Rapid identification of regulatory microRNAs by miTRAP (miRNA trapping by RNA in vitro affinity purification)

Nucleic Acids Research

Volumn 42, Issue 8, 2014, Pages

  Braun, Juliane ^a   Misiak, Danny ^a   Busch, Bianca ^a   Krohn, Knut ^b   Hüttelmaier, Stefan ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY HOSPITAL LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 1248; MICRORNA 125A 3P; MICRORNA 1294; MICRORNA 148 5P; MICRORNA 16 5P; MICRORNA 200 5P; MICRORNA 21 5P; MICRORNA 30 5P; MICRORNA 3159; MICRORNA 34 5P; MICRORNA 34A 5P; MICRORNA 375; MICRORNA 455 3P; MICRORNA 4677 3P; MICRORNA 940; MICRORNA 98 5P; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CELL LYSATE; COMPUTER MODEL; CONTROLLED STUDY; COST EFFECTIVENESS ANALYSIS; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HEK293 CELL LINE; IN VITRO STUDY; MIRNA TRAPPING BY RNA IN VITRO AFFINITY PURIFICATION; ONCOGENE MYC; PRIORITY JOURNAL; REGULATORY RNA SEQUENCE; RNA ANALYSIS; RNA PURIFICATION; RNA SEQUENCE; RNA TRANSCRIPTION; U2OS CELL LINE; UPREGULATION; ZEB2 GENE;

3' UNTRANSLATED REGIONS; CELL LINE; GENE EXPRESSION REGULATION; GENES, MYC; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MICRORNAS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC;

EID: 84899879146     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku127     Document Type: Article

References (67)

