Post-mitotic dynamics of pre-nucleolar bodies is driven by pre-ribosomal RNA processing

Carron, Coralie; Balor, Stéphanie; Delavoie, Franck; Plisson‐Chastang, Célia; Faubladier, Marlène; Gleizes, Pierre‐Emmanuel; O’Donohue, Marie-Françoise

doi:10.1242/jcs.106419

Cited by 24 publications

(28 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These data are in agreement with the results of O'Donahue and colleagues (Carron et al, 2012), who demonstrated that pre-rRNA processing occurred within PNBs. Hence, the disassembly mechanisms of both types of nuclear bodies are dependent on the outflow of RNA molecules.…”

Section: Discussionsupporting

confidence: 93%

“…5A). Pre-rRNA processing was shown to occur within the PNBs of telophase cells (Carron et al, 2012). To determine whether pre-rRNAs were processed in iPNBs, we employed the FISH technique, which was carried out using a combination of eight probes complementary to different segments of the transcribed spacers or mature rRNA to discriminate between early and late precursors (Fig.…”

Section: Ipnbs Are Assembled Around Rnasmentioning

confidence: 99%

“…The probes were as described by Carron et al (2012). The oligonucleotides used for FISH were labeled with 5-carboxy-X-rhodamine (Syntol).…”

Section: Fluorescence Recovery After Photobleachingmentioning

confidence: 99%

See 2 more Smart Citations

RNA-dependent disassembly of nuclear bodies

Musinova

Lisitsyna

Sorokin

et al. 2016

Journal of Cell Science

View full text Add to dashboard Cite

Nuclear bodies are membraneless organelles that play important roles in genome functioning. A specific type of nuclear bodies known as interphase prenucleolar bodies (iPNBs) are formed in the nucleoplasm after hypotonic stress from partially disassembled nucleoli. iPNBs are then disassembled, and the nucleoli are reformed simultaneously. Here, we show that diffusion of B23 molecules (also known as nucleophosmin, NPM1) from iPNBs, but not fusion of iPNBs with the nucleoli, contributes to the transfer of B23 from iPNBs to the nucleoli. Maturation of pre-ribosomal RNAs (rRNAs) and the subsequent outflow of mature rRNAs from iPNBs led to the disassembly of iPNBs. We found that B23 transfer was dependent on the synthesis of pre-rRNA molecules in nucleoli; these pre-rRNA molecules interacted with B23 and led to its accumulation within nucleoli. The transfer of B23 between iPNBs and nucleoli was accomplished through a nucleoplasmic pool of B23, and increased nucleoplasmic B23 content retarded disassembly, whereas B23 depletion accelerated disassembly. Our results suggest that iPNB disassembly and nucleolus assembly might be coupled through RNA-dependent exchange of nucleolar proteins, creating a highly dynamic system with long-distance correlations between spatially distinct processes.

show abstract

Section: Discussionsupporting

confidence: 93%

Section: Ipnbs Are Assembled Around Rnasmentioning

confidence: 99%

See 1 more Smart Citation

RNA-dependent disassembly of nuclear bodies

Musinova

Lisitsyna

Sorokin

et al. 2016

Journal of Cell Science

View full text Add to dashboard Cite

show abstract

“…First, ENDs form during interphase, rather than mitosis. Second, fibrillarin, a methyltransferase that participates in early rRNA processing steps, remains in ENDs for the majority of the cell cycle whereas it is one of the first proteins to leave PNBs in early G1 (21). Finally, unlike PNBs, ENDs appear to lack rRNA.…”

