RNase-mediated protein footprint sequencing reveals protein-binding sites throughout the human transcriptome

Genome Biology

Volumn 15, Issue 1, 2014, Pages

  Silverman, Ian M ^a   Li, Fan ^a   Alexander, Anissa ^a   Goff, Loyal ^b,c   Trapnell, Cole ^b,c   Rinn, John L ^b,c,d   Gregory, Brian D ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Harvard University   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE; RNA BINDING PROTEIN; TRANSCRIPTOME; FORMALDEHYDE; MESSENGER RNA; PROTEINASE K;

ARTICLE; BINDING SITE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; PROTEIN CROSS LINKING; PROTEIN FOOTPRINTING; PROTEIN INTERACTION PROFILE SEQUENCING; PROTEIN MOTIF; PROTEIN RNA BINDING; SEQUENCE ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING AND IMMUNOPRECIPITATION SEQUENCING; EXON; GENE ONTOLOGY; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC PROCEDURES; GLOBAL PHOTOACTIVATABLE RIBONUCLEOSIDE CROSS LINKING AND IMMUNOPRECIPITATION; HELA CELL LINE; INTRON; PHOTOACTIVATABLE RIBONUCLEOSIDE CROSS LINKING AND IMMUNOPRECIPITATION; PROTEIN BINDING SITE DENSITY; PROTEIN PROTECTED SITE; REPRODUCIBILITY; RNA ANALYSIS; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; ULTRAVIOLET RADIATION; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; PROCEDURES;

BINDING SITES; GENETIC ASSOCIATION STUDIES; HELA CELLS; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN FOOTPRINTING; RIBONUCLEASES; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84891697468     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-1-r3     Document Type: Article

References (47)

