Molecular therapy in myotonic dystrophy: Focus on RNA gain-of-function

Human Molecular Genetics

Volumn 19, Issue R1, 2010, Pages

  Mulders, Susan A M ^a,c   van Engelen, Baziel G M ^b   Wieringa, Bé ^a   Wansink, Derick G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b RADBOUD UNIVERSITY   (Netherlands)

^c Prosensa BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CAG 25; CUG BINDING PROTEIN 1; DOUBLE STRANDED RNA; GENE PRODUCT; MYOTONIC DYSTROPHY PROTEIN KINASE; OLIGONUCLEOTIDE PHOSPHOROTHIOATE; PENTAMIDINE; PEPTIDE NUCLEIC ACID; PROTEIN MBNL1; PROTEIN ZNF9; PS 58; RIBOZYME; RNA; RNA BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CAG REPEAT; GENE TARGETING; HUMAN; MOLECULAR THERAPY; MYOBLAST; MYOTONIC DYSTROPHY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; RNA INTERFERENCE; RNA SPLICING; RNA TRANSCRIPTION; SKELETAL MUSCLE; TRINUCLEOTIDE REPEAT;

HUMANS; MYOTONIC DYSTROPHY; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 77953933775     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddq161     Document Type: Article

References (107)

1. Harper, P.S., van Engelen, B.G.M., Eymard, B. and Wilcox, D.E. (eds) (2004) Myotonic Dystrophy. Present Management, Future Therapy, 1st edn. Oxford University Press, Oxford, UK.
2. Day, J.W. and Ranum, L.P. (2005) RNA pathogenesis of the myotonic dystrophies. Neuromuscul. Disord., 15, 5-16.
3. 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.
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 unstable CTG repeat in the 3' untranslated region of the gene. Science, 255, 1253-1255.
5. Liquori, C.L., Ricker, K., Moseley, M.L., Jacobsen, J.F., Kress, W., Naylor, S.L., Day, J.W. and Ranum, L.P.W. (2001) Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science, 293, 864-867.
6. Vihola, A., Bachinski, L.L., Sirito, M., Olufemi, S.E., Hajibashi, S., Baggerly, K.A., Raheem, O., Haapasalo, H., Suominen, T., Holmlund-Hampf, J. et al. (2010) Differences in aberrant expression and splicing of sarcomeric proteins in the myotonic dystrophies DM1 and DM2. Acta. Neuropathol., 119, 465-479.
7. Pearson, C.E., Nichol Edamura, K. and Cleary, J.D. (2005) Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet., 6, 729-742.
8. Mirkin, S.M. (2007) Expandable DNA repeats and human disease. Nature, 447, 932-940.
9. Shelbourne, P.F. and Monckton, D.G. (2006) Somatic mosaicism of. expanded CAG CTG repeats in humans and mice: dynamics, mechanisms, and consequences. Wells, R.D. and Ashizawa, T. (eds), Genetic Instabilities and Neurological Diseases, 2nd edn. Academic Press, Inc., San Diego, CA, pp. 537-561.
10. Braida, C., Stefanatos, R.K., Adam, B., Mahajan, N., Smeets, H.J., Niel, F., Koenig, M., Lagier-Tourenne, C., Mandel, J.L., Faber, C.G. 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.
11. Musova, Z., Mazanec, R., Krepelova, A., Ehler, E., Vales, J., Jaklova, R., Prochazka, T., Koukal, P., Marikova, T., Kraus, J. et al. (2009) Highly unstable sequence interruptions of the CTG repeat in the myotonic dystrophy gene. Am. J. Med. Genet. A, 149A, 1365-1374.
12. Ranum, L.P. and Cooper, T.A. (2006) RNA-mediated neuromuscular disorders. Annu. Rev. Neurosci., 29, 259-277.
13. Wheeler, T.M. and Thornton, C.A. (2007) Myotonic dystrophy: RNA-mediated muscle disease. Curr. Opin. Neurol., 20, 572-576.
14. Mankodi, A., Urbinati, C.R., Yuan, Q.P., Moxley, R.T., Sansone, V., Krym, M., Henderson, D., Schalling, M., Swanson, M.S. and Thornton, C.A. (2001) Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum. Mol. Genet., 10, 2165-2170.
15. 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.
16. 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.
