A High-Resolution Whole-Genome Map of Key Chromatin Modifications in the Adult
Epigenetic research has been focused on cell-type-specific regulation; less is known about common features of epigenetic programming shared by diverse cell types within an organism. Here, we report a modified method for chromatin immunoprecipitation and deep sequencing (ChIP–Seq) and its use to construct a high-resolution map of the Drosophila melanogaster key histone marks, heterochromatin protein 1a (HP1a) and RNA polymerase II (polII). These factors are mapped at 50-bp resolution genome-wide and at 5-bp resolution for regulatory sequences of genes, which reveals fundamental features of chromatin modification landscape shared by major adult Drosophila cell types: the enrichment of both heterochromatic and euchromatic marks in transposons and repetitive sequences, the accumulation of HP1a at transcription start sites with stalled polII, the signatures of histone code and polII level/position around the transcriptional start sites that predict both the mRNA level and functionality of genes, and the enrichment of elongating polII within exons at splicing junctions. These features, likely conserved among diverse epigenomes, reveal general strategies for chromatin modifications.
Vyšlo v časopise:
A High-Resolution Whole-Genome Map of Key Chromatin Modifications in the Adult. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002380
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002380
Souhrn
Epigenetic research has been focused on cell-type-specific regulation; less is known about common features of epigenetic programming shared by diverse cell types within an organism. Here, we report a modified method for chromatin immunoprecipitation and deep sequencing (ChIP–Seq) and its use to construct a high-resolution map of the Drosophila melanogaster key histone marks, heterochromatin protein 1a (HP1a) and RNA polymerase II (polII). These factors are mapped at 50-bp resolution genome-wide and at 5-bp resolution for regulatory sequences of genes, which reveals fundamental features of chromatin modification landscape shared by major adult Drosophila cell types: the enrichment of both heterochromatic and euchromatic marks in transposons and repetitive sequences, the accumulation of HP1a at transcription start sites with stalled polII, the signatures of histone code and polII level/position around the transcriptional start sites that predict both the mRNA level and functionality of genes, and the enrichment of elongating polII within exons at splicing junctions. These features, likely conserved among diverse epigenomes, reveal general strategies for chromatin modifications.
Zdroje
1. BirdA 2007 Perceptions of epigenetics. Nature 447 396 398
2. KouzaridesT 2007 Chromatin modifications and their function. Cell 128 693 705
3. JenuweinTAllisCD 2001 Translating the histone code. Science 293 1074 1080
4. ElginSC 1996 Heterochromatin and gene regulation in Drosophila. Current opinion in genetics & development 6 193 202
5. KharchenkoPVAlekseyenkoAASchwartzYBMinodaARiddleNC 2011 Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471 480 485
6. NegreNBrownCDMaLBristowCAMillerSW 2011 A cis-regulatory map of the Drosophila genome. Nature 471 527 531
7. GraveleyBRBrooksANCarlsonJWDuffMOLandolinJM 2011 The developmental transcriptome of Drosophila melanogaster. Nature 471 473 479
8. EnderleDBeiselCStadlerMBGerstungMAthriP 2011 Polycomb preferentially targets stalled promoters of coding and noncoding transcripts. Genome Res 21 216 226
9. PepkeSWoldBMortazaviA 2009 Computation for ChIP-seq and RNA-seq studies. Nature methods 6 S22 32
10. RosenfeldJAXuanZDeSalleR 2009 Investigating repetitively matching short sequencing reads: the enigmatic nature of H3K9me3. Epigenetics : official journal of the DNA Methylation Society 4 476 486
11. JohanssonAMStenbergPPetterssonFLarssonJ 2007 POF and HP1 bind expressed exons, suggesting a balancing mechanism for gene regulation. PLoS Genet 3 e209 doi:10.1371/journal.pgen.0030209
12. de WitEGreilFvan SteenselB 2005 Genome-wide HP1 binding in Drosophila: developmental plasticity and genomic targeting signals. Genome research 15 1265 1273
13. HeintzmanNDStuartRKHonGFuYChingCW 2007 Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nature genetics 39 311 318
14. Pal-BhadraMLeibovitchBAGandhiSGRaoMBhadraU 2004 Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303 669 672
15. AndreyevaENBelyaevaESSemeshinVFPokholkovaGVZhimulevIF 2005 Three distinct chromatin domains in telomere ends of polytene chromosomes in Drosophila melanogaster Tel mutants. Journal of cell science 118 5465 5477
16. YinHLinH 2007 An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450 304 308
17. KapitonovVVJurkaJ 2003 Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proceedings of the National Academy of Sciences of the United States of America 100 6569 6574
18. RohTYCuddapahSZhaoK 2005 Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes & development 19 542 552
19. BannisterAJZegermanPPartridgeJFMiskaEAThomasJO 2001 Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 120 124
20. LachnerMO'CarrollDReaSMechtlerKJenuweinT 2001 Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 116 120
21. VakocCRMandatSAOlenchockBABlobelGA 2005 Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Molecular cell 19 381 391
