Two-phase kinetics and cell cortex elastic behavior in Xenopus gastrula cell-cell adhesion.

Morphogenetic movements during animal development involve repeated making and breaking of cell-cell contacts. Recent biophysical models of cell-cell adhesion integrate adhesion molecule interactions and cortical cytoskeletal tension modulation, describing equilibrium states for established contacts. We extend this emerging unified concept of adhesion to contact formation kinetics, showing that aggregating Xenopus embryonic cells rapidly achieve Ca2+-independent low-contact states. Subsequent transitions to cadherin-dependent high-contact states show rapid decreases in contact cortical F-actin levels but slow contact area growth. We developed a biophysical model that predicted contact growth quantitatively from known cellular and cytoskeletal parameters, revealing that elastic resistance to deformation and cytoskeletal network turnover are essential determinants of adhesion kinetics. Characteristic time scales of contact growth to low and high states differ by an order of magnitude, being at a few minutes and tens of minutes, respectively, thus providing insight into the timescales of cell-rearrangement-dependent tissue movements.

A cargo model of yolk syncytial nuclear migration during zebrafish epiboly.

In teleost fish, the multinucleate yolk syncytial layer functions as an extra-embryonic signaling center to pattern mesendoderm, coordinate morphogenesis and supply nutrients to the embryo. External yolk syncytial nuclei (e-YSN) undergo microtubule-dependent movements that distribute the nuclei over the large yolk mass. How e-YSN migration proceeds, and the role of the yolk microtubules, is not understood, but it is proposed that e-YSN are pulled vegetally as the microtubule network shortens from the vegetal pole. Live imaging revealed that nuclei migrate along microtubules, consistent with a cargo model in which e-YSN are moved down the microtubules by direct association with motor proteins. We found that blocking the plus-end directed microtubule motor kinesin significantly attenuated yolk nuclear movement. Blocking the outer nuclear membrane LINC complex protein Syne2a also slowed e-YSN movement. We propose that e-YSN movement is mediated by the LINC complex, which functions as the adaptor between yolk nuclei and motor proteins. Our work provides new insights into the role of microtubules in morphogenesis of an extra-embryonic tissue and further contributes to the understanding of nuclear migration mechanisms during development.

Mechanics of Fluid-Filled Interstitial Gaps. I. Modeling Gaps in a Compact Tissue.

Fluid-filled interstitial gaps are a common feature of compact tissues held together by cell-cell adhesion. Although such gaps can in principle be the result of weak, incomplete cell attachment, adhesion is usually too strong for this to occur. Using a mechanical model of tissue cohesion, we show that, instead, a combination of local prevention of cell adhesion at three-cell junctions by fluidlike extracellular material and a reduction of cortical tension at the gap surface are sufficient to generate stable gaps. The size and shape of these interstitial gaps depends on the mechanical tensions between cells and at gap surfaces, and on the difference between intracellular and interstitial pressures that is related to the volume of the interstitial fluid. As a consequence of the dependence on tension/tension ratios, the presence of gaps does not depend on the absolute strength of cell adhesion, and similar gaps are predicted to occur in tissues of widely differing cohesion. Tissue mechanical parameters can also vary within and between cells of a given tissue, generating asymmetrical gaps. Within limits, these can be approximated by symmetrical gaps.

Mechanics of Fluid-Filled Interstitial Gaps. II. Gap Characteristics in Xenopus Embryonic Ectoderm.

