Differential protein occupancy profiling of the mRNA transcriptome

Genome Biology

Volumn 15, Issue 1, 2014, Pages

  Schueler, Markus ^a   Munschauer, Mathias ^a   Gregersen, Lea Haarup ^a   Finzel, Ana ^a   Loewer, Alexander ^a   Chen, Wei ^a   Landthaler, Markus ^a   Dieterich, Christoph ^a,b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b MAX PLANCK INSTITUTE FOR BIOLOGY OF AGEING   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; COMPLEMENTARY RNA; MESSENGER RNA; RNA BINDING PROTEIN; THIOURIDINE; TRANSCRIPTOME;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA CROSS LINKING; EMBRYO; EXON; GENE EXPRESSION; GENE LOCATION; GENETIC VARIABILITY; HEK293 CELL LINE; HUMAN; HUMAN CELL; MCF 7 CELL LINE; PROTEIN ANALYSIS; PROTEIN OCCUPANCY PROFILING; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS; RNA METABOLISM; RNA SEQUENCE; STRUCTURAL BIOINFORMATICS; BIOLOGY; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; SEQUENCE ANALYSIS;

COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION; HEK293 CELLS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MCF-7 CELLS; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84892412330     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-1-r15     Document Type: Article

References (69)

1. Moore MJ: From birth to death: the complex lives of eukaryotic mRNAs. Science 2005, 309:1514-1518.
2. 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.
3. Kwon SC, Yi H, Eichelbaum K, Fohr S, Fischer B, You KT, Castello A, Krijgsveld J, Hentze MW, Kim VN: The RNA-binding protein repertoire of embryonic stem cells. Nat Struct Mol Biol 2013, 20:1122-1130.
4. Auweter SD, Oberstrass FC, Allain FH: Sequence-specific binding of single-stranded RNA: is there a code for recognition? Nucleic Acids Res 2006, 34:4943-4959.
5. Cook KB, Kazan H, Zuberi K, Morris Q, Hughes TR: RBPDB: a database of RNA-binding specificities. Nucleic Acids Res 2011, 39:D301-D308.
6. Lunde BM, Moore C, Varani G: RNA-binding proteins: modular design for efficient function. Nat Rev 2007, 8:479-490.
7. Granneman S, Kudla G, Petfalski E, Tollervey D: Identification of protein binding sites on U3 snoRNA and pre-rRNA by UV cross-linking and high-throughput analysis of cDNAs. Proc Natl Acad Sci U S A 2009, 106:9613-9618.
8. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, 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.
9. 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. 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.
11. 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.
12. Milek M, Wyler E, Landthaler M: Transcriptome-wide analysis of protein-RNA interactions using high-throughput sequencing. Semin Cell Dev Biol 2012, 23:206-212.
13. 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.
14. Munschauer M, Schueler M, Dieterich C, Landthaler M: High-resolution profiling of protein occupancy on polyadenylated RNA transcripts. Methods 2013. S1046-2023(13)00386-1.
15. 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.
16. Levenson AS, Jordan VC: MCF-7: the first hormone-responsive breast cancer cell line. Cancer Res 1997, 57:3071-3078.
17. Soule HD, Vazguez J, Long A, Albert S, Brennan M: A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 1973, 51:1409-1416.
18. Charafe-Jauffret E, Ginestier C, Monville F, Finetti P, Adelaide J, Cervera N, Fekairi S, Xerri L, Jacquemier J, Birnbaum D, Bertucci F: Gene expression profiling of breast cell lines identifies potential new basal markers. Oncogene 2006, 25:2273-2284.
19. Lacroix M, Leclercq G: Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat 2004, 83:249-289.
20. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL: TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013, 14:R36.
21. Pruitt KD, Tatusova T, Brown GR, Maglott DR: NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 2012, 40:D130-D135.
22. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D: The human genome browser at UCSC. Genome Res 2002, 12:996-1006.
23. Consensus protein occupancy profiling. [http://dorina.mdc-berlin.de/cgibin/hgTracks?db=hg18]
24. Wang Y, Thakur A, Sun Y, Wu J, Biliran H, Bollig A, Liao DJ: Synergistic effect of cyclin D1 and c-Myc leads to more aggressive and invasive mammary tumors in severe combined immunodeficient mice. Cancer Res 2007, 67:3698-3707.
25. Faraway J: Practical Regression and Anova using R. 2002: [http://cran.r-project. org/doc/contrib/Faraway-PRA.pdf]
26. Robinson MD, Smyth GK: Moderated statistical tests for assessing differences in tag abundance. Bioinformatics 2007, 23:2881-2887.
27. Robinson MD, McCarthy DJ, Smyth GK: edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
28. Benjamini Y, Hochberg Y: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 1995, 57:289-300.
29. Yekutieli D, Benjamini Y: The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001, 29:1165-1188.
30. Chen K, Xi Y, Pan X, Li Z, Kaestner K, Tyler J, Dent S, He X, Li W: DANPOS: dynamic analysis of nucleosome position and occupancy by sequencing. Genome Res 2013, 23:341-351.
31. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS: Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137.
