scholarly journals Mechanosensitive junction remodelling promotes robust epithelial morphogenesis

2019 ◽  
Author(s):  
Michael F. Staddon ◽  
Kate E. Cavanaugh ◽  
Edwin M. Munro ◽  
Margaret L. Gardel ◽  
Shiladitya Banerjee
Keyword(s):  
Cell Shape ◽  
Strain Relaxation ◽  
Cell Junctions ◽  
Elastic Behaviour ◽  
Model Parameters ◽  
Epithelial Junctions ◽  
Contractile Stress ◽  
Length Changes ◽  
Cell Shape Changes ◽  
Shape Changes

Morphogenesis of epithelial tissues requires tight spatiotemporal coordination of cell shape changes. In vivo, many tissue-scale shape changes are driven by pulsatile contractions of intercellular junctions, which are rectified to produce irreversible deformations. The functional role of this pulsatory ratchet and its mechanistic basis remain unknown. Here we combine theory and biophysical experiments to show that mechanosensitive tension remodelling of epithelial cell junctions promotes robust epithelial shape changes via ratcheting. Using optogenetic control of actomyosin contractility, we find that epithelial junctions show elastic behaviour under low contractile stress, returning to their original lengths after contraction, but undergo irreversible deformation under higher magnitudes of contractile stress. Existing vertex-based models for the epithelium are unable to capture these results, with cell junctions displaying purely elastic or fluid-like behaviours, depending on the choice of model parameters. To describe the experimental results, we propose a modified vertex model with two essential ingredients for junction mechanics: thresholded tension remodelling and continuous strain relaxation. First, a critical strain threshold for tension remodelling triggers irreversible junction length changes for sufficiently strong contractions, making the system robust to small fluctuations in contractile activity. Second, continuous strain relaxation allows for mechanical memory removal, enabling frequency-dependent modulation of cell shape changes via mechanical ratcheting. Taken together, the combination of mechanosensitive tension remodelling and junctional strain relaxation provides a robust mechanism for large-scale morphogenesis.

scholarly journals Direct laser manipulation reveals the mechanics of cell contacts in vivo

2015 ◽  
Vol 112 (5) ◽  
pp. 1416-1421 ◽  
Author(s):  
Kapil Bambardekar ◽  
Raphaël Clément ◽  
Olivier Blanc ◽  
Claire Chardès ◽  
Pierre-François Lenne
Keyword(s):  
Cell Shape ◽  
Constitutive Law ◽  
Cell Junctions ◽  
Scale Model ◽  
Tissue Morphogenesis ◽  
Cell Contacts ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Cell Cell

Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell–cell and cell–ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell–cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue.

scholarly journals Measurement of junctional tension in epithelial cells at the onset of primitive streak formation in the chick embryo via non-destructive optical manipulation

2018 ◽  
Author(s):  
Valentina Ferro ◽  
Manli Chuai ◽  
David McGloin ◽  
Cornelis Weijer
Keyword(s):  
Epithelial Cells ◽  
Cell Shape ◽  
Large Scale ◽  
Cell Sheet ◽  
Primitive Streak ◽  
Cell Junctions ◽  
Optical Manipulation ◽  
Cell Shape Changes ◽  
Non Destructive ◽  
Shape Changes

Oriented cell intercalations and cell shape changes are key determinants of large-scale epithelial cell sheet deformations occurring during gastrulation in many organisms. In several cases directional intercalation and cell shape changes have been shown to be associated with a planar cell polarity in the organisation of the actin-myosin cytoskeleton of epithelial cells. This polarised cytoskeletal organisation has been postulated to reflect the directional tension necessary to drive and orient directional cell intercalations. We have now further characterised and applied a recently introduced non-destructive optical manipulation technique to measure the tension in individual cell junctions in the epiblast of chick embryos in the early stages of primitive streak formation. We have measured junctional tension as a function of position and orientation. Junctional tension of mesendoderm cells, the tissue that drives the formation of the streak, is higher than tension of junctions of cells in other parts of the epiblast. Furthermore, in the mesendoderm junctional tension is higher in the direction of intercalation. The data are fitted best with a Maxwell model and we find that both junctional tension and relaxation time are dependent on myosin activity.

scholarly journals Tissue flow induces cell shape changes during organogenesis

2018 ◽  
Author(s):  
Gonca Erdemci-Tandogan ◽  
Madeline J. Clark ◽  
Jeffrey D. Amack ◽  
M. Lisa Manning
Keyword(s):  
Cell Shape ◽  
Surrounding Tissue ◽  
Model Parameters ◽  
Drag Forces ◽  
Dynamic Forces ◽  
Cell Shapes ◽  
Specific Shape ◽  
Cell Shape Changes ◽  
Shape Changes ◽  
Anterior Posterior

