The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing

Journal of Cell Biology

Volumn 196, Issue 6, 2012, Pages 699-712

  Ravel Chapuis, Aymeric ^a   Bélanger, Guy ^a   Yadava, Ramesh S ^b   Mahadevan, Mani S ^b   DesGroseillers, Luc ^c   Côté, Jocelyn ^a   Jasmin, Bernard J ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; RNA BINDING PROTEIN; RNA BINDING PROTEIN STAUFEN1; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; MOUSE; MYOTONIC DYSTROPHY; MYOTONIC DYSTROPHY TYPE 1; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN TRANSPORT; RNA BINDING; RNA TRANSLATION; SKELETAL MUSCLE; TANDEM REPEAT;

ANIMALS; CYTOSKELETAL PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICE; MICE, INBRED BALB C; MUSCLE, SKELETAL; MYOTONIC DYSTROPHY; RNA PRECURSORS; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSFECTION; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84860308052     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201108113     Document Type: Article

References (51)

1. Amack, J.D., and M.S. Mahadevan. 2001. The myotonic dystrophy expanded CUG repeat tract is necessary but not sufficient to disrupt C2C12 myoblast differentiation. Hum. Mol. Genet. 10:1879-1887. http://dx.doi.org/10.1093/hmg/10.18.1879
2. Bélanger, G., M.A. Stocksley, M. Vandromme, L. Schaeffer, L. Furic, L. DesGroseillers, and B.J. Jasmin. 2003. Localization of the RNAbinding proteins Staufen1 and Staufen2 at the mammalian neuromuscular junction. J. Neurochem. 86:669-677. http://dx.doi.org/10.1046/j.1471-4159.2003.01883.x
3. Buj-Bello, A., D. Furling, H. Tronchère, J. Laporte, T. Lerouge, G.S. Butler-Browne, and J.L. Mandel. 2002. Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum. Mol. Genet. 11:2297-2307. http://dx.doi.org/10.1093/hmg/11.19.2297
4. Charlet-B, N., R.S. Savkur, G. Singh, A.V. Philips, E.A. Grice, and T.A. Cooper. 2002. Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol. Cell. 10:45-53. http://dx.doi.org/10.1016/S1097-2765(02)00572-5
5. Cooper, T.A. 2005. Use of minigene systems to dissect alternative splicing elements. Methods. 37:331-340. http://dx.doi.org/10.1016/j.ymeth.2005.07.015
6. Coté, J., S. Dupuis, Z. Jiang, and J.Y. Wu. 2001. Caspase-2 pre-mRNA alternative splicing: Identification of an intronic element containing a decoy 3' acceptor site. Proc. Natl. Acad. Sci. USA. 98:938-943. http://dx.doi.org/10.1073/pnas.031564098
7. Dugré-Brisson, S., G. Elvira, K. Boulay, L. Chatel-Chaix, A.J. Mouland, and L. DesGroseillers. 2005. Interaction of Staufen1 with the 5' end of mRNA facilitates translation of these RNAs. Nucleic Acids Res. 33:4797-4812. http://dx.doi.org/10.1093/nar/gki794
8. François, V., A.F. Klein, C. Beley, A. Jollet, C. Lemercier, L. Garcia, and D. Furling. 2011. Selective silencing of mutated mRNAs in DM1 by using modified hU7-snRNAs. Nat. Struct. Mol. Biol. 18:85-87. http://dx.doi.org/10.1038/nsmb.1958
9. Ho, T.H., N. Charlet-B, M.G. Poulos, G. Singh, M.S. Swanson, and T.A. Cooper. 2004. Muscleblind proteins regulate alternative splicing. EMBO J. 23:3103-3112. http://dx.doi.org/10.1038/sj.emboj.7600300
10. Ho, T.H., D. Bundman, D.L. Armstrong, and T.A. Cooper. 2005. Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum. Mol. Genet. 14:1539-1547. http://dx.doi.org/10.1093/hmg/ddi162
11. Jones, K., B. Jin, P. Iakova, C. Huichalaf, P. Sarkar, C. Schneider-Gold, B. Schoser, G. Meola, A.B. Shyu, N. Timchenko, and L. Timchenko. 2011. RNA Foci, CUGBP1, and ZNF9 are the primary targets of the mutant CUG and CCUG repeats expanded in myotonic dystrophies type 1 and type 2. Am. J. Pathol. 179:2475-2489. http://dx.doi.org/10.1016/j.ajpath.2011.07.013
12. Kanadia, R.N., K.A. Johnstone, A. Mankodi, C. Lungu, C.A. Thornton, D. Esson, A.M. Timmers, W.W. Hauswirth, and M.S. Swanson. 2003. A muscleblind knockout model for myotonic dystrophy. Science. 302:1978-1980. http://dx.doi.org/10.1126/science.1088583
13. Kiebler, M.A., I. Hemraj, P. Verkade, M. Köhrmann, P. Fortes, R.M. Marión, J. Ortín, and C.G. Dotti. 1999. The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J. Neurosci. 19:288-297.
