Allele-selective inhibition of ataxin-3 (ATX3) expression by antisense oligomers and duplex RNAs

Biological Chemistry

Volumn 392, Issue 4, 2011, Pages 315-325

  Hu, Jiaxin ^a   Gagnon, Keith T ^a   Liu, Jing ^a   Watts, Jonathan K ^a   Syeda Nawaz, Jeja ^a   Bennett, C Frank ^b   Swayze, Eric E ^b   Randolph, John ^c   Chattopadhyaya, Jyoti ^d   Corey, David R ^a  

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

^b ISIS PHARMACEUTICALS   (United States)

^c Glen Research Corporation   (United States)

^d UPPSALA UNIVERSITY   (Sweden)

Author keywords

Allele selective; Ataxin 3; Peptide nucleic acid; SiRNA; Spinocerebellar ataxia 3

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ATAXIN 3; COMPLEMENTARY RNA; MESSENGER RNA; PEPTIDE NUCLEIC ACID; RNA;

ALLELE; ARTICLE; CAG REPEAT; GENE SILENCING; HUMAN; HUMAN CELL; IN VIVO STUDY; INHIBITION KINETICS; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALLELES; BASE SEQUENCE; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDE NUCLEIC ACIDS; PEPTIDES; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA, DOUBLE-STRANDED;

EID: 79955461204     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2011.045     Document Type: Article

References (39)

