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.

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.

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 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.

scholarly journals MEX-3 interacting proteins link cell polarity to asymmetric gene expression in Caenorhabditis elegans

Development ◽  
2002 ◽  
Vol 129 (3) ◽  
pp. 747-759 ◽  
Author(s):  
Nancy N. Huang ◽  
Darcy E. Mootz ◽  
Albertha J. M. Walhout ◽  
Marc Vidal ◽  
Craig P. Hunter
Keyword(s):  
Cell Fate ◽  
Spatial Information ◽  
Zinc Finger Protein ◽  
Early Embryo ◽  
Rna Recognition Motif ◽  
Homeodomain Protein ◽  
Interacting Proteins ◽  
Cell Stage ◽  
C Elegans ◽  
Temporal And Spatial

The KH domain protein MEX-3 is central to the temporal and spatial control of PAL-1 expression in the C. elegans early embryo. PAL-1 is a Caudal-like homeodomain protein that is required to specify the fate of posterior blastomeres. While pal-1 mRNA is present throughout the oocyte and early embryo, PAL-1 protein is expressed only in posterior blastomeres, starting at the four-cell stage. To better understand how PAL-1 expression is regulated temporally and spatially, we have identified MEX-3 interacting proteins (MIPs) and characterized in detail two that are required for the patterning of PAL-1 expression. RNA interference of MEX-6, a CCCH zinc-finger protein, or SPN-4, an RNA recognition motif protein, causes PAL-1 to be expressed in all four blastomeres starting at the four-cell stage. Genetic analysis of the interactions between these mip genes and the par genes, which provide polarity information in the early embryo, defines convergent genetic pathways that regulate MEX-3 stability and activity to control the spatial pattern of PAL-1 expression. These experiments suggest that par-1 and par-4 affect distinct processes. par-1 is required for many aspects of embryonic polarity, including the restriction of MEX-3 and MEX-6 activity to the anterior blastomeres. We find that PAL-1 is not expressed in par-1 mutants, because MEX-3 and MEX-6 remain active in the posterior blastomeres. The role of par-4 is less well understood. Our analysis suggests that par-4 is required to inactivate MEX-3 at the four-cell stage. Thus, PAL-1 is not expressed in par-4 mutants because MEX-3 remains active in all blastomeres. We propose that MEX-6 and SPN-4 act with MEX-3 to translate the temporal and spatial information provided by the early acting par genes into the asymmetric expression of the cell fate determinant PAL-1.

scholarly journals Microfluidic Platform for Analyzing the Thermotaxis of C. elegans in a Linear Temperature Gradient

2017 ◽  
Vol 33 (12) ◽  
pp. 1435-1440 ◽  
Author(s):  
Sunhee YOON ◽  
Hailing PIAO ◽  
Tae-Joon JEON ◽  
Sun Min KIM
Keyword(s):  
Temperature Gradient ◽  
Linear Temperature ◽  
Microfluidic Platform ◽  
C Elegans ◽  
Linear Temperature Gradient

scholarly journals LIN28 coordinately promotes nucleolar/ribosomal functions and represses the 2C-like transcriptional program in pluripotent stem cells

2021 ◽  
Author(s):  
Zhen Sun ◽  
Hua Yu ◽  
Jing Zhao ◽  
Tianyu Tan ◽  
Hongru Pan ◽  
...  
Keyword(s):  
Stem Cells ◽  
Embryo Development ◽  
Pluripotent Stem Cells ◽  
Rna Binding ◽  
Stem Cell Differentiation ◽  
Early Embryo ◽  
Transcriptional Program ◽  
Cell Stage ◽  
Early Embryo Development ◽  
Nucleolar Stress

AbstractLIN28 is an RNA binding protein with important roles in early embryo development, stem cell differentiation/reprogramming, tumorigenesis and metabolism. Previous studies have focused mainly on its role in the cytosol where it interacts with Let-7 microRNA precursors or mRNAs, and few have addressed LIN28’s role within the nucleus. Here, we show that LIN28 displays dynamic temporal and spatial expression during murine embryo development. Maternal LIN28 expression drops upon exit from the 2-cell stage, and zygotic LIN28 protein is induced at the forming nucleolus during 4-cell to blastocyst stage development, to become dominantly expressed in the cytosol after implantation. In cultured pluripotent stem cells (PSCs), loss of LIN28 led to nucleolar stress and activation of a 2-cell/4-cell-like transcriptional program characterized by the expression of endogenous retrovirus genes. Mechanistically, LIN28 binds to small nucleolar RNAs and rRNA to maintain nucleolar integrity, and its loss leads to nucleolar phase separation defects, ribosomal stress and activation of P53 which in turn binds to and activates 2C transcription factor Dux. LIN28 also resides in a complex containing the nucleolar factor Nucleolin (NCL) and the transcriptional repressor TRIM28, and LIN28 loss leads to reduced occupancy of the NCL/TRIM28 complex on the Dux and rDNA loci, and thus de-repressed Dux and reduced rRNA expression. Lin28 knockout cells with nucleolar stress are more likely to assume a slowly cycling, translationally inert and anabolically inactive state, which is a part of previously unappreciated 2C-like transcriptional program. These findings elucidate novel roles for nucleolar LIN28 in PSCs, and a new mechanism linking 2C program and nucleolar functions in PSCs and early embryo development.

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