miR-CLIP capture of a miRNA targetome uncovers a lincRNA H19–miR-106a interaction

Bartel, D.P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215–233 (2009).

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 120, 15–20 (2005).

Flynt, A.S. & Lai, E.C. Biological principles of microRNA-mediated regulation: shared themes amid diversity. Nat. Rev. Genet. 9, 831–842 (2008).

Chekulaeva, M. et al. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat. Struct. Mol. Biol. 18, 1218–1226 (2011).

Fabian, M.R. et al. miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat. Struct. Mol. Biol. 18, 1211–1217 (2011).

Braun, J.E., Huntzinger, E., Fauser, M. & Izaurralde, E. GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol. Cell 44, 120–133 (2011).

Chi, S.W., Hannon, G.J. & Darnell, R.B. An alternative mode of microRNA target recognition. Nat. Struct. Mol. Biol. 19, 321–327 (2012).

Chi, S.W., Zang, J.B., Mele, A. & Darnell, R.B. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460, 479–486 (2009).

Xia, Z. et al. Molecular dynamics simulations of Ago silencing complexes reveal a large repertoire of admissible 'seed-less' targets. Sci Rep 2, 569 (2012); erratum 2, 909 (2012).

Helwak, A., Kudla, G., Dudnakova, T. & Tollervey, D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153, 654–665 (2013).

Hafner, M. et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129–141 (2010).

Beitzinger, M., Peters, L., Zhu, J.Y., Kremmer, E. & Meister, G. Identification of human microRNA targets from isolated argonaute protein complexes. RNA Biol. 4, 76–84 (2007).

Ørom, U.A., Nielsen, F.C. & Lund, A.H. MicroRNA-10a binds the 5′UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30, 460–471 (2008).

Lal, A. et al. Capture of microRNA-bound mRNAs identifies the tumor suppressor miR-34a as a regulator of growth factor signaling. PLoS Genet. 7, e1002363 (2011).

Guo, Y.E. & Steitz, J.A. 3′-Biotin-tagged microRNA-27 does not associate with Argonaute proteins in cells. RNA 20, 985–988 (2014).

Thomas, M., Lieberman, J. & Lal, A. Desperately seeking microRNA targets. Nat. Struct. Mol. Biol. 17, 1169–1174 (2010).

Nonne, N., Ameyar-Zazoua, M., Souidi, M. & Harel-Bellan, A. Tandem affinity purification of miRNA target mRNAs (TAP-Tar). Nucleic Acids Res. 38, e20 (2010).

Baigude, H., Ahsanullah, Li, Z., Zhou, Y. & Rana, T.M. miR-TRAP: a benchtop chemical biology strategy to identify microRNA targets. Angew. Chem. Int. Edn Engl. 51, 5880–5883 (2012).

Grosswendt, S. et al. Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Mol. Cell 54, 1042–1054 (2014).

He, L. et al. A microRNA polycistron as a potential human oncogene. Nature 435, 828–833 (2005).

Brannan, C.I., Dees, E.C., Ingram, R.S. & Tilghman, S.M. The product of the H19 gene may function as an RNA. Mol. Cell. Biol. 10, 28–36 (1990).

Li, Y.M. et al. The H19 transcript is associated with polysomes and may regulate IGF2 expression in trans. J. Biol. Chem. 273, 28247–28252 (1998).

Bartolomei, M.S., Zemel, S. & Tilghman, S.M. Parental imprinting of the mouse H19 gene. Nature 351, 153–155 (1991).

Gabory, A., Jammes, H. & Dandolo, L. The H19 locus: role of an imprinted non-coding RNA in growth and development. Bioessays 32, 473–480 (2010).

Gibb, E.A., Brown, C.J. & Lam, W.L. The functional role of long non-coding RNA in human carcinomas. Mol. Cancer 10, 38 (2011).

Higuchi, M., Kobori, A., Yamayoshi, A. & Murakami, A. Synthesis of antisense oligonucleotides containing 2′-O-psoralenylmethoxyalkyl adenosine for photodynamic regulation of point mutations in RNA. Bioorg. Med. Chem. 17, 475–483 (2009).

Guennewig, B. et al. Synthetic pre-microRNAs reveal dual-strand activity of miR-34a on TNF-α. RNA 20, 61–75 (2014).

