Actomyosin-based Self-organization of cell internalization during C. elegans gastrulation
- PDF / 3,185,675 Bytes
- 16 Pages / 595.28 x 793.7 pts Page_size
- 59 Downloads / 163 Views
RESEARCH ARTICLE
Open Access
Actomyosin-based Self-organization of cell internalization during C. elegans gastrulation Christian Pohl1,2, Michael Tiongson1, Julia L Moore1,3, Anthony Santella1 and Zhirong Bao1*
Abstract Background: Gastrulation 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 selforganization (how global order or coordination can arise from local interactions) are poorly understood. Results: We 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. Conclusions: The 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. Keywords: C. elegans, gastrulation, actomyosin, cellular rosette
Background During gastrulation, an embryo is dramatically restructured by cell and tissue movements [1] to position the three germ layers (endoderm, ectoderm, and mesoderm), and to assemble the organ primordia. The paramount morphogenetic task during this process is to internalize surface cells. Four major mechanisms of internalization have been described: invagination (the inward folding of a group of cells), involution (ingrowth and curling inward of a group of cells), ingression (the migration of individual cells from the surface to the interior) and epiboly (growth of a group of cells around another group) [1]. How different organisms bring about this multiplicity of morphogenetic mechanisms that deploy common molecular machineries is poorly understood. * Correspondence: [email protected] 1 Developmental Biology Program, Sloan-Kettering Institute, 1275 York Avenue, New York, NY, 10065, USA Full list of author information is available at the end of the article
Contractile actomyosin networks are probably the beststudi
Data Loading...
