Polycomb-Dependent Regulatory Contacts between Distant Hox Loci in Drosophila

Bantignies, Frédéric; Roure, Virginie; Comet, Itys; Leblanc, Benjamin; Schuettengruber, Bernd; Bonnet, J.; Tixier, Vanessa; Mas, André; Cavalli, Giacomo

doi:10.1016/j.cell.2010.12.026

Cited by 390 publications

(398 citation statements)

References 66 publications

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“…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). This repressive state is both temporally and spatially dynamic (Akkers et al 2009;Filion et al 2010;Kharchenko et al 2011;Nègre et al 2011).…”

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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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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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“…An important underlying supposition to this cascade of events is that nuclear colocalization among functionally related genes must be conserved across distantly related lineages. This has been demonstrated in mammals, yeast and for the Hox genes between the distantly related species D. melanogaster and D. virilis 36,38,39 .…”

Section: Discussionmentioning

confidence: 97%

“…Additional factors or mechanisms might increase this probability, especially when functionally related genes are involved. For example, the relocation of lab in the D. repleta species group 34,35 has been suggested to result from a rearrangement upon the nuclear colocalization of separated genome neighbourhoods harbouring Hox genes 36 . Specifically, genes from the Antennapedia and Bithorax complexes have been shown to be spatially close to each other during their repression by Polycomb protein complexes in some tissues.…”

Section: Discussionmentioning

confidence: 99%

Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila

et al. 2015

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Genome clustering of homeobox genes is often thought to reflect arrangements of tandem gene duplicates maintained by advantageous coordinated gene regulation. Here we analyse the chromosomal organization of the NK homeobox genes, presumed to be part of a single cluster in the Bilaterian ancestor, across 20 arthropods. We find that the ProtoNK cluster was extensively fragmented in some lineages, showing that NK clustering in Drosophila species does not reflect selectively maintained gene arrangements. More importantly, the arrangement of NK and neighbouring genes across the phylogeny supports that, in two instances within the Drosophila genus, some cluster remnants became reunited via large-scale chromosomal rearrangements. Simulated scenarios of chromosome evolution indicate that these reunion events are unlikely unless the genome neighbourhoods harbouring the participating genes tend to colocalize in the nucleus. Our results underscore how mechanisms other than tandem gene duplication can result in paralogous gene clustering during genome evolution.

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“…4C has been later modified by several groups. This allowed, for instance, the detection of extensive interaction networks of polycomb-repressed Hox genes in Drosophila or of active mouse globin genes in erythroid tissues (Bantignies et al 2011;Schoenfelder et al 2010). In both studies, 3C templates were generated and then amplified with a single biotinylated primer specific to the bait region.…”

Section: The Birth and The Maturation Of 3cmentioning

confidence: 99%

Chromosome conformation capture technologies and their impact in understanding genome function

2016

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It has been more than a decade since the first chromosome conformation capture (3C) assay was described. The assay was originally devised to measure the frequency with which two genomic loci interact within the three-dimensional (3D) nuclear space. Over time, this method has evolved both qualitatively and quantitatively, from detection of pairwise interaction of two unique loci to generating maps for the global chromatin interactome. Combined with the analysis of the epigenetic chromatin context, these advances led to the unmasking of general genome folding principles. The evolution of 3C-based methods has been supported first by the revolution in ChIP and then by sequencingbased approaches, methods that were primarily tools to study the unidimensional genome. The gradual improvement of 3C-based methods illustrates how the field adapted to the need to gradually address more subtle questions, beginning with enquiries of reductionist nature to reach more holistic perspectives, as the technology advanced, in a process that is greatly improving our knowledge on genome behavior and regulation. Here, we describe the evolution of 3C and other 3C-based methods for the analysis of chromatin interactions, along with a brief summary of their contribution in uncovering the significance of the threedimensional world within the nucleus. We also discuss their inherent limitations and caveats in order to provide a critical view of the power and the limits of this technology.

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Polycomb-Dependent Regulatory Contacts between Distant Hox Loci in Drosophila

Cited by 390 publications

References 66 publications

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

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

Remodelling of a homeobox gene cluster by multiple independent gene reunions in Drosophila

Chromosome conformation capture technologies and their impact in understanding genome function

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