Pairing beyond the Seed Supports MicroRNA Targeting Specificity

Molecular Cell

Volumn 64, Issue 2, 2016, Pages 320-333

  Broughton, James P ^a   Lovci, Michael T ^b   Huang, Jessica L ^a   Yeo, Gene W ^b   Pasquinelli, Amy E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ALG 1; C. elegans; chimeras; iCLIP; microRNA; miRNA family

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; NUCLEOTIDE; ALG-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; HELMINTH RNA; LONG UNTRANSLATED RNA; MESSENGER RNA; PROTEIN BINDING; RNA BINDING PROTEIN; SMALL NUCLEOLAR RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASE PAIRING; BINDING SITE; CAENORHABDITIS ELEGANS; CHIMERA; CONTROLLED STUDY; CROSS LINKING; IMMUNOPRECIPITATION; IN VIVO STUDY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REPORTER GENE; REPRODUCIBILITY; RNA ANALYSIS; RNA SEQUENCE; RNA STABILITY; ANIMAL; CLASSIFICATION; EXON; GENE EXPRESSION REGULATION; GENETICS; INTRON; METABOLISM; NUCLEOTIDE SEQUENCE; PROCEDURES;

ANIMALS; BASE PAIRING; BASE SEQUENCE; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; EXONS; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; INTRONS; MICRORNAS; PROTEIN BINDING; RNA, HELMINTH; RNA, LONG NONCODING; RNA, MESSENGER; RNA, SMALL NUCLEOLAR; RNA-BINDING PROTEINS;

EID: 84991012936     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.09.004     Document Type: Article

References (52)

