scholarly journals Unravelling the distinct contribution of cell shape changes and cell intercalation to tissue morphogenesis: the case of the Drosophila trachea

Open Biology ◽  
2020 ◽  
Vol 10 (11) ◽  
pp. 200329
Author(s):  
Sandra Casani ◽  
Jordi Casanova ◽  
Marta Llimargas
Keyword(s):  
Cell Elongation ◽  
Cell Shape ◽  
Convergent Extension ◽  
Experimental Conditions ◽  
Full Extension ◽  
Tracheal System ◽  
Dorsal Branch ◽  
Respective Contribution ◽  
Pulling Force ◽  
Cell Intercalation

Intercalation allows cells to exchange positions in a spatially oriented manner in an array of diverse processes, spanning convergent extension in embryonic gastrulation to the formation of tubular organs. However, given the co-occurrence of cell intercalation and changes in cell shape, it is sometimes difficult to ascertain their respective contribution to morphogenesis. A well-established model to analyse intercalation, particularly in tubular organs, is the Drosophila tracheal system. There, fibroblast growth factor (FGF) signalling at the tip of the dorsal branches generates a ‘pulling’ force believed to promote cell elongation and cell intercalation, which account for the final branch extension. Here, we used a variety of experimental conditions to study the contribution of cell elongation and cell intercalation to morphogenesis and analysed their mutual requirements. We provide evidence that cell intercalation does not require cell elongation and vice versa. We also show that the two cell behaviours are controlled by independent but simultaneous mechanisms, and that cell elongation is sufficient to account for full extension of the dorsal branch, while cell intercalation has a specific role in setting the diameter of this structure. Thus, rather than viewing changes in cell shape and cell intercalation as just redundant events that add robustness to a given morphogenetic process, we find that they can also act by contributing to different features of tissue architecture.

scholarly journals Myosin II activity is not required for Drosophila tracheal branching morphogenesis

2017 ◽  
Author(s):  
Amanda Ochoa-Espinosa ◽  
Stefan Harmansa ◽  
Emmanuel Caussinus ◽  
Markus Affolter
Keyword(s):  
Cell Migration ◽  
Myosin Ii ◽  
Branching Morphogenesis ◽  
Stalk Cell ◽  
Germ Band ◽  
Tracheal System ◽  
Tip Cell ◽  
Dorsal Branch ◽  
Cell Intercalation ◽  
Tip Cells

AbstractThe Drosophila tracheal system consists of an interconnected network of monolayered epithelial tubes that ensures oxygen transport in the larval and adult body. During tracheal dorsal branch (DB) development, individual DBs elongate as a cluster of cells, led by tip cells at the front and trailing cells in the rear. Branch elongation is accompanied by extensive cell intercalation and cell lengthening of the trailing stalk cells. While cell intercalation is governed by Myosin II (MyoII)-dependent forces during tissue elongation in the Drosophila embryo leading to germ-band extension, it remained unclear whether MyoII plays a similar active role during tracheal branch elongation and intercalation. Here, we use a nanobody-based approach to selectively knock-down MyoII in tracheal cells. Our data shows that despite the depletion of MyoII function, tip cells migration and stalk cell intercalation (SCI) proceeds at a normal rate. Therefore, our data confirms a model in which DB elongation and SCI in the trachea occurs as a consequence of tip cell migration, which produces the necessary forces for the branching process.Summary statementBranch elongation during Drosophila tracheal development mechanistically resembles MyoII-independent collective cell migration; tensile forces resulting from tip cell migration are reduced by cell elongation and passive stalk cell intercalation.AbbreviationsDBDorsal branchDCDorsal closureE-CadE-CadherinGBEGerm-band extensionMRLCMyosin regulatory light chainMyoIIMyosin IISCIstalk cell intercalationSqhSpaghetti squashSxllSex lethalTCTip cellTrTracheomere

scholarly journals Single-cell morphometrics reveals ancestral principles of notochord development

2020 ◽  
Author(s):  
Toby GR Andrews ◽  
Wolfram Ponisch ◽  
Ewa K Paluch ◽  
Benjamin Steventon ◽  
Elia Benito-Gutierrez
Keyword(s):  
Single Cell ◽  
Cell Shape ◽  
Cell Length ◽  
Spatial And Temporal Variation ◽  
Second Phase ◽  
Convergent Extension ◽  
Novel Approach ◽  
Specific Shape ◽  
Cell Intercalation ◽  
Anterior Posterior