Section: Significancementioning

confidence: 99%

RNA transcription modulates phase transition-driven nuclear body assembly

Berry

Weber

Vaidya

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

449

426

View full text Add to dashboard Cite

Nuclear bodies are RNA and protein-rich, membraneless organelles that play important roles in gene regulation. The largest and most well-known nuclear body is the nucleolus, an organelle whose primary function in ribosome biogenesis makes it key for cell growth and size homeostasis. The nucleolus and other nuclear bodies behave like liquid-phase droplets and appear to condense from the nucleoplasm by concentration-dependent phase separation. However, nucleoli actively consume chemical energy, and it is unclear how such nonequilibrium activity might impact classical liquid-liquid phase separation. Here, we combine in vivo and in vitro experiments with theory and simulation to characterize the assembly and disassembly dynamics of nucleoli in early Caenorhabditis elegans embryos. In addition to classical nucleoli that assemble at the transcriptionally active nucleolar organizing regions, we observe dozens of "extranucleolar droplets" (ENDs) that condense in the nucleoplasm in a transcription-independent manner. We show that growth of nucleoli and ENDs is consistent with a first-order phase transition in which late-stage coarsening dynamics are mediated by Brownian coalescence and, to a lesser degree, Ostwald ripening. By manipulating C. elegans cell size, we change nucleolar component concentration and confirm several key model predictions. Our results show that rRNA transcription and other nonequilibrium biological activity can modulate the effective thermodynamic parameters governing nucleolar and END assembly, but do not appear to fundamentally alter the passive phase separation mechanism.RNA/protein droplets | intracellular phase separation | Brownian coalescence | Ostwald ripening | Flory-Huggins regular solution theory L iving cells are composed of complex and spatially heterogeneous materials that partition into functional compartments called organelles. Many organelles are vesicle-like structures with an enclosing membrane. However, a large number of RNA and protein-rich bodies maintain a dynamic but coherent structure even in the absence of a membrane. These so-called RNA/ protein granules are found in the cytoplasm and in the nucleus, where they are referred to as nuclear bodies. The mechanisms by which such structures form and stably persist are not well understood. However, recent evidence suggests that these membraneless organelles, such as P granules (1, 2), nucleoli (3), and stress granules (4), are liquid-phase droplets that may assemble by intracellular phase separation (5, 6). This concept is supported by work on synthetic systems, including repetitive protein domains that form droplets in vitro and in the cytoplasm (7) and intrinsically disordered protein domains that show signatures of liquid-liquid phase separation when expressed in the cell nucleus (8).By examining the cell size-dependent assembly of nucleoli in early Caenorhabditis elegans embryos, we previously showed that nucleolar assembly is controlled by a concentration-dependent phase transition (9). Using a simple model based on the de...

show abstract

“…In addition to proteins, small nucleolar RNAs involved in pre-rRNA processing such as U3, U8, and U14 (Dousset et al, 2000;Jiménez-García et al, 1994) are observed in PNBs. Furthermore, in addition to these non-ribosomal processing factors, pre-rRNAs (Boisvert et al, 2007;Carron et al, 2012;DiMario, 2004;Dundr et al, 2000;Fan and Penman, 1971;Phillips, 1972) as well as ribosomal proteins (Carron et al, 2012;Gassmann et al, 2004;Hügle et al, 1985;Ohta et al, 2010) are observed on the chromosome periphery and in PNBs. It was also proposed that the association of pre-rRNAs with proteins in pre-rRNP complexes is maintained during mitosis (Piñol-Roma, 1999), and recently pre-ribosomal particles were reported in PNBs (Carron et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Sharing of mitotic pre-ribosomal particles between daughter cells

Sirri

Jourdan

Hernandez‐Verdun

et al. 2016

Journal of Cell Science

View full text Add to dashboard Cite

Ribosome biogenesis is a fundamental multistep process initiated by the synthesis of 90S pre-ribosomal particles in the nucleoli of higher eukaryotes. Even though synthesis of ribosomes stops during mitosis while nucleoli disappear, mitotic pre-ribosomal particles persist as observed in pre-nucleolar bodies (PNBs) during telophase. To further understand the relationship between the nucleolus and the PNBs, the presence and the fate of the mitotic pre-ribosomal particles during cell division were investigated. We demonstrate that the recently synthesized 45S precursor ribosomal RNAs ( pre-rRNAs) as well as the 32S and 30S pre-rRNAs are maintained during mitosis and associated with the chromosome periphery together with pre-rRNA processing factors. Maturation of the mitotic pre-ribosomal particles, as assessed by the stability of the mitotic pre-rRNAs, is transiently arrested during mitosis by a cyclin-dependent kinase (CDK)1-cyclin-B-dependent mechanism and can be restored by CDK inhibitor treatments. At the M-G1 transition, the resumption of mitotic prerRNA processing in PNBs does not induce the disappearance of PNBs; this only occurs when functional nucleoli reform. Strikingly, during their maturation process, mitotic pre-rRNAs localize in reforming nucleoli.

show abstract

Post-mitotic dynamics of pre-nucleolar bodies is driven by pre-ribosomal RNA processing

Cited by 24 publications

References 53 publications

RNA-dependent disassembly of nuclear bodies

RNA-dependent disassembly of nuclear bodies

RNA transcription modulates phase transition-driven nuclear body assembly

Sharing of mitotic pre-ribosomal particles between daughter cells

Contact Info

Product

Resources

About