1. Tritschler, F., Huntzinger, E. and Izaurralde, E. (2010) Role of GW182 proteins and PABPC1 in the miRNA pathway: a sense of deja vu. Nat. Rev. Mol. Cell Biol., 11, 379-384.
2. Pasquinelli, A.E. (2012) MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet., 13, 271-282.
3. Fang, Z. and Rajewsky, N. (2011) The impact of miRNA target sites in coding sequences and in 3′UTRs. PLoS One, 6, e18067.
4. Wilson, J.A. and Huys, A. (2013) miR-122 Promotion of the hepatitis C virus life cycle: sound in the silence. Wiley Interdiscip. Rev. RNA, 4, 665-676.
5. Griffiths-Jones, S. (2004) The microRNA Registry. Nucleic Acids Res., 32, D109-D111.
6. Griffiths-Jones, S., Grocock, R.J., van Dongen, S., Bateman, A. and Enright, A.J. (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res., 34, D140-D144.
7. Griffiths-Jones, S., Saini, H.K., van Dongen, S. and Enright, A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res., 36, D154-D158.
8. Kozomara, A. and Griffiths-Jones, S. (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res., 39, D152-D157.
9. De Mulder, K. and Berezikov, E. (2010) Tracing the evolution of tissue identity with microRNAs. Genome Biol., 11, 111.
10. Bartel, D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-233.
11. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R. and Ruvkun, G. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901-906.
12. Shin, C., Nam, J.W., Farh, K.K., 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.
13. 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.
14. Thomson, D.W., Bracken, C.P. and Goodall, G.J. (2011) Experimental strategies for microRNA target identification. Nucleic Acids Res., 39, 6845-6853.
15. van Kouwenhove, M., Kedde, M. and Agami, R. (2011) MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat. Rev. Cancer, 11, 644-656.
16. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S. and Johnson, J.M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 433, 769-773.
17. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature, 455, 58-63.
18. Hendrickson, D.G., Hogan, D.J., McCullough, H.L., Myers, J.W., Herschlag, D., Ferrell, J.E. and Brown, P.O. (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol., 7, e1000238.
19. Easow, G., Teleman, A.A. and Cohen, S.M. (2007) Isolation of microRNA targets by miRNP immunopurification. RNA, 13, 1198-1204.
20. Chi, S.W., Zang, J.B., Mele, A. and Darnell, R.B. (2009) Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature, 460, 479-486.
21. Cambronne, X.A., Shen, R., Auer, P.L. and Goodman, R.H. (2012) Capturing microRNA targets using an RNA-induced silencing complex (RISC)-trap approach. Proc. Natl Acad. Sci. USA, 109, 20473-20478.
22. Orom, U.A. and Lund, A.H. (2007) Isolation of microRNA targets using biotinylated synthetic microRNAs. Methods, 43, 162-165.
23. Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M. Jr, Jungkamp, A.C., Munschauer, M. et al. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell, 141, 129-141.
24. Wu, S., Huang, S., Ding, J., Zhao, Y., Liang, L., Liu, T., Zhan, R. and He, X. (2010) Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3′ untranslated region. Oncogene, 29, 2302-2308.
25. Gaken, J., Mohamedali, A.M., Jiang, J., Malik, F., Stangl, D., Smith, A.E., Chronis, C., Kulasekararaj, A.G., Thomas, N.S., Farzaneh, F. et al. (2012) A functional assay for microRNA target identification and validation. Nucleic Acids Res., 40, e75.
26. Vo, N.K., Dalton, R.P., Liu, N., Olson, E.N. and Goodman, R.H. (2010) Affinity purification of microRNA-133a with the cardiac transcription factor, Hand2. Proc. Natl Acad. Sci. USA, 107, 19231-19236.
27. Yoon, J.H., Srikantan, S. and Gorospe, M. (2012) MS2-TRAP (MS2-tagged RNA affinity purification): tagging RNA to identify associated miRNAs. Methods, 58, 81-87.
28. Hassan, T., Smith, S.G., Gaughan, K., Oglesby, I.K., O'Neill, S., McElvaney, N.G. and Greene, C.M. (2013) Isolation and identification of cell-specific microRNAs targeting a messenger RNA using a biotinylated anti-sense oligonucleotide capture affinity technique. Nucleic Acids Res., 41, e71.
29. Schulman, B.R., Esquela-Kerscher, A. and Slack, F.J. (2005) Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Dev. Dyn., 234, 1046-1054.
30. Czaplinski, K., Kocher, T., Schelder, M., Segref, A., Wilm, M. and Mattaj, I.W. (2005) Identification of 40LoVe, a Xenopus hnRNP D family protein involved in localizing a TGF-beta-related mRNA during oogenesis. Dev. Cell, 8, 505-515.
31. Zhou, Z., Licklider, L.J., Gygi, S.P. and Reed, R. (2002) Comprehensive proteomic analysis of the human spliceosome. Nature, 419, 182-185.
32. Riley, K.J., Yario, T.A. and Steitz, J.A. (2012) Association of Argonaute proteins and microRNAs can occur after cell lysis. RNA, 18, 1581-1585.
33. Mathonnet, G., Fabian, M.R., Svitkin, Y.V., Parsyan, A., Huck, L., Murata, T., Biffo, S., Merrick, W.C., Darzynkiewicz, E., Pillai, R.S. et al. (2007) MicroRNA inhibition of translation initiation in vitro by targeting the cap-binding complex eIF4F. Science, 317, 1764-1767.
34. Meyer, N. and Penn, L.Z. (2008) Reflecting on 25 years with MYC. Nat. Rev. Cancer, 8, 976-990.
35. Eilers, M. and Eisenman, R.N. (2008) Myc's broad reach. Genes Dev., 22, 2755-2766.
36. Facchini, L.M., Chen, S., Marhin, W.W., Lear, J.N. and Penn, L.Z. (1997) The Myc negative autoregulation mechanism requires Myc-Max association and involves the c-myc P2 minimal promoter. Mol. Cell Biol., 17, 100-114.