14. Kim, D.H., M.A. Langlois, K.B. Lee, A.D. Riggs, J. Puymirat, and J.J. Rossi. 2005a. HnRNP H inhibits nuclear export of mRNA containing expanded CUG repeats and a distal branch point sequence. Nucleic Acids Res. 33:3866-3874. http://dx.doi.org/10.1093/nar/gki698
15. Kim, Y.K., L. Furic, L. DesGroseillers, and L.E. Maquat. 2005b. Mammalian Staufen1 recruits Upf1 to specific mRNA 3'UTRs so as to elicit mRNA decay. Cell. 120:195-208. http://dx.doi.org/10.1016/j.cell.2004.11.050
16. Kim, Y.K., L. Furic, M. Parisien, F. Major, L. DesGroseillers, and L.E. Maquat. 2007. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J. 26:2670-2681. http://dx.doi.org/10.1038/sj.emboj.7601712
17. Kosaki, A., J. Nelson, and N.J. Webster. 1998. Identification of intron and exon sequences involved in alternative splicing of insulin receptor premRNA. J. Biol. Chem. 273:10331-10337. http://dx.doi.org/10.1074/jbc.273.17.10331
18. Kuyumcu-Martinez, N.M., G.S. Wang, and T.A. Cooper. 2007. Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol. Cell. 28:68-78. http://dx.doi.org/10.1016/j.molcel.2007.07.027
19. Le, S., R. Sternglanz, and C.W. Greider. 2000. Identification of two RNAbinding proteins associated with human telomerase RNA. Mol. Biol. Cell. 11:999-1010.
20. Lee, J.E., and T.A. Cooper. 2009. Pathogenic mechanisms of myotonic dystrophy. Biochem. Soc. Trans. 37:1281-1286. http://dx.doi.org/10.1042/BST0371281
21. Lin, X., J.W. Miller, A. Mankodi, R.N. Kanadia, Y. Yuan, R.T. Moxley, M.S. Swanson, and C.A. Thornton. 2006. Failure of MBNL1-dependent postnatal splicing transitions in myotonic dystrophy. Hum. Mol. Genet. 15:2087-2097. http://dx.doi.org/10.1093/hmg/ddl132
22. Luo, M., T.F. Duchaîne, and L. DesGroseillers. 2002. Molecular mapping of the determinants involved in human Staufen-ribosome association. Biochem. J. 365:817-824. http://dx.doi.org/10.1042/BJ20020263
23. Magaña, J.J., and B. Cisneros. 2011. Perspectives on gene therapy in myotonic dystrophy type 1. J. Neurosci. Res. 89:275-285. http://dx.doi.org/10.1002/jnr.22551
24. Mahadevan, M.S., R.S. Yadava, Q. Yu, S. Balijepalli, C.D. Frenzel-McCardell, T.D. Bourne, and L.H. Phillips. 2006. Reversible model of RNA toxicity and cardiac conduction defects in myotonic dystrophy. Nat. Genet. 38:1066-1070. http://dx.doi.org/10.1038/ng1857
25. Mankodi, A., E. Logigian, L. Callahan, C. McClain, R. White, D. Henderson, M. Krym, and C.A. Thornton. 2000. Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science. 289:1769-1773. http://dx.doi.org/10.1126/science.289.5485.1769
26. Mankodi, A., M.P. Takahashi, H. Jiang, C.L. Beck, W.J. Bowers, R.T. Moxley, S.C. Cannon, and C.A. Thornton. 2002. Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol. Cell. 10:35-44. http://dx.doi.org/10.1016/S1097-2765(02)00563-4
27. Marión, R.M., P. Fortes, A. Beloso, C. Dotti, and J. Ortín. 1999. A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:2212-2219.