During development, embryonic tissues are formed by the dynamic behaviours of their constituent cells, whose collective actions are tightly regulated in space and time. To understand such cell behaviours and how they have evolved, it is necessary to develop quantitative approaches to map out morphogenesis, so comparisons can be made across different tissues and organisms. With this idea in mind, here we sought to investigate ancestral principles of notochord development, by building a quantitative portrait of notochord morphogenesis in the amphioxus embryo, a basally-branching member of the chordate phylum. To this end, we developed a single-cell morphometrics pipeline to comprehensively catalogue the morphologies of thousands of notochord cells, and to project them simultaneously into a common mathematical space termed morphospace. This approach revealed complex patterns of cell-type specific shape trajectories, akin to those obtained using single-cell genomic approaches. By spatially mapping single-cell shape trajectories in whole segmented notochords, we found evidence of spatial and temporal variation in developmental dynamics. Such variations included temporal gradients of morphogenesis across the anterior-posterior embryonic axis, divergence of trajectories to different morphologies, and the convergence of different trajectories onto common morphologies. Through geometric simulations, we also identified an antagonistic relationship between cell shape regulation and growth that enables convergent extension to occur in two steps. First, by allowing growth to counterbalance loss of anterior-posterior cell length during cell intercalation. Secondly, by allowing growth to further increase cell length once cells have intercalated and aligned to the axial midline, thereby facilitating a second phase of tissue elongation. Finally, we show that apart from a complex coordination of individual cellular behaviours, posterior addition from proliferating progenitors is essential for full notochord elongation in amphioxus, a mechanism previously described only in vertebrates. This novel approach to quantifying morphogenesis paves the way towards comparative studies, and mechanistic explanations for the emergence of form over developmental and evolutionary time scales.

Apical control of band elongation in Antithamnion defectum (Ceramiaceae, Rhodophyta)

1988 ◽  
Vol 66 (7) ◽  
pp. 1308-1315 ◽  
Author(s):  
David Garbary ◽  
Daniel Belliveau ◽  
Robert Irwin
Keyword(s):  
Cell Elongation ◽  
Experimental Conditions ◽  
Axial Cell ◽  
Wall Deposition ◽  
Apical Control ◽  
Band Position ◽  
Apical Cells ◽  
In Cells

Cell elongation in the Ceramiaceae typically occurs by means of one or two bands located apically and (or) basally in each cell. In axial cells of Antithamnion defectum two bands are present; however, most cell elongation occurs as a result of new wall deposition in bands at the base of each axial cell. In cells of determinate branches, only the basal band is present. In experimental conditions in which apical cells of indeterminate branches are differentially excised, location of the primary elongation band can be reestablished in relation to remaining indeterminate axes. Thus, the primary elongation band in axial cells is always basal with respect to indeterminate apical cells. When all indeterminate apices are removed, band growth becomes highly disrupted, and diffuse, irregularly located bands are formed. These results suggest that regulation of band position and elongation is through apical control.

scholarly journals Cell Shape and Population Migration Are Distinct Steps ofProteus mirabilisSwarming That Are Decoupled on High-Percentage Agar

2019 ◽  
Vol 201 (11) ◽  
Author(s):  
Kristin Little ◽  
Jacob Austerman ◽  
Jenny Zheng ◽  
Karine A. Gibbs
Keyword(s):  
Cell Motility ◽  
Single Cell ◽  
Cell Elongation ◽  
Cell Shape ◽  
Population Migration ◽  
Content Type ◽  
Agar Concentration ◽  
Collective Interactions ◽  
Cell Phenotypes ◽  
Rigid Surfaces

ABSTRACTSwarming on rigid surfaces requires movement of cells as individuals and as a group of cells. For the bacteriumProteus mirabilis, an individual cell can respond to a rigid surface by elongating and migrating over micrometer-scale distances. Cells can form groups of transiently aligned cells, and the collective population is capable of migrating over centimeter-scale distances. To address howP. mirabilispopulations swarm on rigid surfaces, we asked whether cell elongation and single-cell motility are coupled to population migration. We first measured the relationship between agar concentration (a proxy for surface rigidity), single-cell phenotypes, and swarm colony phenotypes. We find that cell elongation and single-cell motility are coupled with population migration on low-percentage hard agar (1% to 2.5%) and become decoupled on high-percentage hard agar (>2.5%). Next, we evaluate how disruptions in lipopolysaccharide (LPS), specifically the O-antigen components, affect responses to hard agar. We find that LPS is not essential for elongation and motility of individual cells, as predicted, and instead functions to broaden the range of agar concentrations on which cell elongation and motility are coupled with population migration. These findings demonstrate that cell elongation and motility are coupled with population migration under a permissive range of surface conditions; increasing agar concentration is sufficient to decouple these behaviors. Since swarm colonies cover greater distances when these steps are coupled than when they are not, these findings suggest that collective interactions amongP. mirabiliscells might be emerging as a colony expands outwards on rigid surfaces.IMPORTANCEHow surfaces influence cell size, cell-cell interactions, and population migration for robust swarmers likeP. mirabilisis not fully understood. Here, we have elucidated how cells change length along a spectrum of sizes that positively correlates with increases in agar concentration, regardless of population migration. Single-cell phenotypes can be decoupled from collective population migration simply by increasing agar concentration. A cell’s lipopolysaccharides function to broaden the range of agar conditions under which cell elongation and single-cell motility remain coupled with population migration. In eukaryotes, the physical environment, such as a surface matrix, can impact cell development, shape, and migration. These findings support the idea that rigid surfaces similarly act on swarming bacteria to impact cell shape, single-cell motility, and collective population migration.

