Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation

Genome Research

Volumn 23, Issue 4, 2013, Pages 604-615

  Hausser, Jean ^a   Syed, Afzal Pasha ^a   Bilen, Biter ^a   Zavolan, Mihaela ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE TARGETING; GENETIC CODE; GENETIC TRANSFECTION; GENOMICS; PRIORITY JOURNAL; PROTEIN PROCESSING;

3' UNTRANSLATED REGIONS; ANIMALS; BINDING SITES; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EMBRYONIC DEVELOPMENT; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RNA STABILITY; RNA, MESSENGER; SELECTION, GENETIC;

EID: 84875992976     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.139758.112     Document Type: Article

References (64)

1. Alexiou P, Maragkakis M, Papadopoulos GL, Reczko M, Hatzigeorgiou AG. 2009. Lost in translation: An assessment and perspective for computational microRNA target identification. Bioinformatics 25: 3049-3055.
2. Audic Y, Omilli F, Osborne HB. 1997. Postfertilization deadenylation of mRNAs in Xenopus laevis embryos is sufficient to cause their degradation at the blastula stage. Mol Cell Biol 17: 209-218.
3. Baek D, Villén J, Shin C, Camargo F, Gygi S, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
4. Bagga S, Bracht J, Hunter S, Massirer K, Holtz J, Eachus R, Pasquinelli AE. 2005. Regulation by let-7 and lin-4 miRNAs results in target mRNA degradation. Cell 122: 553-563.
5. Balatti V, Maniero S, Ferracin M, Veronese A, Negrini M, Ferrocci G, Martini F, Tognon MG. 2011. MicroRNAs dysregulation in human malignant pleural mesothelioma. J Thorac Oncol 6: 844-851.
6. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
7. Bazzini AA, Lee MT, Giraldez AJ. 2012. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336: 233-237.
8. Béthune J, Artus-Revel CG, Filipowicz W. 2012. Kinetic analysis reveals successive steps leading to miRNA-mediated silencing in mammalian cells. EMBO Rep 13: 716-723.
9. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, FilipowiczW. 2006. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124.
10. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190.
11. Bushati N, Cohen SM. 2007. microRNA functions. Annu Rev Cell Dev Biol 23: 175-205.
12. Chi SW, Zang JB, Mele A, Darnell RB. 2009. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460: 479-486.
13. David R. 2012. miRNAs' strict schedule. Nat Rev Mol Cell Biol 13: 340-341.
14. Djuranovic S, Nahvi A, Green R. 2012. miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336: 237-240.
15. Eulalio A, Huntzinger E, Izaurralde E. 2008. Getting to the root of miRNAmediated gene silencing. Cell 132: 9-14.
16. Fang Z, Rajewsky N. 2011. The impact of miRNA target sites in coding sequences and in 39UTRs. PLoS ONE 6: e18067.
17. Filipowicz W, Bhattacharyya S, Sonenberg N. 2008. Mechanisms of posttranscriptional regulation by microRNAs: Are the answers in sight? Nat Rev Genet 9: 102-114.
18. Forman JJ, Legesse-Miller A, Coller HA. 2008. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci 105: 14879-14884.
19. Forrest ARR, Kanamori-Katayama M, Tomaru Y, Lassmann T, Ninomiya N, Takahashi Y, de Hoon MJL, Kubosaki A, Kaiho A, Suzuki M, et al. 2010. Induction of microRNAs, mir-155, mir-222, mir-424 and mir-503, promotes monocytic differentiation through combinatorial regulation. Leukemia 24: 460-466.
20. Fulci V, Colombo T, Chiaretti S, MessinaM, Citarella F, Tavolaro S, Guarini A, Foa R, Macino G. 2009. Characterization of B- and T-lineage acute lymphoblastic leukemia by integrated analysis of MicroRNA and mRNA expression profiles. Genes Chromosomes Cancer 48: 1069-1082.
21. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M. 2007. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8: 69.
22. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF. 2006. Zebrafish miR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312: 75-79.
23. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ. 2008. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593-601.
24. Grimson A, Farh K, Johnston W, Garrett-Engele P, Lim LP, Bartel DP. 2007. MicroRNA targeting specificity in mammals: Determinants beyond seed pairing. Mol Cell 27: 91-105.
25. Gu S, Jin L, Zhang F, Sarnow P, Kay M. 2009. Biological basis for restriction of microRNA targets to the 39 untranslated region in mammalian mRNAs. Nat Struct Mol Biol 16: 144-150.
26. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNAlevels. Nature 466: 835-840.
27. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, 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.
28. Hausser J, Landthaler M, Jaskiewicz L, Gaidatzis D, Zavolan M. 2009. Relative contribution of sequence and structure features to the mRNA binding of Argonaute/EIF2C-miRNA complexes and the degradation of miRNA targets. Genome Res 19: 2009-2020.
29. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, et al. 2005. A microRNA polycistron as a potential human oncogene. Nature 435: 828-833.
30. Henrion G, Renard JP, Chesné P, Oudin JF, Maniey D, Brunet A, Osborne HB, Duranthon V. 2000. Differential regulation of the translation and the stability of twomaternal transcripts in preimplantation rabbit embryos. Mol Reprod Dev 56: 12-25.
31. Huang Q, Gumireddy K, Schrier M, le Sage C, Nagel R, Nair S, Egan DA, Li A, Huang G, Klein-Szanto AJ, et al. 2008. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10: 202-210.
