scholarly journals Anisotropy links cell shapes to tissue flow during convergent extension

2020 ◽  
Vol 117 (24) ◽  
pp. 13541-13551 ◽  
Author(s):  
Xun Wang ◽  
Matthias Merkel ◽  
Leo B. Sutter ◽  
Gonca Erdemci-Tandogan ◽  
M. Lisa Manning ◽  
...  

Within developing embryos, tissues flow and reorganize dramatically on timescales as short as minutes. This includes epithelial tissues, which often narrow and elongate in convergent extension movements due to anisotropies in external forces or in internal cell-generated forces. However, the mechanisms that allow or prevent tissue reorganization, especially in the presence of strongly anisotropic forces, remain unclear. We study this question in the converging and extendingDrosophilagermband epithelium, which displays planar-polarized myosin II and experiences anisotropic forces from neighboring tissues. We show that, in contrast to isotropic tissues, cell shape alone is not sufficient to predict the onset of rapid cell rearrangement. From theoretical considerations and vertex model simulations, we predict that in anisotropic tissues, two experimentally accessible metrics of cell patterns—the cell shape index and a cell alignment index—are required to determine whether an anisotropic tissue is in a solid-like or fluid-like state. We show that changes in cell shape and alignment over time in theDrosophilagermband predict the onset of rapid cell rearrangement in both wild-type andsnail twistmutant embryos, where our theoretical prediction is further improved when we also account for cell packing disorder. These findings suggest that convergent extension is associated with a transition to more fluid-like tissue behavior, which may help accommodate tissue-shape changes during rapid developmental events.

2019 ◽  
Author(s):  
Xun Wang ◽  
Matthias Merkel ◽  
Leo B. Sutter ◽  
Gonca Erdemci-Tandogan ◽  
M. Lisa Manning ◽  
...  

AbstractWithin developing embryos, tissues flow and reorganize dramatically on timescales as short as minutes. This includes epithelial tissues, which often narrow and elongate in convergent extension movements due to anisotropies in external forces or in internal cell-generated forces. However, the mechanisms that allow or prevent tissue reorganization, especially in the presence of strongly anisotropic forces, remain unclear. We study this question in the converging and extending Drosophila germband epithelium, which displays planar polarized myosin II and experiences anisotropic forces from neighboring tissues, and we show that in contrast to isotropic tissues, cell shape alone is not sufficient to predict the onset of rapid cell rearrangement. From theoretical considerations and vertex model simulations, we predict that in anisotropic tissues two experimentally accessible metrics of cell patterns—the cell shape index and a cell alignment index—are required to determine whether an anisotropic tissue is in a solid-like or fluid-like state. We show that changes in cell shape and alignment over time in the Drosophila germband indicate a solid-to-fluid transition that corresponds to the onset of cell rearrangement and convergent extension in wild-type embryos and are also consistent with more solid-like behavior in bnt mutant embryos. Thus, the onset of cell rearrangement in the germband can be predicted by a combination of cell shape and alignment. These findings suggest that convergent extension is associated with a transition to more fluid-like tissue behavior, which may help accommodate tissue shape changes during rapid developmental events.


2018 ◽  
Author(s):  
Ramya Balaji ◽  
Vanessa Weichselberger ◽  
Anne-Kathrin Classen

AbstractThe role of actomyosin contractility at epithelial adherens junctions has been extensively studied. However, little is known about how external forces are integrated to establish epithelial cell and organ shape in vivo. We use the Drosophila follicle epithelium to investigate how tension at adherens junctions is regulated to integrate external forces arising from changes in germline size and shape. We find that overall tension in the epithelium decreases despite pronounced growth of enclosed germline cells, suggesting that the epithelium relaxes to accommodate growth. However, we find local differences in adherens junction tension correlate with apposition to germline nurse cells or the oocyte. We demonstrate that medial Myosin II coupled to corrugating adherens junctions resists nurse cell-derived forces and thus maintains apical surface areas and cuboidal cell shapes. Furthermore, medial reinforcement of the apical surface ensures cuboidal-to-columnar cell shape transitions and imposes circumferential constraints on nurse cells guiding organ elongation. Our study provides insight into how tension within an adherens junction network integrates growth of a neighbouring tissue, mediates cell shape transitions and channels growth into organ elongation.


