A Computational Algorithm to Predict shRNA Potency

Molecular Cell

Volumn 56, Issue 6, 2014, Pages 796-807

  Knott, Simon R V ^a   Maceli, Ashley R ^a   Erard, Nicolas ^a   Chang, Kenneth ^a   Marran, Krista ^a   Zhou, Xin ^a   Gordon, Assaf ^a   ElDemerdash, Osama ^a   Wagenblast, Elvin ^a   Kim, Sun ^a   Fellmann, Christof ^a,c   Hannon, Gregory J ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MIRIMUS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; MICRORNA;

AB INITIO CALCULATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA BASE COMPOSITION; ESSENTIAL GENE; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LEARNING ALGORITHM; MOUSE; NONHUMAN; PROMOTER REGION; RNA INTERFERENCE; RNA SEQUENCE; ALGORITHM; BIOLOGICAL MODEL; COMPUTER PROGRAM; COMPUTER SIMULATION; CONSENSUS SEQUENCE; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; TUMOR CELL LINE;

MUS;

ALGORITHMS; BASE SEQUENCE; CELL LINE, TUMOR; COMPUTER SIMULATION; CONSENSUS SEQUENCE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICRORNAS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; RNA, SMALL INTERFERING; SOFTWARE;

EID: 84918804365     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.10.025     Document Type: Article

References (67)

