Towards antiviral shRNAs based on the AgoshRNA design

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Liu, Ying Poi ^a   Karg, Margarete ^a   Herrera Carrillo, Elena ^a   Berkhout, Ben ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AGOSHRNA; ANTIVIRUS AGENT; ARGONAUTE 2 PROTEIN; MESSENGER RNA; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIRUS RNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; RIBONUCLEASE III; SMALL INTERFERING RNA;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DRUG DESIGN; DRUG DETERMINATION; DRUG SCREENING; EMBRYO; GENE FUNCTION; GENE IDENTIFICATION; GENE SILENCING; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; RNA INTERFERENCE; RNA STABILITY; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; THERMODYNAMICS; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS INHIBITION; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETICS; HEK293 CELL LINE; METABOLISM; NORTHERN BLOTTING; SYNTHESIS; T LYMPHOCYTE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

ANTI-HIV AGENTS; BLOTTING, NORTHERN; DRUG DESIGN; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HIV-1; HUMANS; RIBONUCLEASE III; RNA, SMALL INTERFERING; T-LYMPHOCYTES;

EID: 84939214352     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128618     Document Type: Article

References (50)

1. Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998; 391(6669):806-11. doi:10.1038/35888 PMID: 9486653.
2. Napoli C, Lemieux C, Jorgensen R. Introduction of a Chimeric Chalcone Synthase Gene into Petunia Results in Reversible Co-Suppression of Homologous Genes in trans. The Plant cell. 1990; 2(4):279- 89. doi:10.1105/tpc.2.4.279 PMID: 12354959; PubMed Central PMCID: PMC159885.
3. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009; 136(2):215-33. doi:10.1016/j.cell.2009.01.002 PMID: 19167326; PubMed Central PMCID: PMC3794896.
4. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell. 2007; 130(1):89-100. doi:10.1016/j.cell.2007.06.028 PMID: 17599402; PubMed Central PMCID: PMC2729315.
5. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature. 2007; 448(7149):83-6. doi:10.1038/nature05983 PMID: 17589500; PubMed Central PMCID: PMC2475599.
6. Berezikov E, Chung WJ, Willis J, Cuppen E, Lai EC. Mammalian mirtron genes. Molecular cell. 2007; 28(2):328-36. doi:10.1016/j.molcel.2007.09.028 PMID: 17964270; PubMed Central PMCID: PMC2763384.
7. Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JW, et al. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. Rna. 2009; 15 (12):2147-60. doi:10.1261/rna.1738409 PMID: 19850906; PubMed Central PMCID: PMC2779667.
8. Haussecker D, Huang Y, Lau A, Parameswaran P, Fire AZ, Kay MA. Human tRNA-derived small RNAs in the global regulation of RNA silencing. Rna. 2010; 16(4):673-95. doi:10.1261/rna.2000810 PMID: 20181738; PubMed Central PMCID: PMC2844617.
9. Ender C, Krek A, Friedlander MR, Beitzinger M, Weinmann L, Chen W, et al. A human snoRNA with microRNA-like functions. Molecular cell. 2008; 32(4):519-28. doi:10.1016/j.molcel.2008.10.017 PMID: 19026782.
10. Glazov EA, Kongsuwan K, Assavalapsakul W, Horwood PF, Mitter N, Mahony TJ. Repertoire of bovine miRNA and miRNA-like small regulatory RNAs expressed upon viral infection. PloS one. 2009; 4(7): E6349. doi:10.1371/journal.pone.0006349 PMID: 19633723; PubMed Central PMCID: PMC2713767.
11. Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS. Small RNAs derived from snoRNAs. Rna. 2009; 15(7):1233-40. doi:10.1261/rna.1528909 PMID: 19474147; PubMed Central PMCID: PMC2704076.
12. Brameier M, Herwig A, Reinhardt R, Walter L, Gruber J. Human box C/D snoRNAs with miRNA like functions: Expanding the range of regulatory RNAs. Nucleic acids research. 2011; 39(2):675-86. doi:10.1093/nar/gkq776 PMID: 20846955; PubMed Central PMCID: PMC3025573.
13. Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature. 2010; 465(7298):584-9. doi:10.1038/nature09092 PMID: 20424607; PubMed Central PMCID: PMC2995450.
14. Cifuentes D, Xue H, Taylor DW, Patnode H, Mishima Y, Cheloufi S, et al. A novel miRNA processing pathway independent of Dicer requires Argonaute2 catalytic activity. Science. 2010; 328(5986):1694- 8. doi:10.1126/science.1190809 PMID: 20448148; PubMed Central PMCID: PMC3093307.