The ectoderm of the Xenopus embryo is permeated by a network of channels that appear in histological sections as interstitial gaps. We characterized this interstitial space by measuring gap sizes, angles formed between adjacent cells, and curvatures of cell surfaces at gaps. From these parameters, and from surface-tension values measured previously, we estimated the values of critical mechanical variables that determine gap sizes and shapes in the ectoderm, using a general model of interstitial gap mechanics. We concluded that gaps of 1-4 µm side length can be formed by the insertion of extracellular matrix fluid at three-cell junctions such that cell adhesion is locally disrupted and a tension difference between cell-cell contacts and the free cell surface at gaps of 0.003 mJ/m2 is generated. Furthermore, a cell hydrostatic pressure of 16.8 ± 1.7 Pa and an interstitial pressure of 3.9 ± 3.6 Pa, relative to the central blastocoel cavity of the embryo, was found to be consistent with the observed gap size and shape distribution. Reduction of cell adhesion by the knockdown of C-cadherin increased gap volume while leaving intracellular and interstitial pressures essentially unchanged. In both normal and adhesion-reduced ectoderm, cortical tension of the free cell surfaces at gaps does not return to the high values characteristic of the free surface of the whole tissue.

Forces driving cell sorting in the amphibian embryo.

Adhesion differences are the main driver of cell sorting and related processes such as boundary formation or tissue positioning. In the early amphibian embryo, graded variations in cadherin density and localized expression of adhesion-modulating factors are associated with regional differences in adhesive properties including overall adhesion strength. The role of these differences in embryonic boundary formation has not been studied extensively, but available evidence suggests that adhesion strength differentials are not essential. On the other hand, the inside-out positioning of the germ layers is correlated with adhesion strength, although the biological significance of this effect is unclear. By contrast, the positioning of dorsal mesoderm tissues along the anterior-posterior body axis is essential for axis elongation, but the underlying sorting mechanism is not correlated with adhesion strength, and may rely on specific cell adhesion. Formation of the ectoderm-mesoderm boundary is the best understood sorting related process in the frog embryo. It relies on contact-induced cell repulsion at the tissue interface, driven by Eph-ephrin signaling and paraxial protocadherin-dependent self/non-self recognition.

PAPC mediates self/non-self-distinction during Snail1-dependent tissue separation.

Cleft-like boundaries represent a type of cell sorting boundary characterized by the presence of a physical gap between tissues. We studied the cleft-like ectoderm-mesoderm boundary in Xenopus laevis and zebrafish gastrulae. We identified the transcription factor Snail1 as being essential for tissue separation, showed that its expression in the mesoderm depends on noncanonical Wnt signaling, and demonstrated that it enables paraxial protocadherin (PAPC) to promote tissue separation through two novel functions. First, PAPC attenuates planar cell polarity signaling at the ectoderm-mesoderm boundary to lower cell adhesion and facilitate cleft formation. Second, PAPC controls formation of a distinct type of adhesive contact between mesoderm and ectoderm cells that shows properties of a cleft-like boundary at the single-cell level. It consists of short stretches of adherens junction-like contacts inserted between intermediate-sized contacts and large intercellular gaps. These roles of PAPC constitute a self/non-self-recognition mechanism that determines the site of boundary formation at the interface between PAPC-expressing and -nonexpressing cells.

Adsorption and desorption behavior of selected pesticides as influenced by decomposition of maize mulch.

Assessing pesticide fate in conservation agricultural systems requires a detailed understanding of their interaction with decomposing surface crop residues (mulch). Adsorption and desorption behavior of glyphosate, s-metolachlor and epoxiconazole was investigated on maize mulch residues decomposed under laboratory and field conditions. Our conceptual approach included characterization of chemical composition and hydrophobicity of mulch residues in order to generate parameters to predict sorption behavior. Adsorption of s-metolachlor and epoxiconazole greatly increased with mulch decomposition, whereas glyphosate adsorption was less affected but its desorption was increased. Mulch characteristics including aromaticity, hydrophobicity and polarity indices were strongly correlated to Koc of the non-ionic pesticides. A predictive model based on compositional data (CoDa) analysis revealed that the sorption capacity of decomposing mulch can be predicted from descriptors such as aromatic and alkyl C corresponding respectively to lignin and NDF biochemical fractions. The decomposition degree of mulch residues should be taken into account while predicting the fate of pesticides.