High-throughput and quantitative assessment of enhancer activity in mammals by CapStarr-seq

Nature Communications

Volumn 6, Issue , 2015, Pages

  Vanhille, Laurent ^a   Griffon, Aurélien ^a   Maqbool, Muhammad Ahmad ^b   Zacarias Cabeza, Joaquin ^c   Dao, Lan T M ^a   Fernandez, Nicolas ^a,d   Ballester, Benoit ^a   Andrau, Jean Christophe ^b   Spicuglia, Salvatore ^a  

^a Aix Marseille university   (France)

^b CNRS   (France)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d Institute of Biomedical Research University of Birmingham ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; IKAROS TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR;

ACCURACY ASSESSMENT; GENE EXPRESSION; GENOME; GERM CELL; MAMMAL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; COST EFFECTIVENESS ANALYSIS; ENHANCER REGION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; HIGH THROUGHPUT SEQUENCING; HISTONE METHYLATION; HOMOLOGOUS RECOMBINATION; LUCIFERASE ASSAY; MALE; MAMMAL; MOUSE; NONHUMAN; NUCLEOSOME; PHYLOGENY; QUANTITATIVE ANALYSIS; THYMOCYTE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; 3T3 CELL LINE; ANIMAL; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; PROCEDURES; PROMOTER REGION;

MAMMALIA;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICE; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 84928136624     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7905     Document Type: Article

References (37)

1. Plank, J. L. & Dean, A. Enhancer function: mechanistic and genome-wide insights come together. Mol. Cell 55, 5-14 (2014).
2. Dickel, D. E. et al. Function-based identification of mammalian enhancers using site-specific integration. Nat. Methods 11, 566-571 (2014).
3. Murtha, M. et al. FIREWACh: high-throughput functional detection of transcriptional regulatory modules in mammalian cells. Nat. Methods 11, 559-565 (2014).
4. Kheradpour, P. et al. Systematic dissection of regulatory motifs in 2000 predicted human enhancers using a massively parallel reporter assay. Genome Res. 23, 800-811 (2013).
5. Arnold, C. D. et al. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 339, 1074-1077 (2013).
6. Arnold, C. D. et al. Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution. Nat. Genet. 46, 685-692 (2014).
7. Shlyueva, D. et al. Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol. Cell 54, 180-192 (2014).
8. Mombaerts, P., Terhorst, C., Jacks, T., Tonegawa, S. & Sancho, J. Characterization of immature thymocyte lines derived from T-cell receptor or recombination activating gene 1 and p53 double mutant mice. Proc. Natl Acad. Sci. USA 92, 7420-7424 (1995).
9. Krangel, M. S. T cell development: better living through chromatin. Nat. Immunol. 7, 687-694 (2007).
10. Spicuglia, S. & Vanhille, L. Chromatin signatures of active enhancers. Nucleus 3, 126-131 (2012).
11. Pekowska, A. et al. H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 30, 4198-4210 (2011).
12. Wang, Z. et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40, 897-903 (2008).
13. Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43-49 (2011).
14. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
15. Zhu, Y., van Essen, D. & Saccani, S. Cell-type-specific control of enhancer activity by H3K9 trimethylation. Mol. Cell 46, 408-423 (2012).
16. McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
17. Sanyal, A., Lajoie, B. R., Jain, G. & Dekker, J. The long-range interaction landscape of gene promoters. Nature 489, 109-113 (2012).
18. Zhang, J. et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13, 86-94 (2012).
19. Hardison, R. C. & Taylor, J. Genomic approaches towards finding cis-regulatory modules in animals. Nat. Rev. Genet. 13, 469-483 (2012).
20. Loven, J. et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320-334 (2013).
21. Whyte, W. A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319 (2013).
22. Natoli, G. Maintaining cell identity through global control of genomic organization. Immunity 33, 12-24 (2010).
23. Rothenberg, E. V., Moore, J. E. & Yui, M. A. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 8, 9-21 (2008).
24. Bernstein, B. E. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
25. Koch, F. et al. Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat. Struct. Mol. Biol. 18, 956-963 (2011).
26. Hesselberth, J. R. et al. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat. Methods 6, 283-289 (2009).
27. Homer, N., Merriman, B. & Nelson, S. F. BFAST: an alignment tool for large scale genome resequencing. PLoS ONE 4, e7767 (2009).
28. 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).
29. Fenouil, R. et al. CpG islands and GC content dictate nucleosome depletion in a transcription-independent manner at mammalian promoters. Genome Res. 22, 2399-2408 (2012).
30. Lepoivre, C. et al. Divergent transcription is associated with promoters of transcriptional regulators. BMC Genomics 14, 914 (2013).
31. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842 (2010).
32. Thomas-Chollier, M. et al. A complete workflow for the analysis of full-size ChIP-seq (and similar) data sets using peak-motifs. Nat. Protoc. 7, 1551-1568 (2012).
33. Thomas-Chollier, M. et al. RSAT 2011: regulatory sequence analysis tools. Nucleic Acids Res. 39, W86-W91 (2011).
34. Medina-Rivera, A. et al. Theoretical and empirical quality assessment of transcription factor-binding motifs. Nucleic Acids Res. 39, 808-824 (2011).
35. Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934-947 (2013).
36. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
37. Mingueneau, M. et al. The transcriptional landscape of alphabeta T cell differentiation. Nat. Immunol. 14, 619-632 (2013).