scholarly journals Contact-dependent cell-cell communications drive morphological invariance during ascidian embryogenesis

2017 ◽  
Author(s):  
Léo Guignard ◽  
Ulla-Maj Fiuza ◽  
Bruno Leggio ◽  
Emmanuel Faure ◽  
Julien Laussu ◽  
...  

ABSTRACTCanalization of developmental processes ensures the reproducibility and robustness of embryogenesis within each species. In its extreme form, found in ascidians, early embryonic cell lineages are invariant between embryos within and between species, despite rapid genomic divergence. To resolve this paradox, we used live light-sheet imaging to quantify individual cell behaviors in digitalized embryos and explore the forces that canalize their development. This quantitative approach revealed that individual cell geometries and cell contacts are strongly constrained, and that these constraints are tightly linked to the control of fate specification by local cell inductions. While in vertebrates ligand concentration usually controls cell inductions, we found that this role is fulfilled in ascidians by the area of contacts between signaling and responding cells. We propose that the duality between geometric and genetic control of inductions contributes to the counterintuitive inverse correlation between geometric and genetic variability during embryogenesis.

Science ◽  
2020 ◽  
Vol 369 (6500) ◽  
pp. eaar5663 ◽  
Author(s):  
Léo Guignard ◽  
Ulla-Maj Fiúza ◽  
Bruno Leggio ◽  
Julien Laussu ◽  
Emmanuel Faure ◽  
...  

Marine invertebrate ascidians display embryonic reproducibility: Their early embryonic cell lineages are considered invariant and are conserved between distantly related species, despite rapid genomic divergence. Here, we address the drivers of this reproducibility. We used light-sheet imaging and automated cell segmentation and tracking procedures to systematically quantify the behavior of individual cells every 2 minutes during Phallusia mammillata embryogenesis. Interindividual reproducibility was observed down to the area of individual cell contacts. We found tight links between the reproducibility of embryonic geometries and asymmetric cell divisions, controlled by differential sister cell inductions. We combined modeling and experimental manipulations to show that the area of contact between signaling and responding cells is a key determinant of cell communication. Our work establishes the geometric control of embryonic inductions as an alternative to classical morphogen gradients and suggests that the range of cell signaling sets the scale at which embryonic reproducibility is observed.


2020 ◽  
Author(s):  
Simone Probst ◽  
Sagar ◽  
Jelena Tosic ◽  
Carsten Schwan ◽  
Dominic Grün ◽  
...  

AbstractAnterior mesoderm (AM) and definitive endoderm (DE) progenitors represent the earliest embryonic cell types that are specified during germ layer formation at the primitive streak (PS) of the mouse embryo. Genetic experiments indicate that both lineages segregate from Eomes expressing progenitors in response to different NODAL signaling levels. However, the precise spatiotemporal pattern of the emergence of these cell types and molecular details of lineage segregation remain unexplored. We combined genetic fate labeling and imaging approaches with scRNA-seq to follow the transcriptional identities and define lineage trajectories of Eomes dependent cell types. All cells moving through the PS during the first day of gastrulation express Eomes. AM and DE specification occurs before cells leave the PS from discrete progenitor populations that are generated in distinct spatiotemporal patterns. Importantly, we don’t find evidence for the existence of progenitors that co-express markers of both cell lineages suggesting an immediate and complete separation of AM and DE lineages.Summary statementCells lineages are specified in the mouse embryo already within the primitive streak where Mesp1+ mesoderm and Foxa2+ endoderm are generated in a spatial and temporal sequence from unbiased progenitors.


eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Alberto Stolfi ◽  
Elijah K Lowe ◽  
Claudia Racioppi ◽  
Filomena Ristoratore ◽  
C Titus Brown ◽  
...  

