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Cell rearrangement induced by filopodial tension accounts for the late phase of convergent extension in the sea urchin archenteron.
Hardin J
,
Weliky M
.
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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.
FIGURE 1:. Vertex-based modeling of rearranging cells. For details of the model, see the text. (A) Adjacent cells share a common junctional vertex node. The node is in mechanical equilibrium when the pressure (Pi) and elastic forces (arrows parallel to membranes) from all cells are balanced. (B) Cell rearrangements can be constructed from the canonical situation illustrated in A. Four cells are shown. The pair of cells (cells 2 and 4), which are separated in the initial configuration, establish contact with one another. The remaining pair (cells 1 and 3), which are initially in contact with one another, separate. Cell rearrangement occurs when two nodes meet, and the junctions “change allegiance.” Here, nodes A and B move toward one another. During junctional rearrangement, new nodes C and D are created, which subsequently separate. In the process edge AB has shortened and vanished, to be replaced by edge CD. The inset shows how the net force imbalance at node B causes the node to slide to the left. Adapted from Weliky and Oster (1990).
FIGURE 2:. Modeling passive rearrangement via externally applied tension mimics key features of archenteron elongation in late L. pictus gastrulae. (A) The model archenteron. Warmer/redder colors indicate greater relative tension; cooler/bluer colors indicate less tension or compression. (B–E) Scanning electron micrographs of L. pictus archenterons at various stages of elongation. Groups of cells are colorized for clarity. (B, midgastrula; C, ⅔ gastrula; D, late gastrula). Scale bar = 10 µm. (E) Tension during archenteron elongation. Frames from a time-lapse movie of an L. pictus embryo at successive stages of archenteron elongation. The cell marked by the arrow undergoes elongation as gastrulation proceeds. Scale bar = 10 µm.
FIGURE 3:. Correlation of cell elongation with extent of cell rearrangement in model and actual archenterons. The length/width ratios of cells in the model archenteron (top) and in actual archenterons processed for scanning electron microscopy were measured and plotted as a function of the number of cells around the circumference. Straight lines represent linear regression; curved lines indicate 95% confidence limits on the mean for each regression.
FIGURE 4:. mAb183 treatment leads to excessive rearrangement in the archenteron. (A) mAb183 was added to the L. pictus embryo cultures when they had developed to the midprimary invagination stage. Four different types of embryos developed following treatment with mAb183. The first type completely loses its invagination and develops a protruding vegetal pole epithelium (unpublished data). (B) The second type retains a small invagination at the vegetal pole; however, it does not elongate and the vegetal epithelium protrudes. (C) The third type of embryo retains its archenteron, which appears to undergo a limited amount of elongation; however, it remains short and the vegetal epithelium is distended. (D) A control late gastrula embryo of the same temporal age as the mAb183-treated embryos in B and C and E and F. The vegetal epithelium does not protrude and the archenteron has a normal lumen and length. (D, E) Two mAb183-treated late gastrulae with abnormally thin archenterons compared with archenteron width of the control in D. In E the midpoint of the archenteron is only one cell wide (arrow). Both embryos in E and F have protruding vegetal epithelia (E, arrow). (F) In some type IV embryos the archenteron rips in two and the two fragments seal their open ends (arrows). Scale bar = 10 µm.
FIGURE 5:. The archenteron does not retract following ablation of SMCs. (A) A late L. pictus gastrula near the end of gastrulation, but before contact of the tip of the archenteron with the animal pole. (B) The same embryo following ablation of the tip of the archenteron. Little retraction of the archenteron occurs. (C) Inset of the boxed region in B. Scale bar = 10 µm.
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