scholarly journals Binary decision between asymmetric and symmetric cell division is defined by the balance of PAR proteins in C. elegans embryos

2020 ◽  
Author(s):  
Yen Wei Lim ◽  
Fu-Lai Wen ◽  
Prabhat Shankar ◽  
Tatsuo Shibata ◽  
Fumio Motegi
Keyword(s):  
Cell Division ◽  
Binary Choice ◽  
Cell Stage ◽  
Par Proteins ◽  
Binary Decision ◽  
C Elegans ◽  
Show Evidence ◽  
Differentiation And Proliferation ◽  
Fate Determinants ◽  
Sister Cells

ABSTRACTCoordination between cell differentiation and proliferation during development requires the balance between asymmetric and symmetric modes of cell division. However, the cellular intrinsic cue underlying the binary choice between these two division modes remains elusive. Here we show evidence in Caenorhabditis elegans that the invariable lineage of the division modes is programmed by the balance between antagonizing complexes of partitioning-defective (PAR) proteins. By uncoupling unequal inheritance of PAR proteins from that of fate determinants during zygote division, we demonstrated that changes in the balance between PAR-2 and PAR-6 are sufficient to re-program the division modes from symmetric to asymmetric and vice versa in two-cell stage embryos. The division mode adopted occurs independently of asymmetry in cytoplasmic fate determinants, cell-size asymmetry, and cell-cycle asynchrony between the sister cells. We propose that the balance between antagonizing PAR proteins represents an intrinsic self-organizing cue for binary specification of the division modes during development.

OOC-3, a novel putative transmembrane protein required for establishment of cortical domains and spindle orientation in the P(1) blastomere of C. elegans embryos

Development ◽  
2000 ◽  
Vol 127 (10) ◽  
pp. 2063-2073 ◽  
Author(s):  
S. Pichler ◽  
P. Gonczy ◽  
H. Schnabel ◽  
A. Pozniakowski ◽  
A. Ashford ◽  
...  
Keyword(s):  
Cell Division ◽  
Asymmetric Cell Division ◽  
Transmembrane Protein ◽  
Cell Stage ◽  
Par Proteins ◽  
Asymmetric Cell Divisions ◽  
C Elegans ◽  
Membrane Compartment ◽  
Chromosome Ii

Asymmetric cell divisions require the establishment of an axis of polarity, which is subsequently communicated to downstream events. During the asymmetric cell division of the P(1) blastomere in C. elegans, establishment of polarity depends on the establishment of anterior and posterior cortical domains, defined by the localization of the PAR proteins, followed by the orientation of the mitotic spindle along the previously established axis of polarity. To identify genes required for these events, we have screened a collection of maternal-effect lethal mutations on chromosome II of C. elegans. We have identified a mutation in one gene, ooc-3, with mis-oriented division axes at the two-cell stage. Here we describe the phenotypic and molecular characterization of ooc-3. ooc-3 is required for the correct localization of PAR-2 and PAR-3 cortical domains after the first cell division. OOC-3 is a novel putative transmembrane protein, which localizes to a reticular membrane compartment, probably the endoplasmic reticulum, that spans the whole cytoplasm and is enriched on the nuclear envelope and cell-cell boundaries. Our results show that ooc-3 is required to form the cortical domains essential for polarity after cell division.

Early transcription in Caenorhabditis elegans embryos

Development ◽  
1994 ◽  
Vol 120 (2) ◽  
pp. 443-451 ◽  
Author(s):  
L.G. Edgar ◽  
N. Wolf ◽  
W.B. Wood
Keyword(s):  
Cell Division ◽  
Caenorhabditis Elegans ◽  
Cell Stage ◽  
Cell Cycles ◽  
Cell Lineages ◽  
C Elegans ◽  
Early Transcription ◽  
Alpha Amanitin ◽  
Autoradiographic Detection ◽  
Specific Timing

We have analysed early transcription in devitellinized, cultured embryos of the nematode Caenorhabditis elegans by two methods: measurement of [32P]UTP uptake into TCA-precipitable material and autoradiographic detection of [3H]UTP labelling both in the presence and absence of alpha-amanitin. RNA synthesis was first detected at the 8- to 12-cell stage, and alpha-amanitin sensitivity also appeared at this time, during the cleavages establishing the major founder cell lineages. The requirements for maternally supplied versus embryonically produced gene products in early embryogenesis were examined in the same culture system by observing the effects of alpha-amanitin on cell division and the early stereotyped lineage patterns. In the presence of high levels of alpha-amanitin added at varying times from two cells onward, cell division continued until approximately the 100-cell stage and then stopped during a single round of cell division. The characteristic unequal early cleavages, orientation of cleavage planes and lineage-specific timing of early divisions were unaffected by alpha-amanitin in embryos up to 87 cells. These results indicate that embryonic transcription starts well before gastrulation in C. elegans embryos, but that although embryonic transcripts may have important early functions, maternal products can support at least the mechanics of the first 6 to 7 cell cycles.

