. Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 1998; 280:737-41; PMID:9563950; http://dx.doi.org/10.1126/science.280.5364.737
   Google Scholar
• Miller JW, Urbinati CR, Teng‐umnuay P, Stenberg MG, Byrne BJ, Thornton CA, Swanson MS. Recruitment of human muscleblind proteins to (CUG) n expansions associated with myotonic dystrophy. EMBO J 2000; 19:4439-48; PMID:10970838; http://dx.doi.org/10.1093/emboj/19.17.4439
   Google Scholar
• Mahadevan M, Tsilfidis C, Sabourin L, Shutler G, Amemiya C, Jansen G, Neville C, Narang M, Barceló J, O'Hoy K, et al. Myotonic dystrophy mutation: an unstable CTG repeat in the 3′untranslated region of the gene. Science 1992; 255:1253-5; PMID:1546325; http://dx.doi.org/10.1126/science.1546325
   Google Scholar
• Ebralidze A, Wang Y, Petkova V, Ebralidse K, Junghans R. RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science 2004; 303:383-7; PMID:14657503; http://dx.doi.org/10.1126/science.1088679
   Google Scholar
• Timchenko L. Molecular mechanisms of muscle atrophy in myotonic dystrophies. Int J Biochem Cell Biol 2013; 45:2280-7; PMID:23796888; http://dx.doi.org/10.1016/j.biocel.2013.06.010
   Google Scholar
• Thornton CA. Myotonic dystrophy. Neurol Clin 2014; 32:705-19; PMID:25037086; http://dx.doi.org/10.1016/j.ncl.2014.04.011
   Google Scholar
• Krol J, Fiszer A, Mykowska A, Sobczak K, de Mezer M, Krzyzosiak WJ. Ribonuclease dicer cleaves triplet repeat hairpins into shorter repeats that silence specific targets. Mol Cell 2007; 25:575-86; PMID:17317629; http://dx.doi.org/10.1016/j.molcel.2007.01.031
   Google Scholar
• Batra R, Charizanis K, Manchanda M, Mohan A, Li M, Finn DJ, Goodwin M, Zhang C, Sobczak K, Thornton CA, et al. Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease. Mol Cell 2014; 56:311-22; PMID:25263597; http://dx.doi.org/10.1016/j.molcel.2014.08.027
   Google Scholar
• Rau F, Freyermuth F, Fugier C, Villemin J-P, Fischer M-C, Jost B, Dembele D, Gourdon G, Nicole A, Duboc D, et al. Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat Struct Mol Biol 2011; 18:840-5; PMID:21685920; http://dx.doi.org/10.1038/nsmb.2067
   Google Scholar
• Zu T, Gibbens B, Doty NS, Gomes-Pereira M, Huguet A, Stone MD, Margolis J, Peterson M, Markowski TW, Ingram MA, et al. Non-ATG–initiated translation directed by microsatellite expansions. Proc Natl Acad Sci 2011; 108:260-5; PMID:21173221; http://dx.doi.org/10.1073/pnas.1013343108
   Google Scholar
• Sicot G, Gourdon G, Gomes-Pereira M. Myotonic dystrophy, when simple repeats reveal complex pathogenic entities: new findings and future challenges. Hum Mol Genet 2011; 20:R116-R23; PMID:21821673; http://dx.doi.org/10.1093/hmg/ddr343
   Google Scholar
• Klinck R, Fourrier A, Thibault P, Toutant J, Durand M, Lapointe E, Caillet-Boudin ML, Sergeant N, Gourdon G, Meola G, et al. RBFOX1 cooperates with MBNL1 to control splicing in muscle, including events altered in myotonic dystrophy type 1. PLoS One 2014; 9:e107324; PMID:25211016; http://dx.doi.org/10.1371/journal.pone.0107324
   Google Scholar
• Sueoka E, Sueoka N, Goto Y, Matsuyama S, Nishimura H, Sato M, Fujimura S, Chiba H, Fujiki H. Heterogeneous nuclear ribonucleoprotein B1 as early cancer biomarker for occult cancer of human lungs and bronchial dysplasia. Cancer Res 2001; 61:1896-902; PMID:11280744
