H3.3-H4 Tetramer Splitting Events Feature Cell-Type Specific Enhancers
Previously, we reported that little canonical (H3.1–H4)2 tetramers split to form “hybrid” tetramers consisted of old and new H3.1–H4 dimers, but approximately 10% of (H3.3–H4)2 tetramers split during each cell cycle. In this report, we mapped the H3.3 nucleosome occupancy, the H3.3 nucleosome turnover rate and H3.3 nucleosome splitting events at the genome-wide level. Interestingly, H3.3 nucleosome turnover rate at the transcription starting sites (TSS) of genes with different expression levels display a bimodal distribution rather than a linear correlation towards the transcriptional activity, suggesting genes are either active with high H3.3 nucleosome turnover or inactive with low H3.3 nucleosome turnover. H3.3 nucleosome splitting events are enriched at active genes, which are in fact better markers for active transcription than H3.3 nucleosome occupancy itself. Although both H3.3 nucleosome turnover and splitting events are enriched at active genes, these events only display a moderate positive correlation, suggesting H3.3 nucleosome splitting events are not the mere consequence of H3.3 nucleosome turnover. Surprisingly, H3.3 nucleosomes with high splitting index are remarkably enriched at enhancers in a cell-type specific manner. We propose that the H3.3 nucleosomes at enhancers may be split by an active mechanism to regulate cell-type specific transcription.
Vyšlo v časopise:
H3.3-H4 Tetramer Splitting Events Feature Cell-Type Specific Enhancers. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003558
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003558
Souhrn
Previously, we reported that little canonical (H3.1–H4)2 tetramers split to form “hybrid” tetramers consisted of old and new H3.1–H4 dimers, but approximately 10% of (H3.3–H4)2 tetramers split during each cell cycle. In this report, we mapped the H3.3 nucleosome occupancy, the H3.3 nucleosome turnover rate and H3.3 nucleosome splitting events at the genome-wide level. Interestingly, H3.3 nucleosome turnover rate at the transcription starting sites (TSS) of genes with different expression levels display a bimodal distribution rather than a linear correlation towards the transcriptional activity, suggesting genes are either active with high H3.3 nucleosome turnover or inactive with low H3.3 nucleosome turnover. H3.3 nucleosome splitting events are enriched at active genes, which are in fact better markers for active transcription than H3.3 nucleosome occupancy itself. Although both H3.3 nucleosome turnover and splitting events are enriched at active genes, these events only display a moderate positive correlation, suggesting H3.3 nucleosome splitting events are not the mere consequence of H3.3 nucleosome turnover. Surprisingly, H3.3 nucleosomes with high splitting index are remarkably enriched at enhancers in a cell-type specific manner. We propose that the H3.3 nucleosomes at enhancers may be split by an active mechanism to regulate cell-type specific transcription.
Zdroje
1. AhmadK, HenikoffS (2002) Histone H3 variants specify modes of chromatin assembly. Proceedings of the National Academy of Sciences of the United States of America 99 Suppl 4: 16477–16484.
2. SarmaK, ReinbergD (2005) Histone variants meet their match. Nature reviews Molecular cell biology 6: 139–149.
3. SzenkerE, Ray-GalletD, AlmouzniG (2011) The double face of the histone variant H3.3. Cell research 21: 421–434.
4. YuanG, ZhuB (2012) Histone variants and epigenetic inheritance. Biochimica et biophysica acta 1819: 222–229.
5. AhmadK, HenikoffS (2002) The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 9: 1191–1200.
6. MitoY, HenikoffJG, HenikoffS (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nature genetics 37: 1090–1097.
7. MitoY, HenikoffJG, HenikoffS (2007) Histone replacement marks the boundaries of cis-regulatory domains. Science 315: 1408–1411.
8. TagamiH, Ray-GalletD, AlmouzniG, NakataniY (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51–61.
9. GoldbergAD, BanaszynskiLA, NohKM, LewisPW, ElsaesserSJ, et al. (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: 678–691.