1. Ascano M, Hafner M, Cekan P, Gerstberger S, Tuschl T. Identification of RNA-protein interaction networks using PAR-CLIP. Wiley Interdiscip Rev RNA 2012, 3:159-177. 10.1002/wrna.1103, 3711140, 22213601.
2. Keene JD. Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc Natl Acad Sci U S A 2001, 98:7018-7024. 10.1073/pnas.111145598, 34616, 11416181.
3. Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 2007, 8:533-543. 10.1038/nrg2111, 17572691.
4. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 2007, 129:1311-1323. 10.1016/j.cell.2007.05.022, 2084369, 17604720.
5. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 2011, 477:295-300. 10.1038/nature10398, 3175327, 21874018.
6. Dreyfuss G, Matunis MJ, Pinol-Roma S, Burd CG. hnRNP proteins and the biogenesis of mRNA. Annu Rev Biochem 1993, 62:289-321. 10.1146/annurev.bi.62.070193.001445, 8352591.
7. Glisovic T, Bachorik JL, Yong J, Dreyfuss G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 2008, 582:1977-1986. 10.1016/j.febslet.2008.03.004, 2858862, 18342629.
8. Cooper TA, Wan L, Dreyfuss G. RNA and disease. Cell 2009, 136:777-793. 10.1016/j.cell.2009.02.011, 2866189, 19239895.
9. Hogan DJ, Riordan DP, Gerber AP, Herschlag D, Brown PO. Diverse RNA-binding proteins interact with functionally related sets of RNAs, suggesting an extensive regulatory system. PLoS Biol 2008, 6:e255. 10.1371/journal.pbio.0060255, 2573929, 18959479.
10. Keene JD, Tenenbaum SA. Eukaryotic mRNPs may represent posttranscriptional operons. Mol Cell 2002, 9:1161-1167. 10.1016/S1097-2765(02)00559-2, 12086614.
11. Aerts S. Computational strategies for the genome-wide identification of cis-regulatory elements and transcriptional targets. Curr Top Dev Biol 2012, 98:121-145.
12. Konig J, Zarnack K, Luscombe NM, Ule J. Protein-RNA interactions: new genomic technologies and perspectives. Nat Rev Genet 2011, 13:77-83.
13. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 2011, 146:247-261. 10.1016/j.cell.2011.06.013, 3232425, 21784246.
14. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jungkamp AC, 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. 10.1016/j.cell.2010.03.009, 2861495, 20371350.
15. Hoell JI, Larsson E, Runge S, Nusbaum JD, Duggimpudi S, Farazi TA, Hafner M, Borkhardt A, Sander C, Tuschl T. RNA targets of wild-type and mutant FET family proteins. Nat Struct Mol Biol 2011, 18:1428-1431. 10.1038/nsmb.2163, 3230689, 22081015.
16. Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, Yan BY, Donohue JP, Shiue L, Hoon S, Brenner S, Ares M, Yeo GW. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Rep 2012, 1:167-178. 10.1016/j.celrep.2012.02.001, 3345519, 22574288.
17. Konig J, Zarnack K, Rot G, Curk T, Kayikci M, Zupan B, Turner DJ, Luscombe NM, Ule J. iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution. Nat Struct Mol Biol 2010, 17:909-915. 10.1038/nsmb.1838, 3000544, 20601959.
18. Lebedeva S, Jens M, Theil K, Schwanhausser B, Selbach M, Landthaler M, Rajewsky N. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 2011, 43:340-352. 10.1016/j.molcel.2011.06.008, 21723171.
19. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M, Tuschl T, Ohler U, Keene JD. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 2011, 43:327-339. 10.1016/j.molcel.2011.06.007, 3220597, 21723170.
20. Sanford JR, Wang X, Mort M, Vanduyn N, Cooper DN, Mooney SD, Edenberg HJ, Liu Y. Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res 2009, 19:381-394. 2661799, 19116412.
21. Xue Y, Zhou Y, Wu T, Zhu T, Ji X, Kwon YS, Zhang C, Yeo G, Black DL, Sun H, Fu XD, Zhang Y. Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol Cell 2009, 36:996-1006. 10.1016/j.molcel.2009.12.003, 2807993, 20064465.
22. Wang Z, Kayikci M, Briese M, Zarnack K, Luscombe NM, Rot G, Zupan B, Curk T, Ule J. iCLIP predicts the dual splicing effects of TIA-RNA interactions. PLoS Biol 2010, 8:e1000530. 10.1371/journal.pbio.1000530, 2964331, 21048981.
23. Macias S, Plass M, Stajuda A, Michlewski G, Eyras E, Caceres JF. DGCR8 HITS-CLIP reveals novel functions for the microprocessor. Nat Struct Mol Biol 2012, 19:760-766. 10.1038/nsmb.2344, 3442229, 22796965.
24. Wilbert ML, Huelga SC, Kapeli K, Stark TJ, Liang TY, Chen SX, Yan BY, Nathanson JL, Hutt KR, Lovci MT, Kazan H, Vu AQ, Massirer KB, Morris Q, Hoon S, Yeo GW. LIN28 binds messenger RNAs at GGAGA motifs and regulates splicing factor abundance. Mol Cell 2012, 48:195-206. 10.1016/j.molcel.2012.08.004, 3483422, 22959275.
