Synthetic RNAs for gene regulation: Design principles and computational tools

Frontiers in Bioengineering and Biotechnology

Volumn 2, Issue DEC, 2014, Pages

  Laganà, Alessandro ^a   Shasha, Dennis ^b   Croce, Carlo Maria ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

A miR; AntagomiR; CRISPRi; MiRNA; RNAi; SiRNA; Sponge

Indexed keywords

BIOINFORMATICS; GENE EXPRESSION; GENE THERAPY; GENES; NUCLEIC ACIDS; RNA; TRANSCRIPTION;

ANTAGOMIR; CRISPRI; MIRNA; RNAI; SIRNA; SPONGE;

GENE EXPRESSION REGULATION;

EID: 84929701098     PISSN: None     EISSN: 22964185     Source Type: Journal    
DOI: 10.3389/fbioe.2014.00065     Document Type: Short Survey

References (93)

1. Arroyo, J. D., Gallichotte, E. N., and Tewari, M. (2014). Systematic design and functional analysis of artificial microRNAs. Nucleic Acids Res. 42, 6064-6077. doi:10.1093/nar/gku171
2. Arvey, A., Larsson, E., Sander, C., Leslie, C. S., and Marks, D. S. (2010). Target mRNA abundance dilutes microRNA and siRNA activity. Mol. Syst. Biol. 6, 1-7. doi:10.1038/msb.2010.24
3. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. doi:10.1016/S0092-8674(04)00045-5
4. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. doi:10.1016/j.cell.2009.01.002
5. Bassett, A. R., Azzam, G., Wheatley, L., Tibbit, C., Rajakumar, T., McGowan, S., et al. (2014). Understanding functional miRNA-target interactions in vivo by site-specific genome engineering. Nat. Commun. 5, 1-11. doi:10.1038/ncomms5640
6. Birmingham, A., Anderson, E. M., Reynolds, A., Ilsley-Tyree, D., Leake, D., Fedorov, Y., et al. (2006). 3' UTR seed matches, but not overall identity, are associated with RNAi off-targets. Nat. Meth. 3, 199-204. doi:10.1038/nmeth854
7. Braasch, D. A., and Corey, D. R. (2001). Locked nucleic acid (LNA): fine-tuning the recognition of DNA and RNA. Chem. Biol. 8, 1-7. doi:10.1016/S1074-5521(00)00058-2
8. Carè, A., Catalucci, D., Felicetti, F., Bonci, D., Addario, A., Gallo, P., et al. (2007). MicroRNA-133 controls cardiac hypertrophy. Nat. Med. 13, 613-618. doi:10.1038/nm1582
9. Chalk, A. M., Wahlestedt, C., and Sonnhammer, E. L. L. (2004). Improved and automated prediction of effective siRNA. Biochem. Biophys. Res. Commun. 319, 264-274. doi:10.1016/j.bbrc.2004.04.181
10. Cheng, T. L., Teng, C. F., Tsai, W. H., Yeh, C. W., Wu, M. P., Hsu, H. C., et al. (2009). Multitarget therapy of malignant cancers by the head-to-tail tandem array multiple shRNAs expression system. Cancer Gene Ther. 16, 516-531. doi:10.1038/cgt.2008.102
11. Chu, C.-Y., and Rana, T. M. (2007). Small RNAs: regulators and guardians of the genome. J. Cell. Physiol. 213, 412-419. doi:10.1002/jcp.21230
12. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., et al. (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823. doi:10.1126/science.1231143
13. 5 genes have substantial off-target activity. Nucleic Acids Res. 41, 9584-9592. doi:10.1093/nar/gkt714
14. Croce, C. M. (2009). Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10, 704-714. doi:10.1038/nrg2634
15. Cui, W., Ning, J., Naik, U. P., and Duncan, M. K. (2004). OptiRNAi, an RNAi design tool. Comput. Methods Programs Biomed. 75, 67-73. doi:10.1016/j.cmpb.2003.09.002
16. Culler, S. J., Hoff, K. G., and Smolke, C. D. (2010). Reprogramming cellular behavior with RNA controllers responsive to endogenous proteins. Science 330, 1251-1255. doi:10.1126/science.1192128
17. Ding, Y., Chan, C. Y., and Lawrence, C. E. (2004). Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Res. 32, W135-W141. doi:10.1093/nar/gkh449
18. Doench, J. G., Hartenian, E., Graham, D. B., Tothova, Z., Hegde, M., Smith, I., et al. (2014). Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat. Biotechnol. doi:10.1038/nbt.3026
