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Transcription landscape at the HoxD locus in developing limbs and brain

ABSTRACT: The emergence and evolution of digits was an essential step in the success of the tetrapod lineage. Amongst the key players, Hoxd genes were functionally co-opted in the developing digital plate, where they help organize growth and patterns. To understand both the evolutionary recruitment and transcriptional regulation of this genomic locus, we analyzed its architecture and chromatin status in developing digits, combined with a deletion approach in vivo. We show that the active and inactive parts of the gene cluster adopt opposite spatial configurations, corresponding to different chromatin domains. Active genes are contacted by several regulatory islands, located within a neighboring gene desert, which contribute quantitatively or qualitatively to the global transcriptional readout. We refer to this novel type of control as a ‘regulatory archipelago’ and discuss the value of this concept to understand both the morphological flexibility of tetrapod digits and the robustness of the underlying developmental process. Transcriptional activity at the Hoxd locus in developing limbs and brain at E12.5

ORGANISM(S): Mus musculus

PROVIDER: GSE31656 | GEO | 2011/11/28

SECONDARY ACCESSION(S): PRJNA155013

REPOSITORIES: GEO

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Spatial organization of chromatin at the HoxD locus in developing limbs and brain

Project description:The emergence and evolution of digits was an essential step in the success of the tetrapod lineage. Amongst the key players, Hoxd genes were functionally co-opted in the developing digital plate, where they help organize growth and patterns. To understand both the evolutionary recruitment and transcriptional regulation of this genomic locus, we analyzed its architecture and chromatin status in developing digits, combined with a deletion approach in vivo. We show that the active and inactive parts of the gene cluster adopt opposite spatial configurations, corresponding to different chromatin domains. Active genes are contacted by several regulatory islands, located within a neighboring gene desert, which contribute quantitatively or qualitatively to the global transcriptional readout. We refer to this novel type of control as a ‘regulatory archipelago’ and discuss the value of this concept to understand both the morphological flexibility of tetrapod digits and the robustness of the underlying developmental process. Chromosome Conformation Capture-on-chip analysis (4C) at the Hoxd locus in developing limbs and brain at E12.5

2011-11-28 | GSE31658 | GEO

Chromatin landscape at the HoxD locus in developing digits and forebrain

Project description:The emergence and evolution of digits was an essential step in the success of the tetrapod lineage. Amongst the key players, Hoxd genes were functionally co-opted in the developing digital plate, where they help organize growth and patterns. To understand both the evolutionary recruitment and transcriptional regulation of this genomic locus, we analyzed its architecture and chromatin status in developing digits, combined with a deletion approach in vivo. We show that the active and inactive parts of the gene cluster adopt opposite spatial configurations, corresponding to different chromatin domains. Active genes are contacted by several regulatory islands, located within a neighboring gene desert, which contribute quantitatively or qualitatively to the global transcriptional readout. We refer to this novel type of control as a ‘regulatory archipelago’ and discuss the value of this concept to understand both the morphological flexibility of tetrapod digits and the robustness of the underlying developmental process. Distribution of histone marks and RNA Pol2 at the Hoxd locus in developing limbs and brain at E12.5

2011-11-28 | GSE31654 | GEO

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (4C-Seq)

Project description:During limb development, Hoxd genes are transcribed in two waves: Early on, when the arm and forearm are specified and subsequently, when digits form. While the latter phase is controlled by enhancers centromeric to the HoxD cluster, we show here that the early phase requires enhancers located in the opposite telomeric gene desert. The transition between the two types of regulations involves a functional switch between two distinct topological domains, as reflected by a subset of genes mapping centrally into the cluster, which initially interact with the telomeric domain and subsequently shift to establish new contacts on the opposite side. This transition between two regulatory landscapes generates an intermediate area of low Hox dose developing into the wrist, the transition between our arms and our hands. This intriguing correspondence between genomic and morphological boundaries illustrates the mechanism underlying collinear Hox gene regulation in our developing appendages. Circular Chromosome Conformation Capture (4C seq) at the HoxD locus in developing proximal and distal limbs at E9.5 and E12.5

2013-06-07 | E-GEOD-45455 | biostudies-arrayexpress

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (ChIP-Seq)

Project description:During limb development, Hoxd genes are transcribed in two waves: Early on, when the arm and forearm are specified and subsequently, when digits form. While the latter phase is controlled by enhancers centromeric to the HoxD cluster, we show here that the early phase requires enhancers located in the opposite telomeric gene desert. The transition between the two types of regulations involves a functional switch between two distinct topological domains, as reflected by a subset of genes mapping centrally into the cluster, which initially interact with the telomeric domain and subsequently shift to establish new contacts on the opposite side. This transition between two regulatory landscapes generates an intermediate area of low Hox dose developing into the wrist, the transition between our arms and our hands. This intriguing correspondence between genomic and morphological boundaries illustrates the mechanism underlying collinear Hox gene regulation in our developing appendages. Chromatin ImmunoPrecipitation and Sequencing (ChIP-seq) of H3K27A in developing proximal and distal limbs at E9.5, E10.5 and E12.5