1. Abbott, A.L., Alvarez-Saavedra, E., Miska, E.A., Lau, N.C., Bartel, D.P., Horvitz, H.R., Ambros, V., The let-7 MicroRNA family members mir-48, mir-84, and mir-241 function together to regulate developmental timing in Caenorhabditis elegans. Dev. Cell 9 (2005), 403–414.
2. Agarwal, V., Bell, G.W., Nam, J.-W., Bartel, D.P., Predicting effective microRNA target sites in mammalian mRNAs. eLife 4 (2015), 1–38.
3. Alvarez-Saavedra, E., Horvitz, H.R., Many families of C. elegans microRNAs are not essential for development or viability. Curr. Biol. 20 (2010), 367–373.
4. Bailey, T.L., Elkan, C., Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2 (1994), 28–36.
5. Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
6. Bosson, A.D., Zamudio, J.R., Sharp, P.A., Endogenous miRNA and target concentrations determine susceptibility to potential ceRNA competition. Mol. Cell 56 (2014), 347–359.
7. Boyerinas, B., Park, S.-M., Hau, A., Murmann, A.E., Peter, M.E., The role of let-7 in cell differentiation and cancer. Endocr. Relat. Cancer 17 (2010), F19–F36.
8. Brennecke, J., Stark, A., Russell, R.B., Cohen, S.M., Principles of microRNA-target recognition. PLoS Biol. 3 (2005), 0404–0418.
9. Broughton, J.P., Pasquinelli, A.E., Identifying Argonaute binding sites in Caenorhabditis elegans using iCLIP. Methods 63 (2013), 119–125.
10. Chandradoss, S.D., Schirle, N.T., Szczepaniak, M., MacRae, I.J., Joo, C., A dynamic search process underlies microRNA targeting. Cell 162 (2015), 96–107.
11. Chi, S.W., Zang, J.B., Mele, A., Darnell, R.B., Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460 (2009), 479–486.
12. 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 (2014), 766–776.
13. Doench, J.G., Sharp, P.A., Specificity of microRNA target selection in translational repression. Genes Dev. 18 (2004), 504–511.
14. Ecsedi, M., Rausch, M., Großhans, H., The let-7 microRNA directs vulval development through a single target. Dev. Cell 32 (2015), 335–344.
15. Eichhorn, S.W., Guo, H., McGeary, S.E., Rodriguez-Mias, R.A., Shin, C., Baek, D., Hsu, S.-H., Ghoshal, K., Villén, J., Bartel, D.P., mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues. Mol. Cell 56 (2014), 104–115.
16. 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 150 (2012), 100–110.
17. Friedman, R.C., Farh, K.K.-H., Burge, C.B., Bartel, D.P., Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19 (2009), 92–105.
18. Grimson, A., Farh, K.K.-H., Johnston, W.K., Garrett-Engele, P., Lim, L.P., Bartel, D.P., MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27 (2007), 91–105.
19. Grosshans, H., Johnson, T., Reinert, K.L., Gerstein, M., Slack, F.J., The temporal patterning microRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev. Cell 8 (2005), 321–330.
20. Grosswendt, S., Filipchyk, A., Manzano, M., Klironomos, F., Schilling, M., Herzog, M., Gottwein, E., Rajewsky, N., Unambiguous identification of miRNA:target site interactions by different types of ligation reactions. Mol. Cell 54 (2014), 1042–1054.
21. Gu, S., Jin, L., Zhang, F., Sarnow, P., Kay, M.A., Biological basis for restriction of microRNA targets to the 3′ untranslated region in mammalian mRNAs. Nat. Struct. Mol. Biol. 16 (2009), 144–150.
22. Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M. Jr., Jungkamp, A.-C., Munschauer, M., et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141 (2010), 129–141.
23. Helwak, A., Kudla, G., Dudnakova, T., Tollervey, D., Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153 (2013), 654–665.
24. Ivanov, A., Memczak, S., Wyler, E., Torti, F., Porath, H.T., Orejuela, M.R., Piechotta, M., Levanon, E.Y., Landthaler, M., Dieterich, C., Rajewsky, N., Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 10 (2015), 170–177.
25. Jo, M.H., Shin, S., Jung, S.-R., Kim, E., Song, J.-J., Hohng, S., Human Argonaute 2 has diverse reaction pathways on target RNAs. Mol. Cell 59 (2015), 117–124.
26. Jovanovic, M., Reiter, L., Picotti, P., Lange, V., Bogan, E., Hurschler, B.A., Blenkiron, C., Lehrbach, N.J., Ding, X.C., Weiss, M., et al. A quantitative targeted proteomics approach to validate predicted microRNA targets in C. elegans. Nat. Methods 7 (2010), 837–842.
27. Kato, M., de Lencastre, A., Pincus, Z., Slack, F.J., Dynamic expression of small non-coding RNAs, including novel microRNAs and piRNAs/21U-RNAs, during Caenorhabditis elegans development. Genome Biol., 10, 2009, R54.