22. WienckeJKZhengSMorrisonZYehRF 2008 Differentially expressed genes are marked by histone 3 lysine 9 trimethylation in human cancer cells. Oncogene 27 2412 2421
23. RastelliLChanCSPirrottaV 1993 Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function. The EMBO journal 12 1513 1522
24. RingroseLEhretHParoR 2004 Distinct contributions of histone H3 lysine 9 and 27 methylation to locus-specific stability of polycomb complexes. Molecular Cell 16 641 653
25. RingroseLRehmsmeierMDuraJMParoR 2003 Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster. Developmental Cell 5 759 771
26. BarskiACuddapahSCuiKRohTYSchonesDE 2007 High-resolution profiling of histone methylations in the human genome. Cell 129 823 837
27. EbertALeinSSchottaGReuterG 2006 Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome research: an international journal on the molecular, supramolecular and evolutionary aspects of chromosome biology 14 377 392
28. BernsteinBEMikkelsenTSXieXKamalMHuebertDJ 2006 A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125 315 326
29. LiuLPNiJQShiYDOakeleyEJSunFL 2005 Sex-specific role of Drosophila melanogaster HP1 in regulating chromatin structure and gene transcription. Nature genetics 37 1361 1366
30. MuseGWGilchristDANechaevSShahRParkerJS 2007 RNA polymerase is poised for activation across the genome. Nature genetics 39 1507 1511
31. ZeitlingerJStarkAKellisMHongJWNechaevS 2007 RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nature genetics 39 1512 1516
32. RougvieAELisJT 1988 The RNA polymerase II molecule at the 5′ end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell 54 795 804
33. SchonesDECuiKCuddapahSRohTYBarskiA 2008 Dynamic regulation of nucleosome positioning in the human genome. Cell 132 887 898
34. WuCHMJ 2000 Neural networks and genome informatics. Methods in computational biology and biochemistry 1 205
35. SchwartzSMeshorerEAstG 2009 Chromatin organization marks exon-intron structure. Nature structural & molecular biology 16 990 995
36. SmithCDShuSMungallCJKarpenGH 2007 The Release 5.1 annotation of Drosophila melanogaster heterochromatin. Science 316 1586 1591
37. SchottaGEbertAKraussVFischerAHoffmannJ 2002 Central role of Drosophila SU(VAR)3–9 in histone H3-K9 methylation and heterochromatic gene silencing. The EMBO journal 21 1121 1131
38. EbertASchottaGLeinSKubicekSKraussV 2004 Su(var) genes regulate the balance between euchromatin and heterochromatin in Drosophila. Genes & development 18 2973 2983
39. SiomiMCSaitoKSiomiH 2008 How selfish retrotransposons are silenced in Drosophila germline and somatic cells. FEBS letters 582 2473 2478
40. KeeneJDTenenbaumSA 2002 Eukaryotic mRNPs may represent posttranscriptional operons. Molecular cell 9 1161 1167
41. GuentherMGLevineSSBoyerLAJaenischRYoungRA 2007 A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130 77 88
42. NechaevSFargoDCdos SantosGLiuLGaoY 2010 Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327 335 338
43. MavrichTNJiangCIoshikhesIPLiXVentersBJ 2008 Nucleosome organization in the Drosophila genome. Nature 453 358 362
44. De LuciaFNiJQVaillantCSunFL 2005 HP1 modulates the transcription of cell-cycle regulators in Drosophila melanogaster. Nucleic acids research 33 2852 2858
45. PiacentiniLFantiLBerlocoMPerriniBPimpinelliS 2003 Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin. The Journal of cell biology 161 707 714
46. PiacentiniLFantiLNegriRDel VescovoVFaticaA 2009 Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila. PLoS Genet 5 e1000670 doi:10.1371/journal.pgen.1000670
47. VermaakDMalikHS 2009 Multiple roles for heterochromatin protein 1 genes in Drosophila. Annual review of genetics 43 467 492
48. de WitEGreilFvan SteenselB 2007 High-resolution mapping reveals links of HP1 with active and inactive chromatin components. PLoS Genet 3 e38 doi:10.1371/journal.pgen.0030038
49. CrydermanDEGradeSKLiYFantiLPimpinelliS 2005 Role of Drosophila HP1 in euchromatic gene expression. Developmental dynamics : an official publication of the American Association of Anatomists 232 767 774
50. KornblihttAR 2007 Coupling transcription and alternative splicing. Advances in experimental medicine and biology 623 175 189
51. AnderssonREnrothSRada-IglesiasAWadeliusCKomorowskiJ 2009 Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome research 19 1732 1741
52. Kolasinska-ZwierzPDownTLatorreILiuTLiuXS 2009 Differential chromatin marking of introns and expressed exons by H3K36me3. Nature genetics 41 376 381
53. NahkuriSTaftRJMattickJS 2009 Nucleosomes are preferentially positioned at exons in somatic and sperm cells. Cell cycle 8 3420 3424
54. TilgnerHNikolaouCAlthammerSSammethMBeatoM 2009 Nucleosome positioning as a determinant of exon recognition. Nature structural & molecular biology 16 996 1001
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 12
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Targeted Proteolysis of Plectin Isoform 1a Accounts for Hemidesmosome Dysfunction in Mice Mimicking the Dominant Skin Blistering Disease EBS-Ogna
- An Assessment of the Individual and Collective Effects of Variants on Height Using Twins and a Developmentally Informative Study Design
- Genomes Reveal Transition of Bacteria from Aquatic to Terrestrial Environments
- A Complex Genomic Rearrangement Involving the Locus Causes Dermal Hyperpigmentation in the Chicken