Toward optimization of agoshRNA molecules that use a non-canonical RNAi pathway: Variations in the top and bottom base pairs

RNA Biology

Volumn 12, Issue 4, 2015, Pages 447-456

  Herrera Carrillo, Elena ^a   Harwig, Alex ^a   Berkhout, Ben ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

AgoshRNA; Argonaute2; Dicer; RNA processing; shRNA

Indexed keywords

AGOSHRNA MOLECULE; ARGONAUTE 2 PROTEIN; ARGONAUTE PROTEIN; DICER; MESSENGER RNA; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; EIF2C2 PROTEIN, HUMAN; DNA; GUIDE RNA; NUCLEOTIDE; REAGENT;

ARTICLE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; EMBRYO; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; MOLECULE; MUTATIONAL ANALYSIS; POSTTRANSCRIPTIONAL GENE SILENCING; PROCESS OPTIMIZATION; PROTEIN SECONDARY STRUCTURE; RNA INTERFERENCE; RNA PROCESSING; TRANSGENE; WILD TYPE; BASE PAIRING; CELL LINE; CHEMISTRY; GENETIC VARIATION; GENETICS; METABOLISM; ANIMAL CELL; BASE MISPAIRING; DNA TRANSFECTION; FEMALE; GENETIC VARIABILITY; HEK293 CELL LINE; NONHUMAN; NORTHERN BLOTTING; PROTEIN PROCESSING; RNA GEL BLOT ANALYSIS; VERO CELL LINE;

ARGONAUTE PROTEINS; BASE PAIRING; CELL LINE; GENETIC VARIATION; HUMANS; METABOLIC NETWORKS AND PATHWAYS; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84928267272     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.1080/15476286.2015.1022024     Document Type: Article

References (35)

