Differential effects on allele selective silencing of mutant huntingtin by two stereoisomers of α,β-constrained nucleic acid

ACS Chemical Biology

Volumn 9, Issue 9, 2014, Pages 1975-1979

  Østergaard, Michael E ^a   Gerland, Béatrice ^b   Escudier, Jean Marc ^b   Swayze, Eric E ^a   Seth, Punit P ^a  

^a ISIS PHARMACEUTICALS   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA CONSTRAINED NUCLEIC ACID; ANTISENSE OLIGONUCLEOTIDE; HUNTINGTIN; NUCLEIC ACID; RIBONUCLEASE H; UNCLASSIFIED DRUG; HTT PROTEIN, HUMAN; NERVE PROTEIN; NUCLEOTIDE; RNA;

ALLELE; ARTICLE; EPIMER; GENE MUTATION; GENE SILENCING; HUMAN; HUNTINGTON CHOREA; HYDROLYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; STEREOISOMERISM; THERMOSTABILITY; WILD TYPE; CELL CULTURE; CHEMISTRY; DRUG EFFECTS; FIBROBLAST; GENETICS; HETERODUPLEX ANALYSIS; METABOLISM; MOLECULARLY TARGETED THERAPY; MUTATION;

ALLELES; CELLS, CULTURED; FIBROBLASTS; GENE SILENCING; HETERODUPLEX ANALYSIS; HUMANS; HYDROLYSIS; MOLECULAR TARGETED THERAPY; MUTATION; NERVE TISSUE PROTEINS; NUCLEOTIDES; OLIGONUCLEOTIDES, ANTISENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; RIBONUCLEASE H; RNA; STEREOISOMERISM;

EID: 84907989506     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb5003027     Document Type: Article

References (30)

