Role of context in RNA structure: Flanking sequences reconfigure CAG motif folding in huntingtin exon 1 transcripts

Biochemistry

Volumn 52, Issue 46, 2013, Pages 8219-8225

  Busan, Steven ^a   Weeks, Kevin M ^a  

^a University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX STRUCTURE; FLANKING SEQUENCE; HAIRPIN STRUCTURES; HUNTINGTON'S DISEASE; RNA STRUCTURES; STRUCTURAL DIFFERENCES; STRUCTURAL STUDIES; THERAPEUTIC INTERVENTION;

BIOCHEMISTRY; CHEMISTRY;

RNA;

ANTISENSE OLIGONUCLEOTIDE; HUNTINGTIN; MESSENGER RNA; RIBONUCLEASE T1;

ARTICLE; BASE PAIRING; CAG REPEAT; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; DISEASE PREDISPOSITION; DNA FLANKING REGION; EXON; GENETIC TRANSCRIPTION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; RESTRICTION SITE; RNA DEGRADATION; RNA FOLDING; RNA STRUCTURE; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE;

5' UNTRANSLATED REGIONS; EXONS; HUMANS; HUNTINGTON DISEASE; NERVE TISSUE PROTEINS; RIBONUCLEASE T1; RNA; RNA FOLDING; RNA, MESSENGER; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84888237702     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401129r     Document Type: Article

References (41)