15. Yang JS, Maurin T, Robine N, Rasmussen KD, Jeffrey KL, Chandwani R, et al. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(34):15163-8. doi:10.1073/pnas.1006432107PMID: 20699384; PubMed Central PMCID: PMC2930549.
16. Liu YP, Schopman NC, Berkhout B. Dicer-independent processing of short hairpin RNAs. Nucleic acids research. 2013; 41(6):3723-33. doi:10.1093/nar/gkt036PMID: 23376931; PubMed Central PMCID: PMC3616727.
17. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G. microRNAs associated with the different human Argonaute proteins. Nucleic acids research. 2012; 40(19):9850-62. doi:10.1093/nar/gks705 PMID: 22844086; PubMed Central PMCID: PMC3479175.
18. Dallas A, Ilves H, Ge Q, Kumar P, Shorenstein J, Kazakov SA, et al. Right- And left-loop short shRNAs have distinct and unusual mechanisms of gene silencing. Nucleic acids research. 2012; 40(18):9255- 71. doi:10.1093/nar/gks662 PMID: 22810205; PubMed Central PMCID: PMC3467060.
19. Ge Q, Ilves H, Dallas A, Kumar P, Shorenstein J, Kazakov SA, et al. Minimal-length short hairpin RNAs: The relationship of structure and RNAi activity. Rna. 2010; 16(1):106-17. doi:10.1261/rna.1894510PMID: 19952116; PubMed Central PMCID: PMC2802021.
20. Berkhout B, Liu YP. Towards improved shRNA and miRNA reagents as inhibitors of HIV-1 replication. Future microbiology. 2014; 9(4):561-71. doi:10.2217/fmb.14.5 PMID: 24810353.
21. Coley W, Van Duyne R, Carpio L, Guendel I, Kehn-Hall K, Chevalier S, et al. Absence of DICER in monocytes and its regulation by HIV-1. The Journal of biological chemistry. 2010; 285(42):31930-43. doi:10.1074/jbc.M110.101709 PMID: 20584909; PubMed Central PMCID: PMC2952194.
22. 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 (9):1410-8. doi:10.1261/rna.043950.113PMID: 25035295; PubMed Central PMCID: PMC4138324.
23. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic acids research. 2003; 31(13):3406-15. PMID: 12824337; PubMed Central PMCID: PMC169194.
24. 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. doi:10.1186/1742-4690-3-2 PMID: 16398936.
25. Li MJ, Rossi JJ. Lentiviral vector delivery of recombinant small interfering RNA expression cassettes. Methods in enzymology. 2005; 392:218-26. doi:10.1016/S0076-6879(04)92013-7 PMID: 15644184.
26. ter Brake O, Konstantinova P, Ceylan M, Berkhout B. Silencing of HIV-1 with RNA interference: A multiple shRNA approach. Molecular therapy: The journal of the American Society of Gene Therapy. 2006; 14(6):883-92. doi:10.1016/j.ymthe.2006.07.007 PMID: 16959541.
27. Seppen J, Rijnberg M, Cooreman MP, Oude Elferink RP. Lentiviral vectors for efficient transduction of isolated primary quiescent hepatocytes. Journal of hepatology. 2002; 36(4):459-65. PMID: 11943415.
28. Kotsopoulou E, Kim VN, Kingsman AJ, Kingsman SM, Mitrophanous KA. A Rev-independent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gag-pol gene. Journal of virology. 2000; 74(10):4839-52. PMID: 10775623; PubMed Central PMCID: PMC112007.
29. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. Journal of virology. 1998; 72(12):9873-80. PMID: 9811723; PubMed Central PMCID: PMC110499.
30. Jeeninga RE, Hoogenkamp M, Armand-Ugon M, de-Baar M, Verhoef K, Berkhout B. Functional differences between the long terminal repeat transcriptional promoters of human immunodeficiency virus type 1 subtypes A through G. Journal of virology. 2000; 74(8):3740-51. PMID: 10729149; PubMed Central PMCID: PMC111883.
31. Konstantinova P, de Haan P, Das AT, Berkhout B. Hairpin-induced tRNA-mediated (HITME) recombination in HIV-1. Nucleic acids research. 2006; 34(8):2206-18. doi:10.1093/nar/gkl226PMID: 16670429; PubMed Central PMCID: PMC1456326.
32. Eekels JJ, Pasternak AO, Schut AM, Geerts D, Jeeninga RE, Berkhout B. A competitive cell growth assay for the detection of subtle effects of gene transduction on cell proliferation. Gene therapy. 2012; 19(11):1058-64. doi:10.1038/gt.2011.191 PMID: 22113311.
