Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators

Abstract

Understanding the links between developmental patterning mechanisms and force-producing cytoskeletal mechanisms is a central goal in studies of morphogenesis. Gastrulation is the first morphogenetic event in the development of many organisms. Gastrulation involves the internalization of surface cells, often driven by the contraction of actomyosin networks that are deployed with spatial precision -- both in specific cells and in a polarized manner within each cell. These cytoskeletal mechanisms rely on different cell fate and cell polarity regulators in different organisms. C. elegans gastrulation presents an opportunity to examine the extent to which diverse mechanisms may be used by dozens of cells that are internalized at distinct times within a single organism. We identified 66 cells that are internalized in C. elegans gastrulation, many of which were not known previously to gastrulate. To gain mechanistic insights into how these cells internalize, we genetically manipulated cell fate, cell polarity and cytoskeletal regulators and determined the effects on cell internalization. We found that cells of distinct lineages depend on common actomyosin-based mechanisms to gastrulate, but different cell fate regulators, and, surprisingly, different cell polarity regulators. We conclude that diverse cell fate and cell polarity regulators control common mechanisms of morphogenesis in C. elegans. The results highlight the variety of developmental patterning mechanisms that can be associated with common cytoskeletal mechanisms in the morphogenesis of an animal embryo.

Quantitative semi-automated analysis of morphogenesis with single-cell resolution in complex embryos

“…The dynamic rearrangements of cells in the C. elegans embryo remain relatively poorly understood, with the exception of the ingression movements of gastrulation (Lee and Goldstein, 2003;Lee et al, 2006;Harrell and Goldstein, 2011). Following gastrulation, the most prominent morphogenetic movements are those of ventral cleft closure and subsequent epidermal enclosure.…”

An E-cadherin-mediated hitchhiking mechanism forC. elegansgerm cell internalization during gastrulation

“…Somatic cells rely on lineage-specific cell fate transcription factors to trigger their ingression movements (Nance and Priess, 2002;Lee et al, 2006;Harrell and Goldstein, 2011). Endodermal cell ingressions, and probably those of mesodermal cells, occur when myosin accumulates at the apical surface and promotes apical constriction (Nance and Priess, 2002;Lee and Goldstein, 2003;Nance et al, 2003).…”

Apical constriction: themes and variations on a cellular mechanism driving morphogenesis

“…In these cases, changes in the geometry and mechanics of constituent cells appear to impact global tissue shape directly (Odell et al, 1981;Escudero et al, 2007;Sherrard et al, 2010;Eiraku et al, 2011). Apical constriction of individual cells can contribute to cell ingression from epithelial tissues, sometimes as a step in an epithelialmesenchymal transition (EMT) (Anstrom, 1992;Nance and Priess, 2002;Harrell and Goldstein, 2011;Williams et al, 2012). Apical constriction is also associated with the extrusion of apoptotic or delaminating cells (Toyama et al, 2008;Slattum et al, 2009;Marinari et al, 2012) and wound contraction and healing (Davidson et al, 2002;Antunes et al, 2013).…”