19. Dua, P., Yoo, J. W., Kim, S., and Lee, D.-K. (2009). Modified siRNA structure with a single nucleotide bulge overcomes conventional siRNA-mediated off-target silencing. Mol. Ther. 19, 1676-1687. doi:10.1038/mt.2011.109
20. Duan, J., Lu, G., Xie, Z., Lou, M., Luo, J., Guo, L., et al. (2014). Genome-wide identification of CRISPR/Cas9 off-targets in human genome. Cell Res. 24, 1009-1012. doi:10.1038/cr.2014.87
21. Ebert, M. S., Neilson, J. R., and Sharp, P. A. (2007). MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Meth. 4, 721-726. doi:10.1038/nmeth1079
22. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001a). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498. doi:10.1038/35078107
23. Elbashir, S. M., Martinez, J., Patkaniowska, A., Lendeckel, W., and Tuschl, T. (2001b). Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 20, 6877-6888. doi:10.1093/emboj/20.23.6877
24. Esquela-Kerscher, A., and Slack, F. J. (2006). Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer 6, 259-269. doi:10.1038/nrc1840
25. Esvelt, K. M., Mali, P., Braff, J. L., Moosburner, M., Yaung, S. J., and Church, G. M. (2013). Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Meth. 10, 1116-1121. doi:10.1038/nmeth.2681
26. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., and Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. doi:10.1038/35888
27. Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio-Somoza, I., et al. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39, 1033-1037. doi:10.1038/ng2079
28. Garofalo, M., Condorelli, G., and Croce, C. M. (2008). MicroRNAs in diseases and drug response. Curr. Opin. Pharmacol. 8, 661-667. doi:10.1016/j.coph.2008.06.005
29. Gilbert, L. A., Horlbeck, M. A., Adamson, B., Villalta, J. E., Chen, Y., Whitehead, E. H., et al. (2014). Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661. doi:10.1016/j.cell.2014.09.029
30. Gilbert, L. A., Larson, M. H., Morsut, L., Liu, Z., Brar, G. A., Torres, S. E., et al. (2013). CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154, 442-451. doi:10.1016/j.cell.2013.06.044
31. Guell, M., Yang, L., and Church, G. M. (2014). Genome editing assessment using CRISPR genome analyzer (CRISPR-GA). Bioinformatics 30, 2968-2970. doi:10.1093/bioinformatics/btu427
32. Gunsalus, K. C., and Piano, F. (2005). RNAi as a tool to study cell biology: building the genome-phenome bridge. Curr. Opin. Cell Biol. 17, 3-8. doi:10.1016/j.ceb.2004.12.008
33. Hale, C. R., Zhao, P., Olson, S., Duff, M. O., Graveley, B. R., Wells, L., et al. (2009). RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139, 945-956. doi:10.1016/j.cell.2009.07.040
34. Haraguchi, T., Nakano, H., Tagawa, T., Ohki, T., Ueno, Y., Yoshida, T., et al. (2012). A potent 2'-O-methylated RNA-based microRNA inhibitor with unique secondary structures. Nucleic Acids Res. 40, e58-e58. doi:10.1093/nar/gkr1317
35. Haraguchi, T., Ozaki, Y., and Iba, H. (2009). Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic Acids Res. 37, e43-e43. doi:10.1093/nar/gkp040
36. Heigwer, F., Kerr, G., and Boutros, M. (2014). Correspondence. Nat. Meth. 11, 122-123. doi:10.1038/nmeth.2812
37. Helwak, A., Kudla, G., Dudnakova, T., and Tollervey, D. (2013). Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153, 654-665. doi:10.1016/j.cell.2013.03.043
38. Hsieh, A., Bo, R., Manola, J., Vazquez, F., Bare, O., Khvorova, A., et al. (2004). A library of siRNA duplexes targeting the phosphoinositide 3-kinase pathway: determinants of gene silencing for use in cell-based screens. Nucleic. Acids Res. 32, 893-901. doi:10.1093/nar/gkh238
39. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., et al. (2013). DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 31, 827-832. doi:10.1038/nbt.2647
40. Hwang, W. Y., Fu, Y., Reyon, D., Maeder, M. L., Tsai, S. Q., Sander, J. D., et al. (2013). Brief communications. Nat. Biotechnol. 31, 227-229. doi:10.1038/nbt.2501
41. Ichihara, M., Murakumo, Y., Masuda, A., Matsuura, T., Asai, N., Jijiwa, M., et al. (2007). Thermodynamic instability of siRNA duplex is a prerequisite for dependable prediction of siRNA activities. Nucleic Acids Res. 35, e123-e123. doi:10.1093/nar/gkm699
42. Jackson, A. L., Burchard, J., Schelter, J., Chau, B. N., Cleary, M., Lim, L., et al. (2006). Widespread siRNA "off-target" transcript silencing mediated by seed region sequence complementarity. RNA 12, 1179-1187. doi:10.1261/rna.25706
43. Jiang, P., Wu, H., Da, Y., Sang, F., Wei, J., Sun, X., et al. (2007). RFRCDB-siRNA: Improved design of siRNAs by random forest regression model coupled with database searching. Comput. Methods Programs Biomed. 87, 230-238. doi:10.1016/j.cmpb.2007.06.001
44. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821. doi:10.1126/science.1225829
45. Katoh, T., and Suzuki, T. (2007). Specific residues at every third position of siRNA shape its efficient RNAi activity. Nucleic Acids Res. 35, e27-e27. doi:10.1093/nar/gkl1120
46. Khvorova, A., Reynolds, A., and Jayasena, S. D. (2003). Functional siRNAs and miRNAs exhibit strand bias. Cell 115, 209-216. doi:10.1016/S0092-8674(03)00801-8
47. Kim, D. H., and Rossi, J. J. (2007). Strategies for silencing human disease using RNA interference. Nat. Rev. Genet. 8, 173-184. doi:10.1038/nrg2006
48. Kluiver, J., Gibcus, J. H., Hettinga, C., Adema, A., Richter, M. K. S., Halsema, N., et al. (2012). Rapid generation of MicroRNA sponges for microRNA inhibition. PLoS ONE 7:e29275. doi:10.1371/journal.pone.0029275
49. Krützfeldt, J., Rajewsky, N., Braich, R., Rajeev, K. G., Tuschl, T., Manoharan, M., et al. (2005). Silencing of microRNAs in vivo with "antagomirs". Nature 438, 685-689. doi:10.1038/nature04303
50. Lagana, A., Acunzo, M., Romano, G., Pulvirenti, A., Veneziano, D., Cascione, L., et al. (2014). miR-Synth: a computational resource for the design of multi-site multi-target synthetic miRNAs. Nucleic Acids Res. 42, 5416-5425. doi:10.1093/nar/gku202
51. Larson, M. H., Gilbert, L. A., Wang, X., Lim, W. A., Weissman, J. S., and Qi, L. S. (2013). CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8, 2180-2196. doi:10.1038/nprot.2013.132
52. Larsson, E., Sander, C., and Marks, D. (2010). mRNA turnover rate limits siRNA and microRNA efficacy. Mol. Syst. Biol. 6, 1-9. doi:10.1038/msb.2010.89
53. Li, X., Yoo, J. W., Lee, J. H., Hahn, Y., Kim, S., and Lee, D.-K. (2010). Identification of sequence features that predict competition potency of siRNAs. Biochem. Biophys. Res. Commun. 398, 92-97. doi:10.1016/j.bbrc.2010.06.041
54. Liang, J. C., Bloom, R. J., and Smolke, C. D. (2011). Engineering biological systems with synthetic RNA molecules. Mol. Cell 43, 915-926. doi:10.1016/j.molcel.2011.08.023
55. Liu, Q., Zhou, H., Cui, J., Cao, Z., and Xu, Y. (2012a). Reconsideration of in-silico siRNA design based on feature selection: a cross-platform data integration perspective. PLoS ONE 7:e37879. doi:10.1371/journal.pone.0037879
56. Liu, Q., Zhou, H., Zhu, R., Xu, Y., and Cao, Z. (2012b). Reconsideration of in silico siRNA design from a perspective of heterogeneous data integration: problems and solutions. Brief Bioinform 15, 292-305. doi:10.1093/bib/bbs073
57. Lu, Z. J., and Mathews, D. H. (2008). OligoWalk: an online siRNA design tool utilizing hybridization thermodynamics. Nucleic Acids Res. 36, W104-W108. doi:10.1093/nar/gkn250
