The emergence of genome architecture and zygotic genome activation

Vallot, Antoine; Tachibana, Kikuë

doi:10.1016/j.ceb.2020.02.002

Cited by 31 publications

(21 citation statements)

References 73 publications

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“…Previous studies reported the existence of chromatin loops typically at considerably large genomic distances spanning two or more TADs 17,44 or concerning Polycomb binding sites 44,84 . Here, we observed that chromatin loops between cis -regulatory elements within Drosophila TADs are widespread, mimicking the common CTCF-mediated chromatin loops present within mammalian TADs 15,39 . In addition, we found that multiple CRMs can cluster together to form cis -regulatory hubs located at the interior of TADs, suggesting a mechanism to sequester enhancers in space to reduce the activation of genes in neighboring TADs.…”

Section: Discussionmentioning

confidence: 77%

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Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development

Götz

Fiche

Bellec

et al. 2020

Preprint

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AbstractDuring development, naïve cells gradually acquire distinct cell fates, through sophisticated mechanisms of precise spatio-temporal gene regulation. Acquisition of cell fate is thought to rely on the specific interaction of remote cis-regulatory modules (e.g. enhancers, silencers) (CRM) and target promoters. However, the precise interplay between chromatin structure and gene expression is still unclear, particularly in single cells within multicellular developing organisms. Here we employ Hi-M, a single-cell spatial genomics approach, to systematically detect CRM-promoter looping interactions within topological associating domains (TADs) during Drosophila development. By comparing cis-regulatory loops in alternate cell types, we show that physical proximity does not necessarily instruct transcriptional states. Moreover, multi-way analyses revealed the existence of local interactions between multiple remote CRMs to form hubs. We found that loops and CRM hubs are established early during development, prior to the emergence of TADs. Moreover, CRM hubs are formed via the action of the pioneer transcription factor Zelda and precede transcriptional activation. Our approach offers a new perspective on the role of CRM-promoter interactions in defining transcriptional activation and repression states, as well as distinct cell types.

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Section: Discussionmentioning

confidence: 77%

“…This model is consistent with multi-way interactions between distal enhancers to regulate promoter activity of single or multiple genes by sharing resources. Whether and how formation of multi-way interactions may be related to the emergence of TADs during development 38,39 is still an open question.…”

Section: Introductionmentioning

confidence: 99%

Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development

Götz

Fiche

Bellec

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

Section: Introductionmentioning

confidence: 99%

Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during early Drosophila development

et al. 2021

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Acquisition of cell fate is thought to rely on the specific interaction of remote cis-regulatory modules (CRMs), e.g. enhancers, and target promoters. However, the precise interplay between chromatin structure and gene expression is still unclear, particularly within multicellular developing organisms. Here we employ Hi-M, a single-cell spatial genomics approach, to detect CRM-promoter looping interactions within topologically associating domains (TADs) during early Drosophila development. By comparing cis-regulatory loops in alternate cell types, we show that physical proximity does not necessarily instruct transcriptional states. Moreover, multi-way analyses reveal multiple CRMs spatially coalesce to form hubs. Loops and CRM hubs are established early during development, prior to the emergence of TADs. Moreover, CRM hubs are formed, in part, via the action of the pioneer transcription factor Zelda and precede transcriptional activation. Our approach provides insight into the role of CRM-promoter interactions in defining transcriptional states, as well as distinct cell types.

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“…In mouse embryogenesis, lamina-associated domains (LADs) are settled in the zygote prior to topologically associating domains (TADs) [ 93 ]. The latter are conserved in evolution [ 94 , 95 ].…”

Section: Phase Transitions Of the Chr Network And Its Determinants In Early Embryo Developmentmentioning

confidence: 99%

Heterochromatin Networks: Topology, Dynamics, and Function (a Working Hypothesis)

Ērenpreisa

Krigerts

Salmiņa

et al. 2021

Cells

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Open systems can only exist by self-organization as pulsing structures exchanging matter and energy with the outer world. This review is an attempt to reveal the organizational principles of the heterochromatin supra-intra-chromosomal network in terms of nonlinear thermodynamics. The accessibility of the linear information of the genetic code is regulated by constitutive heterochromatin (CHR) creating the positional information in a system of coordinates. These features include scale-free splitting-fusing of CHR with the boundary constraints of the nucleolus and nuclear envelope. The analysis of both the literature and our own data suggests a radial-concentric network as the main structural organization principle of CHR regulating transcriptional pulsing. The dynamic CHR network is likely created together with nucleolus-associated chromatin domains, while the alveoli of this network, including springy splicing speckles, are the pulsing transcription hubs. CHR contributes to this regulation due to the silencing position variegation effect, stickiness, and flexible rigidity determined by the positioning of nucleosomes. The whole system acts in concert with the elastic nuclear actomyosin network which also emerges by self-organization during the transcriptional pulsing process. We hypothesize that the the transcriptional pulsing, in turn, adjusts its frequency/amplitudes specified by topologically associating domains to the replication timing code that determines epigenetic differentiation memory.

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The emergence of genome architecture and zygotic genome activation

Cited by 31 publications

References 73 publications

Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development

Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during development

Cis-regulatory chromatin loops arise before TADs and gene activation, and are independent of cell fate during early Drosophila development

Heterochromatin Networks: Topology, Dynamics, and Function (a Working Hypothesis)

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