The molecular basis of ciliopathies and cyst formation

2015 ◽  
Author(s):  
Wolfgang Kühn ◽  
Gerd Walz
Keyword(s):  
Planar Cell Polarity ◽  
Critical Role ◽  
Mammalian Target Of Rapamycin ◽  
Renal Cysts ◽  
Cyst Formation ◽  
Cystic Kidney Disease ◽  
Cystic Kidney ◽  
Convergent Extension ◽  
Diverse Range ◽  
Cell Intercalation

Abnormalities of the cilium, termed ‘ciliopathies’, are the prime suspect in the pathogenesis of renal cyst formation because the gene products of cystic disease-causing genes localize to them, or near them. However, we only partially understand how cilia maintain the geometry of kidney tubules, and how abnormal cilia lead to renal cysts, and the diverse range of diseases attributed to them. Some non-cystic diseases share pathology of the same structures. Although still incompletely understood, cilia appear to orient cells in response to extracellular cues to maintain the overall geometry of a tissue, thereby intersecting with the planar cell polarity (PCP) pathway and the actin cytoskeleton. The PCP pathway controls two morphogenetic programmes, oriented cell division (OCD) and convergent extension (CE) through cell intercalation that both seem to play a critical role in cyst formation. The two-hit theory of cystogenesis, by which loss of the second normal allele causes tubular epithelial cells to form kidney cysts, has been largely borne out. Additional hits and influences may better explain the rate of cyst formation and inter-individual differences in disease progression. Ciliary defects appear to converge on overlapping signalling modules, including mammalian target of rapamycin and cAMP pathways, which can be targeted to treat human cystic kidney disease irrespective of the underlying gene mutation.

scholarly journals Claudins are essential for cell shape changes and convergent extension movements during neural tube closure

2017 ◽  
Vol 428 (1) ◽  
pp. 25-38 ◽  
Author(s):  
Amanda I. Baumholtz ◽  
Annie Simard ◽  
Evanthia Nikolopoulou ◽  
Marcus Oosenbrug ◽  
Michelle M. Collins ◽  
...  
Keyword(s):  
Neural Tube ◽  
Cell Shape ◽  
Neural Tube Closure ◽  
Convergent Extension ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Tube Closure

scholarly journals The Saccharomyces cerevisiae mutation elm4-1 facilitates pseudohyphal differentiation and interacts with a deficiency in phosphoribosylpyrophosphate synthase activity to cause constitutive pseudohyphal growth.

1994 ◽  
Vol 14 (7) ◽  
pp. 4671-4681 ◽  
Author(s):  
M J Blacketer ◽  
P Madaule ◽  
A M Myers
Keyword(s):  
Saccharomyces Cerevisiae ◽  
Cell Elongation ◽  
Cell Shape ◽  
Nitrogen Limitation ◽  
Single Gene ◽  
Dominant Factor ◽  
Rich Medium ◽  
Pseudohyphal Growth ◽  
Gene Coding ◽  
Pseudohyphal Differentiation

