Chemical correction of pre-mRNA splicing defects associated with sequestration of muscleblind-like 1 protein by expanded r(CAG)-containing transcripts

ACS Chemical Biology

Volumn 7, Issue 3, 2012, Pages 496-505

  Kumar, Amit ^a   Parkesh, Raman ^a   Sznajder, Lukasz J ^b   Childs Disney, Jessica L ^a   Sobczak, Krzysztof ^b   Disney, Matthew D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; MUSCLEBLIND LIKE 1 PROTEIN; PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING AFFINITY; CAG REPEAT; EXON; GENE SEQUENCE; HUMAN; HUMAN CELL; NUCLEOTIDE MOTIF; PRIORITY JOURNAL; RNA BINDING;

BENZOATES; GUANIDINES; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; LIGANDS; RNA SPLICING; RNA, MESSENGER; RNA-BINDING PROTEINS; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEATS; TUMOR CELLS, CULTURED;

EID: 84863385282     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb200413a     Document Type: Article

References (65)

1. Doudna, J. A. (2000) Structural genomics of RNA Nat. Struct. Biol. 7 (Suppl.) 954-956
2. Batey, R. T., Rambo, R. P., and Doudna, J. A. (1999) Tertiary motifs in RNA structure and folding Angew. Chem., Int. Ed. 38, 2326-2343 (Pubitemid 29399554)
3. Zaug, A. J. and Cech, T. R. (1986) The intervening sequence RNA of Tetrahymena is an enzyme Science 231, 470-475 (Pubitemid 16163735)
4. Lagos-Quintana, M., Rauhut, R., Lendeckel, W., and Tuschl, T. (2001) Identification of novel genes coding for small expressed RNAs Science 294, 853-858 (Pubitemid 33032103)
5. Winkler, W., Nahvi, A., and Breaker, R. R. (2002) Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression Nature 419, 952-956 (Pubitemid 35339632)
6. Nissen, P., Hansen, J., Ban, N., Moore, P. B., and Steitz, T. A. (2000) The structural basis of ribosome activity in peptide bond synthesis Science 289, 920-930 (Pubitemid 30659940)
7. Gallego, J. and Varani, G. (2001) Targeting RNA with small-molecule drugs: therapeutic promise and chemical challenges Acc. Chem. Res. 34, 836-843 (Pubitemid 32999608)
8. Hamy, F., Felder, E. R., Heizmann, G., Lazdins, J., Aboul-ela, F., Varani, G., Karn, J., and Klimkait, T. (1997) An inhibitor of the Tat/TAR RNA interaction that effectively suppresses HIV-1 replication Proc. Natl. Acad. Sci. U.S.A. 94, 3548-3553 (Pubitemid 27180409)
9. Mathews, D. H., Disney, M. D., Childs, J. L., Schroeder, S. J., Zuker, M., and Turner, D. H. (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure Proc. Natl. Acad. Sci. U.S.A. 101, 7287-7292 (Pubitemid 38638025)
10. Mathews, D. H., Sabina, J., Zuker, M., and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure J. Mol. Biol. 288, 911-940 (Pubitemid 29248642)
11. Woese, C. R., Magrum, L. J., Gupta, R., Siegel, R. B., Stahl, D. A., Kop, J., Crawford, N., Brosius, J., Gutell, R., Hogan, J. J., and Noller, H. F. (1980) Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence Nucleic Acids Res. 8, 2275-2293 (Pubitemid 10025762)
12. 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
13. 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
14. 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
15. Cho, J., Hamasaki, K., and Rando, R. R. (1998) The binding site of a specific aminoglycoside binding RNA molecule Biochemistry 37, 4985-4992 (Pubitemid 28175981)
16. 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
17. Mykowska, A., Sobczak, K., Wojciechowska, M., Kozlowski, P., and Krzyzosiak, W. J. (2011) CAG repeats mimic CUG repeats in the misregulation of alternative splicing Nucleic Acids Res. 39, 8938-8951
18. Sobczak, K., Michlewski, G., de Mezer, M., Kierzek, E., Krol, J., Olejniczak, M., Kierzek, R., and Krzyzosiak, W. J. (2010) Structural diversity of triplet repeat RNAs J. Biol. Chem. 285, 12755-12764