   Google Scholar
• Zhang S, Schlott B, Görlach M, Grosse F. DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner. Nucleic Acids Res 2004; 32:1-10; PMID:14704337; http://dx.doi.org/10.1093/nar/gkg933
   Google Scholar
• Warf MB, Diegel JV, von Hippel PH, Berglund JA. The protein factors MBNL1 and U2AF65 bind alternative RNA structures to regulate splicing. Proc Natl Acad Sci 2009; 106:9203-8; PMID:19470458; http://dx.doi.org/10.1073/pnas.0900342106
   Google Scholar
• Jones K, Wei C, Schoser B, Meola G, Timchenko N, Timchenko L. Reduction of toxic RNAs in myotonic dystrophies type 1 and type 2 by the RNA helicase p68/DDX5. Proc Natl Acad Sci 2015; 112:8041-5; PMID:26080402; http://dx.doi.org/10.1073/pnas.1422273112
   Google Scholar
• Timchenko NA, Patel R, Iakova P, Cai Z-J, Quan L, Timchenko LT. Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J Biol Chem 2004; 279:13129-39; PMID:14722059; http://dx.doi.org/10.1074/jbc.M312923200
   Google Scholar
• Llamusi B, Bargiela A, Fernandez-Costa JM, Garcia-Lopez A, Klima R, Feiguin F, Artero R. Muscleblind, BSF and TBPH are mislocalized in the muscle sarcomere of a Drosophila myotonic dystrophy model. Dis Models Mech 2013; 6:184-96; PMID:23118342; http://dx.doi.org/10.1242/dmm.009563
   Google Scholar
• Paul S, Dansithong W, Kim D, Rossi J, Webster NJ, Comai L, Reddy S. Interaction of musleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J 2006; 25:4271-83; PMID:16946708; http://dx.doi.org/10.1038/sj.emboj.7601296
   Google Scholar
• Pettersson OJ, Aagaard L, Andrejeva D, Thomsen R, Jensen TG, Damgaard CK. DDX6 regulates sequestered nuclear CUG-expanded DMPK-mRNA in dystrophia myotonica type 1. Nucleic Acids Res 2014; 42:7186-200; PMID:24792155; http://dx.doi.org/10.1093/nar/gku352
   Google Scholar
• Laurent F-X, Sureau A, Klein AF, Trouslard F, Gasnier E, Furling D, Marie J. New function for the RNA helicase p68/DDX5 as a modifier of MBNL1 activity on expanded CUG repeats. Nucleic Acids Res 2012; 40:3159-71; PMID:22156369; http://dx.doi.org/10.1093/nar/gkr1228
   Google Scholar
• Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS. A muscleblind knockout model for myotonic dystrophy. Science 2003; 302:1978-80; PMID:14671308; http://dx.doi.org/10.1126/science.1088583
   Google Scholar
• Suenaga K, Lee K-Y, Nakamori M, Tatsumi Y, Takahashi MP, Fujimura H, Jinnai K, Yoshikawa H, Du H, Ares M Jr, et al. Muscleblind-like 1 knockout mice reveal novel splicing defects in the myotonic dystrophy brain. PloS One 2012; 7:e33218-e; PMID:22427994; http://dx.doi.org/10.1371/journal.pone.0033218
   Google Scholar
• Kanadia RN, Shin J, Yuan Y, Beattie SG, Wheeler TM, Thornton CA, Swanson MS. Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly (CUG) model for myotonic dystrophy. Proc Natl Acad Sci U S A 2006; 103:11748-53; http://dx.doi.org/10.1073/pnas.0604970103
   Google Scholar
• Prior TW, Krainer AR, Hua Y, Swoboda KJ, Snyder PC, Bridgeman SJ, Burghes AH, Kissel JT. A positive modifier of spinal muscular atrophy in the SMN2 gene. Am J Hum Genet 2009; 85:408-13; PMID:19716110; http://dx.doi.org/10.1016/j.ajhg.2009.08.002
   Google Scholar