28. Kozomara, A., Griffiths-Jones, S., miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39 (2011), D152–D157.
29. Lewis, B.P., Shih, I.H., Jones-Rhoades, M.W., Bartel, D.P., Burge, C.B., Prediction of mammalian microRNA targets. Cell 115 (2003), 787–798.
30. 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 (2005), 15–20.
31. Lim, L.P., Lau, N.C., Weinstein, E.G., Abdelhakim, A., Yekta, S., Rhoades, M.W., Burge, C.B., Bartel, D.P., The microRNAs of Caenorhabditis elegans. Genes Dev. 17 (2003), 991–1008.
32. Lin, S.Y., Johnson, S.M., Abraham, M., Vella, M.C., Pasquinelli, A., Gamberi, C., Gottlieb, E., Slack, F.J., The C elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev. Cell 4 (2003), 639–650.
33. Lovci, M.T., Ghanem, D., Marr, H., Arnold, J., Gee, S., Parra, M., Liang, T.Y., Stark, T.J., Gehman, L.T., Hoon, S., et al. Rbfox proteins regulate alternative mRNA splicing through evolutionarily conserved RNA bridges. Nat. Struct. Mol. Biol. 20 (2013), 1434–1442.
34. Martinez, N.J., Ow, M.C., Reece-Hoyes, J.S., Barrasa, M.I., Ambros, V.R., Walhout, A.J.M., Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. Genome Res. 18 (2008), 2005–2015.
35. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S.D., Gregersen, L.H., Munschauer, M., et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495 (2013), 333–338.
36. Moore, M.J., Scheel, T.K.H., Luna, J.M., Park, C.Y., Fak, J.J., Nishiuchi, E., Rice, C.M., Darnell, R.B., miRNA-target chimeras reveal miRNA 3′-end pairing as a major determinant of Argonaute target specificity. Nat. Commun., 6, 2015, 8864.
37. Nakanishi, K., Weinberg, D.E., Bartel, D.P., Patel, D.J., Structure of yeast Argonaute with guide RNA. Nature 486 (2012), 368–374.
38. Pasquinelli, A.E., MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 13 (2012), 271–282.
39. Rehmsmeier, M., Steffen, P., Hochsmann, M., Giegerich, R., Fast and effective prediction of microRNA/target duplexes. RNA 10 (2004), 1507–1517.
40. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., Ruvkun, G., The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 (2000), 901–906.
41. Salomon, W.E., Jolly, S.M., Moore, M.J., Zamore, P.D., Serebrov, V., Single-molecule imaging reveals that Argonaute reshapes the binding properties of its nucleic acid guides. Cell 162 (2015), 84–95.
42. Schirle, N.T., MacRae, I.J., The crystal structure of human Argonaute2. Science 336 (2012), 1037–1040.
43. Schirle, N.T., Sheu-Gruttadauria, J., MacRae, I.J., Structural basis for microRNA targeting. Science 346 (2014), 608–613.
44. Schirle, N.T., Sheu-Gruttadauria, J., Chandradoss, S.D., Joo, C., MacRae, I.J., Water-mediated recognition of t1-adenosine anchors Argonaute2 to microRNA targets. eLife 4 (2015), 1–16.
45. Slack, F.J., Basson, M., Liu, Z., Ambros, V., Horvitz, H.R., Ruvkun, G., The lin-41 RBCC gene acts in the C. elegans heterochronic pathway between the let-7 regulatory RNA and the LIN-29 transcription factor. Mol. Cell 5 (2000), 659–669.
46. Sugimoto, Y., König, J., Hussain, S., Zupan, B., Curk, T., Frye, M., Ule, J., Analysis of CLIP and iCLIP methods for nucleotide-resolution studies of protein-RNA interactions. Genome Biol., 13, 2012, R67.
47. Tay, Y., Rinn, J., Pandolfi, P.P., The multilayered complexity of ceRNA crosstalk and competition. Nature 505 (2014), 344–352.
48. Vella, M.C., Choi, E.Y., Lin, S.Y., Reinert, K., Slack, F.J., The C. elegans microRNA let-7 binds to imperfect let-7 complementary sites from the lin-41 3'UTR. Genes Dev. 18 (2004), 132–137.
49. Wee, L.M., Flores-Jasso, C.F., Salomon, W.E., Zamore, P.D., Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Cell 151 (2012), 1055–1067.
50. Westholm, J.O., Miura, P., Olson, S., Shenker, S., Joseph, B., Sanfilippo, P., Celniker, S.E., Graveley, B.R., Lai, E.C., Genome-wide analysis of Drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 9 (2014), 1966–1980.
51. Zhang, H., Artiles, K.L., Fire, A.Z., Functional relevance of “seed” and “non-seed” sequences in microRNA-mediated promotion of C. elegans developmental progression. RNA 21 (2015), 1980–1992.
52. Zisoulis, D.G., Lovci, M.T., Wilbert, M.L., Hutt, K.R., Liang, T.Y., Pasquinelli, A.E., Yeo, G.W., Comprehensive discovery of endogenous Argonaute binding sites in Caenorhabditis elegans. Nat. Struct. Mol. Biol. 17 (2010), 173–179.