19. Chaires, J. B., Ragazzon, P. A., and Garbett, N. C. (2003) A competition dialysis assay for the study of structure-selective binding to nucleic acids, in Current Protocols in Nucleic Acid Chemistry, Unit 8.3, John Wiley and Sons, Inc., New York.
20. Li, N., Ma, Y., Yang, C., Guo, L., and Yang, X. (2005) Interaction of anticancer drug mitoxantrone with DNA analyzed by electrochemical and spectroscopic methods Biophys. Chem. 116, 199-205 (Pubitemid 40962447)
21. Lyles, M. B. and Cameron, I. L. (2002) Interactions of the DNA intercalator acridine orange, with itself, with caffeine, and with double stranded DNA Biophys. Chem. 96, 53-76 (Pubitemid 34303302)
22. Neidle, S., Pearl, L. H., Herzyk, P., and Berman, H. M. (1988) A molecular model for proflavine-DNA intercalation Nucleic Acids Res. 16, 8999-9016
23. Wang, A. H., Ughetto, G., Quigley, G. J., and Rich, A. (1987) Interactions between an anthracycline antibiotic and DNA: molecular structure of daunomycin complexed to d(CpGpTpApCpG) at 1.2-Å resolution Biochemistry 26, 1152-1163 (Pubitemid 17030204)
24. Liu, Y., Peacey, E., Dickson, J., Donahue, C. P., Zheng, S., Varani, G., and Wolfe, M. S. (2009) Mitoxantrone analogues as ligands for a stem-loop structure of tau pre-mRNA J. Med. Chem. 52, 6523-6526
25. Zheng, S., Chen, Y., Donahue, C. P., Wolfe, M. S., and Varani, G. (2009) Structural basis for stabilization of the tau pre-mRNA splicing regulatory element by novantrone (mitoxantrone) Chem. Biol. 16, 557-566
26. Carlson, C. B., Vuyisich, M., Gooch, B. D., and Beal, P. A. (2003) Preferred RNA binding sites for a threading intercalator revealed by in vitro evolution Chem. Biol. 10, 663-672 (Pubitemid 36940943)
27. Marcheschi, R. J., Mouzakis, K. D., and Butcher, S. E. (2009) Selection and characterization of small molecules that bind the HIV-1 frameshift site RNA ACS Chem. Biol. 4, 844-854
28. Tanious, F. A., Veal, J. M., Buczak, H., Ratmeyer, L. S., and Wilson, W. D. (1992) DAPI (4′,6-diamidino-2-phenylindole) binds differently to DNA and RNA: minor-groove binding at AT sites and intercalation at AU sites Biochemistry 31, 3103-3112
29. 1H NMR study Nucleic Acids Res. 23, 1333-1340
30. Trotta, E. and Paci, M. (1998) Solution structure of DAPI selectively bound in the minor groove of a DNA T.T mismatch-containing site: NMR and molecular dynamics studies Nucleic Acids Res. 26, 4706-4713 (Pubitemid 28466619)
31. Disney, M. D., Childs, J. L., and Turner, D. H. (2004) Hoechst 33258 selectively inhibits group I intron self-splicing by affecting RNA folding ChemBioChem 5, 1647-1652 (Pubitemid 39664674)
32. Miletti, K. E. and Leibowitz, M. J. (2000) Pentamidine inhibition of group I intron splicing in Candida albicans correlates with growth inhibition Antimicrob. Agents Chemother. 44, 958-966 (Pubitemid 30165276)
33. Childs-Disney, J. L., Wu, M., Pushechnikov, A., Aminova, O., and Disney, M. D. (2007) A small molecule microarray platform to select RNA internal loop-ligand interactions ACS Chem. Biol. 2, 745-754 (Pubitemid 350285910)
34. Disney, M. D. and Childs-Disney, J. L. (2007) Using selection to identify and chemical microarray to study the RNA internal loops recognized by 6′-N-acylated kanamycin A ChemBioChem 8, 649-656 (Pubitemid 47194857)
35. Bevilacqua, J. M. and Bevilacqua, P. C. (1998) Thermodynamic analysis of an RNA combinatorial library contained in a short hairpin Biochemistry 37, 15877-15884 (Pubitemid 28524759)
36. Serra, M. J. and Turner, D. H. (1995) Predicting thermodynamic properties of RNA Methods Enzymol. 259, 242-261
37. Caskey, C. T., Pizzuti, A., Fu, Y. H., Fenwick, R. G., Jr., and Nelson, D. L. (1992) Triplet repeat mutations in human disease Science 256, 784-789
38. Dervan, P. B. (2001) Molecular recognition of DNA by small molecules Bioorg. Med. Chem. 9, 2215-2235 (Pubitemid 32834613)
39. 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. U.S.A. 106, 16068-16073