1986 ◽  
Vol 83 (1) ◽  
pp. 313-340 ◽  
Author(s):  
G.A. Dunn ◽  
A.F. Brown

The response of chick heart fibroblasts to grooved substrata was studied using microfabricated grooves and new measures of shape and alignment derived from the moments of cell shapes. Cell shape and alignment were measured on 23 different sets of regular, parallel grooves, which ranged in width from 1.65 to 8.96 micron, and in repeat spacing from 3.0 to 32.0 micron. The grooves were of constant depth, 0.69 micron. Digitized video images were analysed to extract the zero-, first- and second-order moments of the cell shapes, from which were calculated three measures of cell shape, and three measures of cell alignment. Regression analyses of the measures against parameters of the substratum such as groove width, repeat spacing and the ridge width between grooves show that ridge width is the main parameter affecting cell alignment (alignment being inversely proportional to ridge width), although groove width has a small additional effect. All the differences in cell shape between the different grooves can be summarized to a very good approximation as simple geometrical stretch transformations of the shapes of cells on planar surfaces. Our principal measure of cell alignment, paraxial elongation, is a measure of the necessary transformation. This finding has the interesting biological implication that the shape and orientation adopted by cells, in response to the grooves, are not governed by independent cellular mechanisms.


Genetics ◽  
1997 ◽  
Vol 147 (1) ◽  
pp. 243-253 ◽  
Author(s):  
Joseph Jack ◽  
Guy Myette

Abstract The products of two genes, raw and ribbon (rib), are required for the proper morphogenesis of a variety of tissues. Malpighian tubules mutant for raw or rib are wider and shorter than normal tubules, which are only two cells in circumference when they are fully formed. The mutations alter the shape of the tubules beginning early in their formation and block cell rearrangement late in development, which normally lengthens and narrows the tubes. Mutations of both genes affect a number of other tissues as well. Both genes are required for dorsal closure and retraction of the CNS during embryonic development. In addition, rib mutations block head involution, and broaden and shorten other tubular epithelia (salivary glands, tracheae, and hindgut) in much same manner as they alter the shape of the Malpighian tubules. In tissues in which the shape of cells can be observed readily, rib mutations alter cell shape, which probably causes the change in shape of the organs that are affected. In double mutants raw enhances the phenotypes of all the tissues that are affected by rib but unaffected by raw alone, indicating that raw is also active in these tissues.


Author(s):  
Hui-Ju Hsu ◽  
Chin-Fu Lee ◽  
Roland Kaunas

Actin stress fibers (SFs) are bundles of actin filaments anchored at each end via focal adhesions. Myosin-generated contraction leads to the development of tension, which extends SFs beyond their unloaded lengths. In human aortic ECs, the level of SF extension is maintained at a set-point level of ∼1.10 (1). SFs are also dynamic structures and their continuous assembly and disassembly is critical to cellular functions involving changes in cell shape. Further, deformation of the extracellular matrix perturbs SF extension, leading to compensatory responses such as the gradual alignment of SFs perpendicular to the principal direction of cyclic stretch. The extent of cell alignment has been shown to depend on the pattern of matrix stretch; however, it is unclear how cells distinguish between different patterns of stretch to determine their unique responses.


