Disease-causing allele-specific silencing by RNA interference

Pharmaceuticals

Volumn 6, Issue 4, 2013, Pages 522-535

  Hohjoh, Hirohiko ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

Author keywords

Allele discrimination; Allele specific silencing; Dominantly inherited disease; Forked siRNA; Nucleotide variation; RNAi; siRNA modification; siRNA selection

Indexed keywords

SHORT HAIRPIN RNA; SMALL INTERFERING RNA;

ALLELE; ALLELE SPECIFIC SILENCING BY RNA INTERFERENCE; ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; CHEMICAL MODIFICATION; CONGENITAL MYASTHENIC SYNDROME; DRUG EFFICACY; EHLERS DANLOS SYNDROME; FAMILIAL AMYLOID POLYNEUROPATHY; FRONTOTEMPORAL DEMENTIA; FRONTOTEMPORAL DEMENTIA WITH PARKINSONISM LINKED TO CHROMOSOME 17; GENE SILENCING; GENE TARGETING; GENETIC DISORDER; HUMAN; HUNTINGTON CHOREA; MACHADO JOSEPH DISEASE; NEOPLASM; NONHUMAN; NONVIRAL GENE THERAPY; OSSIFYING MYOSITIS; PARKINSON DISEASE; REVIEW; RNA INTERFERENCE; SICKLE CELL ANEMIA; SINGLE NUCLEOTIDE POLYMORPHISM; SPINOCEREBELLAR ATAXIA TYPE 1; SPINOCEREBELLAR ATAXIA TYPE 7; SPINOCEREBELLAR DEGENERATION;

EID: 84876166775     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph6040522     Document Type: Review

References (76)