1. Walker, F. O. (2007) Huntington's disease. Lancet 369, 218-228.
2. de la Monte, S. M., Vonsattel, J. P., and Richardson, E. P., Jr. (1988) Morphometric demonstration of atrophic changes in the cerebral cortex, white matter, and neostriatum in Huntington's disease. J. Neuropathol. Exp. Neurol. 47, 516-525.
3. MacDonald, M. E., Ambrose, C. M., Duyao, M. P., Myers, R. H., Lin, C., Srinidhi, L., Barnes, G., Taylor, S. A., James, M., Groot, N., MacFarlane, H., Jenkins, B., Anderson, M. A., Wexler, N. S., Gusella, J. F., Bates, G. P., Baxendale, S., Hummerich, H., Kirby, S., North, M., Youngman, S., Mott, R., Zehetner, G., Sedlacek, Z., Poustka, A., Frischauf, A.-M., Lehrach, H., Buckler, A. J., Church, D., Doucette-Stamm, L., O'Donovan, M. C., Riba-Ramirez, L., Shah, M., Stanton, V. P., Strobel, S. A., Draths, K. M., Wales, J. L., Dervan, P., Housman, D. E., Altherr, M., Shiang, R., Thompson, L., Fielder, T., Wasmuth, J. J., Tagle, D., Valdes, J., Elmer, L., Allard, M., Castilla, L., Swaroop, M., Blanchard, K., Collins, F. S., Snell, R., Holloway, T., Gillespie, K., Datson, N., Shaw, D., and Harper, P. S. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72, 971-983.
4. Nasir, J., Floresco, S. B., O'Kusky, J. R., Diewert, V. M., Richman, J. M., Zeisler, J., Borowski, A., Marth, J. D., Phillips, A. G., and Hayden, M. R. (1995) Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81, 811-823.
5. Zuccato, C., Valenza, M., and Cattaneo, E. (2010) Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 90, 905-981.
6. Wang, Y.-L., Liu, W., Wada, E., Murata, M., Wada, K., and Kanazawa, I. (2005) Clinico-pathological rescue of a model mouse of Huntington's disease by siRNA. Neurosci. Res. 53, 241-249.
7. McBride, J. L., Pitzer, M. R., Boudreau, R. L., Dufour, B., Hobbs, T., Ojeda, S. R., and Davidson, B. L. (2011) Preclinical safety of RNA-inediated HTT suppression in the rhesus macaque as a potential therapy for Huntington's disease. Mol. Ther. 19, 2152-2162.
8. Kordasiewicz, H. B., Stanek, L. M., Wancewicz, E. V., Mazur, C., McAlonis, M. M., Pytel, K. A., Artates, J. W., Weiss, A., Cheng, S. H., Shihabuddin, L. S., Hung, G., Bennett, C. F., and Cleveland, D. W. (2012) Sustained therapeutic reversal of Huntington's disease by transient repression of Huntingtin synthesis. Neuron 74, 1031-1044.
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. 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.
12. 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 2′-4′ conformationaly restricted nucleoside analogues show improved potency without increased toxicity in animals. J. Med. Chem. 52, 10-13.
13. 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., Montailler, C., Lemaitre, M. M., and Corey, D. R. (2010) Allele-selective inhibition of mutant Huntingtin expression with antisense oligonucleotides targeting the expanded CAG repeat. Biochemistry 49, 10166-10178.
14. Ostergaard, M. E., Southwell, A. L., Kordasiewicz, H., Watt, A. T., Skotte, N. H., Doty, C. N., Vaid, K., Villanueva, E. B., Swayze, E. E., Bennett, C. F., Hayden, M. R., and Seth, P. P. (2013) Rational design of antisense oligonucleotides targeting single nucleotide polymorphisms for potent and allele selective suppression of mutant Huntingtin in the CNS. Nucleic Acids Res. 41, 9634-9650.
15. Southwell, A. L., Warby, S. C., Carroll, J. B., Doty, C. N., Skotte, N. H., Zhang, W., Villanueva, E. B., Kovalik, V., Xie, Y., Pouladi, M. A., Collins, J. A., Yang, X. W., Franciosi, S., and Hayden, M. R. (2013) A fully humanized transgenic mouse model of Huntington disease. Hum. Mol. Genet. 22, 18-34.
16. 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 2′,4′-constrained 2′O-methoxyethyl and 2′,4′-constrained 2′O-ethyl nucleic acid analogues. J. Org. Chem. 75, 1569-1581.
17. Teplova, M., Minasov, G., Tereshko, V., Inamati, G. B., Cook, P. D., Manoharan, M., and Egli, M. (1999) Crystal structure and improved antisense properties of 2′-O-(2-methoxyethyl)-RNA. Nat. Struct. Biol. 6, 535-539.
18. Varani, G., and McClain, W. H. (2000) The G x U wobble base pair. A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Rep. 1, 18-23.
19. Catana, D.-A., Renard, B.-L., Maturano, M., Payrastre, C., Tarrat, N., and Escudier, J.-M. (2012) Dioxaphosphorinane-constrained nucleic acid dinucleotides as tools for structural tuning of nucleic acids. J. Nucleic Acids 2012, 17.
20. Le Clezio, I., Escudier, J.-M., and Vigroux, A. (2003) Diastereoselective synthesis of a conformationally restricted dinucleotide with predefined α and β torsional angles for the construction of α,β-constrained nucleic acids (α,β-CNA). Org. Lett. 5, 161-164.
21. Dupouy, C., Iche-Tarrat, N., Durrieu, M. P., Rodriguez, F., Escudier, J. M., and Vigroux, A. (2006) Watson-Crick base-pairing properties of nucleic acid analogues with stereocontrolled α and β torsion angles (α,β-D-CNAs). Angew. Chem., Int. Ed. Engl. 45, 3623-3627.
22. Dupouy, C., Millard, P., Boissonnet, A., and Escudier, J.-M. (2010) α,β-D-CNA preorganization of unpaired loop moiety stabilizes DNA hairpin. Chem. Commun. (Cambridge, U.K.) 46, 5142-5144.
23. Saha, A. K., Caulfield, T. J., Hobbs, C., Upson, D. A., Waychunas, C., and Yawman, A. M. (1995) 5′-Me-DNA. A new oligonucleotide analog: Synthesis and biochemical properties. J. Org. Chem. 60, 788-789.
24. Boissonnet, A., Dupouy, C., Millard, P., Durrieu, M.-P., Tarrat, N., and Escudier, J.-M. (2011) α,β-D-CNA featuring canonical and noncanonical α/β torsional angles behaviors within oligonucleotides. New J. Chem. 35, 1528-1533.
25. Seth, P. P., Allerson, C. R., Siwkowski, A., Vasquez, G., Berdeja, A., Migawa, M. T., Gaus, H., Prakash, T. P., Bhat, B., and Swayze, E. E. (2010) Configuration of the 5′-methyl group modulates the biophysical and biological properties of locked nucleic acid (LNA) oligonucleotides. J. Med. Chem. 53, 8309-8318.
26. Pallan, P. S., Yu, J., Allerson, C. R., Swayze, E. E., Seth, P., and Egli, M. (2012) Insights from crystal structures into the opposite effects on RNA affinity caused by the S- and R-6′-methyl backbone modifications of 3′-fluoro hexitol nucleic acid. Biochemistry 51, 7-9.
27. Seth, P. P., Allerson, C. R., Ostergaard, M. E., and Swayze, E. E. (2012) Structural requirements for hybridization at the 5′-position are different in α-L-LNA as compared to β-D-LNA. Bioorg. Med. Chem. Lett. 22, 296-299.
28. Hanessian, S., Schroeder, B. R., Giacometti, R. D., Merner, B. L., Ostergaard, M., Swayze, E. E., and Seth, P. P. (2012) Structure-based design of a highly constrained nucleic acid analogue: Improved duplex stabilization by restricting sugar pucker and torsion angle gamma. Angew. Chem., Int. Ed. Engl. 51, 11242-11245.
29. Lima, W. F., Nichols, J. G., Wu, H., Prakash, T. P., Migawa, M. T., Wyrzykiewicz, T. K., Bhat, B., and Crooke, S. T. (2004) Structural requirements at the catalytic site of the heteroduplex substrate for human RNase H1 catalysis. J. Biol. Chem. 279, 36317-36326.
30. Nowotny, M., Gaidamakov, S. A., Ghirlando, R., Cerritelli, S. M., Crouch, R. J., and Yang, W. (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: Insight into HIV reverse transcription. Mol. Cell 28, 264-276.