A fly model for the CCUG-repeat expansion of myotonic dystrophy type 2 reveals a novel interaction with MBNL1

Human Molecular Genetics

Volumn 24, Issue 4, 2015, Pages 954-962

  Yu, Zhenming ^a,b   Goodman, Lindsey D ^a   Shieh, Shin Yi ^a   Min, Michelle ^a,c   Teng, Xiuyin ^a   Zhu, Yongqing ^a   Bonini, Nancy M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE RNA SPLICING; ANIMAL MODEL; ARTICLE; CAG REPEAT; CCUG REPEAT EXPANSION; DNA STRUCTURE; FRUIT FLY MODEL; GAIN OF FUNCTION MUTATION; GENE; GENE EXPRESSION; GENE INTERACTION; INTERACTIONS WITH RNA; MBNL1 GENE; MYOTONIC DYSTROPHY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ALLELE; ANIMAL; CELL NUCLEUS; DISEASE MODEL; DROSOPHILA; GENETIC ASSOCIATION; GENETICS; LETHAL GENE; METABOLISM; PHENOTYPE; RNA STABILITY; TRANSGENIC ANIMAL;

ANIMALIA;

REPETITIVE DNA; RNA BINDING PROTEIN; UNTRANSLATED RNA;

ALLELES; ALTERNATIVE SPLICING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL NUCLEUS; DISEASE MODELS, ANIMAL; DNA REPEAT EXPANSION; DROSOPHILA; GENE EXPRESSION; GENES, LETHAL; GENETIC ASSOCIATION STUDIES; MYOTONIC DYSTROPHY; PHENOTYPE; RNA STABILITY; RNA, UNTRANSLATED; RNA-BINDING PROTEINS;

EID: 84922423171     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu507     Document Type: Article

References (63)

