Genome-wide identification of translationally inhibited and degraded miR-155 targets using RNA-interacting protein-IP

RNA Biology

Volumn 10, Issue 6, 2013, Pages 1017-1029

  Meier, Jan ^a   Hovestadt, Volker ^a   Zapatka, Marc ^a   Pscherer, Armin ^a,b   Lichter, Peter ^a   Seiffert, Martina ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b BioRN Cluster Management GmbH   (Germany)

Author keywords

AGO2 IP; miR 155; miRNA activity; miRNA target profiling; RIP Seq; Translational inhibition

Indexed keywords

ARGONAUTE 2 PROTEIN; MICRORNA 155; RNA INDUCED SILENCING COMPLEX; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; MESSENGER RNA; MICRORNA; MIRN155 MICRORNA, HUMAN; MIRN17-92 MICRORNA, HUMAN;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE TARGETING; GENETIC ASSOCIATION; GENETIC IDENTIFICATION; IMMUNOPRECIPITATION; INTERACTIONS WITH RNA; MOUSE; NONHUMAN; RNA ANALYSIS; RNA SEQUENCE; CELL CULTURE; CELL CYCLE; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; RNA STABILITY; SEQUENCE ANALYSIS;

ANIMALIA;

ARGONAUTE PROTEINS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MICRORNAS; RNA STABILITY; RNA, MESSENGER; RNA-INDUCED SILENCING COMPLEX; SEQUENCE ANALYSIS, RNA;

EID: 84894524467     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.24553     Document Type: Article

References (47)

1. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116:281-97; PMID:14744438; http://dx.doi.org/10.1016/S0092-8674(04)00045- 5.
2. Izaurralde E. Elucidating the temporal order of silencing. EMBO Rep 2012; 13:662-3; PMID:22722480; http://dx.doi.org/10.1038/embor.2012.91.
3. Béthune J, Artus-Revel CG, Filipowicz W. Kinetic analysis reveals successive steps leading to miRNA-mediated silencing in mammalian cells. EMBO Rep 2012; 13:716-23; PMID:22677978; http://dx.doi.org/10.1038/embor.2012.82.
4. Braun JE, Huntzinger E, Fauser M, Izaurralde E. GW182 proteins directly recruit cytoplasmic deadenylase complexes to miRNA targets. Mol Cell 2011; 44:120-33; PMID:21981923; http://dx.doi.org/10.1016/j.molcel.2011.09.007.
5. Chekulaeva M, Mathys H, Zipprich JT, Attig J, Colic M, Parker R, et al. miRNA repression involves GW182-mediated recruitment of CCR4-NOT through conserved W-containing motifs. Nat Struct Mol Biol 2011; 18:1218-26; PMID:21984184; http://dx.doi.org/10.1038/nsmb.2166.
6. Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 2008; 9:102-14; PMID:18197166; http://dx.doi.org/10.1038/nrg2290.
7. Fabian MR, Cieplak MK, Frank F, Morita M, Green J, Srikumar T, et al. miRNA-mediated deadenylation is orchestrated by GW182 through two conserved motifs that interact with CCR4-NOT. Nat Struct Mol Biol 2012; 19:364; PMID:21984185; http://dx.doi.org/10.1038/nsmb0312-364c.
8. Costinean S, Sandhu SK, Pedersen IM, Tili E, Trotta R, Perrotti D, et al. Src homology 2 domain-containing inositol-5-phosphatase and CCAAT enhancer-binding protein beta are targeted by miR-155 in B cells of Emicro-MiR-155 transgenic mice. Blood 2009; 114:1374-82; PMID:19520806; http://dx.doi.org/10.1182/blood-2009-05-220814.
9. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z, Kohlhaas S, et al. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 2007; 27:847-59; PMID:18055230; http://dx.doi.org/10. 1016/j.immuni.2007.10.009.
10. Wang WX, Wilfred BR, Hu Y, Stromberg AJ, Nelson PT. Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 2010; 16:394-404; PMID:20042474; http://dx.doi.org/10.1261/rna.1905910.
11. Easow G, Teleman AA, Cohen SM. Isolation of microRNA targets by miRNP immunopurification. RNA 2007; 13:1198-204; PMID:17592038; http://dx.doi.org/10. 1261/rna.563707.
12. Goff LA, Davila J, Swerdel MR, Moore JC, Cohen RI, Wu H, et al. Ago2 immunoprecipitation identifies predicted microRNAs in human embryonic stem cells and neural precursors. PLoS One 2009; 4:e7192; PMID:19784364; http://dx.doi.org/10.1371/journal.pone.0007192.
13. Tan LP, Seinen E, Duns G, de Jong D, Sibon OC, Poppema S, et al. A high throughput experimental approach to identify miRNA targets in human cells. Nucleic Acids Res 2009; 37:e137; PMID:19734348; http://dx.doi.org/10.1093/nar/ gkp715.
14. Hoffman AE, Liu R, Fu A, Zheng T, Slack FJ, Zhu Y. Targetome profiling, pathway analysis and genetic association study implicate miR-202 in lymphomagenesis. Cancer Epidemiol Biomarkers Prev 2013; 22:327-36; PMID:23334589; http://dx.doi.org/10.1158/1055-9965.EPI-12-1131-T.
15. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25:1105-11; PMID:19289445; http://dx.doi.org/10.1093/bioinformatics/btp120.
16. Deshpande A, Pastore A, Deshpande AJ, Zimmermann Y, Hutter G, Weinkauf M, et al. 3′UTR mediated regulation of the cyclin D1 proto-oncogene. Cell Cycle 2009; 8:3584-92; PMID:19823025; http://dx.doi.org/10.4161/cc.8.21.9993.
17. Qin X, Wang X, Wang Y, Tang Z, Cui Q, Xi J, et al. MicroRNA-19a mediates the suppressive effect of laminar flow on cyclin D1 expression in human umbilical vein endothelial cells. Proc Natl Acad Sci USA 2010; 107:3240-4; PMID:20133739; http://dx.doi.org/10.1073/pnas.0914882107.
18. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455:58-63; PMID:18668040; http://dx.doi.org/10.1038/nature07228.
19. Gutsch R, Kandemir JD, Pietsch D, Cappello C, Meyer J, Simanowski K, et al. CCAAT/enhancer-binding protein beta inhibits proliferation in monocytic cells by affecting the retinoblastoma protein/E2F/cyclin E pathway but is not directly required for macrophage morphology. J Biol Chem 2011; 286:22716-29; PMID:21558273; http://dx.doi.org/10.1074/jbc.M110.152538.
20. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. The role of site accessibility in microRNA target recognition. Nat Genet 2007; 39:1278-84; PMID:17893677; http://dx.doi.org/10.1038/ng2135.
21. 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 2010; 11:R90; PMID:20799968; http://dx.doi.org/10.1186/gb-2010-11-8- r90.
22. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 2007; 27:91-105; PMID:17612493; http://dx.doi.org/10.1016/j.molcel.2007. 06.017.
23. Maragkakis M, Reczko M, Simossis VA, Alexiou P, Papadopoulos GL, Dalamagas T, et al. DIANA-microT web server: elucidating microRNA functions through target prediction. Nucleic Acids Res 2009; 37(Web Server issue):W273-6; PMID:19406924; http://dx.doi.org/10.1093/nar/gkp292.
24. Maragkakis M, Alexiou P, Papadopoulos GL, Reczko M, Dalamagas T, Giannopoulos G, et al. Accurate microRNA target prediction correlates with protein repression levels. BMC Bioinformatics 2009; 10:295; PMID:19765283; http://dx.doi.org/10.1186/1471-2105-10-295.
25. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120:15-20; PMID:15652477; http://dx.doi.org/10.1016/j.cell.2004.12.035.
26. Xiang X, Zhuang X, Ju S, Zhang S, Jiang H, Mu J, et al. miR-155 promotes macroscopic tumor formation yet inhibits tumor dissemination from mammary fat pads to the lung by preventing EMT. Oncogene 2011; 30:3440-53; PMID:21460854; http://dx.doi.org/10.1038/onc.2011.54.
27. Yin Q, McBride J, Fewell C, Lacey M, Wang X, Lin Z, et al. MicroRNA-155 is an Epstein-Barr virus-induced gene that modulates Epstein-Barr virus-regulated gene expression pathways. J Virol 2008; 82:5295-306; PMID:18367535; http://dx.doi.org/10.1128/JVI.02380-07.
28. Bazzini AA, Lee MT, Giraldez AJ. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 2012; 336:233-7; PMID:22422859; http://dx.doi.org/10.1126/science.1215704.
29. Djuranovic S, Nahvi A, Green R. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 2012; 336:237-40; PMID:22499947; http://dx.doi.org/10.1126/science.1215691.
30. Willimott S, Wagner SD. miR-125b and miR-155 contribute to BCL2 repression and proliferation in response to CD40 ligand (CD154) in human leukemic B-cells. J Biol Chem 2012; 287:2608-17; PMID:22139839; http://dx.doi.org/10.1074/jbc.M111.285718.
31. Jiang S, Zhang HW, Lu MH, He XH, Li Y, Gu H, et al. MicroRNA-155 functions as an OncomiR in breast cancer by targeting the suppressor of cytokine signaling 1 gene. Cancer Res 2010; 70:3119-27; PMID:20354188; http://dx.doi.org/10.1158/0008-5472.CAN-09-4250.
32. Sumazin P, Yang X, Chiu HS, Chung WJ, Iyer A, Llobet-Navas D, et al. An extensive microRNA-mediated network of RNA-RNA interactions regulates established oncogenic pathways in glioblastoma. Cell 2011; 147:370-81; PMID:22000015; http://dx.doi.org/10.1016/j.cell.2011.09.041.
33. Poliseno L, Salmena L, Zhang JW, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010; 465:1033-8; PMID:20577206; http://dx.doi.org/10.1038/ nature09144.
34. Ebert MS, Sharp PA. Emerging roles for natural microRNA sponges. Curr Biol 2010; 20:R858-61; PMID:20937476; http://dx.doi.org/10.1016/j.cub.2010.08. 052.
35. Arvey A, Larsson E, Sander C, Leslie CS, Marks DS. Target mRNA abundance dilutes microRNA and siRNA activity. Mol Syst Biol 2010; 6:363; PMID:20404830; http://dx.doi.org/10.1038/msb.2010.24.
36. Lössner C, Meier J, Warnken U, Rogers MA, Lichter P, Pscherer A, et al. Quantitative proteomics identify novel miR-155 target proteins. PLoS One 2011; 6:e22146; PMID:21799781; http://dx.doi.org/10.1371/journal.pone.0022146.
37. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010; 141:129-41; PMID:20371350; http://dx.doi.org/10. 1016/j.cell.2010.03.009.
38. Loeb GB, Khan AA, Canner D, Hiatt JB, Shendure J, Darnell RB, et al. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell 2012; 48:760-70; PMID:23142080; http://dx.doi.org/10.1016/j. molcel.2012.10.002.
39. Hendrickson DG, Hogan DJ, Herschlag D, Ferrell JE, Brown PO. Systematic identification of mRNAs recruited to argonaute 2 by specific microRNAs and corresponding changes in transcript abundance. PLoS One 2008; 3:e2126; PMID:18461144; http://dx.doi.org/10.1371/journal.pone.0002126.
40. Burroughs AM, Ando Y, de Hoon MJ, Tomaru Y, Suzuki H, Hayashizaki Y, et al. Deep-sequencing of human Argonaute-associated small RNAs provides insight into miRNA sorting and reveals Argonaute association with RNA fragments of diverse origin. RNA Biol 2011; 8:158-77; PMID:21282978; http://dx.doi.org/10. 4161/rna.8.1.14300.
41. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G. microRNAs associated with the different human Argonaute proteins. Nucleic Acids Res 2012; 40:9850-62; PMID:22844086; http://dx.doi.org/10.1093/nar/gks705.
42. Mullokandov G, Baccarini A, Ruzo A, Jayaprakash AD, Tung N, Israelow B, et al. High-throughput assessment of microRNA activity and function using microRNA sensor and decoy libraries. Nat Methods 2012; 9:840-6; PMID:22751203; http://dx.doi.org/10.1038/nmeth.2078.
43. Schulz A, Toedt G, Zenz T, Stilgenbauer S, Lichter P, Seiffert M. Inflammatory cytokines and signaling pathways are associated with survival of primary chronic lymphocytic leukemia cells in vitro: a dominant role of CCL2. Haematologica 2011; 96:408-16; PMID:21134984; http://dx.doi.org/10.3324/ haematol.2010.031377.
44. Dyer BW, Ferrer FA, Klinedinst DK, Rodriguez R. A noncommercial dual luciferase enzyme assay system for reporter gene analysis. Anal Biochem 2000; 282:158-61; PMID:10860516; http://dx.doi.org/10.1006/abio.2000.4605.
45. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol 2010; 11:R106; PMID:20979621; http://dx.doi.org/10.1186/gb- 2010-11-10-r106.
46. Gottwein E, Mukherjee N, Sachse C, Frenzel C, Majoros WH, Chi JT, et al. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007; 450:1096-9; PMID:18075594; http://dx.doi.org/10.1038/nature05992.
47. Gibcus JH, Tan LP, Harms G, Schakel RN, de Jong D, Blokzijl T, et al. Hodgkin lymphoma cell lines are characterized by a specific miRNA expression profile. Neoplasia 2009; 11:167-76; PMID:19177201.