58. Ma, H., Zhang, J., and Wu, H. (2014). Designing Ago2-specific siRNA/shRNA to avoid competition with endogenous miRNAs. Mol Ther Nucleic Acids 3, e176. doi:10.1038/mtna.2014.27
59. Ma, M., Ye, A. Y., Zheng, W., and Kong, L. (2013). A guide RNA sequence design platform for the CRISPR/Cas9 system for model organism genomes. Biomed Res. Int. 2013, 1-4. doi:10.1155/2013/270805
60. Malefyt, A. P., Wu, M., Vocelle, D. B., Kappes, S. J., Lindeman, S. D., Chan, C., et al. (2014). Improved asymmetry prediction for short interfering RNAs. FEBS J. 281, 320-330. doi:10.1111/febs.12599
61. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., et al. (2013). RNA-guided human genome engineering via Cas9. Science 339, 823-826. doi:10.1126/science.1232033
62. Martin, H. C., Wani, S., Steptoe, A. L., Krishnan, K., Nones, K., Nourbakhsh, E., et al. (2014). Imperfect centered miRNA binding sites are common and can mediate repression of target mRNAs. Genome Biol. 15, R51. doi:10.1186/gb-2014-15-3-r51
63. Matveeva, O., Nechipurenko, Y., Rossi, L., Moore, B., Saetrom, P., Ogurtsov, A. Y., et al. (2007). Comparison of approaches for rational siRNA design leading to a new efficient and transparent method. Nucleic Acids Res. 35, e63-e63. doi:10.1093/nar/gkm088
64. Montague, T. G., Cruz, J. M., Gagnon, J. A., Church, G. M., and Valen, E. (2014). CHOPCHOP: a CRISPR/Cas9 and TALEN web tool for genome editing. Nucleic Acids Res. 42, W401-W407. doi:10.1093/nar/gku410
65. Naito, Y., Ui-Tei, K., Nishikawa, T., Takebe, Y., and Saigo, K. (2006). siVirus: web-based antiviral siRNA design software for highly divergent viral sequences. Nucleic Acids Res. 34, W448-W450. doi:10.1093/nar/gkl214
66. Naito, Y., Yoshimura, J., Morishita, S., and Ui-Tei, K. (2009). siDirect 2.0: updated software for designing functional siRNA with reduced seed-dependent off-target effect. BMC Bioinformatics 10:392. doi:10.1186/1471-2105-10-392
67. Obad, S., Santos dos, C. O., Petri, A., Heidenblad, M., Broom, O., Ruse, C., et al. (2011). Silencing of microRNA families by seed-targeting tiny LNAs. Nat. Genet. 43, 371-378. doi:10.1038/ng.786
68. Petersen, M., and Wengel, J. (2003). LNA: a versatile tool for therapeutics and genomics. Trends Biotechnol. 21, 74-81. doi:10.1016/S0167-7799(02)00038-0
69. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P., et al. (2013). Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152, 1173-1183. doi:10.1016/j.cell.2013.02.022
70. Ran, F. A., Hsu, P. D., Lin, C.-Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., et al. (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389. doi:10.1016/j.cell.2013.08.021
71. Reynolds, A., Leake, D., Boese, Q., Scaringe, S., Marshall, W. S., and Khvorova, A. (2004). Rational siRNA design for RNA interference. Nat. Biotechnol. 22, 326-330. doi:10.1038/nbt936
72. Sayed, D., Rane, S., Lypowy, J., He, M., Chen, I.-Y., Vashistha, H., et al. (2008). MicroRNA-21 targets Sprouty2 and promotes cellular outgrowths. Mol. Biol. Cell 19, 3272-3282. doi:10.1091/mbc.E08-02-0159
73. Schramm, G., and Ramey, R. (2005). siRNA design including secondary structure target site prediction. Nat. Meth. 2. doi:10.1038/nmeth780
74. Shabalina, S. A., Spiridonov, A. N., and Ogurtsov, A. Y. (2006). Computational models with thermodynamic and composition features improve siRNA design. BMC Bioinformatics 7:65. doi:10.1186/1471-2105-7-65
75. Sharma, V., Nomura, Y., and Yokobayashi, Y. (2008). Engineering complex Riboswitch regulation by dual genetic selection. J. Am. Chem. Soc. 130, 16310-16315. doi:10.1021/ja805203w