37. Liao, J.M. and Lu, H. (2011) Autoregulatory suppression of c-Myc by miR-185-3p. J. Biol. Chem., 286, 33901-33909.
38. Shah, Y.M., Morimura, K., Yang, Q., Tanabe, T., Takagi, M. and Gonzalez, F.J. (2007) Peroxisome proliferator-activated receptor alpha regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Mol. Cell Biol., 27, 4238-4247.
39. Sampson, V.B., Rong, N.H., Han, J., Yang, Q., Aris, V., Soteropoulos, P., Petrelli, N.J., Dunn, S.P. and Krueger, L.J. (2007) MicroRNA let-7a down-regulates MYC and reverts MYC-induced growth in Burkitt lymphoma cells. Cancer Res., 67, 9762-9770.
40. Bueno, M.J., Gomez de Cedron, M., Gomez-Lopez, G., Perez de Castro, I., Di Lisio, L., Montes-Moreno, S., Martinez, N., Guerrero, M., Sanchez-Martinez, R., Santos, J. et al. (2011) Combinatorial effects of microRNAs to suppress the Myc oncogenic pathway. Blood, 117, 6255-6266.
41. Kong, Y.W., Cannell, I.G., de Moor, C.H., Hill, K., Garside, P.G., Hamilton, T.L., Meijer, H.A., Dobbyn, H.C., Stoneley, M., Spriggs, K.A. et al. (2008) The mechanism of micro-RNA-mediated translation repression is determined by the promoter of the target gene. Proc. Natl Acad. Sci. USA, 105, 8866-8871.
42. Takwi, A.A., Li, Y., Becker Buscaglia, L.E., Zhang, J., Choudhury, S., Park, A.K., Liu, M., Young, K.H., Park, W.Y., Martin, R.C. et al. (2012) A statin-regulated microRNA represses human c-Myc expression and function. EMBO Mol. Med., 4, 896-909.
43. Lal, A., Navarro, F., Maher, C.A., Maliszewski, L.E., Yan, N., O'Day, E., Chowdhury, D., Dykxhoorn, D.M., Tsai, P., Hofmann, O. et al. (2009) miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to ''seedless'' 3′ UTR microRNA recognition elements. Mol. Cell, 35, 610-625.
44. Sachdeva, M., Zhu, S., Wu, F., Wu, H., Walia, V., Kumar, S., Elble, R., Watabe, K. and Mo, Y.Y. (2009) p53 represses c-Myc through induction of the tumor suppressor miR-145. Proc. Natl Acad. Sci. USA, 106, 3207-3212.
45. Weidensdorfer, D., Stohr, N., Baude, A., Lederer, M., Kohn, M., Schierhorn, A., Buchmeier, S., Wahle, E. and Huttelmaier, S. (2009) Control of c-myc mRNA stability by IGF2BP1-associated cytoplasmic RNPs. RNA, 15, 104-115.
46. Braun, J., Hoang-Vu, C., Dralle, H. and Huttelmaier, S. (2010) Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas. Oncogene, 29, 4237-4244.
47. Wiznerowicz, M. and Trono, D. (2003) Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J. Virol., 77, 8957-8961.
48. 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.
49. Zhou, Z. and Reed, R. (2003) Purification of functional RNA-protein complexes using MS2-MBP. Curr. Protoc. Mol. Biol., Chapter 27, Unit 27.23.
50. Kohn, M., Lederer, M., Wachter, K. and Huttelmaier, S. (2010) Near-infrared (NIR) dye-labeled RNAs identify binding of ZBP1 to the noncoding Y3-RNA. RNA, 16, 1420-1428.
51. Martin, M. (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J., 17, 1.
52. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
53. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G. and Durbin, R. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics, 25, 2078-2079.
54. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, R80.
55. Morgan, M., Anders, S., Lawrence, M., Aboyoun, P., Pages, H. and Gentleman, R. (2009) ShortRead: a bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics, 25, 2607-2608.
56. Robinson, M.D., McCarthy, D.J. and Smyth, G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
57. Robinson, M.D. and Oshlack, A. (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol., 11, R25.
58. Robinson, M.D. and Smyth, G.K. (2008) Small-sample estimation of negative binomial dispersion, with applications to SAGE data. Biostatistics, 9, 321-332.
59. Kress, T.R., Cannell, I.G., Brenkman, A.B., Samans, B., Gaestel, M., Roepman, P., Burgering, B.M., Bushell, M., Rosenwald, A. and Eilers, M. (2011) The MK5/PRAK kinase and Myc form a negative feedback loop that is disrupted during colorectal tumorigenesis. Mol. Cell, 41, 445-457.
60. Cannell, I.G., Kong, Y.W., Johnston, S.J., Chen, M.L., Collins, H.M., Dobbyn, H.C., Elia, A., Kress, T.R., Dickens, M., Clemens, M.J. et al. (2010) p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc. Natl Acad. Sci. USA, 107, 5375-5380.
61. Kim, H.H., Kuwano, Y., Srikantan, S., Lee, E.K., Martindale, J.L. and Gorospe, M. (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev., 23, 1743-1748.
62. Gregory, P.A., Bert, A.G., Paterson, E.L., Barry, S.C., Tsykin, A., Farshid, G., Vadas, M.A., Khew-Goodall, Y. and Goodall, G.J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol., 10, 593-601.
63. McCarthy, D.J., Chen, Y. and Smyth, G.K. (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res., 40, 4288-4297.
64. Doench, J.G. and Sharp, P.A. (2004) Specificity of microRNA target selection in translational repression. Genes Dev., 18, 504-511.
65. Didiano, D. and Hobert, O. (2008) Molecular architecture of a miRNA-regulated 3′ UTR. RNA, 14, 1297-1317.
66. O'Donnell, K.A., Wentzel, E.A., Zeller, K.I., Dang, C.V. and Mendell, J.T. (2005) c-Myc-regulated microRNAs modulate E2F1 expression. Nature, 435, 839-843.
67. Sylvestre, Y., De Guire, V., Querido, E., Mukhopadhyay, U.K., Bourdeau, V., Major, F., Ferbeyre, G. and Chartrand, P. (2007) An E2F/miR-20a autoregulatory feedback loop. J. Biol. Chem., 282, 2135-2143.