In embryonic development, cell shape changes are essential for building functional organs, but in many cases the mechanisms that precisely regulate these changes remain unknown. We propose that fluid-like drag forces generated by the motion of an organ through surrounding tissue could generate changes to its structure that are important for its function. To test this hypothesis, we study the zebrafish left-right organizer, Kupffer’s vesicle (KV), using experiments and mathematical modeling. During development, monociliated cells that comprise the KV undergo region-specific shape changes along the anterior-posterior axis that are critical for KV function: anterior cells become long and thin, while posterior cells become short and squat. Here, we develop a mathematical vertex-like model for cell shapes, which incorporates both tissue rheology and cell motility, and constrain the model parameters using previously published rheological data for the zebrafish tailbud [Serwane et al.] as well as our own measurements of the KV speed. We find that drag forces due to dynamics of cells surrounding the KV could be sufficient to drive KV cell shape changes during KV development. More broadly, these results suggest that cell shape changes could be driven by dynamic forces not typically considered in models or experiments.

scholarly journals A genetic screen for temperature-sensitive morphogenesis-defectiveCaenorhabditis elegansmutants

2021 ◽  
Vol 11 (4) ◽  
Author(s):  
Molly C Jud ◽  
Josh Lowry ◽  
Thalia Padilla ◽  
Erin Clifford ◽  
Yuqi Yang ◽  
...  
Keyword(s):  
Cell Shape ◽  
The Body ◽  
Temperature Sensitive ◽  
Restrictive Temperature ◽  
Fundamental Biological Process ◽  
Embryonic Morphogenesis ◽  
Cell Shape Changes ◽  
Development Temperature ◽  
Multicellular Organisms ◽  
Shape Changes

AbstractMorphogenesis involves coordinated cell migrations and cell shape changes that generate tissues and organs, and organize the body plan. Cell adhesion and the cytoskeleton are important for executing morphogenesis, but their regulation remains poorly understood. As genes required for embryonic morphogenesis may have earlier roles in development, temperature-sensitive embryonic-lethal mutations are useful tools for investigating this process. From a collection of ∼200 such Caenorhabditis elegans mutants, we have identified 17 that have highly penetrant embryonic morphogenesis defects after upshifts from the permissive to the restrictive temperature, just prior to the cell shape changes that mediate elongation of the ovoid embryo into a vermiform larva. Using whole genome sequencing, we identified the causal mutations in seven affected genes. These include three genes that have roles in producing the extracellular matrix, which is known to affect the morphogenesis of epithelial tissues in multicellular organisms: the rib-1 and rib-2 genes encode glycosyltransferases, and the emb-9 gene encodes a collagen subunit. We also used live imaging to characterize epidermal cell shape dynamics in one mutant, or1219ts, and observed cell elongation defects during dorsal intercalation and ventral enclosure that may be responsible for the body elongation defects. These results indicate that our screen has identified factors that influence morphogenesis and provides a platform for advancing our understanding of this fundamental biological process.

Estradiol promotes cell shape changes and glial fibrillary acidic protein redistribution in hypothalamic astrocytes in vitro: A neuronal-mediated effect

Glia ◽  
1992 ◽  
Vol 6 (3) ◽  
pp. 180-187 ◽  
Author(s):  
Ignacio Torres-Aleman ◽  
Maria Teresa Rejas ◽  
Sebastian Pons ◽  
Luis Miguel Garcia-Segura
Keyword(s):  
Glial Fibrillary Acidic Protein ◽  
Cell Shape ◽  
Acidic Protein ◽  
Cell Shape Changes ◽  
Shape Changes

scholarly journals Dependency relationships between IFT-dependent flagellum elongation and cell morphogenesis in Leishmania

Open Biology ◽  
2018 ◽  
Vol 8 (11) ◽  
pp. 180124 ◽  
Author(s):  
Jack Daniel Sunter ◽  
Flavia Moreira-Leite ◽  
Keith Gull
Keyword(s):  
Fluorescence Microscopy ◽  
Cell Shape ◽  
Electron Tomography ◽  
Intraflagellar Transport ◽  
Flagellar Pocket ◽  
Cell Morphogenesis ◽  
Multiple Functions ◽  
Cell Shape Changes ◽  
Shape Changes

Flagella have multiple functions that are associated with different axonemal structures. Motile flagella typically have a 9 + 2 arrangement of microtubules, whereas sensory flagella normally have a 9 + 0 arrangement. Leishmania exhibits both of these flagellum forms and differentiation between these two flagellum forms is associated with cytoskeletal and cell shape changes. We disrupted flagellum elongation in Leishmania by deleting the intraflagellar transport (IFT) protein IFT140 and examined the effects on cell morphogenesis. Δift140 cells have no external flagellum, having only a very short flagellum within the flagellar pocket. This short flagellum had a collapsed 9 + 0 (9v) axoneme configuration reminiscent of that in the amastigote and was not attached to the pocket membrane. Although amastigote-like changes occurred in the flagellar cytoskeleton, the cytoskeletal structures of Δift140 cells retained their promastigote configurations, as examined by fluorescence microscopy of tagged proteins and serial electron tomography. Thus, Leishmania promastigote cell morphogenesis does not depend on the formation of a long flagellum attached at the neck. Furthermore, our data show that disruption of the IFT system is sufficient to produce a switch from the 9 + 2 to the collapsed 9 + 0 (9v) axonemal structure, echoing the process that occurs during the promastigote to amastigote differentiation.

Sign in / Sign up

Export Citation Format

Share Document