Accurate Prediction of Inducible Transcription Factor Binding Intensities In Vivo

English version České info

DNA sequence and local chromatin landscape act jointly to determine transcription factor (TF) binding intensity profiles. To disentangle these influences, we developed an experimental approach, called protein/DNA binding followed by high-throughput sequencing (PB–seq), that allows the binding energy landscape to be characterized genome-wide in the absence of chromatin. We applied our methods to the Drosophila Heat Shock Factor (HSF), which inducibly binds a target DNA sequence element (HSE) following heat shock stress. PB–seq involves incubating sheared naked genomic DNA with recombinant HSF, partitioning the HSF–bound and HSF–free DNA, and then detecting HSF–bound DNA by high-throughput sequencing. We compared PB–seq binding profiles with ones observed in vivo by ChIP–seq and developed statistical models to predict the observed departures from idealized binding patterns based on covariates describing the local chromatin environment. We found that DNase I hypersensitivity and tetra-acetylation of H4 were the most influential covariates in predicting changes in HSF binding affinity. We also investigated the extent to which DNA accessibility, as measured by digital DNase I footprinting data, could be predicted from MNase–seq data and the ChIP–chip profiles for many histone modifications and TFs, and found GAGA element associated factor (GAF), tetra-acetylation of H4, and H4K16 acetylation to be the most predictive covariates. Lastly, we generated an unbiased model of HSF binding sequences, which revealed distinct biophysical properties of the HSF/HSE interaction and a previously unrecognized substructure within the HSE. These findings provide new insights into the interplay between the genomic sequence and the chromatin landscape in determining transcription factor binding intensity.

Vyšlo v časopise: Accurate Prediction of Inducible Transcription Factor Binding Intensities In Vivo. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002610
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002610

Souhrn

Zdroje

1. FieldYSharonESegalE 2011 How transcription factors identify regulatory sites in genomic sequence. Subcell Biochem 52 193 204

2. BergerMFBulykML 2009 Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat Protoc 4 393 411

3. LiuJStormoGD 2005 Combining SELEX with quantitative assays to rapidly obtain accurate models of protein-DNA interactions. Nucleic Acids Res 33 e141

4. HesselberthJRChenXZhangZSaboPJSandstromR 2009 Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat Methods 6 283 289

5. LiuXNollDMLiebJDClarkeND 2005 DIP-chip: Rapid and accurate determination of DNA-binding specificity. Genome Res 15 421 427

6. GuertinMJLisJT 2010 Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6 e1001114 doi:10.1371/journal.pgen.1001114

7. LiXYThomasSSaboPJEisenMBStamatoyannopoulosJA 2011 The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding. Genome Biol 12 R34

8. KaplanTLiXYSaboPJThomasSStamatoyannopoulosJA 2011 Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development. PLoS Genet 7 e1001290 doi:10.1371/journal.pgen.1001290

9. NarlikarLGordanRHarteminkAJ 2007 A nucleosome-guided map of transcription factor binding sites in yeast. PLoS Comput Biol 3 e215 doi:10.1371/journal.pcbi.0030215

10. Pique-RegiRDegnerJFPaiAAGaffneyDJGiladY 2011 Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res 21 447 455

11. BoyleAPSongLLeeBKLondonDKeefeD 2011 High-resolution genome-wide in vivo footprinting of diverse transcription factors in human cells. Genome Res 21 456 464

12. GuertinMJPeteschSJZobeckKLMinIMLisJT 2011 Drosophila heat shock system as a general model to investigate transcriptional regulation. Cold Spring Harb Symp Quant Biol

13. HayashidaNFujimotoMTanKPrakasamRShinkawaT 2010 Heat shock factor 1 ameliorates proteotoxicity in cooperation with the transcription factor NFAT. EMBO J 29 3459 3469

14. GonsalvesSEMosesAMRazakZRobertFWestwoodJT 2011 Whole-genome analysis reveals that active heat shock factor binding sites are mostly associated with non-heat shock genes in Drosophila melanogaster. PLoS ONE 6 e15934 doi:10.1371/journal.pone.0015934