scholarly journals Probing and manipulating embryogenesis via nanoscale thermometry and temperature control

2020 ◽  
Vol 117 (26) ◽  
pp. 14636-14641 ◽  
Author(s):  
Joonhee Choi ◽  
Hengyun Zhou ◽  
Renate Landig ◽  
Hai-Yin Wu ◽  
Xiaofei Yu ◽  
...  
Keyword(s):  
Cell Cycle ◽  
Cell Division ◽  
Cell Communication ◽  
Cycle Duration ◽  
Cell Stage ◽  
C Elegans ◽  
Local Perturbations ◽  
Cell Division Timing ◽  
Nanoscale Thermometry

Understanding the coordination of cell-division timing is one of the outstanding questions in the field of developmental biology. One active control parameter of the cell-cycle duration is temperature, as it can accelerate or decelerate the rate of biochemical reactions. However, controlled experiments at the cellular scale are challenging, due to the limited availability of biocompatible temperature sensors, as well as the lack of practical methods to systematically control local temperatures and cellular dynamics. Here, we demonstrate a method to probe and control the cell-division timing inCaenorhabditis elegansembryos using a combination of local laser heating and nanoscale thermometry. Local infrared laser illumination produces a temperature gradient across the embryo, which is precisely measured by in vivo nanoscale thermometry using quantum defects in nanodiamonds. These techniques enable selective, controlled acceleration of the cell divisions, even enabling an inversion of division order at the two-cell stage. Our data suggest that the cell-cycle timing asynchrony of the early embryonic development inC. elegansis determined independently by individual cells rather than via cell-to-cell communication. Our method can be used to control the development of multicellular organisms and to provide insights into the regulation of cell-division timings as a consequence of local perturbations.

The Caenorhabditis elegans polarity gene ooc-5 encodes a Torsin-related protein of the AAA ATPase superfamily

Development ◽  
2001 ◽  
Vol 128 (22) ◽  
pp. 4645-4656 ◽  
Author(s):  
Stephen E. Basham ◽  
Lesilee S. Rose
Keyword(s):  
Cell Fate ◽  
Protein Complexes ◽  
Sequence Similarity ◽  
Normal Function ◽  
Par Proteins ◽  
Torsion Dystonia ◽  
Aaa Atpase ◽  
C Elegans ◽  
Fate Determinants ◽  
Cell Fate Determinants

The PAR proteins are required for polarity and asymmetric localization of cell fate determinants in C. elegans embryos. In addition, several of the PAR proteins are conserved and localized asymmetrically in polarized cells in Drosophila, Xenopus and mammals. We have previously shown that ooc-5 and ooc-3 mutations result in defects in spindle orientation and polarity in early C. elegans embryos. In particular, mutations in these genes affect the re-establishment of PAR protein asymmetry in the P1 cell of two-cell embryos. We now report that ooc-5 encodes a putative ATPase of the Clp/Hsp100 and AAA superfamilies of proteins, with highest sequence similarity to Torsin proteins; the gene for human Torsin A is mutated in individuals with early-onset torsion dystonia, a neuromuscular disease. Although Clp/Hsp100 and AAA family proteins have roles in diverse cellular activities, many are involved in the assembly or disassembly of proteins or protein complexes; thus, OOC-5 may function as a chaperone. OOC-5 protein co-localizes with a marker of the endoplasmic reticulum in all blastomeres of the early C. elegans embryo, in a pattern indistinguishable from that of OOC-3 protein. Furthermore, OOC-5 localization depends on the normal function of the ooc-3 gene. These results suggest that OOC-3 and OOC-5 function in the secretion of proteins required for the localization of PAR proteins in the P1 cell, and may have implications for the study of torsion dystonia.

Cell polarity and asymmetric cell division: the C. elegans early embryo

2012 ◽  
Vol 53 ◽  
pp. 1-14 ◽  
Author(s):  
Anna Noatynska ◽  
Monica Gotta
Keyword(s):  
Cell Migration ◽  
Cell Division ◽  
Cell Polarity ◽  
Asymmetric Cell Division ◽  
Early Embryo ◽  
Animal Cells ◽  
Par Proteins ◽  
C Elegans ◽  
Lethal Mutations ◽  
Tissue Organization

Cell polarity is crucial for many functions including cell migration, tissue organization and asymmetric cell division. In animal cells, cell polarity is controlled by the highly conserved PAR (PARtitioning defective) proteins. par genes have been identified in Caenorhabditis elegans in screens for maternal lethal mutations that disrupt cytoplasmic partitioning and asymmetric division. Although PAR proteins were identified more than 20 years ago, our understanding on how they regulate polarity and how they are regulated is still incomplete. In this chapter we review our knowledge of the processes of cell polarity establishment and maintenance, and asymmetric cell division in the early C. elegans embryo. We discuss recent findings that highlight new players in cell polarity and/or reveal the molecular details on how PAR proteins regulate polarity processes.