1. Ameres S.L., Zamore P.D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 2013, 14:475-488.
2. Auyeung V.C., Ulitsky I., McGeary S.E., Bartel D.P. Beyond secondary structure: primary-sequence determinants license pri-miRNA hairpins for processing. Cell 2013, 152:844-858.
3. Babij C., Zhang Y., Kurzeja R.J., Munzli A., Shehabeldin A., Fernando M., Quon K., Kassner P.D., Ruefli-Brasse A.A., Watson V.J., et al. STK33 kinase activity is nonessential in KRAS-dependent cancer cells. Cancer Res. 2011, 71:5818-5826.
4. Baek S.T., Kerjan G., Bielas S.L., Lee J.E., Fenstermaker A.G., Novarino G., Gleeson J.G. Off-target effect of doublecortin family shRNA on neuronal migration associated with endogenous microRNA dysregulation. Neuron 2014, 82:1255-1262.
5. Berns K., Hijmans E.M., Mullenders J., Brummelkamp T.R., Velds A., Heimerikx M., Kerkhoven R.M., Madiredjo M., Nijkamp W., Weigelt B., et al. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature 2004, 428:431-437.
6. 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.
7. Breiman L. Random forests. Machine Learning 2001, 45:5-32.
8. Brummelkamp T.R., Bernards R., Agami R. A system for stable expression of short interfering RNAs in mammalian cells. Science 2002, 296:550-553.
9. Chen C.Z., Li L., Lodish H.F., Bartel D.P. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004, 303:83-86.
10. Chiu Y.L., Rana T.M. RNAi in human cells: basic structural and functional features of small interfering RNA. Mol. Cell 2002, 10:549-561.
11. Chuang C.F., Meyerowitz E.M. Specific and heritable genetic interference by double-stranded RNA in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2000, 97:4985-4990.
12. Cleary M.A., Kilian K., Wang Y., Bradshaw J., Cavet G., Ge W., Kulkarni A., Paddison P.J., Chang K., Sheth N., et al. Production of complex nucleic acid libraries using highly parallel insitu oligonucleotide synthesis. Nat. Methods 2004, 1:241-248.
13. Cui Y., Brosnan J.A., Blackford A.L., Sur S., Hruban R.H., Kinzler K.W., Vogelstein B., Maitra A., Diaz L.A., Iacobuzio-Donahue C.A., et al. Genetically defined subsets of human pancreatic cancer show unique invitro chemosensitivity. Clinical cancer research 2012, 18:6519-6530.
14. Cullen B.R. Induction of stable RNA interference in mammalian cells. Gene Ther. 2006, 13:503-508.
15. Denli A.M., Tops B.B., Plasterk R.H., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
16. Dexter D.L., Kowalski H.M., Blazar B.A., Fligiel Z., Vogel R., Heppner G.H. Heterogeneity of tumor cells from a single mouse mammary tumor. Cancer Res. 1978, 38:3174-3181.
17. 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.
18. Elkayam E., Kuhn C.D., Tocilj A., Haase A.D., Greene E.M., Hannon G.J., Joshua-Tor L. The structure of human argonaute-2 in complex with miR-20a. Cell 2012, 150:100-110.
19. Fellmann C., Zuber J., McJunkin K., Chang K., Malone C.D., Dickins R.A., Xu Q., Hengartner M.O., Elledge S.J., Hannon G.J., Lowe S.W. Functional identification of optimized RNAi triggers using a massively parallel sensor assay. Mol. Cell 2011, 41:733-746.
20. Fellmann C., Hoffmann T., Sridhar V., Hopfgartner B., Muhar M., Roth M., Lai D.Y., Barbosa I.A., Kwon J.S., Guan Y., et al. An optimized microRNA backbone for effective single-copy RNAi. Cell Reports 2013, 5:1704-1713.
21. 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.
22. Frank F., Sonenberg N., Nagar B. Structural basis for 5'-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 2010, 465:818-822.
23. Grishok A., Pasquinelli A.E., Conte D., Li N., Parrish S., Ha I., Baillie D.L., Fire A., Ruvkun G., Mello C.C. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 2001, 106:23-34.
24. Gupta S., Schoer R.A., Egan J.E., Hannon G.J., Mittal V. Inducible, reversible, and stable RNA interference in mammalian cells. Proc. Natl. Acad. Sci. USA 2004, 101:1927-1932.
25. 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.
26. Han J., Lee Y., Yeom K.H., Nam J.W., Heo I., Rhee J.K., Sohn S.Y., Cho Y., Zhang B.T., Kim V.N. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125:887-901.
27. Hannon G.J. RNA interference. Nature 2002, 418:244-251.
28. Huesken D., Lange J., Mickanin C., Weiler J., Asselbergs F., Warner J., Meloon B., Engel S., Rosenberg A., Cohen D., et al. Design of a genome-wide siRNA library using an artificial neural network. Nat. Biotechnol. 2005, 23:995-1001.
29. Hutvágner G., Zamore P.D. A microRNA in a multiple-turnover RNAi enzyme complex. Science 2002, 297:2056-2060.
30. Hutvágner G., McLachlan J., Pasquinelli A.E., Bálint E., Tuschl T., Zamore P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293:834-838.
31. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., et al. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 2003, 421:231-237.
32. Kambris Z., Brun S., Jang I.H., Nam H.J., Romeo Y., Takahashi K., Lee W.J., Ueda R., Lemaitre B. Drosophila immunity: a large-scale invivo RNAi screen identifies five serine proteases required for Toll activation. Current biology: CB 2006, 16:808-813.