28. Martel, C., P. Macchi, L. Furic, M.A. Kiebler, and L. DesGroseillers. 2006. Staufen1 is imported into the nucleolus via a bipartite nuclear localization signal and several modulatory determinants. Biochem. J. 393:245-254. http://dx.doi.org/10.1042/BJ20050694
29. Martel, C., S. Dugré-Brisson, K. Boulay, B. Breton, G. Lapointe, S. Armando, V. Trépanier, T. Duchaîne, M. Bouvier, and L. DesGroseillers. 2010. Multimerization of Staufen1 in live cells. RNA. 16:585-597. http://dx.doi.org/10.1261/rna.1664210
30. Michalowski, S., J.W. Miller, C.R. Urbinati, M. Paliouras, M.S. Swanson, and J. Griffith. 1999. Visualization of double-stranded RNAs from the myotonic dystrophy protein kinase gene and interactions with CUG-binding protein. Nucleic Acids Res. 27:3534-3542. http://dx.doi.org/10.1093/nar/27.17.3534
31. Miller, J.W., C.R. Urbinati, P. Teng-Umnuay, M.G. Stenberg, B.J. Byrne, C.A. Thornton, and M.S. Swanson. 2000. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 19:4439-4448. http://dx.doi.org/10.1093/emboj/19.17.4439
32. Orengo, J.P., P. Chambon, D. Metzger, D.R. Mosier, G.J. Snipes, and T.A. Cooper. 2008. Expanded CTG repeats within the DMPK 3' UTR causes severe skeletal muscle wasting in an inducible mouse model for myotonic dystrophy. Proc. Natl. Acad. Sci. USA. 105:2646-2651. http://dx.doi.org/10.1073/pnas.0708519105
33. O'Rourke, J.R., and M.S. Swanson. 2009. Mechanisms of RNA-mediated disease. J. Biol. Chem. 284:7419-7423. http://dx.doi.org/10.1074/jbc.R800025200
34. Paul, S., W. Dansithong, D. Kim, J. Rossi, N.J. Webster, L. Comai, and S. Reddy. 2006. Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J. 25:4271-4283. http://dx.doi.org/10.1038/sj.emboj.7601296
35. Querido, E., F. Gallardo, M. Beaudoin, C. Ménard, and P. Chartrand. 2011. Stochastic and reversible aggregation of mRNA with expanded CUG-triplet repeats. J. Cell Sci. 124:1703-1714. http://dx.doi.org/10.1242/jcs.073270
36. Ranum, L.P., and T.A. Cooper. 2006. RNA-mediated neuromuscular disorders. Annu. Rev. Neurosci. 29:259-277. http://dx.doi.org/10.1146/annurev.neuro.29.051605.113014
37. Rau, F., F. Freyermuth, C. Fugier, J.P. Villemin, M.C. Fischer, B. Jost, D. Dembele, G. Gourdon, A. Nicole, D. Duboc, et al. 2011. Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat. Struct. Mol. Biol. 18:840-845. http://dx.doi.org/10.1038/nsmb.2067
38. Ravel-Chapuis, A., M. Vandromme, J.L. Thomas, and L. Schaeffer. 2007. Postsynaptic chromatin is under neural control at the neuromuscular junction. EMBO J. 26:1117-1128. http://dx.doi.org/10.1038/sj.emboj.7601572
39. Savkur, R.S., A.V. Philips, and T.A. Cooper. 2001. Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet. 29:40-47. http://dx.doi.org/10.1038/ng704