17. Philips, A.V., Timchenko, L.T. and Cooper, T.A. (1998) Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science, 280, 737-740.
18. Savkur, R.S., Philips, A. and Cooper, T.A. (2001) Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat. Genet., 29, 40-47.
19. Timchenko, N.A., Cai, Z.J., Welm, A.L., Reddy, S., Ashizawa, T. and Timchenko, L.T. (2001) RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J. Biol. Chem., 276, 7820-7826.
20. Kuyumcu-Martinez, N.M., Wang, G.S. and Cooper, T.A. (2007) Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation. Mol. Cell, 28, 68-78.
21. 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, 1140-1147.
22. Zhang, L., Lee, J.E., Wilusz, J. and Wilusz, C.J. (2008) The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy. J. Biol. Chem., 283, 22457-22463.
23. Salisbury, E., Sakai, K., Schoser, B., Huichalaf, C., Schneider-Gold, C., Nguyen, H., Wang, G.L., Albrecht, J.H. and Timchenko, L.T. (2008) Ectopic expression of cyclin D3 corrects differentiation of DM1 myoblasts through activation of RNA CUG-binding protein, CUGBP1. Exp. Cell Res., 314, 2266-2278.
24. Ikezoe, K., Nakamori, M., Furuya, H., Arahata, H., Kanemoto, S., Kimura, T., Imaizumi, K., Takahashi, M.P., Sakoda, S., Fujii, N. et al. (2007) Endoplasmic reticulum stress in myotonic dystrophy type 1 muscle. Acta Neuropathol., 114, 527-535.
25. Bigot, A., Klein, A.F., Gasnier, E., Jacquemin, V., Ravassard, P., Butler-Browne, G., Mouly, V. and Furling, D. (2009) Large CTG repeats trigger p16-dependent premature senescence in myotonic dystrophy type 1 muscle precursor cells. Am. J. Pathol., 174, 1435-1442.
26. 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 of RNA CCUG repeats dysregulates translation and degradation of proteins in myotonic dystrophy 2 patients. Am. J. Pathol., 175, 748-762.
27. Ebralidze, A., Wang, Y., Petkova, V., Ebralidse, K. and Junghans, R.P. (2004) RNA leaching of transcription factors disrupts transcription in myotonic dystrophy. Science, 303, 383-387.
28. Osborne, R.J., Lin, X., Welle, S., Sobczak, K., O'Rourke, J.R., Swanson, M.S. and Thornton, C.A. (2009) Transcriptional and post-transcriptional impact of toxic RNA in myotonic dystrophy. Hum. Mol. Genet., 18, 1471-1481.
29. 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.
30. Paul, S., Dansithong, W., Kim, D., Rossi, J., Webster, N.J., Comai, L. and Reddy, S. (2006) Interaction of muscleblind, CUG-BP1 and hnRNP H proteins in DM1-associated aberrant IR splicing. EMBO J., 25, 4271-4283.
31. 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 reprograms alternative splicing in the developing heart. Proc. Natl Acad. Sci. USA, 105, 20333-20338.
32. Mankodi, A., Logigian, E., Callahan, L., McClain, C., White, R., Henderson, D., Krym, M. and Thornton, C.A. (2000) Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science, 289, 1769-1772.
33. 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.
34. Timchenko, N.A., Patel, R., Iakova, P., Cai, Z.J., Quan, L. and Timchenko, L.T. (2004) Overexpression of CUG triplet repeat-binding protein, CUGBP1, in mice inhibits myogenesis. J. Biol. Chem., 279, 13129-13139.
35. Ho, T.H., Bundman, D., Armstrong, D.L. and Cooper, T.A. (2005) Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum. Mol. Genet., 14, 1539-1547.
36. Koshelev, M., Sarma, S., Price, R.E., Wehrens, X.H. and Cooper, T.A. (2010) Heart-specific overexpression of CUGBP1 reproduces functional and molecular abnormalities of myotonic dystrophy type 1. Hum. Mol. Genet., 19, 1066-1075.
37. 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.
38. Groenen, P. and Wieringa, B. (1998) Expanding complexity in myotonic dystrophy. BioEssays, 20, 901-912.
39. Wansink, D.G. and Wieringa, B. (2003) Transgenic mouse models for myotonic dystrophy type 1 (DM1). Cytogenet. Genome Res., 100, 230-242.