1985 ◽  
Vol 74 (1) ◽  
pp. 219-237
Author(s):  
C.L. Lachney ◽  
T.A. Lonergan

The role of cytoplasmic microtubules in a recently reported biological clock-controlled rhythm in cell shape of the alga Euglena gracilis (strain Z) was examined using indirect immunofluorescence microscopy. The resulting fluorescent patterns indicated that, unlike many other cell systems, Euglena cells apparently change from round to long to round cell shape without associated cytoplasmic microtubule assembly and disassembly. Instead, the different cell shapes were correlated with microtubule patterns, which suggested that movement of stable microtubules to accomplish cell shape changes. In live intact cells, these microtubules were demonstrated by immunofluorescence to be stable to lowered temperature and elevated intracellular Ca2+ levels, treatments that are commonly used to depolymerize microtubules. In cells extracted in detergent at low temperature or in the presence of elevated Ca2+ levels, the fluorescent image of the microtubules was disrupted. Transmission electron microscopy confirmed the loss of one subset of pellicle microtubules. The difference in microtubule stability to these agents between live intact cells and cells extracted in detergent suggested the presence of a microtubule-stabilizing factor in live cells, which is released from the cell by extraction with detergent, thereby permitting microtubule depolymerization by Ca2+ or lowered temperature. The calmodulin antagonist trifluoperazine prevented the Ca2+-induced disruption of the fluorescent microtubule pattern in cells extracted in detergent. These results implied the involvement of calmodulin in the sensitivity to Ca2+ of the microtubules of cells extracted in detergent.


2019 ◽  
Vol 30 (16) ◽  
pp. 1911-1919 ◽  
Author(s):  
Jeff Hardin ◽  
Michael Weliky

George Oster was a pioneer in using mechanical models to interrogate morphogenesis in animal embryos. Convergent extension is a particularly important morphogenetic process to which George Oster gave significant attention. Late elongation of the sea urchin archenteron is a classic example of convergent extension in a monolayered tube, which has been proposed to be driven by extrinsic axial tension due to the activity of secondary mesenchyme cells. Using a vertex-based mechanical model, we show that key features of archenteron elongation can be accounted for by passive cell rearrangement due to applied tension. The model mimics the cell elongation and the Poisson effect (necking) that occur in actual archenterons. We also show that, as predicted by the model, ablation of secondary mesenchyme cells late in archenteron elongation does not result in extensive elastic recoil. Moreover, blocking the addition of cells to the base of the archenteron late in archenteron elongation leads to excessive cell rearrangement consistent with tension-induced rearrangement of a smaller cohort of cells. Our mechanical simulation suggests that responsive rearrangement can account for key features of archenteron elongation and provides a useful starting point for designing future experiments to examine the mechanical properties of the archenteron.


2019 ◽  
Vol 98 (11) ◽  
pp. 1253-1261 ◽  
Author(s):  
S. Yamada ◽  
R. Lav ◽  
J. Li ◽  
A.S. Tucker ◽  
J.B.A. Green

Tooth germs undergo a series of dynamic morphologic changes through bud, cap, and bell stages, in which odontogenic epithelium continuously extends into the underlying mesenchyme. During the transition from the bud stage to the cap stage, the base of the bud flattens and then bends into a cap shape whose edges are referred to as “cervical loops.” Although genetic mechanisms for cap formation have been well described, little is understood about the morphogenetic mechanisms. Computer modeling and cell trajectory tracking have suggested that the epithelial bending is driven purely by differential cell proliferation and adhesion in different parts of the tooth germ. Here, we show that, unexpectedly, inhibition of cell proliferation did not prevent bud-to-cap morphogenesis. We quantified cell shapes and actin and myosin distributions in different parts of the tooth epithelium at the critical stages and found that these are consistent with basal relaxation in the forming cervical loops and basal constriction around enamel knot at the center of the cap. Inhibition of focal adhesion kinase, which is required for basal constriction in other systems, arrested the molar explant morphogenesis at the bud stage. Together, these results show that the bud-to-cap transition is largely proliferation independent, and we propose that it is driven by classic actomyosin-driven cell shape–dependent mechanisms. We discuss how these results can be reconciled with the previous models and data.


2017 ◽  
Vol 428 (1) ◽  
pp. 25-38 ◽  
Author(s):  
Amanda I. Baumholtz ◽  
Annie Simard ◽  
Evanthia Nikolopoulou ◽  
Marcus Oosenbrug ◽  
Michelle M. Collins ◽  
...  

Author(s):  
Gonca Erdemci-Tandogan ◽  
M. Lisa Manning

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.


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