1. Havens MA, Reich AA, Duelli DM, Hastings ML. Biogenesis of mammalian microRNAs by a non-canonical processing pathway. Nucleic Acids Res 2012; 40:4626-40 ; PMID:22270084; http://dx.doi.org/10.1093/nar/gks026
2. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J Virol 1998; 72:8150-7 ; PMID:9733856
3. Yang JS, Lai EC. AlternativemiRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011; 43:892-903 ; PMID:21925378; http://dx.doi.org/10.1016/j.molcel.2011.07.024
4. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. A dicer-independentmiRNA biogenesis pathway that requires ago catalysis. Nature 2010; 465:584-9 ; PMID:20424607; http://dx.doi.org/10.1038/nature09092
5. Berkhout B, Liu YP. Towards improved shRNA and miRNA reagents as inhibitors of HIV-1 replication. Future Microbiol 2014; 9:561-71 ; PMID:24810353; http://dx.doi.org/10.2217/fmb.14.5
6. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005; 6:376-85 ; PMID:15852042; http://dx.doi.org/10.1038/nrm1644
7. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007; 131: 1097-108 ; PMID:18083100; http://dx.doi.org/10.1016/j. cell.2007.10.032
8. Tam OH, Aravin AA, Stein P, Girard A, Murchison EP, Cheloufi S, Hodges E, Anger M, Sachidanandam R, Schultz RM, et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008; 453:534-8 ; PMID:18404147; http://dx. doi.org/10.1038/nature06904
9. Siolas D, Lerner C, Burchard J, Ge W, Linsley PS, Paddison PJ, Hannon GJ, Cleary MA. Synthetic shRNAs as potent RNAi triggers. Nat Biotechnol 2005; 23:227-31 ; PMID:15619616; http://dx.doi.org/10.1038/nbt1052
10. Li N, You X, Chen T, Mackowiak SD, Friedläander MR, Weigt M, Du H, Gogol-Doring A, Chang Z, Dieterich C, et al. Global profiling of miRNAs and the hairpin precursors: insights into miRNA processing and novel miRNA discovery. Nucleic Acids Res 2013; 41:3619-34 ; PMID:23396444; http://dx.doi.org/10.1093/nar/gkt072
11. Yang JS, Maurin T, Lai EC. Functional parameters of dicer-independent microRNA biogenesis. RNA 2012; 18:945-57 ; PMID:22461413; http://dx.doi.org/10.1261/rna.032938.112
12. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G. microRNAs associated with the different human argonaute proteins. Nucleic Acids Res 2012; 40:9850-62 ; PMID:22844086; http://dx.doi.org/10.1093/nar/gks705
13. Dallas A, Ilves H, Ge Q, Kumar P, Shorenstein J, Kazakov SA, Cuellar TL, McManus MT, Behlke MA, Johnston BH. Right- and left-loop short shRNAs have distinct and unusual mechanisms of gene silencing. Nucleic Acids Res 2012; 40:9255-71 ; PMID:22810205; http://dx.doi.org/10.1093/nar/gks662
14. Ge Q, Ilves H, Dallas A, Kumar P, Shorenstein J, Kazakov SA, Johnston BH. Minimal-length short hairpin RNAs: the relationship of structure and RNAi activity. RNA 2010; 16:106-17 ; PMID:19952116; http://dx. doi.org/10.1261/rna.1894510
15. Liu YP, Schopman NC, Berkhout B. Dicer-independent processing of short hairpin RNAs. Nucleic Acids Res 2013; 41:3723-33 ; PMID:23376931; http://dx. doi.org/10.1093/nar/gkt036
16. Herrera-Carrillo E, Harwig A, Liu YP, Berkhout B. Probing the shRNA characteristics that hinder dicer recognition and consequently allow ago-mediated processing and agoshRNA activity. RNA 2014; 20: 1410-18 ; PMID:25035295; http://dx.doi.org/10.1261/rna.043950.113
17. Yoda M, Cifuentes D, Izumi N, Sakaguchi Y, Suzuki T, Giraldez AJ, Tomari Y. Poly(A)-specific ribonuclease mediates 30-end trimming of argonaute2-cleaved precursor microRNAs. Cell Rep. 2013 Nov 14;5(3):715-26 ; PMID:24209750; http://dx.doi.org/10.1016/j.celrep. 2013.09.029
18. Jackson AL, Burchard J, Schelter J, Chau BN, Cleary M, Lim L, Linsley PS. Widespread siRNA "off-target"transcript silencing mediated by seed region sequence complementarity. RNA 2006; 12:1179-87 ; PMID:16682560; http://dx.doi.org/10.1261/rna.25706
19. Liu YP, von Eije KJ, Schopman NC, Westerink JT, ter Brake O, Haasnoot J, Berkhout B. Combinatorial RNAi against HIV-1 using extended short hairpin RNAs. Mol Ther 2009; 17:1712-23 ; PMID:19672247; http://dx.doi. org/10.1038/mt.2009.176
20. McIntyre GJ, Yu YH, Lomas M, Fanning GC. The effects of stem length and core placement on shRNA activity. BMC Mol Biol 2011; 12:34 ; PMID:21819628; http://dx.doi.org/10.1186/1471-2199-12-34
21. Li L, Lin X, Khvorova A, Fesik SW, Shen Y. Defining the optimal parameters for hairpin-based knockdown constructs. RNA 2007; 13:1765-74 ; PMID:17698642; http://dx.doi.org/10.1261/rna.599107
22. Sano M, Kato Y, Akashi H, Miyagishi M, Taira K. Novel methods for expressing RNA interference in human cells. Methods Enzymol 2005; 392:97-112 ; PMID:15644177; http://dx.doi.org/10.1016/S0076- 6879(04)92006-X
23. Tuschl T. Expanding small RNA interference. Nat Biotechnol 2002; 20:446-8 ; PMID:11981553; http://dx. doi.org/10.1038/nbt0502-446
24. Frank F, Sonenberg N, Nagar B. Structural basis for 50- nucleotide base-specific recognition of guide RNA by human AGO2. Nature 2010; 465:818-22 ; PMID:20505670; http://dx.doi.org/10.1038/nature09039
25. Ma H, Zhang J, Wu H. Designing ago2-specific siRNA/shRNA to avoid competition with endogenous miRNAs. Mol Ther Nucleic Acids 2014; 3:e176 ; PMID:25025466; http://dx.doi.org/10.1038/mtna.2014.27
26. Bridge AJ, Pebernard S, Ducraux A, Nicoulaz AL, Iggo R. Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 2003; 34:263-4 ; PMID:12796781; http://dx.doi.org/10.1038/ng1173
27. Gu S, Jin L, Zhang Y, Huang Y, Zhang F, Valdmanis PN, Kay MA. The loop position of shRNAs and premiRNAs is critical for the accuracy of dicer processing in vivo. Cell 2012; 151:900-11 ; PMID:23141545; http://dx.doi.org/10.1016/j.cell.2012.09.042
28. Ma H, Dallas A, Ilves H, Shorenstein J, MacLachlan I, Klumpp K, Johnston BH. Formulated minimal-length synthetic small hairpin RNAs are potent inhibitors of hepatitis C virus in mice with humanized livers. Gastroenterology. 2014 Jan;146(1):63-6.e5 ; PMID:24076507; http://dx.doi.org/10.1053/j.gastro.2013.09.049
29. Brummelkamp TR, Bernards R, Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002; 296:550-3 ; PMID:11910072; http://dx.doi.org/10.1126/science.1068999
30. Schopman NC, Liu YP, Konstantinova P, Ter Brake O, Berkhout B. Optimization of shRNA inhibitors by variation of the terminal loop sequence. Antiviral Res 2010; 86:204-11 ; PMID:20188764; http://dx.doi.org/10.1016/j.antiviral.2010.02.320
31. Ter Brake O, Konstantinova P, Ceylan M, Berkhout B. Silencing of HIV-1 with RNA interference: a multiple shRNA approach. Mol Ther 2006; 14: 883-92 ; PMID:16959541; http://dx.doi.org/10.1016/j. ymthe.2006.07.007
32. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003; 31:3406-15 ; PMID:12824337; http://dx.doi.org/10.1093/nar/gkg595
33. Westerhout EM, Ooms M, Vink M, Das AT, Berkhout B. HIV-1 can escape from RNA interference by evolving an alternative structure in its RNA genome. Nucleic Acids Res 2005; 33: 796-804 ; PMID:15687388; http://dx.doi.org/10.1093/nar/gki220
34. Ruijter JM, Thygesen HH, Schoneveld OJ, Das AT, Berkhout B, Lamers WH. Factor correction as a tool to eliminate between-session variation in replicate experiments: application to molecular biology and retrovirology. Retrovirology 2006; 3:2 ; PMID:16398936; http://dx.doi.org/10.1186/1742-4690-3-2
35. Liu YP, Haasnoot J, Ter Brake O, Berkhout B, Konstantinova P. Inhibition of HIV-1 by multiple siRNAs expressed from a single microRNA polycistron. Nucleic Acids Res 2008; 36:2811-24 ; PMID:18346971; http://dx.doi.org/10.1093/nar/gkn109