Saccharomyces cerevisiae mutant E124 was selected in a visual screen based on elongated cell shape. Genetic analysis showed that E124 contains two separate mutations, pps1-1 and elm4-1, each causing a distinct phenotype inherited as a single-gene trait. In rich medium, pps1-1 by itself causes increased doubling time but does not affect cell shape, whereas elm4-1 results in a moderate cell elongation phenotype but does not affect growth rate. Reconstructed elm4-1 pps1-1 double mutants display a synthetic phenotype in rich medium including extreme cell elongation and delayed cell separation, both characteristics of pseudohyphal differentiation. The elm4-1 mutation was shown to act as a dominant factor that potentiates pseudohyphal differentiation in response to general nitrogen starvation in a genetic background in which pseudohyphal growth normally does not occur. Thus, elm4-1 allows recognition of, or response to, a pseudohyphal differentiation signal that results from nitrogen limitation. PPS1 was isolated and shown to be a previously undescribed gene coding for a protein similar in amino acid sequence to phosphoribosylpyrophosphate synthase, a rate-limiting enzyme in the biosynthesis of nucleotides, histidine, and tryptophan. Thus, the pps1-1 mutation may generate a nitrogen limitation signal, which when coupled with elm4-1 results in pseudohyphal growth even in rich medium.

scholarly journals SEDS-bPBP pairs direct Lateral and Septal Peptidoglycan Synthesis in Staphylococcus aureus

2019 ◽  
Author(s):  
Nathalie T. Reichmann ◽  
Andreia C. Tavares ◽  
Bruno M. Saraiva ◽  
Ambre Jousselin ◽  
Patricia Reed ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Cell Wall ◽  
Cell Division ◽  
Late Stage ◽  
Cell Elongation ◽  
Cell Shape ◽  
Protein A ◽  
Interacting Proteins ◽  
Peptidoglycan Synthesis ◽  
Multiple Rings

Peptidoglycan (PGN) is the major component of the bacterial cell wall, a structure essential for the physical integrity and shape of the cell. Bacteria maintain cell shape by directing PGN incorporation to distinct regions of the cell, namely through the localisation of the late stage PGN synthesis proteins. These include two key protein families, SEDS transglycosylases and the bPBP transpeptidases, proposed to function in cognate pairs. Rod-shaped bacteria have two SEDS-bPBP pairs, involved in cell elongation and cell division. Here, we elucidate why coccoid bacteria, such as Staphylococcus aureus, also possess two SEDS-bPBP pairs. We determined that S. aureus RodA-PBP3 and FtsW-PBP1 likely constitute cognate pairs of interacting proteins. Lack of RodA-PBP3 decreased cell eccentricity due to deficient pre-septal PGN synthesis, whereas the depletion of FtsW-PBP1 arrested normal septal PGN incorporation. Although PBP1 is an essential protein, a mutant lacking PBP1 transpeptidase activity is viable, showing that this protein has a second function. We propose that the FtsW-PBP1 pair has a role in stabilising the divisome at midcell. In the absence of these proteins, the divisome appears as multiple rings/arcs that drive lateral PGN incorporation, leading to cell elongation. We conclude that RodA-PBP3 and FtsW-PBP1 mediate lateral and septal PGN incorporation, respectively, and that the activity of these pairs must be balanced in order to maintain coccoid morphology.

scholarly journals Effect of cellular rearrangement time delays on the rheology of vertex models for confluent tissues

2021 ◽  
Author(s):  
Gonca Erdemci-Tandogan ◽  
M. Lisa Manning
Keyword(s):  
Delay Time ◽  
Cell Shape ◽  
Large Scale ◽  
Molecular Mechanisms ◽  
Tissue Mechanics ◽  
Tissue Response ◽  
Biological Processes ◽  
Convergent Extension ◽  
Vertex Models ◽  
Long Time

Large-scale tissue deformation during biological processes such as morphogenesis requires cellular rearrangements. The simplest rearrangement in confluent cellular monolayers involves neighbor exchanges among four cells, called a T1 transition, in analogy to foams. But unlike foams, cells must execute a sequence of molecular processes, such as endocytosis of adhesion molecules, to complete a T1 transition. Such processes could take a long time compared to other timescales in the tissue. In this work, we incorporate this idea by augmenting vertex models to require a fixed, finite time for T1 transitions, which we call the “T1 delay time”. We study how variations in T1 delay time affect tissue mechanics, by quantifying the relaxation time of tissues in the presence of T1 delays and comparing that to the cell-shape based timescale that characterizes fluidity in the absence of any T1 delays. We show that the molecular-scale T1 delay timescale dominates over the cell shape-scale collective response timescale when the T1 delay time is the larger of the two. We extend this analysis to tissues that become anisotropic under convergent extension, finding similar results. Moreover, we find that increasing the T1 delay time increases the percentage of higher-fold coordinated vertices and rosettes, and decreases the overall number of successful T1s, contributing to a more elastic-like – and less fluid-like – tissue response. Our work suggests that molecular mechanisms that act as a brake on T1 transitions could stiffen global tissue mechanics and enhance rosette formation during morphogenesis.

Sign in / Sign up

Export Citation Format

Share Document