Seq and CLIP through the miRNA world

Genome Biology

Volumn 15, Issue 1, 2014, Pages

  Mittal, Nitish ^a   Zavolan, Mihaela ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; MICRORNA; SMALL NUCLEOLAR RNA; UNTRANSLATED RNA;

CAENORHABDITIS ELEGANS; CROSS LINKING; CROSSLINKING IMMUNOPRECIPITATION; GENE CONTROL; GENE IDENTIFICATION; HIGH THROUGHPUT SEQUENCING; IMMUNOPRECIPITATION; NONHUMAN; PHOTOACTIVATABLE RIBONUCLEOSIDE ENHANCED CROSSLINKING AND IMMUNOPRECIPITATION; PROTEIN CLEAVAGE; PROTEIN RNA BINDING; QUANTITATIVE ANALYSIS; REVIEW; RNA SEQUENCE; STRESS; ANIMAL; BINDING SITE; GENETICS; HUMAN; METABOLISM; PROCEDURES; SEQUENCE ANALYSIS;

ANIMALS; ARGONAUTE PROTEINS; BINDING SITES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOPRECIPITATION; MICRORNAS; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, RNA;

EID: 84892892266     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb4151     Document Type: Review

References (91)

1. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233. 3794896, 19167326.
2. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet 2011, 12:99-110.
3. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
4. Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
5. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403:901-906.
6. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 2000, 408:86-89.
7. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39(Database issue):D152-D157. 3013655, 21037258.
8. Nicholson AW. Ribonuclease III mechanisms of double-stranded RNA cleavage. Wiley Interdiscip Rev RNA 2014, 5:31-48.
9. Kim VN. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005, 6:376-385.
10. Okamura K, Hagen JW, Duan H, Tyler DM, Lai EC. The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 2007, 130:89-100. 2729315, 17599402.
11. Cheloufi S, Dos Santos CO, Chong MMW, Hannon GJ. A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465:584-589. 2995450, 20424607.
12. Ha I, Wightman B, Ruvkun G. A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. Genes Dev 1996, 10:3041-3050.
13. Vella MC, Reinert K, Slack FJ. Architecture of a validated microRNA: target interaction. Chem Biol 2004, 11:1619-1623.
14. Shin C, Nam J-W, Farh KK-H, Chiang HR, Shkumatava A, Bartel DP. Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell 2010, 38:789-802. 2942757, 20620952.
15. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, O'Day E, Chowdhury D, Dykxhoorn DM, Tsai P, Hofmann O, Becker KG, Gorospe M, Hide W, Lieberman J. 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 2009, 35:610-625. 2757794, 19748357.
16. Chi SW, Hannon GJ, Darnell RB. An alternative mode of microRNA target recognition. Nat Struct Mol Biol 2012, 19:321-327. 3541676, 22343717.
17. 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.
18. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 2007, 8:69. 1838429, 17331257.
19. Khorshid M, Hausser J, Zavolan M, van Nimwegen E. A biophysical miRNA-mRNA interaction model infers canonical and noncanonical targets. Nat Methods 2013, 10:253-255.
20. Joshua-Tor L, Hannon GJ. Ancestral roles of small RNAs: an Ago-centric perspective. Cold Spring Harb Perspect Biol 2011, 3:a003772. 3179341, 20810548.
21. Dueck A, Ziegler C, Eichner A, Berezikov E, Meister G. MicroRNAs associated with the different human Argonaute proteins. Nucleic Acids Res 2012, 40:9850-9862. 3479175, 22844086.
22. Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
23. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol 2002, 12:735-739.
24. Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T. New microRNAs from mouse and human. RNA 2003, 9:175-179. 1370382, 12554859.
25. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju J, Sheridan R, Sander C, Zavolan M, Tuschl T. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006, 442:203-207.
26. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006, 442:199-202.
27. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, Kingston RE. Characterization of the piRNA complex from rat testes. Science 2006, 313:363-367.
28. Hafner M, Landgraf P, Ludwig J, Rice A, Ojo T, Lin C, Holoch D, Lim C, Tuschl T. Identification of microRNAs and other small regulatory RNAs using cDNA library sequencing. Methods 2008, 44:3-12. 2847350, 18158127.
29. Ender C, Krek A, Friedländer MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G. A human snoRNA with microRNA-like functions. Mol Cell 2008, 32:519-528.
30. Burroughs AM, Ando Y, de Hoon MJL, Tomaru Y, Suzuki H, Hayashizaki Y, Daub CO. 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, 8:158-177. 3127082, 21282978.
31. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB. CLIP identifies Nova-regulated RNA networks in the brain. Science 2003, 302:1212-1215.
32. Chi SW, Zang JB, Mele A, Darnell RB. Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 2009, 460:479-486. 2733940, 19536157.
33. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp A-C, Munschauer M, Ulrich A, Wardle GS, Dewell S, Zavolan M, Tuschl T. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141. 2861495, 20371350.
34. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M. A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 2011, 8:559-564.
35. Ascano M, Hafner M, Cekan P, Gerstberger S, Tuschl T. Identification of RNA-protein interaction networks using PAR-CLIP. Wiley Interdiscip Rev RNA 2011, 3:159-177. 3711140, 22213601.
36. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J. iCLIP - transcriptome-wide mapping of protein-RNA interactions with individual nucleotide resolution. J Vis Exp 2011, 2638.
37. Broughton JP, Pasquinelli AE. Identifying Argonaute binding sites in Caenorhabditis elegans using iCLIP. Methods 2013, 63:119-125.
38. Jungkamp A-C, Stoeckius M, Mecenas D, Grün D, Mastrobuoni G, Kempa S, Rajewsky N. In vivo and transcriptome-wide identification of RNA binding protein target sites. Mol Cell 2011, 44:828-840. 3253457, 22152485.
39. Burger K, Mühl B, Kellner M, Rohrmoser M, Gruber-Eber A, Windhager L, Friedel CC, Dölken L, Eick D. 4-Thiouridine inhibits rRNA synthesis and causes a nucleolar stress response. RNA Biol 2013, 10:1623-1630.
40. 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 2012, 13:R67.
41. Zhang C, Darnell RB. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 2011, 29:607-614. 3400429, 21633356.
42. Helwak A, Kudla G, Dudnakova T, Tollervey D. Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 2013, 153:654-665. 3650559, 23622248.
43. Kudla G, Granneman S, Hahn D, Beggs JD, Tollervey D. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc Natl Acad Sci U S A 2011, 108:10010-10015. 3116431, 21610164.
44. Lewis BP, Shih I-H, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003, 115:787-798.
45. Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS. MicroRNA targets in Drosophila. Genome Biol 2003, 5:R1. 395733, 14709173.
46. Rajewsky N, Socci ND. Computational identification of microRNA targets. Dev Biol 2004, 267:529-535.
47. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
48. Brennecke J, Stark A, Russell RB, Cohen SM. Principles of microRNA - target recognition. PLoS Biol 2005, 3:e85. 1043860, 15723116.
49. Friedman RC, Farh KK-H, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009, 19:92-105. 2612969, 18955434.
50. Loeb GB, Khan AA, Canner D, Hiatt JB, Shendure J, Darnell RB, Leslie CS, Rudensky AY. Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol Cell 2012, 48:760-770. 3562697, 23142080.