Ascidians present a striking dichotomy between conserved phenotypes and divergent genomes: embryonic cell lineages and gene expression patterns are conserved between distantly related species. Much research has focused on Ciona or Halocynthia spp. but development in other ascidians remains poorly characterized. In this study, we surveyed the multipotent myogenic B7.5 lineage in Molgula spp. Comparisons to the homologous lineage in Ciona revealed identical cell division and fate specification events that result in segregation of larval, cardiac, and pharyngeal muscle progenitors. Moreover, the expression patterns of key regulators are conserved, but cross-species transgenic assays uncovered incompatibility, or ‘unintelligibility’, of orthologous cis-regulatory sequences between Molgula and Ciona. These sequences drive identical expression patterns that are not recapitulated in cross-species assays. We show that this unintelligibility is likely due to changes in both cis- and trans-acting elements, hinting at widespread and frequent turnover of regulatory mechanisms underlying otherwise conserved aspects of ascidian embryogenesis.


Genetics ◽  
1980 ◽  
Vol 96 (2) ◽  
pp. 435-454 ◽  
Author(s):  
H Robert Horvitz ◽  
John E Sulston

ABSTRACT Twenty-four mutants that alter the normally invariant post-embryonic cell lineages of the nematode Caenorhabditis elegans have been isolated and genetically characterized. In some of these mutants, cell divisions fail that occur in wild-type animals; in other mutants, cells divide that do not normally do so. The mutants differ in the specificities of their defects, so that it is possible to identify mutations that affect some cell lineages but not others. These mutants define 14 complementation groups, which have been mapped. The abnormal phenotype of most of the cell-lineage mutants results from a single recessive mutation; however, the excessive cell divisions characteristic of one strain, CB1322, require the presence of two unlinked recessive mutations. All 24 cell-lineage mutants display incomplete penetrance and/or variable expressivity. Three of the mutants are suppressed by pleiotropic suppressors believed to be specific for null alleles, suggesting that their phenotypes result from the complete absence of gene activity.


Author(s):  
Yanzhu Yue ◽  
Xin Li ◽  
Youdong Zhang ◽  
Aibin He

Abstract Mapping holistic cell behaviors sculpting mammalian heart has been a goal, but so far only successes in transparent invertebrates and lower vertebrates. Using a live-imaging system comprising a customized vertical light-sheet microscope equipped with a culture module, a heartbeat-gated imaging strategy, and a digital image processing framework, we realized imaging of developing mouse hearts with uninterrupted cell lineages for up to 1.5 days. Four-dimensional landscapes of cell behaviors revealed a blueprint for ventricle chamber formation in which biased outward migration of outermost cardiomyocytes coupled with cell intercalation and horizontal division. The trabeculae, an inner muscle architecture, was developed through early fate segregation and transmural cell arrangement involving both oriented cell division and directional migration. Thus, live-imaging reconstruction affords a transformative means for deciphering mammalian organogenesis.


Blood ◽  
1985 ◽  
Vol 66 (2) ◽  
pp. 327-332 ◽  
Author(s):  
AG Leary ◽  
LC Strauss ◽  
CI Civin ◽  
M Ogawa

Abstract We analyzed the differentiation of hemopoietic colonies derived from human paired daughter cells. Candidate progenitor cells were isolated by use of a micromanipulation technique from cultures of My-10 antigen- positive cord blood cells. Then nine to 36 hours later, the paired daughter cells were separated with a micromanipulator and allowed to form colonies in methylcellulose medium containing erythropoietin, phytohemagglutinin leukocyte-conditioned medium, and platelet-poor plasma. The cellular composition of the colonies was determined by differentiating all of the cells of the May-Grunwald-Giemsa-stained preparation. Of a total of 75 evaluable pairs of colonies, 35 consisted of 28 types of disparate pairs revealing nonhomologous lineage combinations. Forty pairs were homologous in lineage expression. However, the proportions of the individual cell lineages were significantly different in the members of some of the homologous pairs. Some pairs revealed significant differences in colony size. These observations are similar to those reported for murine paired progenitors and are consistent with the stochastic model of human stem cell differentiation.


2021 ◽  
Author(s):  
Laura Glorieux ◽  
Aleksandra Sapala ◽  
David Willnow ◽  
Manon Moulis ◽  
Shlomit Edri ◽  
...  