15. PepkeSWoldBMortazaviA 2009 Computation for ChIP-seq and RNA-seq studies. Nat Methods 6 S22 32

16. ChenRSnyderM 2010 Yeast proteomics and protein microarrays. J Proteomics 73 2147 2157

17. GordanRHarteminkAJBulykML 2009 Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res 19 2090 2100

18. KharchenkoPVAlekseyenkoAASchwartzYBMinodaARiddleNC 2011 Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471 480 485

19. GilchristDADos SantosGFargoDCXieBGaoY 2010 Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143 540 551

20. FriedmanJHPopescuBE 2008 Predictive learning via rule ensembles. Ann Appl Stat 2 916 954

21. LeeHKrausKWWolfnerMFLisJT 1992 DNA sequence requirements for generating paused polymerase at the start of Hsp70. Genes Dev 6 284 295

22. JohnSSaboPJThurmanRESungMHBiddieSC 2011 Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43 264 268

23. RobertsonAGBilenkyMTamAZhaoYZengT 2008 Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res 18 1906 1917

24. WuWChengYKellerCAErnstJKumarSA 2011 Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration. Genome Res 21 1659 1671

25. TursunBPatelTKratsiosPHobertO 2011 Direct conversion of C. elegans germ cells into specific neuron types. Science 331 304 308

26. BiddieSCJohnSSaboPJThurmanREJohnsonTA 2011 Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol Cell 43 145 155

27. von HippelPHRevzinAGrossCAWangAC 1974 Non-specific DNA binding of genome regulating proteins as a biological control mechanism: I. the lac operon: Equilibrium aspects. Proc Natl Acad Sci U S A 71 4808 4812

28. LinSRiggsAD 1975 The general affinity of lac repressor for E. coli DNA: Implications for gene regulation in procaryotes and eucaryotes. Cell 4 107 111

29. FritschMWuC 1999 Phosphorylation of Drosophila heat shock transcription factor. Cell Stress Chaperones 4 102 117

30. VossTCSchiltzRLSungMHYenPMStamatoyannopoulosJA 2011 Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell 146 544 554

31. HeHHMeyerCAShinHBaileySTWeiG 2010 Nucleosome dynamics define transcriptional enhancers. Nat Genet 42 343 347

32. HuGSchonesDECuiKYbarraRNorthrupD 2011 Regulation of nucleosome landscape and transcription factor targeting at tissue-specific enhancers by BRG1. Genome Res 21 1650 1658

33. JohnSSaboPJJohnsonTASungMHBiddieSC 2008 Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 29 611 624

34. SharonELublinerSSegalE 2008 A feature-based approach to modeling protein-DNA interactions. PLoS Comput Biol 4 e1000154 doi:10.1371/journal.pcbi.1000154

35. HeXChenCCHongFFangFSinhaS 2009 A biophysical model for analysis of transcription factor interaction and binding site arrangement from genome-wide binding data. PLoS ONE 4 e8155 doi:10.1371/journal.pone.0008155

36. EnokiYSakuraiH 2011 Diversity in DNA recognition by heat shock transcription factors (HSFs) from model organisms. FEBS Lett 585 1293 1298

37. SakuraiHTakemoriY 2007 Interaction between heat shock transcription factors (HSFs) and divergent binding sequences: Binding specificities of yeast HSFs and human HSF1. J Biol Chem 282 13334 13341

38. TaoHLiuWSimmonsBNHarrisHKCoxTC 2010 Purifying natively folded proteins from inclusion bodies using sarkosyl, triton X-100, and CHAPS. BioTechniques 48 61 64

39. LiHDurbinR 2009 Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25 1754 1760

40. BarrettTTroupDBWilhiteSELedouxPRudnevD 2009 NCBI GEO: Archive for high-throughput functional genomic data. Nucleic Acids Res 37 D885 90

41. ZhangYLiuTMeyerCAEeckhouteJJohnsonDS 2008 Model-based analysis of ChIP-seq (MACS). Genome Biol 9 R137

42. BaileyTLWilliamsNMislehCLiWW 2006 MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res 34 W369 73