1. Harper, P.S. (2001) Myotonic Dystrophy. 3rd edn, WB Saunders, London.
2. Udd, B., Meola, G., Krahe, R., Wansink, D.G., Bassez, G., Kress, W., Schoser, B. and Moxley, R. (2011) Myotonic dystrophy type 2 (DM2) and related disorders report of the 180th ENMC workshop including guidelines on diagnostics and management 3-5 December 2010, Naarden, The Netherlands. Neuromuscul. Disord., 21, 443-450.
3. Fu, Y.H., Pizzuti, A., Fenwick, R.G., King, J., Rajnarayan, S., Dunne, P.W., Dubel, J., Nasser, G.A., Ashizawa, T., Dejong, P. et al. (1992) An unstable triplet repeat in a gene related to myotonic muscular-dystrophy. Science, 255, 1256-1258.
4. Mahadevan, M., Tsilfidis, C., Sabourin, L., Shutler, G., Amemiya, C., Jansen, G., Neville, C., Narang, M., Barcelo, J., O'Hoy, K. et al. (1992) Myotonic dystrophy mutation: an unstableCTGrepeat in the 3' untranslated region of the gene. Science, 255, 1253-1255.
5. Brook, J.D., McCurrach, M.E., Harley, H.G., Buckler, A.J., Church, D., Aburatani, H., Hunter, K., Stanton, V.P., Thirion, J.-P., Hudson, T. et al. (1992) 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, 68, 799-808.
6. Liquori, C.L., Ricker, K., Moseley, M.L., Jacobsen, J.F., Kress, W., Naylor, S.L., Day, J.W. and Ranum, L.P. (2001) Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science, 293, 864-867.
7. Minnerop, M., Weber, B., Schoene-Bake, J.C., Roeske, S., Mirbach, S., Anspach, C., Schneider-Gold, C., Betz, R.C., Helmstaedter, C., Tittgemeyer, M. et al. (2011) The brain in myotonic dystrophy 1 and 2: evidence for a predominant white matter disease. Brain, 134, 3530-3546.
8. Ranum, L.P. and Cooper, T.A. (2006) RNA-mediated neuromuscular disorders. Ann. Rev. Neurosci., 29, 259-277.
9. Day, J.W. and Ranum, L.P. (2005) RNA pathogenesis of the myotonic dystrophies. Neuromuscul. Disord., 15, 5-16.
10. Wheeler, T.M. and Thornton, C.A. (2007) Myotonic dystrophy: RNA-mediated muscle disease. Curr. Opin. Neurol., 20, 572-576.
11. Poulos, M.G., Batra, R., Charizanis, K. and Swanson, M.S. (2011) Developments in RNA splicing and disease. Cold Spring Harb. Perspect. Biol., 3, a000778.
12. Fardaei, M., Rogers, M.T., Thorpe, H.M., Larkin, K., Hamshere, M.G., Harper, P.S. and Brook, J.D. (2002) Three proteins, MBNL, MBLL and MBXL, co-localize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum. Mol. Genet., 11, 805-814.
13. Jiang, H., Mankodi, A., Swanson, M.S., Moxley, R.T. and Thornton, C.A. (2004) Myotonic dystrophy type 1 is associated with nuclear foci of mutant RNA, sequestration of muscleblind proteins and deregulated alternative splicing in neurons. Hum. Mol. Genet., 13, 3079-3088.
14. Lin, X., Miller, J.W., Mankodi, A., Kanadia, R.N., Yuan, Y., Moxley, R.T., Swanson, M.S. and Thornton, C.A. (2006) Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet., 15, 2087-2097.
15. Mankodi, A., Teng-Umnuay, P., Krym, M., Henderson, D., Swanson, M.and Thornton, C.A. (2003) Ribonuclear inclusions in skeletal muscle in myotonic dystrophy types 1 and 2. Ann. Neurol., 54, 760-768.
16. Miller, J.W., Urbinati, C.R., Teng-Umnuay, P., Stenberg, M.G., Byrne, B.J., Thornton, C.A. and Swanson, M.S. (2000) Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. Embo J., 19, 4439-4448.
17. Begemann, G., Paricio, N., Artero, R., Kiss, I., Perez-Alonso, M. and Mlodzik, M. (1997) Muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development, 124, 4321-4331.
18. Artero, R., Prokop, A., Paricio, N., Begemann, G., Pueyo, I., Mlodzik, M., Perez-Alonso, M. and Baylies, M.K. (1998) The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2. Dev. Biol., 195, 131-143.
19. Kalsotra, A., Xiao, X., Ward, A.J., Castle, J.C., Johnson, J.M., Burge, C.B. and Cooper, T.A. (2008) A postnatal switch of CELF and MBNL proteins reprogramsalternative splicing in the developing heart. Proc. Natl Acad. Sci. USA, 105, 20333-20338.
20. Kanadia, R.N., Johnstone, K.A., Mankodi, A., Lungu, C., Thornton, C.A., Esson, D., Timmers, A.M., Hauswirth, W.W. and Swanson, M.S. (2003) A muscleblind knockout model for myotonic dystrophy. Science, 302, 1978-1980.
21. Pascual, M., Vicente, M., Monferrer, L. and Artero, R. (2006) The Muscleblind family of proteins: an emerging class of regulators of developmentally programmed alternative splicing. Differentiation, 74, 65-80.