Gibcus, J.H. et al. MiR-17/106b seed family regulates p21 in Hodgkin's lymphoma. J. Pathol. 225, 609–617 (2011).

Jiang, Y. et al. miR-106a–mediated malignant transformation of cells induced by anti-benzo[a]pyrene-trans-7,8-diol-9,10-epoxide. Toxicol. Sci. 119, 50–60 (2011).

Beitzinger, M. & Meister, G. Experimental identification of microRNA targets by immunoprecipitation of Argonaute protein complexes. Methods Mol. Biol. 732, 153–167 (2011).

Khorshid, M., Rodak, C. & Zavolan, M. CLIPZ: a database and analysis environment for experimentally determined binding sites of RNA-binding proteins. Nucleic Acids Res. 39, D245–D252 (2011).

Khorshid, M., Hausser, J., Zavolan, M. & van Nimwegen, E. A biophysical miRNA-mRNA interaction model infers canonical and noncanonical targets. Nat. Methods 10, 253–255 (2013).

Coley, W. et al. Absence of DICER in monocytes and its regulation by HIV-1. J. Biol. Chem. 285, 31930–31943 (2010).

Poliseno, L. et al. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465, 1033–1038 (2010).

Cesana, M. et al. A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147, 358–369 (2011).

Hansen, T.B. et al. Natural RNA circles function as efficient microRNA sponges. Nature 495, 384–388 (2013).

Memczak, S. et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333–338 (2013).

Weinmann, L. et al. Importin 8 is a gene silencing factor that targets argonaute proteins to distinct mRNAs. Cell 136, 496–507 (2009).

Jeggari, A., Marks, D.S. & Larsson, E. miRcode: a map of putative microRNA target sites in the long non-coding transcriptome. Bioinformatics 28, 2062–2063 (2012).

Kallen & Amanda, N. et al. The imprinted H19 LncRNA antagonizes Let-7 microRNAs. Mol. Cell 52, 101–121 (2013).

Shimakami, T. et al. Stabilization of hepatitis C virus RNA by an Ago2–miR-122 complex. Proc. Natl. Acad. Sci. USA 109, 941–946 (2012).

Wang, Y. et al. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev. Cell 25, 69–80 (2013).

Nielsen, F.C., Nielsen, J. & Christiansen, J. A family of IGF-II mRNA binding proteins (IMP) involved in RNA trafficking. Scand. J. Clin. Lab. Invest. Suppl. 234, 93–99 (2001).

Weinlich, S. et al. IGF2BP1 enhances HCV IRES-mediated translation initiation via the 3′UTR. RNA 15, 1528–1542 (2009).

Salmena, L., Poliseno, L., Tay, Y., Kats, L. & Pandolfi, P.P. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell 146, 353–358 (2011).

Denzler, R., Agarwal, V., Stefano, J., Bartel, D.P. & Stoffel, M. Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance. Mol. Cell 54, 766–776 (2014).

Milligan, L. et al. H19 gene expression is up-regulated exclusively by stabilization of the RNA during muscle cell differentiation. Oncogene 19, 5810–5816 (2000).

Dey, B.K., Gagan, J., Yan, Z. & Dutta, A. miR-26a is required for skeletal muscle differentiation and regeneration in mice. Genes Dev. 26, 2180–2191 (2012).

Hausser, J. & Zavolan, M. Identification and consequences of miRNA-target interactions—beyond repression of gene expression. Nat. Rev. Genet. 15, 599–612 (2014).

Hassan, T. et al. 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 (2013).

Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).

Friedman, R.C., Farh, K.K., Burge, C.B. & Bartel, D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92–105 (2009).

Gaidatzis, D., van Nimwegen, E., Hausser, J. & Zavolan, M. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8, 69 (2007).

Betel, D., Koppal, A., Agius, P., Sander, C. & Leslie, C. Comprehensive modeling of microRNA targets predicts functional non-conserved and non-canonical sites. Genome Biol. 11, R90 (2010).

Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U. & Segal, E. The role of site accessibility in microRNA target recognition. Nat. Genet. 39, 1278–1284 (2007).

Miranda, K.C. et al. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203–1217 (2006).

Garcia, D.M. et al. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat. Struct. Mol. Biol. 18, 1139–1146 (2011).