51. Wee LM, Flores-Jasso CF, Salomon WE, Zamore PD. Argonaute divides its RNA guide into domains with distinct functions and RNA-binding properties. Cell 2012, 151:1055-1067. 3595543, 23178124.
52. Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V. Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS One 2013, 8:e53823. 3566149, 23405074.
53. Li J-H, Liu S, Zhou H, Qu L-H, Yang J-H. starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein-RNA interaction networks from large-scale CLIP-Seq data. Nucleic Acids Res 2013, 10.1093/nar/gkt1248.
54. Ebert MS, Neilson JR, Sharp PA. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat Methods 2007, 4:721-726. 3857099, 17694064.
55. Cazalla D, Yario T, Steitz JA, Steitz J. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 2010, 328:1563-1566. 3075239, 20558719.
56. Marcinowski L, Tanguy M, Krmpotic A, Rädle B, Lisnić VJ, Tuddenham L, Chane-Woon-Ming B, Ruzsics Z, Erhard F, Benkartek C, Babic M, Zimmer R, Trgovcich J, Koszinowski UH, Jonjic S, Pfeffer S, Dölken L. Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog 2012, 8:e1002510. 3276556, 22346748.
57. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 2010, 465:1033-1038. 3206313, 20577206.
58. Ebert MS, Sharp PA. Emerging roles for natural microRNA sponges. Curr Biol 2010, 20:R858-R861.
59. Kallen AN, Zhou X-B, Xu J, Qiao C, Ma J, Yan L, Lu L, Liu C, Yi J-S, Zhang H, Min W, Bennett AM, Gregory RI, Ding Y, Huang Y. The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol Cell 2013, 52:101-112.
60. Wang Y, Xu Z, Jiang J, Xu C, Kang J, Xiao L, Wu M, Xiong J, Guo X, Liu H. Endogenous miRNA sponge lincRNA-RoR regulates Oct4, Nanog, and Sox2 in human embryonic stem cell self-renewal. Dev Cell 2013, 25:69-80.
61. Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, Kinzler KW, Vogelstein B. Scrambled exons. Cell 1991, 64:607-613.
62. Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993, 73:1019-1030.
63. Cocquerelle C, Mascrez B, Hétuin D, Bailleul B. Mis-splicing yields circular RNA molecules. FASEB J 1993, 7:155-160.
64. Zaphiropoulos PG. Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc Natl Acad Sci U S A 1996, 93:6536-6541. 39059, 8692851.
65. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One 2012, 7:e30733. 3270023, 22319583.
66. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet 2013, 9:e1003777. 3764148, 24039610.
67. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013, 19:141-157. 3543092, 23249747.
68. Zhang Y, Zhang X-O, Chen T, Xiang J-F, Yin Q-F, Xing Y-H, Zhu S, Yang L, Chen L-L. Circular intronic long noncoding RNAs. Mol Cell 2013, 51:792-806.
69. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, le Noble F, Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013, 495:333-338.
70. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Natural RNA circles function as efficient microRNA sponges. Nature 2013, 495:384-388.
71. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu A-L, Zhao Y, McDonald H, Zeng T, Hirst M, Eaves CJ, Marra MA. Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 2008, 18:610-621. 2279248, 18285502.
72. Taft RJ, Glazov EA, Lassmann T, Hayashizaki Y, Carninci P, Mattick JS. Small RNAs derived from snoRNAs. RNA 2009, 15:1233-1240. 2704076, 19474147.
73. Kuchenbauer F, Morin RD, Argiropoulos B, Petriv OI, Griffith M, Heuser M, Yung E, Piper J, Delaney A, Prabhu A-L, Zhao Y, McDonald H, Zeng T, Hirst M, Hansen CL, Marra MA, Humphries RK. In-depth characterization of the microRNA transcriptome in a leukemia progression model. Genome Res 2008, 18:1787-1797. 2577858, 18849523.
74. Taft RJ, Simons C, Nahkuri S, Oey H, Korbie DJ, Mercer TR, Holst J, Ritchie W, Wong JJ-L, Rasko JEJ, Rokhsar DS, Degnan BM, Mattick JS. Nuclear-localized tiny RNAs are associated with transcription initiation and splice sites in metazoans. Nat Struct Mol Biol 2010, 17:1030-1034.