22. Squillace, R.M., Chenault, D.M.andWang, E.H. (2002) Inhibition of muscle differentiation by the novel muscleblind-related protein CHCR. Dev. Biol., 250, 218-230.
23. Han, H., Irimia, M., Ross, P.J., Sung, H.K., Alipanahi, B., David, L., Golipour, A., Gabut, M., Michael, I.P., Nachman, E.N. et al. (2013) MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature, 498, 241-245.
24. Du, H., Cline, M.S., Osborne, R.J., Tuttle, D.L., Clark, T.A., Donohue, J.P., Hall, M.P., Shiue, L., Swanson, M.S., Thornton, C.A. et al. (2010) Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat. Struct. Mol. Biol., 17, 187-193.
25. Adereth, Y., Dammai, V., Kose, N., Li, R. and Hsu, T. (2005) RNA-dependent integrin alpha3 protein localization regulated by the Muscleblind-like protein MLP1. Nat. Cell Biol., 7, 1240-1247.
26. Wang, E.T., Cody, N.A., Jog, S., Biancolella, M., Wang, T.T., Treacy, D.J., Luo, S., Schroth, G.P., Housman, D.E., Reddy, S. et al. (2012) Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell, 150, 710-724.
27. Masuda, A., Andersen, H.S., Doktor, T.K., Okamoto, T., Ito, M., Andresen, B.S. and Ohno, K. (2012) CUGBP1 and MBNL1 preferentially bind to 3' UTRs and facilitate mRNA decay. Sci. Rep., 2, 209.
28. Poulos, M.G., Batra, R., Li, M., Yuan, Y., Zhang, C., Darnell, R.B. and Swanson, M.S. (2013) Progressive impairment of muscle regeneration in muscleblind-like 3 isoformknockoutmice. Hum. Mol. Genet., 22, 3547-3558.
29. Kanadia, R.N., Shin, J., Yuan, Y., Beattie, S.G., Wheeler, T.M., Thornton, C.A. and Swanson, M.S. (2006) Reversal ofRNAmissplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc. Natl Acad. Sci. USA, 103, 11748-11753.
30. Teplova, M. and Patel, D.J. (2008) Structural insights into RNA recognition by the alternative-splicing regulator muscleblind-like MBNL1. Nat. Struct. Mol. Biol., 15, 1343-1351.
31. Kino, Y., Mori, D., Oma, Y., Takeshita, Y., Sasagawa, N. and Ishiura, S. (2004) Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum. Mol. Genet., 13, 495-507.
32. Dhaenens, C.M., Schraen-Maschke, S., Tran, H., Vingtdeux, V., Ghanem, D., Leroy, O., Delplanque, J., Vanbrussel, E., Delacourte, A., Vermersch, P. et al. (2008) Overexpression ofMBNL1fetal isoforms and modified splicing of Tau in theDM1brain: two individual consequences ofCUGtrinucleotide repeats. Exp. Neurol., 210, 467-478.
33. Tran, H., Gourrier, N., Lemercier-Neuillet, C., Dhaenens, C.M., Vautrin, A., Fernandez-Gomez, F.J., Arandel, L., Carpentier, C., Obriot, H., Eddarkaoui, S. et al. (2011) Analysis of exonic regions involved in nuclear localization, splicing activity, and dimerization of Muscleblind-like-1 isoforms. J. Biol. Chem., 286, 16435-16446.
34. Osborne, R.J. and Thornton, C.A. (2008) Cell-free cloning of highly expanded CTG repeats by amplification of dimerized expanded repeats. Nucl. Acids Res., 36, e24.
35. Kim, S.H., Cai, L., Pytlos, M.J., Edwards, S.F. and Sinden, R.R. (2005) Generation of long tracts of disease-associatedDNArepeats. Biotechniques, 38, 247-253.
36. Wells, R.D., Dere, R., Hebert, M.L., Napierala, M. and Son, L.S. (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucl. Acids Res., 33, 3785-3798.
37. Jung, J. and Bonini, N. (2007) CREB-binding protein modulates repeat instability in a Drosophila model for polyQ disease. Science, 315, 1857-1859.
38. Yu, Z., Teng, X. and Bonini, N.M. (2011) Triplet repeat-derived siRNAs enhance RNA-mediated toxicity in a Drosophila model for myotonic dystrophy. PLoS Genet., 7, e1001340.
39. Mahadevan, M.S., Yadava, R.S., Yu, Q., Balijepalli, S., Frenzel-McCardell, C.D., Bourne, T.D. and Phillips, L.H. (2006) Reversible model of RNA toxicity and cardiac conduction defects in myotonic dystrophy. Nat. Genet., 38, 1066-1070.
40. Yu, Z. and Bonini, N.M. (2011) Modeling human trinucleotide repeat diseases in Drosophila. Int. Rev. Neurobiol., 99, 191-212.
41. Ho, T.H., Charlet, B.N., Poulos, M.G., Singh, G., Swanson, M.S. and Cooper, T.A. (2004) Muscleblind proteins regulate alternative splicing. Embo. J., 23, 3103-3112.
42. Li, L.B., Yu, Z., Teng, X. and Bonini, N.M. (2008) RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature, 453, 1107-1111.