1. Sharp, P.A. RNAi and double-strand RNA. Genes Dev. 1999, 13, 139-41.
2. Bosher, J.M.; Labouesse, M. RNA interference: genetic wand and genetic watchdog. Nat. Cell. Biol. 2000, 2, E31-E36.
3. Vaucheret, H.;Beclin, C.; Fagard, M. Post-transcriptional gene silencing in plants. J. Cell. Sci. 2001, 114, 3083-3091.
4. Cerutti, H. RNA interference: Traveling in the cell and gaining functions? Trends Genet. 2003, 19, 39-46.
5. Fire, A.; Xu, S.;Montgomery, M.K.;Kostas, S.A.;Driver, S.E.;Mello, C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391, 806-811.
6. Hammond, S.M.; Bernstein, E.;Beach, D.;Hannon, G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000, 404, 293-296.
7. Zamore, P.D.; Tuschl, T.;Sharp, P.A.; Bartel, D.P. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 2000, 101, 25-33.
8. Elbashir, S.M.; Lendeckel, W.; Tuschl, T. RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev. 2001, 15, 188-200.
9. Bernstein, E.;Caudy, A.A.; Hammond, S.M.; Hannon, G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409, 363-366.
10. Nykanen, A.; Haley, B.; Zamore, P.D. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 2001, 107, 309-321.
11. Martinez, J.; Patkaniowska, A.; Urlaub, H.; Luhrmann, R.; Tuschl, T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002, 110, 563-574.
12. Lewis, B.P.; Burge, C.B.; Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120, 15-20.
13. Elbashir, S.M.; Martinez, J.; Patkaniowska, A.; Lendeckel, W.; Tuschl, T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 2001, 20, 6877-6888.
14. Schwarz, D.S.; Hutvagner, G.; Haley, B.; Zamore, P.D. Evidence that siRNAs function as guides, not primers, in the Drosophila and human RNAi pathways. Mol. Cell. 2002, 10, 537-548.
15. Liu, J.; Carmell, M.A.; Rivas, F.V.; Marsden, C.G.; Thomson, J.M.; Song, J.J.; Hammond, S.M.; Joshua-Tor, L.; Hannon, G.J. Argonaute2 is the catalytic engine of mammalian RNAi. Science 2004, 305, 1437-1441.
16. Meister, G.; Landthaler, M.; Patkaniowska, A.; Dorsett, Y.; Teng, G.; Tuschl, T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol. Cell. 2004, 15, 185-97.
17. Haley, B.; Zamore, P.D. Kinetic analysis of the RNAi enzyme complex. Nat. Struct Mol. Biol. 2004, 11, 599-606.
18. Rivas, F.V.; Tolia, N.H.; Song, J.J.; Aragon, J.P.; Liu, J.; Hannon, G.J.; Joshua-Tor, L. Purified Argonaute2 and an siRNA form recombinant human RISC. Nat. Struct. Mol. Biol. 2005, 12, 340-349.
19. Hammond, S.M.; Boettcher, S.; Caudy, A.A.; Kobayashi, R.; Hannon, G.J. Argonaute2, a link between genetic and biochemical analyses of RNAi. Science 2001, 293, 1146-1150.
20. Rand, T.A.; Ginalski, K.; Grishin, N.V.; Wang, X. Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity. Proc. Natl. Acad. Sci. USA 2004, 101, 14385-14389.
21. Song, J.J.; Smith, S.K.; Hannon, G.J.; Joshua-Tor, L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 2004, 305, 1434-1437.
22. Svoboda, P.; Stein, P.; Hayashi, H.; Schultz, R.M. Selective reduction of dormant maternal mRNAs in mouse oocytes by RNA interference. Development 2000, 127, 4147-4156.
23. Wianny, F.; Zernicka-Goetz, M. Specific interference with gene function by double-stranded RNA in early mouse development. Nat. Cell. Biol. 2000, 2, 70-75.
24. Svoboda, P.; Stein, P.; Schultz, R.M. RNAi in mouse oocytes and preimplantation embryos: Effectiveness of hairpin dsRNA. Biochem. Biophys. Res. Commun. 2001, 287, 1099-1104.
25. Player, M.R.; Torrence, P.F. The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol. Ther. 1998, 78, 55-113.
26. Clemens, M.J.; Elia, A. The double-stranded RNA-dependent protein kinase PKR: Structure and function. J. Interferon. Cytokine Res. 1997, 17, 503-524.
27. Gale, M., Jr.; Katze, M.G. Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol. Ther. 1998, 78, 29-46.
28. Caplen, N.J.; Fleenor, J.; Fire, A.; Morgan, R.A. dsRNA-mediated gene silencing in cultured Drosophila cells: A tissue culture model for the analysis of RNA interference. Gene 2000, 252, 95-105.
29. Yang, S.; Tutton, S.; Pierce, E.; Yoon, K. Specific double-stranded RNA interference in undifferentiated mouse embryonic stem cells. Mol. Cell. Biol. 2001, 21, 7807-7816.
30. Billy, E.; Brondani, V.; Zhang, H.; Muller, U.; Filipowicz, W. Specific interference with gene expression induced by long, double-stranded RNA in mouse embryonal teratocarcinoma cell lines. Proc. Natl. Acad. Sci. USA 2001, 98, 14428-14433.
31. Ui-Tei, K.; Zenno, S.; Miyata, Y.; Saigo, K. Sensitive assay of RNA interference in Drosophila and Chinese hamster cultured cells using firefly luciferase gene as target. FEBS Lett. 2000, 479, 79-82.
