Ss-siRNAs allele selectively inhibit ataxin-3 expression: Multiple mechanisms for an alternative gene silencing strategy

Nucleic Acids Research

Volumn 41, Issue 20, 2013, Pages 9570-9583

  Liu, Jing ^a   Yu, Dongbo ^a   Aiba, Yuichiro ^a   Pendergraff, Hannah ^a,c   Swayze, Eric E ^b   Lima, Walt F ^b   Hu, Jiaxin ^a   Prakash, Thazha P ^b   Corey, David R ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b ISIS PHARMACEUTICALS   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; ATAXIN 3; HUNTINGTIN; POLYGLUTAMINE; SINGLE STRANDED RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; BASE MISPAIRING; BASE PAIRING; BINDING AFFINITY; BIOTINYLATION; CAG REPEAT; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; RNA INTERFERENCE;

ALLELES; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; CELL LINE; HUMANS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRINUCLEOTIDE REPEATS;

EID: 84890015655     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt693     Document Type: Article

References (33)

1. Watts, J.K. and Corey, D.R. (2012) Silencing disease genes in the laboratory and the clinic. J. Pathol., 226, 365-379.
2. Robinson, J.G. (2013) Management of familial hypercholesterolemia: a review of the recommendations from the national lipid association expert panel on familial hypercholesterolemia. J. Manag. Care Pharm., 19, 139-149.
3. Tabernero, J., Shapiro, G.I., LoRusso, P.M., Cervantes, A., Schwartz, G.K., Weiss, G.J., Paz-Ares, L., Cho, D.C., Infante, J.R., Alsina, M. et al. (2013) First-in-humans trial of an RNA interference therapeutic targeting VEGF and KSP in cancer patients with liver involvement. Cancer Discov., 3, 406-417.
4. Schwarz, D.S., Hutvagner, G., Haley, B. and Zamore, P.D. (2002) Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell, 10, 537-548.
5. Martinez, J., Patkaniowska, A., Urlaub, H., Luhrmann, R. and Tuschl, T. (2002) Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell, 110, 563-574.
6. Chorn, G., Klein-McDowell, M., Zhao, L., Saunders, M.A., Flanagan, W.M., Willingham, A.T. and Lim, L.P. (2012) Singlestranded microRNA mimics. RNA, 18, 1796-1804.
7. Hall, A.H., Wan, J., Spesock, A., Sergueeva, Z., Shaw, B.R. and Alexander, K.A. (2006) High potency silencing by single-stranded boranophosphate siRNA. Nucleic Acids Res., 34, 2773-2781.
8. Haringsma, H.J., Li, J.J., Soriano, F., Kenski, D.M., Flanagan, W.M. and Willingham, A.T. (2012) mRNA knockdown by single strand RNA is improved by chemical modifications. Nucleic Acids Res., 40, 4125-4136.
9. Holen, T., Amarzguioui, M., Babaie, E. and Prydz, H. (2003) Similar behaviour of single-strand and double-strand siRNAs suggests they act through a common RNAi pathway. Nucleic Acids Res., 31, 2401-2407.
10. Xu, Y., Linde, A., Larsson, O., Thormeyer, D., Elmen, J., Wahlestedt, C. and Liang, Z. (2004) Functional comparison of single- and double-stranded siRNAs in mammalian cells. Biochem. Biophys. Res. Commun., 316, 680-687.
11. Lima, W.F., Prakash, T.P., Murray, H.M., Kinberger, G.A., Li, W., Chappell, A.E., Li, C.S., Murray, S.F., Gaus, H., Seth, P.P. et al. (2012) Single-stranded siRNAs activate RNAi in animals. Cell, 150, 883-894.
12. Yu, D., Pendergraff, H., Liu, J., Kordasiewicz, H.B., Cleveland, D.W., Swayze, E.E., Lima, W.F., Crooke, S.T., Prakash, T.P. and Corey, D.R. (2012) Single-stranded RNAs use RNAi to potently and allele-selectively inhibit mutant huntingtin expression. Cell, 150, 895-908.
13. Orr, H.T. and Zoghbi, H.Y. (2007) Trinucleotide repeat disorders. Annu. Rev. Neurosci., 30, 575-621.
14. Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T. and Patel, D.J. (2008) Structure of an argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature, 456, 921-926.
15. Matsui, M., Prakash, T.P. and Corey, D.R. (2013) Transcriptional silencing by single-stranded RNAs targeting a noncoding RNA that overlaps a gene promoter. ACS Chem. Biol., 8, 122-126.