40. Junghans, R.P. (2009) Dystrophia myotonia: why focus on foci? Eur. J. Hum. Genet., 17, 543-553.
41. Cho, D.H., Thienes, C.P., Mahoney, S.E., Analau, E., Filippova, G.N. and Tapscott, S.J. (2005) Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol. Cell, 20, 483-489.
42. Olsen, P.A., Solhaug, A., Booth, J.A., Gelazauskaite, M. and Krauss, S. (2009) Cellular responses to targeted genomic sequence modification using single-stranded oligonucleotides and zinc-finger nucleases. DNA Repair (Amst), 8, 298-308.
43. Mittelman, D., Moye, C., Morton, J., Sykoudis, K., Lin, Y., Carroll, D. and Wilson, J.H. (2009) Zinc-finger directed double-strand breaks within CAG repeat tracts promote repeat instability in human cells. Proc. Natl Acad. Sci. USA, 106, 9607-9612.
44. Aarts, M., Dekker, M., Dekker, R., de Vries, S., van der Wal, A., Wielders, E. and Riele, H.T. (2009) Gene modification in embryonic stem cells by single-stranded DNA oligonucleotides. Methods Mol. Biol., 530, 79-99.
45. Gomes-Pereira, M. and Monckton, D.G. (2006) Chemical modifiers of unstable expanded simple sequence repeats: what goes up, could come down. Mutat. Res., 598, 15-34.
46. Wheeler, T.M., Lueck, J.D., Swanson, M.S., Dirksen, R.T. and Thornton, C.A. (2007) Correction of ClC-1 splicing eliminates chloride channelopathy and myotonia in mouse models of myotonic dystrophy. J. Clin. Invest., 117, 3952-3957.
47. Kanadia, R.N., Shin, J., Yuan, Y., Beattie, S.G., Wheeler, T.M., Thornton, C.A. and Swanson, M.S. (2006) Reversal of RNA missplicing and myotonia after muscleblind overexpression in a mouse poly(CUG) model for myotonic dystrophy. Proc. Natl Acad. Sci. USA, 103, 11748-11753.
48. Wang, G.S., Kuyumcu-Martinez, M.N., Sarma, S., Mathur, N., Wehrens, X.H. and Cooper, T.A. (2009) PKC inhibition ameliorates the cardiac phenotype in a mouse model of myotonic dystrophy type 1. J. Clin. Invest., 119, 3797-3806.
49. Amack, J.D., Paguio, A.P. and Mahadevan, M.S. (1999) Cis and trans effects of the myotonic dystrophy (DM) mutation in a cell culture model. Hum. Mol. Genet., 8, 1975-1984.
50. Amack, J.D. and Mahadevan, M.S. (2001) The myotonic dystrophy expanded CUG repeat tract is necessary but not sufficient to disrupt C2C12 myoblast differentiation. Hum. Mol. Genet., 10, 1879-1887.
51. Wang, G.S., Kearney, D.L., De Biasi, M., Taffet, G. and Cooper, T.A. (2007) Elevation of RNA-binding protein CUGBP1 is an early event in an inducible heart-specific mouse model of myotonic dystrophy. J. Clin. Invest., 117, 2802-2811.
52. 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.
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. 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.
55. Yadava, R.S., Frenzel-McCardell, C.D., Yu, Q., Srinivasan, V., Tucker, A.L., Puymirat, J., Thornton, C.A., Prall, O.W., Harvey, R.P. and Mahadevan, M.S. (2008) RNA toxicity in myotonic muscular dystrophy induces NKX2-5 expression. Nat. Genet., 40, 61-68.
56. Jansen, G., Groenen, P.J., Bachner, D., Jap, P.H., Coerwinkel, M., Oerlemans, F., van den Broek, W., Gohlsch, B., Pette, D., Plomp, J.J. et al. (1996) Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat. Genet., 13, 316-324.
57. Reddy, S., Smith, D.B.J., Rich, M.M., Leferovich, J.M., Reilly, P., Davis, B.M., Tran, K., Rayburn, H., Bronson, R., Cros, D. et al. (1996) Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy. Nat. Genet., 13, 325-335.
58. Zuhlke, C., Roeder, E., Purmann, S., Wieczorek, D., Curry, C., Loustalet, C., Hellenbroich, Y., Richardt, H.H. and Gillessen-Kaesbach, G. (2007) Homozygous myotonic dystrophy: clinical findings in two patients and review of the literature. Am. J. Med. Genet. A, 143A, 2058-2061.