2013-06-07 | E-GEOD-45456 | biostudies-arrayexpress

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (ChIP-Seq)

2013-06-07 | GSE45456 | GEO

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (4C-Seq)

2013-06-07 | GSE45455 | GEO

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (ChIP-chip)

2013-06-07 | GSE45454 | GEO

A Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs (ChIP-chip)

Project description:During limb development, Hoxd genes are transcribed in two waves: Early on, when the arm and forearm are specified and subsequently, when digits form. While the latter phase is controlled by enhancers centromeric to the HoxD cluster, we show here that the early phase requires enhancers located in the opposite telomeric gene desert. The transition between the two types of regulations involves a functional switch between two distinct topological domains, as reflected by a subset of genes mapping centrally into the cluster, which initially interact with the telomeric domain and subsequently shift to establish new contacts on the opposite side. This transition between two regulatory landscapes generates an intermediate area of low Hox dose developing into the wrist, the transition between our arms and our hands. This intriguing correspondence between genomic and morphological boundaries illustrates the mechanism underlying collinear Hox gene regulation in our developing appendages. Chromatin ImmoPrecipitation on chip (Tiling array): Distribution of H3K4me3 and H3K27me3 in early limb buds at E9.5, E10.5 and proximal late limbs E12.5. Distribution of H3K27me3 in del(8-13) and del(8-13)/del(attP-TpSB3) E10.5 limb buds. Distribution of H3K27me3 in WT and homozygote del(Nsi-Atf2) (Montavon et al., 2011) forelimb autopods.

2013-06-07 | E-GEOD-45454 | biostudies-arrayexpress

Conservation and divergence of regulatory strategies and the origin of tetrapod digits

Project description:The evolution of tetrapod limbs from fish fins enabled the conquest of land by vertebrates and thus represents a key step in evolution. Despite the use of comparative gene expression analyses, critical aspects of this transformation remain controversial, in particularly the origin of digits. Hoxa and Hoxd genes are essential for the specification of the different limb segments and their functional abrogation leads to large truncations of the appendages. Here we show that the selective transcription of mouse Hoxa genes in proximal and distal limbs is related to a bimodal higher order chromatin structure, similar to that reported for Hoxd genes, thus revealing a generic regulatory strategy implemented by both gene clusters during limb development. We found the same bimodal chromatin architecture in fish embryos, indicating that the regulatory strategy used to pattern tetrapod limbs predates the divergence between fish and tetrapods. However, when assessed in mice, both fish regulatory domains triggered transcription in proximal, rather than distal limb territories, supporting an evolutionary scenario whereby digits arose as true tetrapod novelties through genetic retrofitting of a preexisting bimodal chromatin framework. We discuss the possibility to consider regulatory circuitries, rather than expression patterns, as essential parameters to define evolutionary synapomorphies. Circular Chromosome Conformation Capture (4C seq) at the mouse HoxA and HoxD loci in proximal and distal forelimbs and forebrain at E12.5 and at the zebrafish HoxAa, HoxAb and HoxDa loci in 5 dpf whole embryos.

2014-01-21 | E-GEOD-47644 | biostudies-arrayexpress

Large-scale genomic reorganizations of topological domains (TADs) at the HoxD locus (4C-Seq)

Project description:The transcriptional activation of Hoxd genes during mammalian limb development involves dynamic interactions with the two Topologically Associating Domains (TADs) flanking the HoxD cluster. In particular, the activation of the most posterior Hoxd genes in developing digits is controlled by regulatory elements located in the centromeric TAD (C-DOM) through long-range contacts. To assess the structure-function relationships underlying such interactions, we measured compaction levels and TAD discreteness using a combination of chromosome conformation capture (4C-seq) and DNA FISH. We challenged the robustness of the TAD architecture by using a series of genomic deletions and inversions that impact the integrity of this chromatin domain and that remodel the long-range contacts. We report multi-partite associations between Hoxd genes and up to three enhancers and show that breaking the native chromatin topology leads to the remodelling of TAD structure. Our results reveal that the re-composition of TADs architectures after severe genomic re-arrangements depends on a boundary-selection mechanism that uses CTCF-mediated gating of long-range contacts in combination with genomic distance and, to a certain extent, sequence specificity.

2017-07-12 | GSE98861 | GEO

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