33. Von-Eije KJ, ter Brake O, Berkhout B. Human immunodeficiency virus type 1 escape is restricted when conserved genome sequences are targeted by RNA interference. Journal of virology. 2008; 82 (6):2895-903. doi:10.1128/JVI.02035-07 PMID: 18077712; PubMed Central PMCID: PMC2258968.
34. Low JT, Knoepfel SA, Watts JM, ter Brake O, Berkhout B, Weeks KM. SHAPE-directed discovery of potent shRNA inhibitors of HIV-1. Molecular therapy: The journal of the American Society of Gene Therapy. 2012; 20(4):820-8. doi:10.1038/mt.2011.299PMID: 22314289; PubMed Central PMCID: PMC3321596.
35. Knoepfel SA, Centlivre M, Liu YP, Boutimah F, Berkhout B. Selection of RNAi-based inhibitors for anti- HIV gene therapy. World journal of virology. 2012; 1(3):79-90. doi:10.5501/wjv.v1.i3.79 PMID: 24175213; PubMed Central PMCID: PMC3782270.
36. Petri S, Dueck A, Lehmann G, Putz N, Rudel S, Kremmer E, et al. Increased siRNA duplex stability correlates with reduced off-target and elevated on-target effects. Rna. 2011; 17(4):737-49. doi:10.1261/rna.2348111 PMID: 21367974; PubMed Central PMCID: PMC3062184.
37. Gu S, Jin L, Zhang Y, Huang Y, Zhang F, Valdmanis PN, et al. The loop position of shRNAs and premiRNAs is critical for the accuracy of dicer processing in vivo. Cell. 2012; 151(4):900-11. doi:10.1016/j.cell.2012.09.042 PMID: 23141545; PubMed Central PMCID: PMC3499986.
38. Denise H, Moschos SA, Sidders B, Burden F, Perkins H, Carter N, et al. Deep Sequencing Insights in Therapeutic shRNA Processing and siRNA Target Cleavage Precision. Molecular therapy Nucleic acids. 2014; 3:e145. doi:10.1038/mtna.2013.73 PMID: 24496437; PubMed Central PMCID: PMC3951910.
39. Fukunaga R, Han BW, Hung JH, Xu J, Weng Z, Zamore PD. Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell. 2012; 151(3):533-46. doi:10.1016/j.cell.2012.09.027 PMID: 23063653; PubMed Central PMCID: PMC3609031.
40. ter Brake O, t Hooft K, Liu YP, Centlivre M, von-Eije KJ, Berkhout B. Lentiviral vector design for multiple shRNA expression and durable HIV-1 inhibition. Molecular therapy: The journal of the American Society of Gene Therapy. 2008; 16(3):557-64. doi:10.1038/sj.mt.6300382 PMID: 18180777.
41. Khvorova A, Reynolds A, Jayasena SD. Functional siRNAs and miRNAs exhibit strand bias. Cell. 2003; 115(2):209-16. PMID: 14567918.
42. Schwarz DS, Hutvagner G, Du T, Xu Z, Aronin N, Zamore PD. Asymmetry in the assembly of the RNAi enzyme complex. Cell. 2003; 115(2):199-208. PMID: 14567917.
43. Reynolds A, Leake D, Boese Q, Scaringe S, Marshall WS, Khvorova A. Rational siRNA design for RNA interference. Nature biotechnology. 2004; 22(3):326-30. doi:10.1038/nbt936. PMID: 14758366.
44. Tomari Y, Zamore PD. Perspective: Machines for RNAi. Genes & development. 2005; 19(5):517-29. doi:10.1101/gad.1284105 PMID: 15741316.
45. 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 research. 2005; 33(2):796-804. doi:10.1093/nar/gki220 PMID: 15687388; PubMed Central PMCID: PMC548362.
46. Westerhout EM, ter Brake O, Berkhout B. The virion-associated incoming HIV-1 RNA genome is not targeted by RNA interference. Retrovirology. 2006; 3:57. doi:10.1186/1742-4690-3-57 PMID: 16948865; PubMed Central PMCID: PMC1569866.
47. Westerhout EM, Berkhout B. A systematic analysis of the effect of target RNA structure on RNA interference. Nucleic acids research. 2007; 35(13):4322-30. doi:10.1093/nar/gkm437 PMID: 17576691; PubMed Central PMCID: PMC1934999.
48. Centlivre M, Legrand N, Klamer S, Liu YP, Jasmijn von-Eije K, Bohne M, et al. Preclinical in vivo evaluation of the safety of a multi-shRNA-based gene therapy against HIV-1. Molecular therapy Nucleic acids. 2013; 2:e120. doi:10.1038/mtna.2013.48 PMID: 24002730; PubMed Central PMCID: PMC3808742.
49. Siegfried NA, Busan S, Rice GM, Nelson JA, Weeks KM. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nature methods. 2014; 11(9):959-65. doi:10.1038/nmeth.3029 PMID: 25028896; PubMed Central PMCID: PMC4259394.
50. Fellmann C, Hoffmann T, Sridhar V, Hopfgartner B, Muhar M, Roth M, et al. An optimized microRNA backbone for effective single-copy RNAi. Cell reports. 2013; 5(6):1704-13. doi:10.1016/j.celrep.2013.11.020 PMID: 24332856.