Mechanisms of cell positioning during C. elegans gastrulation

Abstract

Cell rearrangements are crucial during development. In this study, we use C. elegans gastrulation as a simple model to investigate the mechanisms of cell positioning. During C. elegans gastrulation, two endodermal precursor cells move from the ventral surface to the center of the embryo, leaving a gap between these ingressing cells and the eggshell. Six neighboring cells converge under the endodermal precursors, filling this gap. Using an in vitro system, we observed that these movements occurred consistently in the absence of the eggshell and the vitelline envelope. We found that movement of the neighbors towards each other is not dependent on chemotactic signaling between these cells. We further found that C. elegans gastrulation requires intact microfilaments, but not microtubules. The primary mechanism of microfilament-based motility does not appear to be through protrusive structures, such as lamellipodia or filopodia. Instead, our results suggest an alternative mechanism. We found that myosin activity is required for gastrulation, that the apical sides of the ingressing cells contract, and that the ingressing cells determine the direction of movement of their neighboring cells. Based on these results, we propose that ingression is driven by an actomyosin-based contraction of the apical side of the ingressing cells, which pulls neighboring cells underneath. We conclude that apical constriction can function to position blastomeres in early embryos, even before anchoring junctions form between cells.Movies available on-line

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

“…Following A/P polarization, chiral cortical actomyosin activity patterns the D/V and L/R axes [187,188,191,192,197] (see above), and cortical contractility drives cell internalization and most likely also cell sorting during gastrulation [197,[262][263][264][265][266][267]. The central inductive cue(s) that drives non-muscle myosin II activation during gastrulation is constituted by Wnt signaling [200,265].…”

Shroom family proteins regulate γ-tubulin distribution and microtubule architecture during epithelial cell shape change

“…Apical localization and contraction of actin and myosin appear to be universal, driving apical constriction in Volvox, Drosophila, Caenorhabditis elegans and vertebrates (Hildebrand, 2005;Lee and Goldstein, 2003;Nance and Priess, 2002;Nishii and Ogihara, 1999;Young et al, 1993). Likewise, an increase in cell length is observed in apically constricting cells across taxa, including Volvox, Drosophila, shrimps, sand dollars, mice, chicks and frogs (Burnside, 1973;Hertzler and Clark, Jr, 1992;Kam et al, 1991;Kominami and Takata, 2000;Nishii and Ogihara, 1999;Schoenwolf and Franks, 1984;Schroeder, 1970;Sweeton et al, 1991;Viamontes and Kirk, 1977).…”

“…For example, apical constriction in the roundworm is not apparently associated with apicobasal cell heightening (Lee and Goldstein, 2003;Nance and Priess, 2002). Moreover, Shroom3 controls the apical accumulation of ␥-tubulin, a MT minus-end-associated protein (Figs 4, 6), whereas DRhoGEF2 directs the apical localization of EB1, a plus-end binding protein (Rogers et al, 2004).…”

Control of developmental networks by Rac/Rho small GTPases: How cytoskeletal changes during embryogenesis are orchestrated

“…Actomyosin contractility is essential for the ingression of cells during gastrulation 32. Gastrulation in C. elegans is not as spectacular as in many other animal embryos, because cells move only over short distances, and the blastocoel space is small 33 as can be observed in Supplementary Movie S1.…”