75. Karginov F, Hannon G. Remodeling of Ago2-mRNA interactions upon cellular stress reflects miRNA complementarity and correlates with altered translation rates. Genes Dev 2013, 27:1624-1632. 3731550, 23824327.
76. Starega-Roslan J, Krol J, Koscianska E, Kozlowski P, Szlachcic WJ, Sobczak K, Krzyzosiak WJ. Structural basis of microRNA length variety. Nucleic Acids Res 2011, 39:257-268. 3017592, 20739353.
77. Liu N, Abe M, Sabin LR, Hendriks G-J, Naqvi AS, Yu Z, Cherry S, Bonini NM. The exoribonuclease Nibbler controls 3' end processing of microRNAs in Drosophila. Curr Biol 2011, 21:1888-1893. 3255556, 22055292.
78. Xue Z, Yuan H, Guo J, Liu Y. Reconstitution of an Argonaute-dependent small RNA biogenesis pathway reveals a handover mechanism involving the RNA exosome and the exonuclease QIP. Mol Cell 2012, 46:299-310. 3351553, 22516970.
79. Lee HY, Doudna JA. TRBP alters human precursor microRNA processing in vitro. RNA 2012, 18:2012-2019. 3479391, 23006623.
80. Fukunaga R, Han BW, Hung J-H, Xu J, Weng Z, Zamore PD. Dicer partner proteins tune the length of mature miRNAs in flies and mammals. Cell 2012, 151:533-546. 3609031, 23063653.
81. Cloonan N, Wani S, Xu Q, Gu J, Lea K, Heater S, Barbacioru C, Steptoe AL, Martin HC, Nourbakhsh E, Krishnan K, Gardiner B, Wang X, Nones K, Steen JA, Matigian NA, Wood DL, Kassahn KS, Waddell N, Shepherd J, Lee C, Ichikawa J, McKernan K, Bramlett K, Kuersten S, Grimmond SM. MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol 2011, 12:R126. 3334621, 22208850.
82. Wyman SK, Knouf EC, Parkin RK, Fritz BR, Lin DW, Dennis LM, Krouse MA, Webster PJ, Tewari M. Post-transcriptional generation of miRNA variants by multiple nucleotidyl transferases contributes to miRNA transcriptome complexity. Genome Res 2011, 21:1450-1461. 3166830, 21813625.
83. Knouf EC, Wyman SK, Tewari M. The human TUT1 nucleotidyl transferase as a global regulator of microRNA abundance. PLoS One 2013, 8:e69630. 3715485, 23874977.
84. Kishore S, Gruber AR, Jedlinski DJ, Syed AP, Jorjani H, Zavolan M. Insights into snoRNA biogenesis and processing from PAR-CLIP of snoRNA core proteins and small RNA sequencing. Genome Biol 2013, 14:R45.
85. Maute RL, Schneider C, Sumazin P, Holmes A, Califano A, Basso K, Dalla-Favera R. tRNA-derived microRNA modulates proliferation and the DNA damage response and is down-regulated in B cell lymphoma. Proc Natl Acad Sci U S A 2013, 110:1404-1409. 3557069, 23297232.
86. Cole C, Sobala A, Lu C, Thatcher SR, Bowman A, Brown JWS, Green PJ, Barton GJ, Hutvagner G. Filtering of deep sequencing data reveals the existence of abundant Dicer-dependent small RNAs derived from tRNAs. RNA 2009, 15:2147-2160. 2779667, 19850906.
87. Li Z, Ender C, Meister G, Moore PS, Chang Y, John B. Extensive terminal and asymmetric processing of small RNAs from rRNAs, snoRNAs, snRNAs, and tRNAs. Nucleic Acids Res 2012, 40:6787-6799. 3413118, 22492706.
88. Yamasaki S, Ivanov P, Hu G-F, Anderson P. Angiogenin cleaves tRNA and promotes stress-induced translational repression. J Cell Biol 2009, 185:35-42. 2700517, 19332886.
89. Lee YS, Shibata Y, Malhotra A, Dutta A. A novel class of small RNAs: tRNA-derived RNA fragments (tRFs). Genes Dev 2009, 23:2639-2649. 2779758, 19933153.
90. Macias S, Plass M, Stajuda A, Michlewski G, Eyras E, Cáceres JF. DGCR8 HITS-CLIP reveals novel functions for the microprocessor. Nat Struct Mol Biol 2012, 19:760-766. 3442229, 22796965.
91. Knuckles P, Vogt MA, Lugert S, Milo M, Chong MMW, Hautbergue GM, Wilson SA, Littman DR, Taylor V. Drosha regulates neurogenesis by controlling neurogenin 2 expression independent of microRNAs. Nat Neurosci 2012, 15:962-969.