Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre

Hacisuleyman, Ezgi; Goff, Loyal A.; Trapnell, Cole; Williams, Adam; Henao‐Mejia, Jorge; Sun, Li; McClanahan, Patrick D.; Hendrickson, David G.; Sauvageau, Martin; Kelley, David R.; Morse, Michael A.; Engreitz, Jesse M.; Lander, Eric S.; Guttman, Mitch; Lodish, Harvey F.; Flavell, Richard A.; Raj, Arjun; Rinn, John L.

doi:10.1038/nsmb.2764

Cited by 579 publications

(637 citation statements)

References 59 publications

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“…Contrary to the focal nuclear localization of Firre transcripts described previously (Hacisuleyman et al 2014), we instead detected a disperse distribution of Firre transcripts within the nucleoplasm of ESCs and NPCs (Figs. 2B, 5A).…”

Section: Wwwgenomeorgcontrasting

confidence: 52%

“…The previous deletion of its >70 kb genomic locus (Hacisuleyman et al 2014) does not allow one to distinguish between RNA-dependent effects and those mediated by the loss of the chromosomal region, including potential regulatory sites (Bassett et al 2014), and long-term culture further precludes the discrimination between direct and indirect changes. We thus decided to investigate the immediate impact of Firre depletion on the ESC gene expression profile.…”

Section: Wwwgenomeorgmentioning

confidence: 99%

“…We also found the lncRNA Firre to display moderately high expression and pronounced nuclear localization in both ESCs and NPCs. Firre, which escapes X inactivation in female mouse ESCs (Yang et al 2010), was recently reported to show exclusive focal enrichment at its transcription start site (Hacisuleyman et al 2014). Compared to mRNAs and lncRNAs, pseudogene transcripts displayed the strongest shift toward cytoplasmic localization ( Fig.…”

Section: Global Identification Of Nuclear-enriched Lncrnasmentioning

confidence: 99%

“…lncRNA Firre is integrated into the control of a modular gene expression program Firre was previously proposed to act as a molecular scaffold required for the spatial clustering of five genic regions in ESCs and other cell lines (Hacisuleyman et al 2014). Contrary to the focal nuclear localization of Firre transcripts described previously (Hacisuleyman et al 2014), we instead detected a disperse distribution of Firre transcripts within the nucleoplasm of ESCs and NPCs (Figs.…”

Section: Wwwgenomeorgmentioning

confidence: 99%

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Regulation of the ESC transcriptome by nuclear long noncoding RNAs

Bergmann

Eckersley-Maslin

et al. 2015

Genome Res.

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Long noncoding (lnc)RNAs have recently emerged as key regulators of gene expression. Here, we performed high-depth poly(A)+ RNA sequencing across multiple clonal populations of mouse embryonic stem cells (ESCs) and neural progenitor cells (NPCs) to comprehensively identify differentially regulated lncRNAs. We establish a biologically robust profile of lncRNA expression in these two cell types and further confirm that the majority of these lncRNAs are enriched in the nucleus. Applying weighted gene coexpression network analysis, we define a group of lncRNAs that are tightly associated with the pluripotent state of ESCs. Among these, we show that acute depletion of Platr14 using antisense oligonucleotides impacts the differentiation- and development-associated gene expression program of ESCs. Furthermore, we demonstrate that Firre, a lncRNA highly enriched in the nucleoplasm and previously reported to mediate chromosomal contacts in ESCs, controls a network of genes related to RNA processing. Together, we provide a comprehensive, up-to-date, and high resolution compilation of lncRNA expression in ESCs and NPCs and show that nuclear lncRNAs are tightly integrated into the regulation of ESC gene expression.

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Section: Wwwgenomeorgcontrasting

confidence: 52%

Section: Wwwgenomeorgmentioning

confidence: 99%

Section: Global Identification Of Nuclear-enriched Lncrnasmentioning

confidence: 99%

Section: Wwwgenomeorgmentioning

confidence: 99%

See 2 more Smart Citations

Regulation of the ESC transcriptome by nuclear long noncoding RNAs

Bergmann

Eckersley-Maslin

et al. 2015

Genome Res.

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“…Specific RNAs have also been implicated in chromatin organization. For example, the non-coding RNAs Xist and Firre establish chromatin microarchitectures (Engreitz et al, 2013;Hacisuleyman et al, 2014). Furthermore, chromatin associated RNAs are required for efficient oligomerization of SAF-A protein, which results in decompaction of transcribed euchromatin (Nozawa et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Transcription organizes euchromatin similar to an active microemulsion

Hilbert

Sato

Kimurâ

et al. 2017

Preprint

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Graphical abstract HighlightsThe copyright holder for this preprint (which was . http://dx.doi.org/10.1101/234112 doi: bioRxiv preprint first posted online Dec. 15, 2017; Page 2 of 46 SummaryThe three-dimensional organization of the genome is essential for development and health. Although the organization of euchromatin (transcriptionally permissive chromatin) dynamically adjusts to changes in transcription, the underlying mechanisms remain elusive. Here, we studied how transcription organizes euchromatin, using experiments in zebrafish embryonic cells and theory. We show that transcription establishes an interspersed pattern of chromatin domains and RNA-enriched microenvironments. Specifically, accumulation of RNA in the vicinity of transcription sites creates microenvironments that locally remodel chromatin by displacing not transcribed chromatin. Ongoing transcriptional activity stabilizes the interspersed pattern of chromatin domains and RNA-enriched microenvironments by establishing contacts between chromatin and RNA. We explain our observations with an active microemulsion model based on two macromolecular mechanisms: RNA/RNA-binding protein complexes generally segregate from chromatin, while transcribed chromatin is retained among RNA/RNA-binding protein accumulations. We propose that microenvironments might be central to genome architecture and serve as gene regulatory hubs.

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Challenges in the analysis of long noncoding RNA functionality

Leone

Santoro

2016

FEBS Letters

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Long noncoding RNA (lncRNA) are emerging as important regulators of diverse biological functions. Although mechanistic models are starting to emerge, it is also clear that the lncRNA field needs appropriate model systems in order to better elucidate the functions of lncRNA and their roles in both physiological and pathological conditions. The field of lncRNA is new, and the biochemical and genetic methods used to address function and mechanisms of lncRNA have only recently been developed or adapted from techniques used to investigate protein-coding genes. In this review, we discuss the strengths and weaknesses of available techniques for the analysis of chromatin-associated lncRNA and emerging models for the recruitment to specific genomic sites such as triple-helix, RNA-protein-DNA recognition and proximity-guided search models.

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Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre

Cited by 579 publications

References 59 publications

Regulation of the ESC transcriptome by nuclear long noncoding RNAs

Regulation of the ESC transcriptome by nuclear long noncoding RNAs

Transcription organizes euchromatin similar to an active microemulsion

Challenges in the analysis of long noncoding RNA functionality

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