AbstractGenerating comprehensive image maps, while preserving spatial 3D context, is essential to quantitatively assess and locate specific cellular features and cell-cell interactions during organ development. Despite the recent advances in 3D imaging approaches, our current knowledge of the spatial organization of distinct cell types in the embryonic pancreatic tissue is still largely based on 2D histological sections. Here, we present a light-sheet fluorescence microscopy approach to image the pancreas in 3D and map tissue interactions at key development time points in the mouse embryo. We used transgenic mouse models and antibodies to visualize the three main cellular components within the developing pancreas, including epithelial, mesenchymal and endothelial cell populations. We demonstrated the utility of the approach by providing volumetric data, 3D distribution of distinct progenitor populations and quantification of relative cellular abundance within the tissue. Lastly, our image data were combined in an open source online repository (referred to as Pancreas Embryonic Cell Atlas). This image dataset will serve the scientific community by enabling further investigation on pancreas organogenesis but also for devising strategies for the in vitro generation of transplantable pancreatic tissue for regenerative therapies.


2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Benedict Borer ◽  
Davide Ciccarese ◽  
David Johnson ◽  
Dani Or

AbstractEvidence suggests that bacterial community spatial organization affects their ecological function, yet details of the mechanisms that promote spatial patterns remain difficult to resolve experimentally. In contrast to bacterial communities in liquid cultures, surface-attached range expansion fosters genetic segregation of the growing population with preferential access to nutrients and reduced mechanical restrictions for cells at the expanding periphery. Here we elucidate how localized conditions in cross-feeding bacterial communities shape community spatial organization. We combine experiments with an individual based mathematical model to resolve how trophic dependencies affect localized growth rates and nucleate successful cell lineages. The model tracks individual cell lineages and attributes these with trophic dependencies that promote counterintuitive reproductive advantages and result in lasting influences on the community structure, and potentially, on its functioning. We examine persistence of lucky lineages in structured habitats where expansion is interrupted by physical obstacles to gain insights into patterns in porous domains.


Author(s):  
G. v. Ehrenstein ◽  
J. E. Sulston ◽  
E. Schierenberg ◽  
J. S. Laufer ◽  
T. Cole

Development ◽  
1995 ◽  
Vol 121 (10) ◽  
pp. 3175-3185 ◽  
Author(s):  
M.Q. Martindale ◽  
J.Q. Henry

The nemerteans belong to a phylum of coelomate worms that display a highly conserved pattern of cell divisions referred to as spiral cleavage. It has recently been shown that the fates of the four embryonic cell quadrants in two species of nemerteans are not homologous to those in other spiralian embryos, such as the annelids and molluscs (Henry, J. Q. and Martindale, M. Q. (1994a) Develop. Genetics 15, 64–78). Equal-cleaving molluscs utilize inductive interactions to establish quadrant-specific cell fates and embryonic symmetry properties following fifth cleavage. In order to elucidate the manner in which cell fates are established in nemertean embryos, we have conducted cell isolation and deletion experiments to examine the developmental potential of the early cleavage blastomeres of two equal-cleaving nemerteans, Nemertopsis bivittata and Cerebratulus lacteus. These two species display different modes of development: N. bivittata develops directly via a non-feeding larvae, while C. lacteus develops to form a feeding pilidium larva which undergoes a radical metamorphosis to give rise to the juvenile worm. By examining the development of certain structures and cell types characteristic of quadrant-specific fates for each of these species, we have shown that isolated blastomeres of the indirect-developing nemertean, C. lacteus, are capable of generating cell fates that are not a consequence of that cell's normal developmental program. For instance, dorsal blastomeres can form muscle fibers when cultured in isolation. In contrast, isolated blastomeres of the direct-developing species, N. bivittata do not regulate their development to the same extent. Some cell fates are specified in a precocious manner in this species, such as those that give rise to the eyes. Thus, these findings indicate that equal-cleaving spiralian embryos can utilize different mechanisms of cell fate and axis specification. The implications of these patterns of nemertean development are discussed in relation to experimental work in other spiralian embryos, and a model is presented that accounts for possible evolutionary changes in cell lineage and the process of cell fate specification amongst these protostome phyla.


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