33. Ketting R.F., Fischer S.E., Bernstein E., Sijen T., Hannon G.J., Plasterk R.H. Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans. Genes Dev. 2001, 15:2654-2659.
34. Khvorova A., Reynolds A., Jayasena S.D. Functional siRNAs and miRNAs exhibit strand bias. Cell 2003, 115:209-216.
35. Lai E.C. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 2002, 30:363-364.
36. Lee Y., Ahn C., Han J., Choi H., Kim J., Yim J., Lee J., Provost P., Rådmark O., Kim S., Kim V.N. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
37. 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.
38. Lund E., Güttinger S., Calado A., Dahlberg J.E., Kutay U. Nuclear export of microRNA precursors. Science 2004, 303:95-98.
39. Luo J., Emanuele M.J., Li D., Creighton C.J., Schlabach M.R., Westbrook T.F., Wong K.K., Elledge S.J. A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009, 137:835-848.
40. Malone C., Brennecke J., Czech B., Aravin A., Hannon G.J. Preparation of small RNA libraries for high-throughput sequencing. Cold Spring Harbor protocols 2012, 2012:1067-1077.
41. Martinez J., Patkaniowska A., Urlaub H., Lührmann R., Tuschl T. Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 2002, 110:563-574.
42. Matveeva O.V., Nazipova N.N., Ogurtsov A.Y., Shabalina S.A. Optimized models for design of efficient miR30-based shRNAs. Front. Genet. 2012, 3:163.
43. Nakanishi K., Weinberg D.E., Bartel D.P., Patel D.J. Structure of yeast Argonaute with guide RNA. Nature 2012, 486:368-374.
44. 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.
45. Paddison P.J., Silva J.M., Conklin D.S., Schlabach M., Li M., Aruleba S., Balija V., O'Shaughnessy A., Gnoj L., Scobie K., et al. A resource for large-scale RNA-interference-based screens in mammals. Nature 2004, 428:427-431.
46. Reynolds A., Leake D., Boese Q., Scaringe S., Marshall W.S., Khvorova A. Rational siRNA design for RNA interference. Nat. Biotechnol. 2004, 22:326-330.
47. Sánchez Alvarado A., Newmark P.A. Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc. Natl. Acad. Sci. USA 1999, 96:5049-5054.
48. Scholl C., Fröhling S., Dunn I.F., Schinzel A.C., Barbie D.A., Kim S.Y., Silver S.J., Tamayo P., Wadlow R.C., Ramaswamy S., et al. Synthetic lethal interaction between oncogenic KRAS dependency and STK33 suppression in human cancer cells. Cell 2009, 137:821-834.
49. Schwarz D.S., Hutvágner G., Du T., Xu Z., Aronin N., Zamore P.D. Asymmetry in the assembly of the RNAi enzyme complex. Cell 2003, 115:199-208.
50. Seitz H., Zamore P.D. Rethinking the microprocessor. Cell 2006, 125:827-829.
51. * strands in flies. Current biology: CB 2008, 18:147-151.
52. Silva J.M., Li M.Z., Chang K., Ge W., Golding M.C., Rickles R.J., Siolas D., Hu G., Paddison P.J., Schlabach M.R., et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 2005, 37:1281-1288.
53. Sims D., Mendes-Pereira A.M., Frankum J., Burgess D., Cerone M.A., Lombardelli C., Mitsopoulos C., Hakas J., Murugaesu N., Isacke C.M., et al. High-throughput RNA interference screening using pooled shRNA libraries and next generation sequencing. Genome Biol. 2011, 12:R104.
54. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical applications in genetics and molecular biology 2004, 3. Article3.
55. 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.
56. Tibshirani R. Regression Shrinkage and Selection via the Lasso. J.R. Stat. Soc. Ser. A Stat. Soc. 1996, 58:267-288.
57. Timmons L., Fire A. Specific interference by ingested dsRNA. Nature 1998, 395:854.
58. Tuschl T., Zamore P.D., Lehmann R., Bartel D.P., Sharp P.A. Targeted mRNA degradation by double-stranded RNA invitro. Genes Dev. 1999, 13:3191-3197.
59. 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.
60. Vacic V., Iakoucheva L.M., Radivojac P. Two Sample Logo: a graphical representation of the differences between two sets of sequence alignments. Bioinformatics 2006, 22:1536-1537.
61. Vert J.P., Foveau N., Lajaunie C., Vandenbrouck Y. An accurate and interpretable model for siRNA efficacy prediction. BMC Bioinformatics 2006, 7:520.
62. Wang Y., Sheng G., Juranek S., Tuschl T., Patel D.J. Structure of the guide-strand-containing argonaute silencing complex. Nature 2008, 456:209-213.
63. Yi R., Qin Y., Macara I.G., Cullen B.R. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 2003, 17:3011-3016.
64. Yuan Y.R., Pei Y., Chen H.Y., Tuschl T., Patel D.J. A potential protein-RNA recognition event along the RISC-loading pathway from the structure of A. aeolicus Argonaute with externally bound siRNA. Structure (London, England: 1993) 2006, 14:1557-1565.
65. Zender L., Xue W., Zuber J., Semighini C.P., Krasnitz A., Ma B., Zender P., Kubicka S., Luk J.M., Schirmacher P., et al. An oncogenomics-based invivo RNAi screen identifies tumor suppressors in liver cancer. Cell 2008, 135:852-864.
66. Zeng Y., Cullen B.R. Sequence requirements for micro RNA processing and function in human cells. RNA 2003, 9:112-123.
67. Zhang X., Zeng Y. The terminal loop region controls microRNA processing by Drosha and Dicer. Nucleic Acids Res. 2010, 38:7689-7697.