Actomyosin-based Self-organization of cell internalization during C. elegans gastrulation

Abstract

BackgroundGastrulation is a key transition in embryogenesis; it requires self-organized cellular coordination, which has to be both robust to allow efficient development and plastic to provide adaptability. Despite the conservation of gastrulation as a key event in Metazoan embryogenesis, the morphogenetic mechanisms of self-organization (how global order or coordination can arise from local interactions) are poorly understood.ResultsWe report a modular structure of cell internalization in Caenorhabditis elegans gastrulation that reveals mechanisms of self-organization. Cells that internalize during gastrulation show apical contractile flows, which are correlated with centripetal extensions from surrounding cells. These extensions converge to seal over the internalizing cells in the form of rosettes. This process represents a distinct mode of monolayer remodeling, with gradual extrusion of the internalizing cells and simultaneous tissue closure without an actin purse-string. We further report that this self-organizing module can adapt to severe topological alterations, providing evidence of scalability and plasticity of actomyosin-based patterning. Finally, we show that globally, the surface cell layer undergoes coplanar division to thin out and spread over the internalizing mass, which resembles epiboly.ConclusionsThe combination of coplanar division-based spreading and recurrent local modules for piecemeal internalization constitutes a system-level solution of gradual volume rearrangement under spatial constraint. Our results suggest that the mode of C. elegans gastrulation can be unified with the general notions of monolayer remodeling and with distinct cellular mechanisms of actomyosin-based morphogenesis.

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

“…Due to complex cell rearrangements during late stages of gastrulation, the global asymmetry is gradually transformed into superficial L/R symmetry with a symmetrically positioned midline (Figure 6c, left) [197]. A comprehensive analysis of these cell rearrangements uncovered a chiral collective migration phase which seems to be driven by cortical actomyosin dynamics (Figure 6c, right) [197]. This migration resembles the directional rotation in a plane.…”

“…Importantly, this asymmetrically positioned midline is maintained during the time window of all major asymmetric inductions that differentially pattern left and right body halves [195,196]. Due to complex cell rearrangements during late stages of gastrulation, the global asymmetry is gradually transformed into superficial L/R symmetry with a symmetrically positioned midline (Figure 6c, left) [197]. A comprehensive analysis of these cell rearrangements uncovered a chiral collective migration phase which seems to be driven by cortical actomyosin dynamics (Figure 6c, right) [197].…”

“…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].…”

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

“…However, laser cuts have shown that the low level of tension in neighboring cells does not decrease further as apical constriction begins (Roh-Johnson et al, 2012). Alternatively, cell division in neighboring cells might relieve tension on cells undergoing apical constriction, because dividing cells have been shown to spread along the surface of the embryo (Pohl et al, 2012;Chihara and Nance, 2012). However, divisions of neighboring cells are unlikely to contribute significantly to apical constriction of the endoderm precursor cells in C. elegans, because most of the apical cell shape changes occur when neighboring cells are not dividing (Roh-Johnson et al, 2012).…”

Acute heat shock leads to cortical domain internalization and polarity loss in the C. elegans embryo

“…Integrated C. elegans strains expressing lifeact-fusion proteins expressed from pie-1 promoters have been described previously (Pohl et al, 2012;Singh and Pohl, 2014). Strain TH252 (Ppie-1::gpr-1::GFP) was kindly provided by H. Bringmann (Bringmann et al, 2007) …”