40. Mills, J. E. and Dean, P. M. (1996) Three-dimensional hydrogen-bond geometry and probability information from a crystal survey J. Comput. Aided Mol. Des. 10, 607-622 (Pubitemid 126712453)
41. Grant, J. A., Gallardo, M. A., and Pickup, B. T. (1996) A fast method of molecular shape comparison. A simple application of a Gaussian description of molecular shape J. Comput. Chem. 17, 1653-1666 (Pubitemid 126535414)
42. Haigh, J. A., Pickup, B. T., Grant, J. A., and Nicholls, A. (2005) Small molecule shape-fingerprints J. Chem. Inf. Model. 45, 673-684 (Pubitemid 40795171)
43. 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 (Pubitemid 37523508)
44. 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, 1769-1773
45. Day, J. W. and Ranum, L. P. (2005) RNA pathogenesis of the myotonic dystrophies Neuromuscular Disord. 15, 5-16 (Pubitemid 41556627)
46. Li, L. B. and Bonini, N. M. (2010) Roles of trinucleotide-repeat RNA in neurological disease and degeneration Trends Neurosci. 33, 292-298
47. Wojciechowska, M. and Krzyzosiak, W. J. Cellular toxicity of expanded RNA repeats: focus on RNA foci. Hum. Mol. Genet. 2011, in press.
48. Shieh, S. Y. and Bonini, N. M. (2011) Genes and pathways affected by CAG-repeat RNA-based toxicity in Drosophila Hum. Mol. Genet. 20, 4810-4821
49. Tsoi, H., Lau, C. K., Lau, K. F., and Chan, H. Y. (2011) Perturbation of U2AF65/NXF1-mediated RNA nuclear export enhances RNA toxicity in polyQ diseases Hum. Mol. Genet. 20, 3787-3797
50. Ho, T. H., Savkur, R. S., Poulos, M. G., Mancini, M. A., Swanson, M. S., and Cooper, T. A. (2005) Colocalization of muscleblind with RNA foci is separable from mis-regulation of alternative splicing in myotonic dystrophy J. Cell Sci. 118, 2923-2933 (Pubitemid 41136369)
51. Hsu, R. J., Hsiao, K. M., Lin, M. J., Li, C. Y., Wang, L. C., Chen, L. K., and Pan, H. (2011) Long tract of untranslated CAG repeats is deleterious in transgenic mice PLoS One 6, e16417
52. Wang, L. C., Chen, K. Y., Pan, H., Wu, C. C., Chen, P. H., Liao, Y. T., Li, C., Huang, M. L., and Hsiao, K. M. (2011) Muscleblind participates in RNA toxicity of expanded CAG and CUG repeats in Caenorhabditis elegans Cell. Mol. Life Sci. 68, 1255-1267
53. 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 (Pubitemid 351871727)
54. 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. U.S.A. 106, 18551-18556
55. 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 (Pubitemid 34428648)
56. 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 (Pubitemid 40045262)
57. 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 (Pubitemid 32998828)
58. 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
59. Taneja, K. L., McCurrach, M., Schalling, M., Housman, D., and Singer, R. H. (1995) Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues J. Cell. Biol. 128, 995-1002
60. Gomes-Pereira, M., Cooper, T. T., and Gourdon, G. (2011) Myotonic Dystrophy mouse models: towards rational therapy development Trends in Mol. Med. 17, 506-17
61. Childs-Disney, J. L., Tsitovich, P. B., and Disney, M. D. (2011) Using modularly assembled ligands to bind RNA internal loops separated by different distances ChemBioChem 12, 2143-2146
62. Yu, Z., Wang, A. M., Robins, D. M., and Lieberman, A. P. (2009) Altered RNA splicing contributes to skeletal muscle pathology in Kennedy disease knock-in mice Dis. Models Mech. 2, 500-507
63. Peyret, N., Seneviratne, P. A., Allawi, H. T., and SantaLucia, J., Jr. (1999) Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A.A, C.C, G.G, and T.T mismatches Biochemistry 38, 3468-3477
64. SantaLucia, J., Jr. (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics Proc. Natl. Acad. Sci. U.S.A. 95, 1460-1465
65. Puglisi, J. D. and Tinoco, I., Jr. (1989) Absorbance melting curves of RNA Methods Enzymol. 180, 304-325 (Pubitemid 20039582)