43. Charles, P., Camuzat, A., Benammar, N., Sellal, F., Destee, A., Bonnet, A.M., Lesage, S., Le Ber, I., Stevanin, G., Durr, A. et al. (2007) Are interrupted SCA2 CAG repeat expansions responsible for parkinsonism? Neurology, 69, 1970-1975.
44. Braida, C., Stefanatos, R.K., Adam, B., Mahajan, N., Smeets, H.J., Niel, F., Goizet, C., Arveiler, B., Koenig, M., Lagier-Tourenne, C. et al. (2010) Variant CCG and GGC repeats within the CTG expansion dramatically modify mutational dynamics and likely contribute toward unusual symptoms in some myotonic dystrophy type 1 patients. Hum. Mol. Genet., 19, 1399-1412.
45. Zu, T., Gibbens, B., Doty, N.S., Gomes-Pereira, M., Huguet, A., Stone, M.D., Margolis, J., Peterson, M., Markowski, T.W., Ingram, M.A. et al. (2011) Non-ATG-initiated translation directedby microsatellite expansions. Proc. Natl Acad. Sci. USA, 108, 260-265.
46. Muqit, M.M.and Feany, M.B. (2002) Modelling neurodegenerative diseases in Drosophila: a fruitful approach? Nat. Rev. Neurosci., 3, 237-243.
47. Bilen, J. and Bonini, N.M. (2005) Drosophila as a model for human neurodegenerative disease. Annu. Rev. Genet., 39, 153-171.
48. Fortini, M.E. and Bonini, N.M. (2000) Modeling human neurodegenerative diseases in Drosophila: on a wing and a prayer. Trends Genet., 16, 161-167.
49. Sang, T.K. and Jackson, G.R. (2005) Drosophila models of neurodegenerative disease. NeuroRx, 2, 438-446.
50. Bakhoum, M.F. and Jackson, G.R. (2011) Demise of the flies: why Drosophila models still matter. Prog. Mol. Biol. Transl. Sci., 100, 483-498.
51. Zoghbi, H.Y. and Botas, J. (2002) Mouse and fly models of neurodegeneration. Trends Genet., 18, 463-471.
52. Salisbury, E., Schoser, B., Schneider-Gold, C., Wang, G.L., Huichalaf, C., Jin, B., Sirito, M., Sarkar, P., Krahe, R., Timchenko, N.A. et al. (2009) Expression ofRNACCUG repeats dysregulates translation and degradation of proteins in myotonic dystrophy 2 patients. Am. J. Pathol., 175, 748-762.
53. Garcia-Lopez, A., Monferrer, L., Garcia-Alcover, I., Vicente-Crespo, M., Alvarez-Abril, M.C. and Artero, R.D. (2008) Genetic and chemical modifiers of a CUG toxicity model in Drosophila. PLoS One, 3, e1595.
54. de Haro, M., Al-Ramahi, I., De Gouyon, B., Ukani, L., Rosa, A., Faustino, N.A., Ashizawa, T., Cooper, T.A. and Botas, J. (2006) MBNL1 and CUGBP1 modify expanded CUG-induced toxicity in a Drosophila model of myotonic dystrophy type 1. Hum. Mol. Genet., 15, 2138-2145.
55. Houseley, J.M., Wang, Z., Brock, G.J., Soloway, J., Artero, R., Perez-Alonso, M., O'Dell, K.M. and Monckton, D.G. (2005) Myotonic dystrophy associated expanded CUG repeat muscleblind positive ribonuclear foci are not toxic to Drosophila.Hum. Mol. Genet., 14, 873-883.
56. Tian, B., White, R.J., Xia, T., Welle, S., Turner, D.H., Mathews, M.B. and Thornton, C.A. (2000) Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA, 6, 79-87.
57. Michalowski, S., Miller, J.W., Urbinati, C.R., Paliouras, M., Swanson, M.S. and Griffith, J. (1999) Visualization of double-stranded RNAs from the myotonic dystrophy protein kinase gene and interactions with CUG-binding protein. Nucl. Acids Res., 27, 3534-3542.
58. Mooers, B.H., Logue, J.S. and Berglund, J.A. (2005) The structural basis of myotonic dystrophy from the crystal structure of CUG repeats. Proc. Natl Acad. Sci. USA, 102, 16626-16631.
59. Dere, R., Napierala, M., Ranum, L.P. and Wells, R.D. (2004) Hairpin structure-forming propensity of the (CCTG.CAGG) tetranucleotide repeats contributes to the genetic instability associated with myotonic dystrophy type 2. J. Biol. Chem., 279, 41715-41726.
60. Sobczak, K., de Mezer, M., Michlewski, G., Krol, J. and Krzyzosiak, W.J. (2003) RNA structure of trinucleotide repeats associated with human neurological diseases. Nucl. Acids Res., 31, 5469-5482.
61. Obenauer, J.C., Cantley, L.C. and Yaffe, M.B. (2003) Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucl. Acids Res., 31, 3635-3641.
62. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012) Fiji: an open-source platform for biological-imageanalysis. Nat. Methods, 9, 676-682.
63. Bolte, S. and Cordelieres, F.P. (2006) A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc., 224, 213-232.