32. Elbashir, S.M.; Harborth, J.; Lendeckel, W.; Yalcin, A.; Weber, K.; Tuschl, T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411, 494-498.
33. McManus, M.T.; Petersen, C.P.; Haines, B.B.; Chen, J.; Sharp, P.A. Gene silencing using micro-RNA designed hairpins. RNA 2002, 8, 842-850.
34. Yu, J.Y.; DeRuiter, S.L.; Turner, D.L. RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 2002, 99, 6047-6052.
35. Paddison, P.J.; Caudy, A.A.; Bernstein, E.; Hannon, G.J.; Conklin, D.S. Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 2002, 16, 948-958.
36. Zhou, H.; Xia, X.G.; Xu, Z. An RNA polymerase II construct synthesizes short-hairpin RNA with a quantitative indicator and mediates highly efficient RNAi. Nucleic Acids Res. 2005, 33, e62.
37. Stegmeier, F.; Hu, G.; Rickles, R.J.; Hannon, G.J.; Elledge, S.J. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 2005, 102, 13212-13217.
38. Hohjoh, H. RNA interference (RNA(i) induction with various types of synthetic oligonucleotide duplexes in cultured human cells. FEBS Lett. 2002, 521, 195-199.
39. Ui-Tei, K.; Naito, Y.; Takahashi, F.; Haraguchi, T.; Ohki-Hamazaki, H.; Juni, A.; Ueda, R.; Saigo, K. Guidelines for the selection of highly effective siRNA sequences for mammalian and chick RNA interference. Nucleic Acids Res. 2004, 32, 936-948.
40. Schwarz, D.S.; Hutvagner, G.; Du, T.; Xu, Z.; Aronin, N.;Zamore, P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003, 115, 199-208.
41. Khvorova, A.; Reynolds, A.; Jayasena, S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115, 209-216.
42. Rodriguez-Lebron, E.; Paulson, H.L. Allele-specific RNA interference for neurological disease. Gene Ther. 2006, 13, 576-581.
43. Miller, V.M.; Gouvion, C.M.; Davidson, B.L.; Paulson, H.L. Targeting Alzheimer's disease genes with RNA interference: An efficient strategy for silencing mutant alleles. Nucleic Acids Res. 2004, 32, 661-668.
44. Ohnishi, Y.; Tokunaga, K.; Kaneko, K.; Hohjoh, H. Assessment of allele-specific gene silencing by RNA interference with mutant and wild-type reporter alleles. J. RNAi Gene Silencing 2006, 2, 154-160.
45. Feng, X.; Zhao, P.; He, Y.; Zuo, Z. Allele-specific silencing of Alzheimer's disease genes: The amyloid precursor protein genes with Swedish or London mutations. Gene 2006, 371, 68-74.
46. Ohnishi, Y.; Tamura, Y.; Yoshida, M.; Tokunaga, K.; Hohjoh, H. Enhancement of allele discrimination by introduction of nucleotide mismatches into siRNA in allele-specific gene silencing by RNAi. PLoS One 2008, 3, e2248.
47. Sierant, M.; Paduszynska, A.; Kazmierczak-Baranska, J.; Nacmias, B.; Sorbi, S.; Bagnoli, S.; Sochacka, E.; Nawrot, B. Specific silencing of L392V PSEN1 mutant allele by RNA Interference. Int. J. Alzheimers Dis. 2011, 2011, 809218.
48. Xia, X.; Zhou, H.; Huang, Y.; Xu, Z. Allele-specific RNAi selectively silences mutant SOD1 and achieves significant therapeutic benefit in vivo. Neurobiol. Dis. 2006, 23, 578-586.
49. Schwarz, D.S.; Ding, H.; Kennington, L.; Moore, J.T.; Schelter, J.; Burchard, J.; Linsley, P.S.; Aronin, N.; Xu, Z.; Zamore, P.D. Designing siRNA that distinguish between genes that differ by a single nucleotide. PLoS Genet. 2006, 2, e140.
50. Abdelgany, A.; Wood, M.; Beeson, D. Allele-specific silencing of a pathogenic mutant acetylcholine receptor subunit by RNA interference. Hum. Mol. Genet. 2003, 12, 2637-2644.
51. Miller, V.M.; Xia, H.; Marrs, G.L.; Gouvion, C.M.; Lee, G.; Davidson, B.L.; Paulson, H.L. Allele-specific silencing of dominant disease genes. Proc. Natl. Acad. Sci. USA 2003, 100, 7195-7200.
52. Muller, G.A.; Hansen, U.; Xu, Z.; Griswold, B.; Talan, M.I.; McDonnell, N.B.; Briest, W. Allele-specific siRNA knockdown as a personalized treatment strategy for vascular Ehlers-Danlos syndrome in human fibroblasts. FASEB J. 2012, 26, 668-677.
53. Dykxhoorn, D.M.; Schlehuber, L.D.; London, I.M.; Lieberman, J. Determinants of specific RNA interference-mediated silencing of human beta-globin alleles differing by a single nucleotide polymorphism. Proc. Natl. Acad. Sci. USA 2006, 103, 5953-5958.
54. Kurosawa, T.; Igarashi, S.; Nishizawa, M.; Onodera, O. Selective silencing of a mutant transthyretin allele by small interfering RNAs. Biochem. Biophys. Res. Commun. 2005, 337, 1012-1018.
55. Takahashi, M.; Katagiri, T.; Furuya, H.; Hohjoh, H. Disease-causing allele-specific silencing against the ALK2 mutants, R206H and G356D, in fibrodysplasia ossificans progressiva. Gene Ther. 2012, 19, 781-785.