1. Kremer, B., Goldberg, P., Andrew, S. E., Theilmann, J., Telenius, H., Zeisler, J., Squitieri, F., Lin, B., Bassett, A., and Almqvist, E. 1994, A worldwide study of the Huntington's disease mutation. The sensitivity and specificity of measuring CAG repeats N. Engl. J. Med. 330, 1401-1406
2. Lee, J. M., Ramos, E. M., Lee, J. H., Gillis, T., Mysore, J. S., Hayden, M. R., Warby, S. C., Morrison, P., Nance, M., and Ross, C. A. (2012) CAG repeat expansion in Huntington disease determines age at onset in a fully dominant fashion Neurology 78, 690-695
3. 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, e16417-1-e16417-11
4. 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
5. Velier, J., Kim, M., Schwarz, C., Kim, T. W., Sapp, E., Chase, K., Aronin, N., and DiFiglia, M. (1998) Wild-type and mutant huntingtin's function in vesicle trafficking in the secretory and endocytotic pathways Exp. Neurol. 152, 34-40
6. Gauthier, L. R., Charrin, B. C., Borrell-Pagès, M., Dompierre, J. P., Rangone, H., Cordelières, F. P., De Mey, J., MacDonald, M. E., Lessmann, V., and Humbert, S. 2004, Huntingtin controls neurotrophic support and survival of neurons by enhancing BDNF vesicular transport along microtubules Cell 118, 127-138
7. Caviston, J. P. and Holzbaur, E. L. F. (2009) Huntingtin as an essential integrator of intracellular vesicular trafficking Trends Cell Biol. 19, 147-155
8. Zala, D., Hinckelmann, M. V., and Saudou, F. (2013) Huntingtin's function in axonal transport is conserved in drosophila melanogaster PLoS One 8, e60162-1-e60162-10
9. Pfister, E. L., Kennington, L., Straubhaar, J., Wagh, S., Liu, W., DiFiglia, M., Landwehrmeyer, B., Vonsattel, J.-P., Zamore, P. D., and Aronin, N. (2009) Five siRNAs targeting three SNPs may provide therapy for three-quarters of huntington's disease patients Curr. Biol. 19, 774-778
10. Carroll, J. B., Warby, S. C., Southwell, A. L., Doty, C. N., Greenlee, S., Skotte, N., Hung, G., Bennett, C. F., Freier, S. M., and Hayden, M. R. (2011) Potent and selective antisense oligonucleotides targeting single-nucleotide polymorphisms in the Huntington disease gene/allele-specific silencing of mutant huntingtin Mol. Ther. 19, 2178-2185
11. Gagnon, K. T., Pendergraff, H. M., Deleavey, G. F., Swayze, E. E., Potier, P., Randolph, J., Roesch, E. B., Chattopadhyaya, J., Damha, M. J., and Bennett, C. F. 2010, Allele-selective inhibition of mutant huntingtin expression with antisense oligonucleotides targeting the expanded CAG repeat Biochemistry 49, 10166-10178
12. Sobczak, K., de Mezer, M., Michiewski, G., Kroi, J., and Krzyzosiak, W. J. (2003) RNA structure of trinucleotide repeats associated with human neurological diseases Nucleic Acids Res. 31, 5469-5482
13. Michlewski, G. and Krzyzosiak, W. J. (2004) Molecular architecture of CAG repeats in human disease related transcripts J. Mol. Biol. 340, 665-679
14. 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
15. Yuan, Y., Compton, S. A., Sobczak, K., Stenberg, M. G., Thornton, C. A., Griffith, J. D., and Swanson, M. S. (2007) Muscleblind-like 1 interacts with RNA hairpins in splicing target and pathogenic RNAs Nucleic Acids Res. 35, 5474-5486
16. Kiliszek, A., Kierzek, R., Krzyzosiak, W. J., and Rypniewski, W. (2010) Atomic resolution structure of CAG RNA repeats: Structural insights and implications for the trinucleotide repeat expansion diseases Nucleic Acids Res. 38, 8370-8376
17. de Mezer, M., Wojciechowska, M., Napierala, M., Sobczak, K., and Krzyzosiak, W. J. (2011) Mutant CAG repeats of Huntingtin transcript fold into hairpins, form nuclear foci and are targets for RNA interference Nucleic Acids Res. 39, 3852-3863
18. Vester, B. and Wengel, J. (2004) LNA (locked nucleic acid): High-affinity targeting of complementary RNA and DNA Biochemistry 43, 13233-13241
19. Wyatt, J. R., Chastain, M., and Puglisi, J. D. (1991) Synthesis and purification of large amounts of RNA oligonucleotides Biotechniques 11, 764-769
20. Mortimer, S. A. and Weeks, K. M. (2007) A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry J. Am. Chem. Soc. 129, 4144-4145
21. Karabiber, F., McGinnis, J. L., Favorov, O. V., and Weeks, K. M. (2012) QuShape: Rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis RNA 19, 63-73
22. Wilkinson, K. A., Merino, E. J., and Weeks, K. M. (2006) Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): Quantitative RNA structure analysis at single nucleotide resolution Nat. Protoc. 1, 1610-1616
23. Reuter, J. S. and Mathews, D. H. (2010) RNAstructure: Software for RNA secondary structure prediction and analysis BMC Bioinf. 11, 116
24. Deigan, K. E., Li, T. W., Mathews, D. H., and Weeks, K. M. (2009) Accurate SHAPE-directed RNA structure determination Proc. Natl. Acad. Sci. U.S.A. 106, 97-102
25. Hajdin, C. E., Bellaousov, S., Huggins, W., Leonard, C. W., Mathews, D. H., and Weeks, K. M. (2013) Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots Proc. Natl. Acad. Sci. U.S.A. 110, 5498-5503
26. Merino, E. J., Wilkinson, K. A., Coughlan, J. L., and Weeks, K. M. (2005) RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE) J. Am. Chem. Soc. 127, 4223-4231
27. Weeks, K. M. and Mauger, D. M. (2011) Exploring RNA structural codes with SHAPE chemistry Acc. Chem. Res. 44, 1280-1291
28. Lin, B., Nasir, J., Kalchman, M. A., McDonald, H., Zeisler, J., Goldberg, Y. P., and Hayden, M. R. (1995) Structural analysis of the 5′ region of mouse and human huntington disease genes reveals conservation of putative promoter region and di-and trinucleotide polymorphisms Genomics 25, 707-715
29. Lee, J., Park, E. H., Couture, G., Harvey, I., Garneau, P., and Pelletier, J. (2002) An upstream open reading frame impedes translation of the huntingtin gene Nucleic Acids Res. 30, 5110-5119
30. Nalavade, R., Griesche, N., Ryan, D. P., Hildebrand, S., and Krau, S. (2013) Mechanisms of RNA-induced toxicity in CAG repeat disorders Cell Death Dis. 4, e752-1-e752-11
31. Galka-Marciniak, P., Urbanek, M. O., and Krzyzosiak, W. J. (2012) Triplet repeats in transcripts: Structural insights into RNA toxicity Biol. Chem. 393, 1299-1315
32. Hodgson, J. G., Smith, D. J., McCutcheon, K., Koide, H. B., Nishiyama, K., Dinulos, M. B., Stevens, M. E., Bissada, N., Nasir, J., and Kanazawa, I. 1996, Human huntingtin derived from YAC transgenes compensates for loss of murine huntingtin by rescue of the embryonic lethal phenotype Hum. Mol. Genet. 5, 1875-1885
33. Ehrnhoefer, D. E., Butland, S. L., Pouladi, M. A., and Hayden, M. R. (2009) Mouse models of Huntington disease: Variations on a theme Dis. Models & Mech. 2, 123-129
34. Southwell, A. L., Warby, S. C., Carroll, J. B., Doty, C. N., Skotte, N. H., Zhang, W., Villanueva, E. B., Kovalik, V., Xie, Y., and Pouladi, M. A. 2013, A fully humanized transgenic mouse model of Huntington disease Hum. Mol. Genet. 22, 18-34
35. Slow, E. J., van Raamsdonk, J., Rogers, D., Coleman, S. H., Graham, R. K., Deng, Y., Oh, R., Bissada, N., Hossain, S. M., and Yang, Y. Z. 2003, Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease Hum. Mol. Genet. 12, 1555-1567
36. Gray, M., Shirasaki, D. I., Cepeda, C., Andre, V. M., Wilburn, B., Lu, X. H., Tao, J., Yamazaki, I., Li, S. H., and Sun, Y. E. 2008, Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice J. Neurosci. 28, 6182-6195
37. Pouladi, M. A., Stanek, L. M., Xie, Y., Franciosi, S., Southwell, A. L., Deng, Y., Butland, S., Zhang, W., Cheng, S. H., and Shihabuddin, L. S. 2012, Marked differences in neurochemistry and aggregates despite similar behavioral and neuropathological features of Huntington disease in full-length BACHD and YAC128 mice Hum. Mol. Genet. 21, 2219-2232
38. Sobczak, K. and Krzyzosiak, W. J. (2005) CAG repeats containing CAA interruptions form branched hairpin structures in spinocerebellar ataxia type 2 transcripts J. Biol. Chem. 280, 3898-3910
39. 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
40. Sathasivam 2013, Aberrant splicing of HTT generates the pathogenic exon 1 protein in Huntington disease Proc. Natl. Acad. Sci. U.S.A. 110, 2366-2370
41. Pickering, B. M. and Willis, A. E. (2005) The implications of structured 5′ untranslated regions on translation and disease Semin. Cell Dev. Biol. 16, 39-47