59. Phylactou, L.A., Darrah, C. and Wood, M.J. (1998) Ribozyme-mediated trans-splicing of a trinucleotide repeat. Nat. Genet., 18, 378-381.
60. Chen, H.Y., Kathirvel, P., Yee, W.C. and Lai, P.S. (2009) Correction of dystrophia myotonica type 1 pre-mRNA transcripts by artificial trans-splicing. Gene Ther., 16, 211-217.
61. Mansfield, S.G., Chao, H. and Walsh, C.E. (2004) RNA repair using spliceosome-mediated RNA trans-splicing. Trends Mol. Med., 10, 263-268.
62. Margolis, J.M., Schoser, B.G., Moseley, M.L., Day, J.W. and Ranum, L.P. (2006) DM2 intronic expansions: evidence for CCUG accumulation without flanking sequence or effects on ZNF9 mRNA processing or protein expression. Hum. Mol. Genet., 15, 1808-1815.
63. Langlois, M.A., Lee, N.S., Rossi, J.J. and Puymirat, J. (2003) Hammerhead ribozyme-mediated destruction of nuclear foci in myotonic dystrophy myoblasts. Mol. Ther., 7, 670-680.
64. Furling, D., Doucet, G., Langlois, M.A., Timchenko, L., Belanger, E., Cossette, L. and Puymirat, J. (2003) Viral vector producing antisense RNA restores myotonic dystrophy myoblast functions. Gene Ther., 10, 795-802.
65. Kurreck, J. (2003) Antisense technologies. Improvement through novel chemical modifications. Eur. J. Biochem., 270, 1628-1644.
66. Rudnick, S.I., Swaminathan, J., Sumaroka, M., Liebhaber, S. and Gewirtz, A.M. (2008) Effects of local mRNA structure on posttranscriptional gene silencing. Proc. Natl Acad. Sci. USA, 105, 13787-13792.
67. Napierala, M. and Krzyzosiak, W.J. (1997) CUG repeats present in myotonin kinase RNA form metastable 'slippery' hairpins. J. Biol. Chem., 272, 31079-31085.
68. Krzyzosiak, W.J., Sobczak, K. and Napierala, M. (2006) Structural characteristics of trinucleotide repeats in transcripts. In Ashizawa, T. and Wells, R. (eds), Genetic Instabilities and Neurological Diseases, 2nd edn. Academic Press, Inc., San Diego, CA, pp. 705-713.
69. Broda, M., Kierzek, E., Gdaniec, Z., Kulinski, T. and Kierzek, R. (2005) Thermodynamic stability of RNA structures formed by CNG trinucleotide repeats. Implication for prediction of RNA structure. Biochemistry, 44, 10873-10882.
70. 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.
71. Malinina, L. (2005) Possible involvement of the RNAi pathway in trinucleotide repeat expansion diseases. J. Biomol. Struct. Dyn., 23, 233-235.
72. Krol, J., Fiszer, A., Mykowska, A., Sobczak, K., de Mezer, M. and Krzyzosiak, W.J. (2007) Ribonuclease dicer cleaves triplet repeat hairpins into shorter repeats that silence specific targets. Mol. Cell, 25, 575-586.
73. Ghildiyal, M. and Zamore, P.D. (2009) Small silencing RNAs: an expanding universe. Nat. Rev. Genet., 10, 94-108.
74. Langlois, M.A., Boniface, C., Wang, G., Alluin, J., Salvaterra, P.M., Puymirat, J., Rossi, J.J. and Lee, N.S. (2005) Cytoplasmic and nuclear retained DMPK mRNAs are targets for RNA interference in myotonic dystrophy cells. J. Biol. Chem., 280, 16949-16954.
75. Robb, G.B., Brown, K.M., Khurana, J. and Rana, T.M. (2005) Specific and potent RNAi in the nucleus of human cells. Nat. Struct. Mol. Biol., 12, 133-137.
76. Caplen, N.J., Taylor, J.P., Statham, V.S., Tanaka, F., Fire, A. and Morgan, R.A. (2002) Rescue of polyglutamine-mediated cytotoxicity by double-stranded RNA-mediated RNA interference. Hum. Mol. Genet., 11, 175-184.