56. Kaplan, J.; Kaplan, F.S.; Shore, E.M. Restoration of normal BMP signaling levels and osteogenic differentiation in FOP mesenchymal progenitor cells by mutant allele-specific targeting. Gene Ther. 2012, 19, 786-790.
57. Huang, H.; Qiao, R.; Zhao, D.; Zhang, T.; Li, Y.; Yi, F.; Lai, F.; Hong, J.; Ding, X.; Yang, Z.; et al. Profiling of mismatch discrimination in RNAi enabled rational design of allele-specific siRNAs. Nucleic Acids Res. 2009, 37, 7560-7569.
58. Xia, H.; Mao, Q.; Eliason, S.L.; Harper, S.Q.; Martins, I.H.; Orr, H.T.; Paulson, H.L.; Yang, L.; Kotin, R.M.; Davidson, B.L. RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat. Med. 2004, 10, 816-820.
59. Alves, S.; Nascimento-Ferreira, I.; Auregan, G.; Hassig, R.; Dufour, N.; Brouillet, E.; Pedroso de Lima, M.C.; Hantraye, P.; Pereira de Almeida, L.; Deglon, N. Allele-specific RNA silencing of mutant ataxin-3 mediates neuroprotection in a rat model of Machado-Joseph disease. PLoS One 2008, 3, e3341.
60. Nobrega, C.; Nascimento-Ferreira, I.; Onofre, I.; Albuquerque, D.; Hirai, H.; Deglon, N.; de Almeida, L.P. Silencing mutant ataxin-3 rescues motor deficits and neuropathology in machado-joseph disease transgenic mice. PLoS One 2013, 8, e52396.
61. Scholefield, J.; Greenberg, L.J.; Weinberg, M.S.; Arbuthnot, P.B.; Abdelgany, A.; Wood, M.J. Design of RNAi hairpins for mutation-specific silencing of ataxin-7 and correction of a SCA7 phenotype. PLoS One 2009, 4, e7232.
62. De Ynigo-Mojado, L.; Martin-Ruiz, I.; Sutherland, J.D. Efficient allele-specific targeting of LRRK2 R1441 mutations mediated by RNAi. PLoS One 2011, 6, e21352.
63. Sibley, C.R.; Wood, M.J. Identification of allele-specific RNAi effectors targeting genetic forms of Parkinson's disease. PLoS One 2011, 6, e26194.
64. Pfister, E.L.; Kennington, L.; Straubhaar, J.; Wagh, S.; Liu, W.; DiFiglia, M.; Landwehrmeyer, B.; Vonsattel, J.P.; Zamore, P.D.; Aronin, N. Five siRNAs targeting three SNPs may provide therapy for three-quarters of Huntington's disease patients. Curr. Biol. 2009, 19, 774-778.
65. Takahashi, M.; Watanabe, S.; Murata, M.; Furuya, H.; Kanazawa, I.; Wada, K.; Hohjoh, H. Tailor-made RNAi knockdown against triplet repeat disease-causing alleles. Proc. Natl. Acad. Sci. USA 2010, 107, 21731-21736.
66. Hohjoh, H. Allele-specific silencing by RNA interference. Methods Mol. Biol. 2010, 623, 67-79.
67. Rodriguez-Lebron, E.; Gouvion, C.M.; Moore, S.A.; Davidson, B.L.; Paulson, H.L. Allele-specific RNAi mitigates phenotypic progression in a transgenic model of Alzheimer's disease. Mol. Ther. 2009, 17, 1563-1573.
68. Towne, C.; Raoul, C.; Schneider, B.L.; Aebischer, P. Systemic AAV6 delivery mediating RNA interference against SOD1: neuromuscular transduction does not alter disease progression in fALS mice. Mol. Ther. 2008, 16, 1018-1025.
69. Hamasaki, M.; Hashizume, Y.; Yamada, Y.; Katayama, T.; Hohjoh, H.; Fusaki, N.; Nakashima, Y.; Furuya, H.; Haga, N.; Takami, Y.; Era, T. Pathogenic mutation of ALK2 inhibits induced pluripotent stem cell reprogramming and maintenance: mechanisms of reprogramming and strategy for drug identification. Stem Cells 2012, 30, 2437-2449.
70. Ohnishi, Y.; Tokunaga, K.; Hohjoh, H. Influence of assembly of siRNA elements into RNA-induced silencing complex by fork-siRNA duplex carrying nucleotide mismatches at the 3'-or 5'-end of the sense-stranded siRNA element. Biochem. Biophys. Res. Commun. 2005, 329, 516-521.
71. Hohjoh, H. Enhancement of RNAi activity by improved siRNA duplexes. FEBS Lett. 2004, 557, 193-198.
72. Chiu, Y.L.; Rana, T.M. siRNA function in RNAi: A chemical modification analysis. RNA 2003, 9, 1034-1048.
73. Czauderna, F.; Fechtner, M.; Dames, S.; Aygun, H.; Klippel, A.; Pronk, G.J.; Giese, K.; Kaufmann, J. Structural variations and stabilising modifications of synthetic siRNAs in mammalian cells. Nucleic Acids Res. 2003, 31, 2705-2716.
74. Choung, S.; Kim, Y.J.; Kim, S.; Park, H.O.; Choi, Y.C. Chemical modification of siRNAs to improve serum stability without loss of efficacy. Biochem Biophys Res. Commun. 2006, 342, 919-927.
75. Elmen, J.; Thonberg, H.; Ljungberg, K.; Frieden, M.; Westergaard, M.; Xu, Y.; Wahren, B.; Liang, Z.; Orum, H.; Koch, T.; Wahlestedt, C. Locked nucleic acid (LNA) mediated improvements in siRNA stability and functionality. Nucleic Acids Res. 2005, 33, 439-447.
76. Dowler, T.; Bergeron, D.; Tedeschi, A.L.; Paquet, L.; Ferrari, N.; Damha, M.J. Improvements in siRNA properties mediated by 2'-deoxy-2'-fluoro-beta-D-arabinonucleic acid (FANA). Nucleic Acids Res. 2006, 34, 1669-1675.