The nucleolus: a raft adrift in the nuclear sea or the keystone in nuclear structure?

O’Sullivan, Justin M.; Pai, Dave A.; Cridge, Andrew G.; Engelke, David R.; Ganley, Austen R. D.

doi:10.1515/bmc-2012-0043

Cited by 28 publications

(15 citation statements)

References 117 publications

(124 reference statements)

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“…While the data also suggested variation across ESC and ESC-derived cell types, greater coverage for these cells is necessary to draw sufficiently dense contact maps for a more fine-grained and meaningful biological contrast. An intriguing suggestion is that the rDNA/nucleolus represents a keystone in nuclear structure around which the rest of the genome is functionally organized [ 26 ] [ 24 ]. In this case, rDNA-contact differences between cells are bound to emerge and reflect functional variation.…”

Section: Discussionmentioning

confidence: 99%

The long-range interaction map of ribosomal DNA arrays

Yu¹,

Lemos²

2018

PLoS Genet

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The repeated rDNA array gives rise to the nucleolus, an organelle that is central to cellular processes as varied as stress response, cell cycle regulation, RNA modification, cell metabolism, and genome stability. The rDNA array is also responsible for the production of more than 70% of all cellular RNAs (the ribosomal RNAs). The rRNAs are produced from two sets of loci: the 5S rDNA array resides exclusively on human chromosome 1 while the 45S rDNA arrays reside on the short arm of five human acrocentric chromosomes. These critical genome elements have remained unassembled and have been excluded from all Hi-C analyses to date. Here we built the first high resolution map of 5S and 45S rDNA array contacts with the rest of the genome combining over 15 billion Hi-C reads from several experiments. The data enabled sufficiently high coverage to map rDNA-genome interactions with 1MB resolution and identify rDNA-gene contacts. The map showed that the 5S and 45S arrays display preferential contact at common sites along the genome but are not themselves sufficiently close to yield 5S-45S Hi-C contacts. Ribosomal DNA contacts are enriched in segments of closed, repressed, and late replicating chromatin, as well as CTCF binding sites. Finally, we identified functional categories whose dispersed genes coalesced in proximity to the rDNA arrays or instead avoided proximity with the rDNA arrays. The observations further our understanding of the spatial localization of rDNA arrays and their contribution to the architecture of the cell nucleus.

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Section: Discussionmentioning

confidence: 99%

The long-range interaction map of ribosomal DNA arrays

Yu¹,

Lemos²

2018

PLoS Genet

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“…To use an analogy, in fast-growing cells, most of the bacterial RNAP functions as eukaryotic Pol I/III activities to promote growth. In eukaryotic cells Pol I is responsible for the synthesis of rRNA at the nucleolus (O'Sullivan et al, 2013 ) and Pol III makes small RNAs including tRNAs. Consequently, only a small fraction of E. coli RNAP engages in transcription of other genes in the remaining ~99% of the genome, consistent with the finding that most regions of the chromatin spreads appeared to be “naked,” or devoid of RNAP (French and Miller, 1989 ).…”

Section: Differential Allocation Of Rna Polymerase Between mentioning

confidence: 99%

The dynamic nature and territory of transcriptional machinery in the bacterial chromosome

Cagliero

2015

Front. Microbiol.

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Our knowledge of the regulation of genes involved in bacterial growth and stress responses is extensive; however, we have only recently begun to understand how environmental cues influence the dynamic, three-dimensional distribution of RNA polymerase (RNAP) in Escherichia coli on the level of single cell, using wide-field fluorescence microscopy and state-of-the-art imaging techniques. Live-cell imaging using either an agarose-embedding procedure or a microfluidic system further underscores the dynamic nature of the distribution of RNAP in response to changes in the environment and highlights the challenges in the study. A general agreement between live-cell and fixed-cell images has validated the formaldehyde-fixing procedure, which is a technical breakthrough in the study of the cell biology of RNAP. In this review we use a systems biology perspective to summarize the advances in the cell biology of RNAP in E. coli, including the discoveries of the bacterial nucleolus, the spatial compartmentalization of the transcription machinery at the periphery of the nucleoid, and the segregation of the chromosome territories for the two major cellular functions of transcription and replication in fast-growing cells. Our understanding of the coupling of transcription and bacterial chromosome (or nucleoid) structure is also summarized. Using E. coli as a simple model system, co-imaging of RNAP with DNA and other factors during growth and stress responses will continue to be a useful tool for studying bacterial growth and adaptation in changing environment.

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“…Nuclear bodies, previously known as interchromatin structures, typically exhibit non-overlapping spatial distributions with the genome ( Brasch and Ochs, 1992 , Sternsdorf et al., 1997 ). With an exception of nucleoli, which are positioned near ribosomal DNA (rDNA) ( O'Sullivan et al., 2013 ), it remains challenging to identify the genomic sequences near most of the nuclear bodies, especially nuclear speckles ( Lamond and Spector, 2003 ). Chromatin immunoprecipitation sequencing (ChIP-seq) targeting nuclear speckle core proteins rarely produces reproducible peaks ( Kim et al., 2018 ), likely due to the lack of stable physical interactions between nuclear speckle core proteins and chromatin ( Spector and Lamond, 2011 , Chen, 2016 , Kim et al., 2018 ).…”

Section: Introductionmentioning

confidence: 99%

RNAs as Proximity-Labeling Media for Identifying Nuclear Speckle Positions Relative to the Genome

Chen

Yan

et al. 2018

iScience

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SummaryIt remains challenging to identify all parts of the nuclear genome that are in proximity to nuclear speckles, due to physical separation between the nuclear speckle cores and chromatin. We hypothesized that noncoding RNAs including small nuclear RNA (snRNAs) and Malat1, which accumulate at the periphery of nuclear speckles (nsaRNA [nuclear speckle-associated RNA]), may extend to sufficient proximity to the genome. Leveraging a transcriptome-genome interaction assay (mapping of RNA-genome interactions [MARGI]), we identified clusters of nsaRNA-interacting genomic sequences (nsaPeaks). Posttranscriptional pre-mRNAs, which also accumulate to nuclear speckles, exhibited proximity to nsaPeaks but rarely to other genomic regions. Our combined DNA fluorescence in situ hybridization and immunofluorescence analysis in 182 single cells revealed a 3-fold increase in odds for nuclear speckles to localize near an nsaPeak than its neighboring genomic sequence. These data suggest a model that nsaRNAs are located in sufficient proximity to the nuclear genome and leave identifiable genomic footprints, thus revealing the parts of genome proximal to nuclear speckles.

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The nucleolus: a raft adrift in the nuclear sea or the keystone in nuclear structure?

Cited by 28 publications

References 117 publications

The long-range interaction map of ribosomal DNA arrays

The long-range interaction map of ribosomal DNA arrays

The dynamic nature and territory of transcriptional machinery in the bacterial chromosome

RNAs as Proximity-Labeling Media for Identifying Nuclear Speckle Positions Relative to the Genome

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