1. 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.
2. Alves, S., Nascimento-Ferreira, I., Dufour, N., Hassig, R., Auregan, G., Nobrega, C., Brouillet, E., Hantraye, P., Pedroso de Lima, M.C., Deglon, N., et al. (2010). Silencing ataxin-3 mitigates degeneration in a rat model of Machado-Joseph disease: No role for wild-type ataxin-3? Hum. Mol. Genet. 19, 2380-2394.
3. Boy, J., Schmidt, T., Wolburg, H., Mack, A., Nuber, S., Bottcher, M., Schmitt, I., Holzmann, C., Zimmermann, F., Servadio, A., et al. (2009). Reversibility of symptoms in a conditional mouse model of spinocerebellar ataxia type 3. Hum. Mol. Genet. 18, 4282-4295.
4. Braasch, D.A., Liu, Y., and Corey, D.R. (2002). Antisense inhibition of gene expression in cells by oligonucleotides incorporating locked nucleic acids: Effect of mRNA target sequence and chimera design. Nucleic Acids Res. 30, 5160-5167. (Pubitemid 36033034)
5. De Souza, E.B., Cload, S.T., Pendergrast, P.S., and Sah, D.W. (2009). Novel therapeutic modalities to address nondrugable protein interaction targets. Neuropsychopharmacology 34, 142-158.
6. Denovan-Wright, E.M. and Davidson, B.L. (2006). RNAi: A potential therapy for the dominantly inherited nucleotide repeat diseases. Gene Ther. 13, 525-531.
7. Du, Q., Thonberg, H., Wang, J., Wahlestedt, C., and Liang, Z. (2005). A systematic analysis of the silencing effects of an active siRNA at all single-nucleotide mismatched target sites. Nucleic Acids Res. 33, 1671-1677. (Pubitemid 41418395)
8. Filipowicz, W., Bhattacharyya, S.N., and Sonenberg, N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet. 9, 102-114.
9. Gagnon, K.T., Pendergraff, H.M., Deleavey, G.F., Swayze, E.E., Potier, P., Randolph, J., Roesch, E.B., Chattopadhyaya, J., Damha, M.J., Bennett, C.F., et al. (2010). Allele-selective inhibition of mutant huntingtin expression with antisense oligonucleotides targeting the expanded CAG repeat. Biochemistry 49, 2243-2252.
10. Gonzalez-Alegre, P. and Paulson, H.L. (2007). Technology insight: Therapeutic RNA interference - how far from the neurology clinic? Nat. Clin. Pract. Neurol. 3, 394-404. (Pubitemid 47040329)
11. Hu, J. and Corey, D.R. (2007). Inhibiting gene expression with peptide nucleic acid (PNA) - peptide conjugates that target chromosomal DNA. Biochemistry 46, 7581-7589. (Pubitemid 46986382)
12. Hu, J., Matsui, M., Gagnon, K.T., Schwartz, J.C., Gabillet, S., Arar, K., Wu, J., Bezprozvanny, I., and Corey, D.R. (2009a). Allelespecific silencing of mutant huntingtin and ataxin-3 genes by targeting expanded CAG repeats in mRNAs. Nat. Biotechnol. 27, 478-484.
13. Hu, J., Dodd, D.W., Hudson, R.H., and Corey, D.R. (2009b). Cellular localization and allele-selective inhibition of mutant huntingtin protein by peptide nucleic acid oligomers containing the fluorescent nucleobase wbis-o-(aminoethoxy)phenylxpyrrolocytosine. Bioorg. Med. Chem. Lett. 19, 6181-6184.
14. Hu, J., Matsui, M., and Corey, D.R. (2009c). Allele-selective inhibition of mutant huntingtin by peptide nucleic acid-peptide conjugates, locked nucleic acid, and small interfering RNA. Ann. NY Acad. Sci. 1175, 24-31.
15. Hu, J., Liu, J., and Corey, D.R. (2010). Allele-selective inhibition of huntingtin expression by switching RNAi mechanisms. Chem. Biol. 17, 1183-1188.
16. Janowski, B.A., Hu, J., and Corey, D.R. (2006). Silencing gene expression by targeting chromosomal DNA with antigene peptide nucleic acids and duplex RNAs. Nat. Protoc. 1, 436-443.
17. 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.
18. Kumar, R., Singh, S.K., Koshkin, A.A., Rajwanshi, V.K., Meldgaard, M., and Wengel, J. (1998). The first analogues of LNA (locked nucleic acids): Phosphorothioate-LNA and 29-thio-LNA. Bioorg. Med. Chem. Lett. 8, 2219-2222. (Pubitemid 28561609)
19. Kurreck, J. (2009). RNA interference: From basic research to therapeutic applications. Angew. Chem. Int. Ed. 48, 1378-1398.
20. Kwon, Y.U. and Kodadek, T. (2007). Quantitative evaluation of the relative cell permeability of peptoids and peptides. J. Am. Chem. Soc. 129, 1508-1509.
21. 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). Argonaute 2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441. (Pubitemid 39167657)
22. Marin, V.L. and Armitage, B.A. (2005). RNA guanine quadruplex invasion by complementary and homologous PNA probes. J. Am. Chem. Soc. 127, 8032-8033. (Pubitemid 40799655)
23. 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. (Pubitemid 36706415)
24. 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.
25. Nielsen, P.E., Egholm, M., Berg, R.H., and Buchardt, O. (1991). Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide. Science 254, 1497-1500. (Pubitemid 21917487)
26. Obika, S., Nanbu, D., Hari, Y., Andoh, J., Morio, K., Doi, T., and Imanishi, T. (1998). Stability and structural features of the duplexes containing nucleoside analogues with a fixed N-type conformation, 29-O,49-C-methyleneribonucleosides. Tetrahedron Lett. 39, 5401-5404. (Pubitemid 28295121)
27. Olivos, H.J., Alluri, P.G., Reddy, M.M., Salony, D., and Kodadek, T. (2002). Microwave-assisted solid phase synthesis of peptoids. Org. Lett. 4, 4057-4059.
28. Orr, H.T. and Zoghbi, H.Y. (2007). Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30, 575-621. (Pubitemid 47218768)
29. Paulson, H.L. (2007a). Dominantly inherited ataxias: Lessons learned from Machado-Joseph disease/spinocerebellar ataxia type 3. Semin. Neurol. 27, 133-142. (Pubitemid 46564474)
30. Paulson, H.L. (2007b). Spinocerebeller ataxia type 3. In: Gene- Reviews (Internet), R.A. Pagon, T.C. Bird, C.R. Dolan and K. Stephens, eds. (Seattle, WA: University of Washington). Available at: Http://www.ncbi.nlm.nih.gov/books/ NBK1196/.
31. Prakash, T.P., Siwkowski, A., Allerson, C.R., Migawa, M.T., Lee, S., Gaus, H.J., Black, C., Seth, P.P., Swayze, E.E., and Bhat, B. (2010). Antisense oligonucleotides containing conformationally constrained 29,49-(N-methoxy) aminomethylene and 29,49-aminooxymethylene and 29-O,49-C-aminomethylene bridged nucleoside analogues show improved potency in animal models. J. Med. Chem. 53, 1636-1650.
32. 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.
33. Scholefield, J. and Wood, M.J. (2010). Therapeutic gene silencing strategies for polyglutamine disorders. Trends Genet. 26, 29-38.
34. Seth, P.P., Vasquez, G., Allerson, C.A., Berdeja, A., Gaus, H., Kinberger, G.A., Prakash, T.P., Migawa, M.T., Bhat, B., and Swayze, E.E. (2010). Synthesis and biophysical evaluation of 29,49- constrained 29O-methoxyethyl and 29,49-constrained 29O-ethyl nucleic acid analogues. J. Org. Chem. 75, 1569-1581.
35. Smith, R.A., Miller, T.M., Yamanaka, K., Monia, B.P., Condon, T.P., Hung, G., Lobsiger, C.S., Ward, C.M., McAlonis-Downes, M., Wei, H., et al. (2006). Antisense oligonucleotide therapy for neurodegenerative disease. J. Clin. Invest. 116, 2290-2296. (Pubitemid 44162339)
36. Sobczak, K., de Mezer, M., Michlewski, G., Krol, J., and Krzyzosiak, W.J. (2003). RNA structure of trinucleotide repeats associated with human neurological diseases. Nucleic Acids Res. 31, 5469-5482. (Pubitemid 37441917)
37. Srivastava, P., Barman, J., Pathmasiri, W., Plashkevych, O.,Wenska, M., and Chattopadhyaya, J. (2007). Five- and six-membered conformationally locked 29,49-carbocyclic ribo-thymidines: Synthesis, structure, and biochemical studies. J. Am. Chem. Soc. 129, 8362-8379. (Pubitemid 47035147)
38. Wang, Y., Juranek, S., Li, H., Sheng, G., Tuschl, T., and Patel, D.J. (2008). Structure of an argonaute silencing complex with a seedcontaining guide DNA and target RNA duplex. Nature 456, 921-926.
39. 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.