Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA

Nature Communications

Volumn 6, Issue , 2015, Pages

  Léveillé, Nicolas ^a   Melo, Carlos A ^a,b   Rooijers, Koos ^a   Díaz Lagares, Angel ^c   Melo, Sonia A ^d   Korkmaz, Gozde ^a   Lopes, Rui ^a   Moqadam, Farhad Akbari ^e   Maia, Ana R ^a   Wijchers, Patrick J ^f   Geeven, Geert ^f   Den Boer, Monique L ^e   Kalluri, Raghu ^d   De Laat, Wouter ^f   Esteller, Manel ^c,g,h   Agami, Reuven ^a,i  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^d UNIVERSITY OF TEXAS   (United States)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g UNIVERSITY OF BARCELONA   (Spain)

^h INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

ⁱ ROTTERDAM UNIVERSITY OF APPLIED SCIENCES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; LONG UNTRANSLATED RNA; PROTEIN P53; CDKN1A PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

CANCER; CHROMOSOME; GENOME; INHIBITOR; PUBLIC HEALTH; RNA; TUMOR;

ARTICLE; BINDING SITE; CELL CYCLE ARREST; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; ENHANCER REGION; GENE EXPRESSION; GENE MAPPING; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA SYNTHESIS; ADENOCARCINOMA; BREAST TUMOR; CHROMATIN IMMUNOPRECIPITATION; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS;

ADENOCARCINOMA; BREAST NEOPLASMS; CHROMATIN IMMUNOPRECIPITATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA METHYLATION; ENHANCER ELEMENTS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MCF-7 CELLS; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; RNA, LONG NONCODING; SEQUENCE ANALYSIS, RNA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84925760606     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7520     Document Type: Article

References (43)

1. Crick, F. H., Barnett, L., Brenner, S. & Watts-Tobin, R. J. General nature of the genetic code for proteins. Nature 192, 1227-1232 (1961).
2. Guttman, M. et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458, 223-227 (2009).
3. Heintzman, N. D. et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nature Genet. 39, 311-318 (2007).
4. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009).
5. Creyghton, M. P. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. USA 107, 21931-21936 (2010).
6. Huarte, M. et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142, 409-419 (2010).
7. Lam, M. T. et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription. Nature 498, 511-515 (2013).
8. Li, W. et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498, 516-520 (2013).
9. Melo, C. A. et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 49, 524-535 (2013).
10. Beckerman, R. & Prives, C. Transcriptional regulation by p53. Cold Spring Harb. Perspect. Biol. 2, a000935 (2010).
11. Momand, J., Jung, D., Wilczynski, S. & Niland, J. The MDM2 gene amplification database. Nuclei. Acids Res. 26, 3453-3459 (1998).
12. Gembarska, A. et al. MDM4 is a key therapeutic target in cutaneous melanoma. Nature Med. 18, 1239-1247 (2012).
13. Wei, C. L. et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 124, 207-219 (2006).
14. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
15. Nikulenkov, F. et al. Insights into p53 transcriptional function via genome-wide chromatin occupancy and gene expression analysis. Cell Death Differ. 19, 1992-2002 (2012).
16. Wang, B., Xiao, Z. & Ren, E. C. Redefining the p53 response element. Proc. Natl Acad. Sci. USA 106, 14373-14378 (2009).
17. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
18. Vance, K. W. et al. The long non-coding RNA Paupar regulates the expression of both local and distal genes. EMBO J. 33, 296-311 (2014).
19. Yang, L. et al. lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature 500, 598-602 (2013).
20. Cabili, M. N. et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25, 1915-1927 (2011).
21. Allen, M. A. et al. Global analysis of p53-regulated transcription identifies its direct targets and unexpected regulatory mechanisms. eLife 3, e02200 (2014).
22. Rashi-Elkeles, S. et al. Parallel profiling of the transcriptome, cistrome, and epigenome in the cellular response to ionizing radiation. Sci. Signal. 7, rs3 (2014).
23. Chu, C., Qu, K., Zhong, F. L., Artandi, S. E. & Chang, H. Y. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol. Cell 44, 667-678 (2011).
24. Heintzman, N. D. et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112 (2009).
25. Birney, E. et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447, 799-816 (2007).
26. Core, L. J., Waterfall, J. J. & Lis, J. T. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322, 1845-1848 (2008).
27. Hah, N., Murakami, S., Nagari, A., Danko, C. G. & Kraus, W. L. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res. 23, 1210-1223 (2013).
28. Gupta, R. A. et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464, 1071-1076 (2010).
29. Wang, K. C. et al. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472, 120-124 (2011).
30. Hollstein, M., Sidransky, D., Vogelstein, B. & Harris, C. C. p53 mutations in human cancers. Science 253, 49-53 (1991).
31. Leveille, N. et al. Selective inhibition of microRNA accessibility by RBM38 is required for p53 activity. Nat. Commun. 2, 513 (2011).
32. Voorhoeve, P. M. et al. A genetic screen implicates miRNA-372 and miRNA- 373 as oncogenes in testicular germ cell tumors. Cell 124, 1169-1181 (2006).
33. Yap, K. L. et al. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol. Cell 38, 662-674 (2010).
34. Prensner, J. R. et al. The long noncoding RNA SChLAP1 promotes aggressive prostate cancer and antagonizes the SWI/SNF complex. Nature Genet. 45, 1392-1398 (2013).
35. Mourtada-Maarabouni, M., Pickard, M. R., Hedge, V. L., Farzaneh, F. & Williams, G. T. GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 28, 195-208 (2009).
36. Wang, D. et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA. Nature 474, 390-394 (2011).
37. Lee, B. K. et al. Cell-type specific and combinatorial usage of diverse transcription factors revealed by genome-wide binding studies in multiple human cells. Genome Res. 22, 9-24 (2012).
38. Johnson, D. S., Mortazavi, A., Myers, R. M. & Wold, B. Genome-wide mapping of in vivo protein-DNA interactions. Science 316, 1497-1502 (2007).
39. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
40. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
41. Chu, C., Quinn, J. & Chang, H. Y. Chromatin isolation by RNA purification (ChIRP). J. Vis. Exp. doi: 10.3791/3912 (2012).
42. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
43. Splinter, E. et al. The inactive X chromosome adopts a unique threedimensional conformation that is dependent on Xist RNA. Genes Dev. 25, 1371-1383 (2011).