32. Huang FWD, Qin J, Reidys CM, Stadler PF. 2010. Target prediction and a statistical sampling algorithm for RNA-RNA interaction. Bioinformatics 26: 175-181.
33. Hurst LD. 2006. Preliminary assessment of the impact of microRNAmediated regulation on coding sequence evolution in mammals. J Mol Evol 63: 174-182.
34. Jones-Rhoades MW, Bartel DP, Bartel B. 2006. MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53.
35. Karginov FV, Conaco C, Xuan Z, Schmidt BH, Parker JS, Mandel G, Hannon GJ. 2007. A biochemical approach to identifying microRNA targets. Proc Natl Acad Sci 104: 19291-19296.
36. Kedde M, Agami R. 2008. Interplay between microRNAs and RNA-binding proteins determines developmental processes. Cell Cycle 7: 899-903.
37. Kedde M, Strasser MJ, Boldajipour B, Oude Vrielink JA, Slanchev K, le Sage C, Nagel R, Voorhoeve PM, van Duijse J, Ørom UA, et al. 2007. RNAbinding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131: 1273-1286.
38. Khorshid M, Rodak C, Zavolan M. 2011. CLIPZ: A database and analysis environment for experimentally determined binding sites of RNA-binding proteins. Nucleic Acids Res 39: D245-D252.
39. Kim HD, Shay T, O'Shea EK, Regev A. 2009. Transcriptional regulatory circuits: Predicting numbers from alphabets. Science 325: 429-432.
40. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M. 2011. A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 8: 559-564.
41. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. 2005. Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
42. Lanet E, Delannoy E, Sormani R, Floris M, Brodersen P, Crété P, Voinnet O, Robaglia C. 2009. Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21: 1762-1768.
43. Lee RC, Feinbaum RL, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
44. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
45. Linsley P, Schelter JM, Burchard J, Kibukawa M, Martin M, Bartz S, Johnson J, Cummins J, Raymond C, Dai H, et al. 2007. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 27: 2240-2252.
46. Lund E, Sheets MD, Imboden SB, Dahlberg JE. 2011. Limiting Ago protein restricts RNAi and microRNA biogenesis during early development in Xenopus laevis. Genes Dev 25: 1121-1131.
47. Mateescu B, Batista L, Cardon M, Gruosso T, de Feraudy Y, Mariani O, Nicolas A, Meyniel J-P, Cottu P, Sastre-Garau X, et al. 2011. miR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat Med 17: 1627-1635.
48. Olive V, Bennett MJ,Walker JC, Ma C, Jiang I, Cordon-Cardo C, Li Q-J, Lowe SW, Hannon GJ, He L, et al. 2009. miR-19 is a key oncogenic component of mir-17-92. Genes Dev 23: 2839-2849.
49. Ott CE, Grünhagen J, Jäger M, Horbelt D, Schwill S, Kallenbach K, Guo G, Manke T, Knaus P, Mundlos S, et al. 2011. MicroRNAs differentially expressed in postnatal aortic development downregulate elastin via 39 UTR and coding-sequence binding sites. PLoS ONE 6: e16250.
50. Qin W, Shi Y, Zhao B, Yao C, Jin L, Ma J, Jin Y. 2010. miR-24 regulates apoptosis by targeting the open reading frame (ORF) region of FAF1 in cancer cells. PLoS ONE 5: e9429.
51. Schnall-Levin M, Zhao Y, Perrimon N, Berger B. 2010. Conserved microRNA targeting in Drosophila is as widespread in coding regions as in 39 UTRs. Proc Natl Acad Sci 107: 15751-15756.
52. Schnall-Levin M, Rissland OS, Johnston W, Perrimon N, Bartel DP, Berger B. 2011. Unusually effective microRNA targeting within repeat-rich coding regions of mammalian mRNAs. Genome Res 21: 1395-1403.
53. Selbach M, Schwanhäusser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. 2008.Widespread changes in protein synthesis induced by microRNAs. Nature 455: 58-63.
54. ShiW, Gerster K, Alajez NM, Tsang J,Waldron L, Pintilie M, Hui AB, Sykes J, P'ng C, Miller N, et al. 2011. MicroRNA-301 mediates proliferation and invasion in human breast cancer. Cancer Res 71: 2926-2937.
55. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
56. Smrt RD, Szulwach KE, Pfeiffer RL, Li X, GuoW, Pathania M, Teng Z-Q, Luo Y, Peng J, Bordey A, et al. 2010. MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 28: 1060-1070.
57. Stadler B, Ivanovska I, Mehta K, Song S, Nelson A, Tan Y, Mathieu J, Darby C, Blau CA,Ware C, et al. 2010. Characterization ofmicroRNAs involved in embryonic stem cell states. Stem Cells Dev 19: 935-950.
58. Sturm M, Hackenberg M, Langenberger D, Frishman D. 2010. TargetSpy: A supervised machine learning approach for microRNA target prediction. BMC Bioinformatics 11: 292.
59. Suh M-R, Lee Y, Kim JY, Kim S-K, Moon S-H, Lee JY, Cha K-Y, Chung HM, Yoon HS, Moon SY, et al. 2004. Human embryonic stem cells express a unique set of microRNAs. Dev Biol 270: 488-498.
60. Sun G, Ye P, Murai K, Lang M-F, Li S, Zhang H, LiW, Fu C, Yin J,Wang A, et al. 2011. miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat Commun 2: 529.
61. Telford NA, Watson AJ, Schultz GA. 1990. Transition from maternal to embryonic control in early mammalian development: A comparison of several species. Mol Reprod Dev 26: 90-100.
62. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, et al. 2008. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132: 875-886.
63. Voorhoeve PM, le Sage C, Schrier M, Gillis AJM, Stoop H, Nagel R, Liu Y-P, van Duijse J, Drost J, Griekspoor A, et al. 2006. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124: 1169-1181.
64. Wightman B, Ha I, Ruvkun G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.