32. POPPI. [http://www.sourceforge.net/projects/proteinoccupancyprofiling]
33. Lange SJ, Maticzka D, Mohl M, Gagnon JN, Brown CM, Backofen R: Global or local? Predicting secondary structure and accessibility in mRNAs. Nucleic Acids Res 2012, 40:5215-5226.
34. Aviv T, Lin Z, Ben-Ari G, Smibert CA, Sicheri F: Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol 2006, 13:168-176.
35. 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.
36. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, Laishram RS, Qiao M, Lipshitz HD, Piano F, Corbett AH, Carstens RP, Frey BJ, Anderson RA, Lynch KW, Penalva LO, et al: A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177.
37. Mazan-Mamczarz K, Hagner PR, Corl S, Srikantan S, Wood WH, Becker KG, Gorospe M, Keene JD, Levenson AS, Gartenhaus RB: Post-transcriptional gene regulation by HuR promotes a more tumorigenic phenotype. Oncogene 2008, 27:6151-6163.
38. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M Jr, 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.
39. Biedermann B, Hotz HR, Ciosk R: The Quaking family of RNA-binding proteins: coordinators of the cell cycle and differentiation. Cell Cycle 2010, 9:1929-1933.
40. Sawicka K, Bushell M, Spriggs KA, Willis AE: Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans 2008, 36:641-647.
41. Wang ET, Cody NA, Jog S, Biancolella M, Wang TT, Treacy DJ, Luo S, Schroth GP, Housman DE, Reddy S, Lécuyer E, Burge CB: Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 2012, 150:710-724.
42. Herjan T, Novotny M, Hamilton TA: Diversity in sequence-dependent control of GRO chemokine mRNA half-life. J Leukoc Biol 2013, 93:895-904.
43. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, Landthaler M, Dieterich C: doRiNA: a database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res 2012, 40:D180-D186.
44. doRiNA. [http://dorina.mdc-berlin.de].
45. Ray D, Kazan H, Chan ET, Pena Castillo L, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR: Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 2009, 27:667-670.
46. Barreau C, Paillard L, Osborne HB: AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 2005, 33:7138-7150.
47. Weidensdorfer D, Stohr N, Baude A, Lederer M, Kohn M, Schierhorn A, Buchmeier S, Wahle E, Huttelmaier S: Control of c-myc mRNA stability by IGF2BP1-associated cytoplasmic RNPs. RNA 2009, 15:104-115.
48. Reimand J, Arak T, Vilo J: g:Profiler-a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res 2011, 39:W307-W315.
49. Reimand J, Kull M, Peterson H, Hansen J, Vilo J: g:Profiler-a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 2007, 35:W193-W200.
50. Dolken L, Ruzsics Z, Radle B, Friedel CC, Zimmer R, Mages J, Hoffmann R, Dickinson P, Forster T, Ghazal P, Koszinowski UH: High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA 2008, 14:1959-1972.
51. Schwanhausser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M: Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
52. Brennan CM, Steitz JA: HuR and mRNA stability. Cell Mol Life Sci 2001, 58:266-277.
53. Muller-McNicoll M, Neugebauer KM: How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet 2013, 14:275-287.
54. Latorre E, Tebaldi T, Viero G, Sparta AM, Quattrone A, Provenzani A: Downregulation of HuR as a new mechanism of doxorubicin resistance in breast cancer cells. Mol Cancer 2012, 11:13.
55. Denkert C, Koch I, von Keyserlingk N, Noske A, Niesporek S, Dietel M, Weichert W: Expression of the ELAV-like protein HuR in human colon cancer: association with tumor stage and cyclooxygenase-2. Mod Pathol 2006, 19:1261-1269.
56. Heinonen M, Bono P, Narko K, Chang SH, Lundin J, Joensuu H, Furneaux H, Hla T, Haglund C, Ristimaki A: Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res 2005, 65:2157-2161.
57. Lopez de Silanes I, Fan J, Yang X, Zonderman AB, Potapova O, Pizer ES, Gorospe M: Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 2003, 22:7146-7154.
58. Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM: Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 2001, 108:1657-1665.
59. Lopez de Silanes I, Lal A, Gorospe M: HuR: post-transcriptional paths to malignancy. RNA Biol 2005, 2:11-13.
60. Nabors LB, Gillespie GY, Harkins L, King PH: HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3' untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res 2001, 61:2154-2161.
61. Chen CY, Shyu AB: AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 1995, 20:465-470.
62. 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.
63. Nielsen CB, Shomron N, Sandberg R, Hornstein E, Kitzman J, Burge CB: Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 2007, 13:1894-1910.
64. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
65. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
66. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J: Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80.
67. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25:1105-1111.
68. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR: STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29:15-21.
69. cisBP-RNA. [http://cisbp-rna.ccbr.utoronto.ca]