16. Krzyzosiak, W.J., Sobczak, K., Wojciechowska, M., Fiszer, A., Mykowska, A. and Kozlowski, P. (2011) Triplet repeat RNA structure and its role as pathogenic agent and therapeutic target. Nucleic Acids Res., 40, 11-26.
17. Costa Mdo, C. and Paulson, H.L. (2012) Toward understanding Machado-Joseph disease. Prog. Neurobiol., 97, 239-257.
18. 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.
19. Alves, S., Nascimento-Ferreira, I., Auregan, G., Hassig, R., Dufour, N., Brouillet, E., Pedroso de Lima, M.C., Hantraye, P., Pereira de Almeida, L. and Deglon, N. (2008) Allele-specific RNA silencing of mutant ataxin-3 mediates neuroprotection in a rat model of Machado-Joseph disease. PLoS One, 3, e3341.
20. Hu, J., Gagnon, K.T., Liu, J., Watts, J.K., Syeda-Nawaz, J., Bennett, C.F., Swayze, E.E., Randolph, J., Chattopadhyaya, J. and Corey, D.R. (2011) Allele-selective inhibition of ataxin-3 (ATX3) expression by antisense oligomers and duplex RNAs. Biol. Chem., 392, 315-325.
21. Sasaki, H., Wakisaka, A., Fukazawa, T., Iwabuchi, K., Hamada, T., Takada, A., Mukai, E., Matsuura, T., Yoshiki, T. and Tashiro, K. (1995) CAG repeat expansion of Machado-Joseph disease in the Japanese: analysis of the repeat instability for parental transmission, and correlation with disease phenotype. J. Neurol. Sci., 133, 128-133.
22. Prakash, T.P., Lima, W.F., Murray, H.M., Elbashir, S., Cantley, W., Foster, D., Jayaraman, M., Chappell, A.E., Manoharan, M., Swayze, E.E. et al. (2013) Lipid nanoparticles improve activity of single-stranded siRNA and gapmer antisense oligonucleotides in animals. ACS Chem. Biol., 8, 1402-1406.
23. 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.
24. Hu, J., Liu, J. and Corey, D.R. (2010) Allele-selective inhibition of huntingtin expression by switching to an miRNA-like RNAi mechanism. Chem. Biol., 17, 1183-1188.
25. Meister, G., Landthaler, M., Patkaniowska, A., Dorsett, Y., Teng, G. and Tuschl, T. (2004) Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell, 15, 185-197.
26. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., Hammond, S.M., Joshua-Tor, L. and Hannon, G.J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science, 305, 1437-1441.
27. Hu, J., Liu, J., Yu, D., Chu, Y. and Corey, D.R. (2012) Mechanism of allele-selective inhibition of huntingtin expression by duplex RNAs that target CAG repeats: function through the RNAi pathway. Nucleic Acids Res., 40, 11270-11280.
28. Fiszer, A., Mykowska, A. and Krzyzosiak, W.J. (2011) Inhibition of mutant huntingtin expression by RNA duplex targeting expanded CAG repeats. Nucleic Acids Res., 39, 5578-5585.
29. Eulalio, A., Tritschler, F. and Izaurralde, E. (2009) The GW182 protein family in animal cells: new insights into domains required for miRNA-mediated gene silencing. RNA, 15, 1433-1442.
30. Kole, R., Krainer, A.R. and Altman, S. (2012) RNA therapeutics: beyond RNA interference and antisense oligonucleotides. Nat. Rev. Drug Discov., 11, 125-140.
31. Seth, P.P., Siwkowski, A., Allerson, C.R., Vasquez, G., Lee, S., Prakash, T.P., Wancewicz, E.V., Witchell, D. and Swayze, E.E. (2009) Short antisense oligonucleotides with novel 20-40 conformationaly restricted nucleoside analogues show improved potency without increased toxicity in animals. J. Med. Chem., 52, 10-13.
32. Rigo, F., Hua, Y., Chun, S.J., Prakash, T.P., Krainer, A.R. and Bennett, C.F. (2012) Synthetic oligonucleotides recruit ILF2/3 to RNA transcripts to modulate splicing. Nat. Chem. Biol., 8, 555-561.
33. Evers, M.M., Tran, H.D., Zalachoras, I., Pepers, B.A., Meijer, O.C., den Dunnen, J.T., van Ommen, G.J., Aartsma-Rus, A. and van Roon-Mom, W.M. (2013) Ataxin-3 protein modification as a treatment strategy for spinocerebellar ataxia type 3: removal of the CAG containing exon. Neurobiol. Dis., 58C, 49-56.