Systematic Protein Location Mapping Reveals Five Principal Chromatin Types in Drosophila Cells

Filion, Guillaume J.; Bemmel, Joke G. van; Braunschweig, Ulrich; Talhout, Wendy; Kind, Jop; Ward, Lucas D.; Brugman, Wim; Castro, Inês J. de; Kerkhoven, Ron; Bussemaker, Harmen J.; Steensel, Bas van

doi:10.1016/j.cell.2010.09.009

Cited by 859 publications

(1,100 citation statements)

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“…Indeed, previous studies have detected transcription within rice centromeres (Nagaki et al, 2004), human neocentromeres (Saffery et al, 2003) and also within the alphoid array of a derivative of the synthetic HAC used in the present study (Iida et al, 2010). The chromatin profile at active kinetochores resembles the 'yellow' chromatin described in a recent paper (Filion et al, 2010). This chromatin type is characteristic of genes with broad expression patterns ('housekeeping' genes).…”

Section: Discussionsupporting

confidence: 72%

Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function

Bergmann

Jakubsche

Martins

et al. 2012

Journal of Cell Science

101

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SummaryHuman kinetochores are transcriptionally active, producing very low levels of transcripts of the underlying alpha-satellite DNA. However, it is not known whether kinetochores can tolerate acetylated chromatin and the levels of transcription that are characteristic of housekeeping genes, or whether kinetochore-associated 'centrochromatin', despite being transcribed at a low level, is essentially a form of repressive chromatin. Here, we have engineered two types of acetylated chromatin within the centromere of a synthetic human artificial chromosome. Tethering a minimal NF-kB p65 activation domain within kinetochore-associated chromatin produced chromatin with high levels of histone H3 acetylated on lysine 9 (H3K9ac) and an ,10-fold elevation in transcript levels, but had no substantial effect on kinetochore assembly or function. By contrast, tethering the herpes virus VP16 activation domain produced similar modifications in the chromatin but resulted in an ,150-fold elevation in transcripts, approaching the level of transcription of an endogenous housekeeping gene. This rapidly inactivated kinetochores, causing a loss of assembled CENP-A and blocking further CENP-A assembly. Our data reveal that functional centromeres in vivo show a remarkable plasticity -kinetochores tolerate profound changes to their chromatin environment, but appear to be critically sensitive to the level of centromeric transcription.

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Section: Discussionsupporting

confidence: 72%

Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function

Bergmann

Jakubsche

Martins

et al. 2012

Journal of Cell Science

101

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“…These more 'compact' regions are referred to as heterochromatin. This is clearly a simplistic view, as recent work in D. melanogaster has shown that there are five genomic domains of chromatin structure based on analysing the pattern of binding of many chromatin proteins [84]. However, given that most is known about the two simple domains described above, references below will be defined to these two types of genomic domains.…”

Section: Genomic Localization Of Histone Modificationsmentioning

confidence: 99%

Regulation of chromatin by histone modifications

2011

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Chromatin is not an inert structure, but rather an instructive DNA scaffold that can respond to external cues to regulate the many uses of DNA. A principle component of chromatin that plays a key role in this regulation is the modification of histones. There is an ever-growing list of these modifications and the complexity of their action is only just beginning to be understood. However, it is clear that histone modifications play fundamental roles in most biological processes that are involved in the manipulation and expression of DNA. Here, we describe the known histone modifications, define where they are found genomically and discuss some of their functional consequences, concentrating mostly on transcription where the majority of characterisation has taken place.

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“…Unlike TFBSs, PREs are compound regulatory elements composed of multiple, sometimes partially redundant, sequence elements (Delest et al 2012). Although the exact biochemical binding site composition and structural constraints upon PREs are not completely resolved, a group of coordinately binding proteins called Polycomb group (PcG) factors recruit Polycomb Repressive Complexes, which are necessary to deposit and maintain H3K27me3 and have been associated genome wide with H3K27me3 domains (Lanzuolo and Orlando 2012).The effect of H3K27me3 is unambiguously and strongly repressive (Filion et al 2010;Kharchenko et al 2011;Li et al 2014). H3K27me3-associated loci have been proposed to congregate in silenced foci called Polycomb factories, which inhibit transcription by preventing access to RNA polymerase II and other transfactors (Bantignies et al 2011;Sexton et al 2012).…”

mentioning

confidence: 99%

Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification

Arthur

Slattery

et al. 2014

Genome Res.

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Histone modifications are critical for the regulation of gene expression, cell type specification, and differentiation. However, evolutionary patterns of key modifications that regulate gene expression in differentiating organisms have not been examined. Here we mapped the genomic locations of the repressive mark histone 3 lysine 27 trimethylation (H3K27me3) in four species of Drosophila, and compared these patterns to those in C. elegans. We found that patterns of H3K27me3 are highly conserved across species, but conservation is substantially weaker among duplicated genes. We further discovered that retropositions are associated with greater evolutionary changes in H3K27me3 and gene expression than tandem duplications, indicating that local chromatin constraints influence duplicated gene evolution. These changes are also associated with concomitant evolution of gene expression. Our findings reveal the strong conservation of genomic architecture governed by an epigenetic mark across distantly related species and the importance of gene duplication in generating novel H3K27me3 profiles.[Supplemental material is available for this article.]While transcriptional regulation has long been recognized as a significant target of evolutionary change (King and Wilson 1975), the specific mechanisms behind regulatory divergence have been difficult to dissect (Carroll 2008). In most cases, research has focused on recognizable cis-elements where transcription factors bind in a sequence-specific manner (Borneman et al. 2007;Bradley et al. 2010;Dowell 2010;Ni et al. 2012). Changes to either a transcription factor's DNA-binding properties or transcription factor binding sites (TFBS) enable the evolution of differential regulation, and numerous examples of this phenomenon have been observed (Ludwig et al. 2005;Shultzaberger et al. 2012).Whereas changes in cis-regulatory elements have been implicated in phenotypic and specifically morphological changes (Carroll 2008;Stern and Orgogozo 2008), other components of transcriptional regulation such as the chromatin environment have been scarcely explored (Lenhard et al. 2012). Histone modifications, which are chemical alterations of the histone spools upon which DNA is threaded, constitute one of the best-described elements of chromatin state (Zhou et al. 2011). These modifications can act directly or indirectly (through recruited enzymes) to alter DNA accessibility, thereby controlling other DNA-protein interactions (Campos and Reinberg 2009). Unlike TFBSs, however, histone modifications are not necessarily easily localizable to particular sequence elements, making their evolution difficult to study (Delest et al. 2012).Histone 3 lysine 27 trimethylation (H3K27me3) is one of the best-known histone modifications, in terms of both its biogenesis and effects. H3K27me3 is associated with complex cis-regulatory elements called Polycomb Response Elements (PREs) (Delest et al. 2012). Unlike TFBSs, PREs are compound regulatory elements composed of multiple, sometimes partially redundant, sequen...

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Systematic Protein Location Mapping Reveals Five Principal Chromatin Types in Drosophila Cells

Cited by 859 publications

References 65 publications

Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function

Epigenetic engineering: histone H3K9 acetylation is compatible with kinetochore structure and function

Regulation of chromatin by histone modifications

Evolution of H3K27me3-marked chromatin is linked to gene expression evolution and to patterns of gene duplication and diversification

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