10. DraneP, OuararhniK, DepauxA, ShuaibM, HamicheA (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes & development 24: 1253–1265.
11. WongLH, McGhieJD, SimM, AndersonMA, AhnS, et al. (2010) ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells. Genome research 20: 351–360.
12. Allis CD, Jenuwein T, Reinberg D (2007) Epigenetics. Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press. x, 502 p.p.
13. CamposEI, ReinbergD (2009) Histones: annotating chromatin. Annual review of genetics 43: 559–599.
14. BannisterAJ, KouzaridesT (2011) Regulation of chromatin by histone modifications. Cell research 21: 381–395.
15. ZhuB, ReinbergD (2011) Epigenetic inheritance: Uncontested? Cell research 21: 435–441.
16. XuM, ZhuB (2010) Nucleosome assembly and epigenetic inheritance. Protein & cell 1: 820–829.
17. ProbstAV, DunleavyE, AlmouzniG (2009) Epigenetic inheritance during the cell cycle. Nature reviews Molecular cell biology 10: 192–206.
18. MartinC, ZhangY (2007) Mechanisms of epigenetic inheritance. Current opinion in cell biology 19: 266–272.
19. MargueronR, ReinbergD (2010) Chromatin structure and the inheritance of epigenetic information. Nature reviews Genetics 11: 285–296.
20. XuM, WangW, ChenS, ZhuB (2012) A model for mitotic inheritance of histone lysine methylation. EMBO reports 13: 60–67.
21. ChenX, XiongJ, XuM, ChenS, ZhuB (2011) Symmetrical modification within a nucleosome is not required globally for histone lysine methylation. EMBO reports 12: 244–251.
22. XuM, LongC, ChenX, HuangC, ChenS, et al. (2010) Partitioning of histone H3–H4 tetramers during DNA replication-dependent chromatin assembly. Science 328: 94–98.
23. WuH, ZhuB (2011) Split decision: why it matters? Front Biol 6: 88–92.
24. Ray-GalletD, AlmouzniG (2010) Molecular biology. Mixing or not mixing. Science 328: 56–57.
25. HenikoffS (2008) Nucleosome destabilization in the epigenetic regulation of gene expression. Nature reviews Genetics 9: 15–26.
26. DealRB, HenikoffJG, HenikoffS (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: 1161–1164.
27. HeintzmanND, HonGC, HawkinsRD, KheradpourP, StarkA, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108–112.
28. Katan-KhaykovichY, StruhlK (2011) Splitting of H3–H4 tetramers at transcriptionally active genes undergoing dynamic histone exchange. Proceedings of the National Academy of Sciences of the United States of America 108: 1296–1301.
29. HenikoffS, HenikoffJG, SakaiA, LoebGB, AhmadK (2009) Genome-wide profiling of salt fractions maps physical properties of chromatin. Genome research 19: 460–469.
30. ZhangY, ShinH, SongJS, LeiY, LiuXS (2008) Identifying positioned nucleosomes with epigenetic marks in human from ChIP-Seq. BMC Genomics 9: 537.
31. CherbasL, WillinghamA, ZhangD, YangL, ZouY, et al. (2011) The transcriptional diversity of 25 Drosophila cell lines. Genome research 21: 301–314.
32. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.
33. TrapnellC, WilliamsBA, PerteaG, MortazaviA, KwanG, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature biotechnology 28: 511–515.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 6
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- BMS1 Is Mutated in Aplasia Cutis Congenita
- Sex-stratified Genome-wide Association Studies Including 270,000 Individuals Show Sexual Dimorphism in Genetic Loci for Anthropometric Traits
- Distinctive Expansion of Potential Virulence Genes in the Genome of the Oomycete Fish Pathogen
- Distinct Neuroblastoma-associated Alterations of Impair Sympathetic Neuronal Differentiation in Zebrafish Models