• Oprea GE, Kröber S, McWhorter ML, Rossoll W, Müller S, Krawczak M, Bassell GJ, Beattie CE, Wirth B. Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 2008; 320:524-7; PMID:18440926; http://dx.doi.org/10.1126/science.1155085
   Google Scholar
• Flanigan KM, Ceco E, Lamar KM, Kaminoh Y, Dunn DM, Mendell JR, King WM, Pestronk A, Florence JM, Mathews KD, et al. LTBP4 genotype predicts age of ambulatory loss in Duchenne muscular dystrophy. Ann Neurol 2013; 73:481-8; PMID:23440719; http://dx.doi.org/10.1002/ana.23819
   Google Scholar
• Charizanis K, Lee K-Y, Batra R, Goodwin M, Zhang C, Yuan Y, Shiue L, Cline M, Scotti MM, Xia G, et al. Muscleblind-like 2-mediated alternative splicing in the developing brain and dysregulation in myotonic dystrophy. Neuron 2012; 75:437-50; PMID:22884328; http://dx.doi.org/10.1016/j.neuron.2012.05.029
   Google Scholar
• Kiebler MA, Hemraj I, Verkade P, Köhrmann M, Fortes P, Marión RM, Ortín J, Dotti CG. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J Neurosci 1999; 19:288-97; PMID:9870958
   Google Scholar
• Goetze B, Tuebing F, Xie Y, Dorostkar MM, Thomas S, Pehl U, Boehm S, Macchi P, Kiebler MA. The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J Cell Biol 2006; 172:221-31; PMID:16418534; http://dx.doi.org/10.1083/jcb.200509035
   Google Scholar
• Orengo JP, Ward AJ, Cooper TA. Alternative splicing dysregulation secondary to skeletal muscle regeneration. Ann Neurol 2011; 69:681-90; PMID:21400563; http://dx.doi.org/10.1002/ana.22278
   Google Scholar
• Ravel-Chapuis A, Crawford TE, Blais-Crépeau M-L, Bélanger G, Richer CT, Jasmin BJ. The RNA-binding protein Staufen1 impairs myogenic differentiation via a c-myc–dependent mechanism. Mol Biol Cell 2014; 25:3765-78; PMID:25208565; http://dx.doi.org/10.1091/mbc.E14-04-0895
   Google Scholar
• Lin X, Miller JW, Mankodi A, Kanadia RN, Yuan Y, Moxley RT, Swanson MS, Thornton CA. Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum Mol Genet 2006; 15:2087-97; PMID:16717059; http://dx.doi.org/10.1093/hmg/ddl132
   Google Scholar
• Amack JD, Mahadevan MS. Myogenic defects in myotonic dystrophy. Dev Biol 2004; 265:294-301; PMID:14732393; http://dx.doi.org/10.1016/j.ydbio.2003.07.021
   Google Scholar
• Thomas MG, Tosar LJM, Desbats MA, Leishman CC, Boccaccio GL. Mammalian Staufen 1 is recruited to stress granules and impairs their assembly. J Cell Sci 2009; 122:563-73; PMID:19193871; http://dx.doi.org/10.1242/jcs.038208
   Google Scholar
• Ravel-Chapuis A, Gunnewiek AK, Bélanger G, Parks TEC, Côté J, Jasmin BJ. Staufen1 impairs stress granule formation in skeletal muscle cells from myotonic dystrophy type 1 patients. Mol Biol Cell 2016; 27:1728-39; PMID:27030674; http://dx.doi.org/10.1091/mbc.E15-06-0356
   Google Scholar
• Peredo J, Villacé P, Ortín J, de Lucas S. Human Staufen1 associates to miRNAs involved in neuronal cell differentiation and is required for correct dendritic formation. PloS One 2014; 9:e113704; PMID:25423178; http://dx.doi.org/10.1371/journal.pone.0113704
   Google Scholar
• Gleghorn ML, Gong C, Kielkopf CL, Maquat LE. Staufen1 dimerizes through a conserved motif and a degenerate dsRNA-binding domain to promote mRNA decay. Nat Struct Mol Biol 2013; 20:515-24; PMID:23524536; http://dx.doi.org/10.1038/nsmb.2528
   Google Scholar