scholarly journals Early C. elegans embryos modulate cell division timing to compensate for, and survive, the discordant conditions of a severe temperature gradient

2020 ◽  
Author(s):  
Eric Terry ◽  
Bilge Birsoy ◽  
David Bothman ◽  
Marin Sigurdson ◽  
Pradeep M. Joshi ◽  
...  
Keyword(s):  
Cell Division ◽  
Temperature Gradient ◽  
Early Embryo ◽  
Cell Stage ◽  
Division Rate ◽  
Cellular Division ◽  
C Elegans ◽  
Average Decrease ◽  
Slow Development ◽  
Steep Temperature Gradient

AbstractDespite a constant barrage of intrinsic and environmental noise, embryogenesis is remarkably reliable, suggesting the existence of systems that ensure faithful execution of this complex process. We report that early C. elegans embryos, which normally show a highly reproducible lineage and cellular geometry, can compensate for deviations imposed by the discordant conditions of a steep temperature gradient generated in a microfluidic device starting at the two-cell stage. Embryos can survive a gradient of up to 7.5°C across the 50-micron axis through at least three rounds of division. This response is orientation-dependent: survival is higher when the normally faster-dividing anterior daughter of the zygote, AB, but not its sister, the posterior P1, is warmer. We find that temperature-dependent cellular division rates in the early embryo can be effectively modeled by a modification of the Arrhenius equation. Further, both cells respond to the gradient by dramatically reducing division rates compared to the predicted rates for the temperature experienced by the cell even though the temperature extremes are well within the range for normal development. This finding suggests that embryos may sense discordance and slow development in response. We found that in the cohort of surviving embryos, the cell on the warmer side at the two-cell stage shows a greater average decrease in expected division rate than that on the cooler side, thereby preserving the normal cellular geometry of the embryo under the discordant conditions. A diminished average slow-down response correlated with lethality, presumably owing to disruption of normal division order and developmental fidelity. Remarkably, some inviable embryos in which the canonical division order was reversed nonetheless proceeded through relatively normal morphogenesis, suggesting a subsequent compensation mechanism independent of cell division control. These findings provide evidence for a previously unrecognized process in C. elegans embryos that may serve to compensate for deviations imposed by aberrant environmental conditions, thereby resulting in a high-fidelity output.

Cell division and cell allocation in early mouse development

Development ◽  
1978 ◽  
Vol 48 (1) ◽  
pp. 37-51
Author(s):  
S. J. Kelly ◽  
J. G. Mulnard ◽  
C. F. Graham
Keyword(s):  
Cell Division ◽  
Tritiated Thymidine ◽  
Mouse Embryos ◽  
Mouse Development ◽  
Stages Of Development ◽  
Cell Stage ◽  
Cell Cycles ◽  
Short Cell ◽  
Early Mouse

Cell division was observed in intact and dissociated mouse embryos between the 2-cell stage and the blastocyst in embryos developing in culture. Division to the 4-cell stage was usually asynchronous. The first cell to divide to the 4-cell stage produced descendants which tended to divide ahead of those cells produced by its slow partner at all subsequent stages of development up to the blastocyte stage. The descendants of the first cell to divide to the 4-cell stage did not subsequently have short cell cycles. The first cell or last cell to divide from the 4-cell stage was labelled with tritiated thymidine. The embryo was reassembled, and it was found that the first pair of cells to reach the 8-cell stage contributed disproportionately more descendants to the ICM when compared with the last cell to divide to the 8-cell stage.

When and how does cell division order influence cell allocation to the inner cell mass of the mouse blastocyst?

Development ◽  
1987 ◽  
Vol 100 (2) ◽  
pp. 325-332
Author(s):  
C.L. Garbutt ◽  
M.H. Johnson ◽  
M.A. George
Keyword(s):  
Cell Division ◽  
Cell Population ◽  
Inner Cell Mass ◽  
Cell Mass ◽  
Cell Lineage ◽  
The Other ◽  
Mouse Blastocyst ◽  
Short Term ◽  
Cell Stage ◽  
Cell Embryo

Aggregate 8-cell embryos were constructed from four 2/8 pairs of blastomeres, one of which was marked with a short-term cell lineage marker and was also either 4 h older (derived from an early-dividing 4-cell) or 4 h younger (derived from a late-dividing 4-cell) than the other three pairs. The aggregate embryos were cultured to the 16-cell stage, at which time a second marker was used to label the outside cell population. The embryos were then disaggregated and each cell was examined to determine its labelling pattern. From this analysis, we calculated the relative contributions to the inside cell population of the 16-cell embryo of older and younger cells. Older cells were found to contribute preferentially. However, if the construction of the aggregate 8-cell embryo was delayed until each of the contributing 2/8 cell pairs had undergone intercellular flattening and then had been exposed to medium low in calcium to reverse this flattening immediately prior to aggregation, the advantage possessed by the older cells was lost. These results support the suggestion that older cells derived from early-dividing 4-cell blastomeres contribute preferentially to the inner cell mass as a result of being early-flattening cells.

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