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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.
Adelson,
Sea urchin morphogenesis and cell-hyalin adhesion are perturbed by a monoclonal antibody specific for hyalin.
1988, Pubmed,
Echinobase
Adelson,
Sea urchin morphogenesis and cell-hyalin adhesion are perturbed by a monoclonal antibody specific for hyalin.
1988,
Pubmed
,
Echinobase
Alt,
Vertex models: from cell mechanics to tissue morphogenesis.
2017,
Pubmed
Beloussov,
Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos.
2000,
Pubmed
Bertet,
Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation.
2004,
Pubmed
Blankenship,
Multicellular rosette formation links planar cell polarity to tissue morphogenesis.
2006,
Pubmed
Burke,
Cell movements during the initial phase of gastrulation in the sea urchin embryo.
1991,
Pubmed
,
Echinobase
Butler,
Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension.
2009,
Pubmed
Chen,
Cell-level finite element studies of viscous cells in planar aggregates.
2000,
Pubmed
Coffman,
A hyaline layer protein that becomes localized to the oral ectoderm and foregut of sea urchin embryos.
1990,
Pubmed
,
Echinobase
Edelstein,
Advanced methods of microscope control using μManager software.
2014,
Pubmed
Ettensohn,
Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells.
1985,
Pubmed
,
Echinobase
Fletcher,
Vertex models of epithelial morphogenesis.
2014,
Pubmed
GUSTAFSON,
Microaquaria for time-lapse cinematographic studies of morphogenesis in swimming larvae and observations on sea urchin gastrulation.
1956,
Pubmed
,
Echinobase
GUSTAFSON,
Cellular mechanisms in morphogenesis of the sea urchin gastrula. The oral contact.
1960,
Pubmed
,
Echinobase
Hardin,
The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation.
1988,
Pubmed
,
Echinobase
Hardin,
Imaging embryonic morphogenesis in C. elegans.
2011,
Pubmed
Hardin,
The behaviour and function of bottle cells during gastrulation of Xenopus laevis.
1988,
Pubmed
Hardin,
Models of morphogenesis: the mechanisms and mechanics of cell rearrangement.
2004,
Pubmed
Hardin,
The cellular basis of sea urchin gastrulation.
1996,
Pubmed
,
Echinobase
Hardin,
Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation.
1989,
Pubmed
,
Echinobase
Honda,
Cell movements in a living mammalian tissue: long-term observation of individual cells in wounded corneal endothelia of cats.
1982,
Pubmed
Huebner,
Coming to Consensus: A Unifying Model Emerges for Convergent Extension.
2018,
Pubmed
Hutson,
Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics.
2009,
Pubmed
Jacinto,
Mechanisms of epithelial fusion and repair.
2001,
Pubmed
Jacobson,
Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation.
1976,
Pubmed
Jacobson,
Neurulation and the cortical tractor model for epithelial folding.
1986,
Pubmed
Jaźwińska,
Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein.
2003,
Pubmed
Kimberly,
Bottle cells are required for the initiation of primary invagination in the sea urchin embryo.
1998,
Pubmed
,
Echinobase
KINNANDER,
Further studies on the cellular basis of gastrulation in the sea urchin larva.
1960,
Pubmed
,
Echinobase
Levayer,
Oscillation and polarity of E-cadherin asymmetries control actomyosin flow patterns during morphogenesis.
2013,
Pubmed
Logan,
The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo.
1997,
Pubmed
,
Echinobase
Mancuso,
Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans.
2012,
Pubmed
Martik,
New insights from a high-resolution look at gastrulation in the sea urchin, Lytechinus variegatus.
2017,
Pubmed
,
Echinobase
Martin,
Pulsed contractions of an actin-myosin network drive apical constriction.
2009,
Pubmed
Martins,
Cells are added to the archenteron during and following secondary invagination in the sea urchin Lytechinus variegatus.
1998,
Pubmed
,
Echinobase
Munro,
Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord.
2002,
Pubmed
Odell,
The mechanical basis of morphogenesis. I. Epithelial folding and invagination.
1981,
Pubmed
Piston,
Characterization of Involution during Sea Urchin Gastrulation Using Two-Photon Excited Photorelease and Confocal Microscopy.
1998,
Pubmed
,
Echinobase
Ransick,
Late specification of Veg1 lineages to endodermal fate in the sea urchin embryo.
1998,
Pubmed
,
Echinobase
Rauzi,
Planar polarized actomyosin contractile flows control epithelial junction remodelling.
2010,
Pubmed
Schindelin,
Fiji: an open-source platform for biological-image analysis.
2012,
Pubmed
Schneider,
NIH Image to ImageJ: 25 years of image analysis.
2012,
Pubmed
Schoenwolf,
Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate.
1989,
Pubmed
Shindo,
PCP-dependent transcellular regulation of actomyosin oscillation facilitates convergent extension of vertebrate tissue.
2019,
Pubmed
Simões,
Rho GTPase and Shroom direct planar polarized actomyosin contractility during convergent extension.
2014,
Pubmed
Simões,
Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation.
2010,
Pubmed
Umetsu,
Local increases in mechanical tension shape compartment boundaries by biasing cell intercalations.
2014,
Pubmed
Vanderleest,
Vertex sliding drives intercalation by radial coupling of adhesion and actomyosin networks during Drosophila germband extension.
2018,
Pubmed
Walck-Shannon,
Cell intercalation from top to bottom.
2014,
Pubmed
Walck-Shannon,
Polarized Rac-dependent protrusions drive epithelial intercalation in the embryonic epidermis of C. elegans.
2015,
Pubmed
Weliky,
The mechanical basis of cell rearrangement. I. Epithelial morphogenesis during Fundulus epiboly.
1990,
Pubmed
Weliky,
Notochord morphogenesis in Xenopus laevis: simulation of cell behavior underlying tissue convergence and extension.
1991,
Pubmed
Wessel,
How to grow a gut: ontogeny of the endoderm in the sea urchin embryo.
1999,
Pubmed
,
Echinobase
Williams,
Distinct apical and basolateral mechanisms drive planar cell polarity-dependent convergent extension of the mouse neural plate.
2014,
Pubmed
Williams-Masson,
The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis.
1998,
Pubmed
