Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos

Rose, Lesilee S.; Gönczy, Pierre

doi:10.1895/wormbook.1.30.2

Cited by 178 publications

(225 citation statements)

References 111 publications

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“…Once the centrosome is attached to the male pronucleus, the female pronucleus captures a microtubule from the aster that is associated with the male pronucleus before dynein on the female pronucleus pulls the two pronuclei together ( Fig. 1B) (Malone et al, 2003;Rose and Gonczy, 2014). In zebrafish, pronuclear migration uses a similar mechanism.…”

Section: Pronuclear Migration In the Newly Fertilized Zygotementioning

confidence: 99%

Nuclear migration events throughout development

Bone

Starr

2016

Journal of Cell Science

103

113

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Moving the nucleus to a specific position within the cell is an important event during many cell and developmental processes. Several different molecular mechanisms exist to position nuclei in various cell types. In this Commentary, we review the recent progress made in elucidating mechanisms of nuclear migration in a variety of important developmental models. Genetic approaches to identify mutations that disrupt nuclear migration in yeast, filamentous fungi, Caenorhabditis elegans, Drosophila melanogaster and plants led to the identification of microtubule motors, as well as Sad1p, UNC-84 (SUN) domain and Klarsicht, ANC-1, Syne homology (KASH) domain proteins (LINC complex) that function to connect nuclei to the cytoskeleton. We focus on how these proteins and various mechanisms move nuclei during vertebrate development, including processes related to wound healing of fibroblasts, fertilization, developing myotubes and the developing central nervous system. We also describe how nuclear migration is involved in cells that migrate through constricted spaces. On the basis of these findings, it is becoming increasingly clear that defects in nuclear positioning are associated with human diseases, syndromes and disorders.

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Section: Pronuclear Migration In the Newly Fertilized Zygotementioning

confidence: 99%

Nuclear migration events throughout development

Bone

Starr

2016

Journal of Cell Science

103

113

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“…To study nucleolar assembly dynamics, we use the C. elegans embryo system (19), which exhibits stereotyped cycles of nucleolar…”

Section: In Vivo Measurements Of Nuclear Body Dynamicsmentioning

confidence: 99%

RNA transcription modulates phase transition-driven nuclear body assembly

Berry

Weber

Vaidya

et al. 2015

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

439

426

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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...

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“…The two cells also divide asynchronously with the former dividing approximately 2 min earlier than the latter (2). Maternally provided PAR proteins were found to regulate the asynchrony by controlling the timing of mitotic entry and the rate of DNA replication (5,6). Recent developments in live cell imaging and automated cell tracking have greatly facilitated systematic and accurate measurement of cell division timing during entire or partial embryogenesis (7)(8)(9), which allows for identification of genes that control temporal coordination of cell division during metazoan embryogenesis.…”

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confidence: 99%

Timing of Tissue-specific Cell Division Requires a Differential Onset of Zygotic Transcription during Metazoan Embryogenesis

Wong

Guan

et al. 2016

Journal of Biological Chemistry

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Metazoan development demands not only precise cell fate differentiation but also accurate timing of cell division to ensure proper development. How cell divisions are temporally coordinated during development is poorly understood. Caenorhabditis elegans embryogenesis provides an excellent opportunity to study this coordination due to its invariant development and widespread division asynchronies. One of the most pronounced asynchronies is a significant delay of cell division in two endoderm progenitor cells, Ea and Ep, hereafter referred to as E2, relative to its cousins that mainly develop into mesoderm organs and tissues. To unravel the genetic control over the endodermspecific E2 division timing, a total of 822 essential and conserved genes were knocked down using RNAi followed by quantification of cell cycle lengths using in toto imaging of C. elegans embryogenesis and automated lineage. Intriguingly, knockdown of numerous genes encoding the components of general transcription pathway or its regulatory factors leads to a significant reduction in the E2 cell cycle length but an increase in cell cycle length of the remaining cells, indicating a differential requirement of transcription for division timing between the two. Analysis of lineage-specific RNA-seq data demonstrates an earlier onset of transcription in endoderm than in other germ layers, the timing of which coincides with the birth of E2, supporting the notion that the endoderm-specific delay in E2 division timing demands robust zygotic transcription. The reduction in E2 cell cycle length is frequently associated with cell migration defect and gastrulation failure. The results suggest that a tissue-specific transcriptional activation is required to coordinate fate differentiation, division timing, and cell migration to ensure proper development.Proper development of metazoans depends not only on precise differentiation of cell fate but also on tight control over division timing or division pace between cells, which we refer to as temporal coordination. A normal fate specification without correct division timing may lead to catastrophes, for example, cancerous development (1). Therefore, metazoan development demonstrates stereotyped division timing (2, 3). Despite intensive studies on the regulation of cell fate differentiation, genetic control over temporal coordination of cell division during metazoan development is poorly understood. Timing of cell division is particularly critical during early developmental stages such as embryogenesis when cells undergo rapid division and migration, which is concomitant with cell fate differentiation.Because of technical challenges in quantifying cell division timing especially when an embryo undergoes rapid cell division, most of the studies on cell division timing focus on the earliest stage of development (4). For example, the first embryonic division in Caenorhabditis elegans produces two daughters, namely AB and P1, with differential developmental potential. The two cells also divide asynchronously with the ...

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Polarity establishment, asymmetric division and segregation of fate determinants in early C. elegans embryos

Cited by 178 publications

References 111 publications

Nuclear migration events throughout development

Nuclear migration events throughout development

RNA transcription modulates phase transition-driven nuclear body assembly

Timing of Tissue-specific Cell Division Requires a Differential Onset of Zygotic Transcription during Metazoan Embryogenesis

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