76. Shin, C., Nam, J.-W., Farh, K. K.-H., Chiang, H. R., Shkumatava, A., and Bartel, D. P. (2010). Expanding the microRNA targeting code: functional sites with centered pairing. Mol. Cell 38, 789-802. doi:10.1016/j.molcel.2010.06.005
77. Straka, M., and Boese, Q. (2010). Current topics in RNAi: why rational pooling of siRNAs is SMART. Thermo Fisher Scientific Inc
78. Strapps, W. R., Pickering, V., Muiru, G. T., Rice, J., Orsborn, S., Polisky, B. A., et al. (2010). The siRNA sequence and guide strand overhangs are determinants of in vivo duration of silencing. Nucleic Acids Res. 38, 4788-4797. doi:10.1093/nar/gkq206
79. Summerton, J., and Weller, D. (1997). Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev. 7, 187-195. doi:10.1089/oli.1.1997.7.187
80. Tafer, H., Ameres, S. L., Obernosterer, G., Gebeshuber, C. A., Schroeder, R., Martinez, J., et al. (2008). The impact of target site accessibility on the design of effective siRNAs. Nat. Biotechnol. 26, 578-583. doi:10.1038/nbt1404
81. Tanenbaum, M. E., Gilbert, L. A., Qi, L. S., Weissman, J. S., and Vale, R. D. (2014). A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159, 635-646. doi:10.1016/j.cell.2014.09.039
82. Thomas, M., Lieberman, J., and Lal, A. (2010). Desperately seeking microRNA targets. Nat. Struct. Mol. Biol. 17, 1169-1174. doi:10.1038/nsmb.1921
83. Ui-Tei, K., Naito, Y., Takahashi, F., Haraguchi, T., Ohki-Hamazaki, H., Juni, A., et al. (2004). Guidelines for the selection of highly effective siRNA sequences for mammalian and chick RNA interference. Nucleic Acids Res. 32, 936-948. doi:10.1093/nar/gkh247
84. Upadhyay, S. K., and Sharma, S. (2014). SSFinder: high throughput CRISPR-Cas target sites prediction tool. Biomed Res. Int. 2014, 1-4. doi:10.1155/2014/742482
85. Vert, J. P., Foveau, N., Lajaunie, C., and Vandenbrouck, Y. (2006). An accurate and interpretable model for siRNA efficacy prediction. BMC Bioinformatics 7:520. doi:10.1186/1471-2105-7-520
86. Xiao, A., Cheng, Z., Kong, L., Zhu, Z., Lin, S., Gao, G., et al. (2014). CasOT: a genome-wide Cas9/gRNA off-target searching tool. Bioinformatics 30, 1180-1182. doi:10.1093/bioinformatics/btt764
87. Xie, S., Shen, B., Zhang, C., Huang, X., and Zhang, Y. (2014). sgRNAcas9: a software package for designing CRISPR sgRNA and evaluating potential off-target cleavage sites. PLoS ONE 9:e100448. doi:10.1371/journal.pone.0100448
88. Xu, P., Zhang, Y., Kang, L., Roossinck, M. J., and Mysore, K. S. (2006). Computational estimation and experimental verification of off-target silencing during posttranscriptional gene silencing in plants. Plant Physiol. 142, 429-440. doi:10.1104/pp.106.083295
89. Yoo, J. W., Kim, S., and Lee, D.-K. (2008). Competition potency of siRNA is specified by the 5'-half sequence of the guide strand. Biochem. Biophys. Res. Commun. 367, 78-83. doi:10.1016/j.bbrc.2007.12.099
90. Zebec, Z., Manica, A., Zhang, J., White, M. F., and Schleper, C. (2014). CRISPR-mediated targeted mRNA degradation in the Archaeon Sulfolobus solfataricus. Nucleic Acids Res. 42, 5280-5288. doi:10.1093/nar/gku161
91. Zhao, Y., Dai, Z., Liang, Y., Yin, M., Ma, K., He, M., et al. (2014). Sequence-specific inhibition of microRNA via CRISPR/CRISPRi system. Sci. Rep. 4:3943. doi:10.1038/srep03943
92. Zhu, L. J., Holmes, B. R., Aronin, N., and Brodsky, M. H. (2014). CRISPRseek: a bioconductor package to identify target-specific guide RNAs for CRISPR-Cas9 genome-editing systems. PLoS ONE 9:e108424. doi:10.1371/journal.pone.0108424
93. Ziegler, S., Eberle, M. E., Wölfle, S. J., Heeg, K., and Bekeredjian-Ding, I. (2013). Bifunctional oligodeoxynucleotide/antagomir constructs: evaluation of a new tool for microRNA silencing. Nucleic Acid Therapeut. 23, 427-434. doi:10.1089/nat.2013.0447