25. 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. 10.1038/nmeth.1608, 21572407.
26. Sievers C, Schlumpf T, Sawarkar R, Comoglio F, Paro R. Mixture models and wavelet transforms reveal high confidence RNA-protein interaction sites in MOV10 PAR-CLIP data. Nucleic Acids Res 2012, 40:e160. 10.1093/nar/gks697, 3488208, 22844102.
27. Baltz AG, Munschauer M, Schwanhausser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K, Milek M, Wyler E, Bonneau R, Selbach M, Dieterich C, Landthaler M. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012, 46:674-690. 10.1016/j.molcel.2012.05.021, 22681889.
28. Freeberg MA, Han T, Moresco JJ, Kong A, Yang YC, Lu ZJ, Yates JR, Kim JK. Pervasive and dynamic protein binding sites of the mRNA transcriptome in Saccharomyces cerevisiae. Genome Biol 2013, 14:R13. 10.1186/gb-2013-14-2-r13, 23409723.
29. Li F, Zheng Q, Ryvkin P, Dragomir I, Desai Y, Aiyer S, Valladares O, Yang J, Bambina S, Sabin LR, Murray JI, Lamitina T, Raj A, Cherry S, Wang LS, Gregory BD. Global analysis of RNA secondary structure in two metazoans. Cell Rep 2012, 1:69-82. 10.1016/j.celrep.2011.10.002, 22832108.
30. Zheng Q, Ryvkin P, Li F, Dragomir I, Valladares O, Yang J, Cao K, Wang LS, Gregory BD. Genome-wide double-stranded RNA sequencing reveals the functional significance of base-paired RNAs in Arabidopsis. PLoS Genet 2010, 6:e1001141. 10.1371/journal.pgen.1001141, 2947979, 20941385.
31. Jensen KB, Darnell RB. CLIP: cross-linking and immunoprecipitation of in vivo RNA targets of RNA-binding proteins. Methods Mol Biol 2008, 488:85-98. 10.1007/978-1-60327-475-3_6, 18982285.
32. Tenenbaum SA, Lager PJ, Carson CC, Keene JD. Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 2002, 26:191-198. 10.1016/S1046-2023(02)00022-1, 12054896.
33. Gilbert C, Svejstrup JQ. RNA immunoprecipitation for determining RNA-protein associations in vivo. Curr Protoc Mol Biol 2006, 27:24.
34. Muino JM, Kaufmann K, van Ham RC, Angenent GC, Krajewski P. ChIP-seq analysis in R (CSAR): an R package for the statistical detection of protein-bound genomic regions. Plant Methods 2011, 7:11. 10.1186/1746-4811-7-11, 3114017, 21554688.
35. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208. 10.1093/nar/gkp335, 2703892, 19458158.
36. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011, 27:1017-1018. 10.1093/bioinformatics/btr064, 3065696, 21330290.
37. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
38. Capon F, Allen MH, Ameen M, Burden AD, Tillman D, Barker JN, Trembath RC. A synonymous SNP of the corneodesmosin gene leads to increased mRNA stability and demonstrates association with psoriasis across diverse ethnic groups. Hum Mol Genet 2004, 13:2361-2368. 10.1093/hmg/ddh273, 15333584.
39. Chamary JV, Parmley JL, Hurst LD. Hearing silence: non-neutral evolution at synonymous sites in mammals. Nat Rev Genet 2006, 7:98-108. 10.1038/nrg1770, 16418745.
40. Brest P, Lapaquette P, Souidi M, Lebrigand K, Cesaro A, Vouret-Craviari V, Mari B, Barbry P, Mosnier JF, Hebuterne X, Harel-Bellan A, Mograbi B, Darfeuille-Michaud A, Hofman P. A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in Crohn's disease. Nat Genet 2011, 43:242-245. 10.1038/ng.762, 21278745.
41. Sauna ZE, Kimchi-Sarfaty C. Understanding the contribution of synonymous mutations to human disease. Nat Rev Genet 2011, 12:683-691. 10.1038/nrg3051, 21878961.
42. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, Collins FS, Manolio TA. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A 2009, 106:9362-9367. 10.1073/pnas.0903103106, 2687147, 19474294.
43. Habegger L, Sboner A, Gianoulis TA, Rozowsky J, Agarwal A, Snyder M, Gerstein M. RSEQtools: a modular framework to analyze RNA-seq data using compact, anonymized data summaries. Bioinformatics 2011, 27:281-283. 10.1093/bioinformatics/btq643, 3018817, 21134889.
44. Garber M, Guttman M, Clamp M, Zody MC, Friedman N, Xie X. Identifying novel constrained elements by exploiting biased substitution patterns. Bioinformatics 2009, 25:i54-i62. 10.1093/bioinformatics/btp190, 2687944, 19478016.
45. PIP-seq. http://gregorylab.bio.upenn.edu/PIPseq/.
46. Jbrowse. http://gregorylab.bio.upenn.edu/jbrowse/?data=data/HeLa_PIPseq.
47. UCSC genome browser. http://genome.ucsc.edu/cgi-bin/hgTracks?hgS_doOtherUser=submit&hgS_otherUserName=pipseq&hgS_otherUserSessionName=PPS.