77. Miller, V.M., Xia, H., Marrs, G.L., Gouvion, C.M., Lee, G., Davidson, B.L. and Paulson, H.L. (2003) Allele-specific silencing of dominant disease genes. Proc. Natl Acad. Sci. USA, 100, 7195-7200.
78. Mulders, S.A., van den Broek, W.J., Wheeler, T.M., Croes, H.J., van Kuik-Romeijn, P., de Kimpe, S.J., Furling, D., Platenburg, G.J., Gourdon, G., Thornton, C.A. et al. (2009) Triplet-repeat oligonucleotide-mediated reversal of RNA toxicity in myotonic dystrophy. Proc. Natl Acad. Sci. USA, 106, 13915-13920.
79. Groenen, P.J.T.A., Wansink, D.G., Coerwinkel, M., van den Broek, W., Jansen, G. and Wieringa, B. (2000) Constitutive and regulated modes of splicing produce six major myotonic dystrophy protein kinase (DMPK) isoforms with distinct properties. Hum. Mol. Genet., 9, 605-616.
80. Tiscornia, G. and Mahadevan, M.S. (2000) Myotonic dystrophy: the role of the CUG triplet repeats in splicing of a novel DMPK exon and altered cytoplasmic DMPK mRNA isoform ratios. Mol. Cell, 5, 959-967.
81. Doma, M.K. and Parker, R. (2007) RNA quality control in eukaryotes. Cell, 131, 660-668.
82. Garneau, N.L., Wilusz, J. and Wilusz, C.J. (2007) The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol., 8, 113-126.
83. Seznec, H., Lia-Baldini, A.S., Duros, C., Fouquet, C., Lacroix, C., Hofmann-Radvanyi, H., Junien, C. and Gourdon, G. (2000) Transgenic mice carrying large human genomic sequences with expanded CTG repeat mimic closely the DM CTG repeat intergenerational and somatic instability. Hum. Mol. Genet., 9, 1185-1194.
84. Wheeler, T.M., Sobczak, K., Lueck, J.D., Osborne, R.J., Lin, X., Dirksen, R.T. and Thornton, C.A. (2009) Reversal of RNA dominance by displacement of protein sequestered on triplet repeat RNA. Science, 325, 336-339.
85. Hu, J., Matsui, M., Gagnon, K.T., Schwartz, J.C., Gabillet, S., Arar, K., Wu, J., Bezprozvanny, I. and Corey, D.R. (2009) Allele-specific silencing of mutant huntingtin and ataxin-3 genes by targeting expanded CAG repeats in mRNAs. Nat. Biotechnol., 27, 478-484.
86. Bhindi, R., Fahmy, R.G., Lowe, H.C., Chesterman, C.N., Dass, C.R., Cairns, M.J., Saravolac, E.G., Sun, L.Q. and Khachigian, L.M. (2007) Brothers in arms: DNA enzymes, short interfering RNA, and the emerging wave of small-molecule nucleic acid-based gene-silencing strategies. Am. J. Pathol., 171, 1079-1088.
87. Yen, L., Strittmatter, S.M. and Kalb, R.G. (1999) Sequence-specific cleavage of Huntingtin mRNA by catalytic DNA. Ann. Neurol., 46, 366-373.
88. Bauman, J., Jearawiriyapaisarn, N. and Kole, R. (2009) Therapeutic potential of splice-switching oligonucleotides. Oligonucleotides, 19, 1-14.
89. Kaihatsu, K., Janowski, B.A. and Corey, D.R. (2004) Recognition of chromosomal DNA by PNAs. Chem. Biol., 11, 749-758.
90. Boffa, L.C., Morris, P.L., Carpaneto, E.M., Louissaint, M. and Allfrey, V.G. (1996) Invasion of the CAG triplet repeats by a complementary peptide nucleic acid inhibits transcription of the androgen receptor and TATA-binding protein genes and correlates with refolding of an active nucleosome containing a unique AR gene sequence. J. Biol. Chem., 271, 13228-13233.
91. Belotserkovskii, B.P., Liu, R. and Hanawalt, P.C. (2009) Peptide nucleic acid (PNA) binding and its effect on in vitro transcription in friedreich's ataxia triplet repeats. Mol. Carcinog., 48, 299-308.