40. Schoser, B., and L. Timchenko. 2010. Myotonic dystrophies 1 and 2: complex diseases with complex mechanisms. Curr. Genomics. 11:77-90. http://dx.doi.org/10.2174/138920210790886844
41. Seznec, H., O. Agbulut, N. Sergeant, C. Savouret, A. Ghestem, N. Tabti, J.C. Willer, L. Ourth, C. Duros, E. Brisson, et al. 2001. Mice transgenic for the human myotonic dystrophy region with expanded CTG repeats display muscular and brain abnormalities. Hum. Mol. Genet. 10:2717-2726. http://dx.doi.org/10.1093/hmg/10.23.2717
42. Tian, B., R.J. White, T. Xia, S. Welle, D.H. Turner, M.B. Mathews, and C.A. Thornton. 2000. Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA. 6:79-87. http://dx.doi.org/10.1017/S1355838200991544
43. Timchenko, L.T., N.A. Timchenko, C.T. Caskey, and R. Roberts. 1996. Novel proteins with binding specificity for DNA CTG repeats and RNA CUG repeats: implications for myotonic dystrophy. Hum. Mol. Genet. 5:115-121. http://dx.doi.org/10.1093/hmg/5.1.115
44. Timchenko, N.A., P. Iakova, Z.J. Cai, J.R. Smith, and L.T. Timchenko. 2001. Molecular basis for impaired muscle differentiation in myotonic dystrophy. Mol. Cell. Biol. 21:6927-6938. http://dx.doi.org/10.1128/MCB.21.20.6927-6938.2001
45. Timchenko, N.A., R. Patel, P. Iakova, Z.J. Cai, L. Quan, and L.T. Timchenko. 2004. Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J. Biol. Chem. 279:13129-13139. http://dx.doi.org/10.1074/jbc.M312923200
46. Warf, M.B., and J.A. Berglund. 2007. MBNL binds similar RNA structures in the CUG repeats of myotonic dystrophy and its pre-mRNA substrate cardiac troponin T. RNA. 13:2238-2251. http://dx.doi.org/10.1261/rna.610607
47. Warf, M.B., J.V. Diegel, P.H. von Hippel, and J.A. Berglund. 2009. The protein factors MBNL1 and U2AF65 bind alternative RNA structures to regulate splicing. Proc. Natl. Acad. Sci. USA. 106:9203-9208. http://dx.doi.org/10.1073/pnas.0900342106
48. Wheeler, T.M., and C.A. Thornton. 2007. Myotonic dystrophy: RNA-mediated muscle disease. Curr. Opin. Neurol. 20:572-576. http://dx.doi.org/10.1097/WCO.0b013e3282ef6064
49. Wheeler, T.M., K. Sobczak, J.D. Lueck, R.J. Osborne, X. Lin, R.T. Dirksen, and C.A. Thornton. 2009. Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science. 325:336-339. http://dx.doi.org/10.1126/science.1173110
50. Wickham, L., T. Duchaîne, M. Luo, I.R. Nabi, and L. DesGroseillers. 1999. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19:2220-2230.
51. Yuan, Y., S.A. Compton, K. Sobczak, M.G. Stenberg, C.A. Thornton, J.D. Griffith, and M.S. Swanson. 2007. Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs. Nucleic Acids Res. 35:5474-5486. http://dx.doi.org/10.1093/nar/gkm601