92. Janowski, B.A., Huffman, K.E., Schwartz, J.C., Ram, R., Hardy, D., Shames, D.S., Minna, J.D. and Corey, D.R. (2005) Inhibiting gene expression at transcription start sites in chromosomal DNA with antigene RNAs. Nat. Chem. Biol., 1, 216-222.
93. Janowski, B.A., Younger, S.T., Hardy, D.B., Ram, R., Huffman, K.E. and Corey, D.R. (2007) Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat. Chem. Biol., 3, 166-173.
94. Summerton, J. (1999) Morpholino antisense oligomers: the case for an RNase H-independent structural type. Biochim. Biophys. Acta, 1489, 141-158.
95. Warf, M.B., Nakamori, M., Matthys, C.M., Thornton, C.A. and Berglund, J.A. (2009) Pentamidine reverses the splicing defects associated with myotonic dystrophy. Proc. Natl Acad. Sci. USA, 106, 18551-18556.
96. Arambula, J.F., Ramisetty, S.R., Baranger, A.M. and Zimmerman, S.C. (2009) A simple ligand that selectively targets CUG trinucleotide repeats and inhibits MBNL protein binding. Proc. Natl Acad. Sci. USA, 106, 16068-16073.
97. Gareiss, P.C., Sobczak, K., McNaughton, B.R., Palde, P.B., Thornton, C.A. and Miller, B.L. (2008) Dynamic combinatorial selection of molecules capable of inhibiting the (CUG) repeat RNA-MBNL1 interaction in vitro: discovery of lead compounds targeting myotonic dystrophy (DM1). J. Am. Chem. Soc., 130, 16254-16261.
98. Lee, M.M., Pushechnikov, A. and Disney, M.D. (2009) Rational and modular design of potent ligands targeting the RNA that causes myotonic dystrophy 2. ACS Chem. Biol., 4, 345-355.
99. Lee, M.M., Childs-Disney, J.L., Pushechnikov, A., French, J.M., Sobczak, K., Thornton, C.A. and Disney, M.D. (2009) Controlling the specificity of modularly assembled small molecules for RNA via ligand module spacing: targeting the RNAs that cause myotonic muscular dystrophy. J. Am. Chem. Soc., 131, 17464-17472.
100. Pushechnikov, A., Lee, M.M., Childs-Disney, J.L., Sobczak, K., French, J.M., Thornton, C.A. and Disney, M.D. (2009) Rational design of ligands targeting triplet repeating transcripts that cause RNA dominant disease: application to myotonic muscular dystrophy type 1 and spinocerebellar ataxia type 3. J. Am. Chem. Soc., 131, 9767-9779.
101. Disney, M.D., Lee, M.M., Pushechnikov, A. and Childs-Disney, J.L. (2010) The role of flexibility in the rational design of modularly assembled ligands targeting the RNAs that cause the myotonic dystrophies. Chembiochem., 11, 375-382.
102. Mastroyiannopoulos, N.P., Feldman, M.L., Uney, J.B., Mahadevan, M.S. and Phylactou, L.A. (2005) Woodchuck post-transcriptional element induces nuclear export of myotonic dystrophy 3' untranslated region transcripts. EMBO Rep., 6, 458-463.
103. Mastroyiannopoulos, N.P., Chrysanthou, E., Kyriakides, T.C., Uney, J.B., Mahadevan, M.S. and Phylactou, L.A. (2008) The effect of myotonic dystrophy transcript levels and location on muscle differentiation. Biochem. Biophys. Res. Commun., 377, 526-531.
104. Dansithong, W., Wolf, C.M., Sarkar, P., Paul, S., Chiang, A., Holt, I., Morris, G.E., Branco, D., Sherwood, M.C., Comai, L. et al. (2008) Cytoplasmic CUG RNA foci are insufficient to elicit key DM1 features. PLoS One, 3, e3968.
105. White, P.J., Anastasopoulos, F., Pouton, C.W. and Boyd, B.J. (2009) Overcoming biological barriers to in vivo efficacy of antisense oligonucleotides. Expert Rev. Mol. Med., 11, e10.
106. Juliano, R., Bauman, J., Kang, H. and Ming, X. (2009) Biological barriers to therapy with antisense and siRNA oligonucleotides. Mol. Pharm., 6, 686-695.
107. Banks, W.A. (2009) Characteristics of compounds that cross the blood-brain barrier. BMC Neurol., 9 (Suppl. 1), S3.