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Review
. 2023 Jan 15:133:107-122.
doi: 10.1016/j.semcdb.2022.03.028. Epub 2022 Apr 5.

Membrane-actin interactions in morphogenesis: Lessons learned from Drosophila cellularization

Anna Marie Sokac  1 , Natalie Biel  2 , Stefano De Renzis  3
Affiliations
Review

Membrane-actin interactions in morphogenesis: Lessons learned from Drosophila cellularization

Anna Marie Sokac et al. Semin Cell Dev Biol. .

Abstract

During morphogenesis, changes in the shapes of individual cells are harnessed to mold an entire tissue. These changes in cell shapes require the coupled remodeling of the plasma membrane and underlying actin cytoskeleton. In this review, we highlight cellularization of the Drosophila embryo as a model system to uncover principles of how membrane and actin dynamics are co-regulated in space and time to drive morphogenesis.

Keywords: Actin; Cortical compartments; Cytokinesis; Endocytosis; Exocytosis; Membrane reservoir; Membrane trafficking; Myosin-2; Phosphoinositides.

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Conflict of interest statement

Conflicts of Interest The authors declare that they have no conflicts of interest associated with this article.

Figures

Fig. 1.
Fig. 1.. Cross sectional view of the early developing Drosophila embryo.
Anterior (A) and posterior (P) poles indicated. Post-fertilization times (PF) at 25°C and Bownes Stage provided. Nuclei shown in purple. Nuclear divisions occur in the embryo interior during nuclear cycles (NC) 1-7. Nuclei are transported towards the embryo periphery during NC 8-9. Nuclei divide at the embryo periphery from NC 10-13, generating a regularly packed monolayer of ~6000 nuclei. Pole cells, which are the future germline, are emitted. At the onset of NC 14, cellularization starts and plasma membrane furrows form between every nucleus. Over one hour, furrows invaginate to make an epithelial sheet of mononucleate cells.
Fig. 2.
Fig. 2.. Furrow assembly and compartmentalization during cellularization.
Chromosomes/nuclei and microtubules/MTOCs shown in purple and gray, respectively. (A) In mitosis of NC 13, metaphase furrows invaginate around every spindle, but no furrow forms at central spindles. At the end of NC 13, metaphase furrows partially regress. Once the embryo transitions to NC 14 and cellularization, remnants of metaphase furrows become “old furrows” and cortical flow drives recruitment of Myosin-2 and other components to assemble “new furrows” between daughter nuclei. As furrows form, they also polarize to generate distinct cortical compartments or domains as indicated. Establishment of a subapical domain is first seen at cellularization. (B) Endocytosis at the basal compartment in early cellularization and at the apical compartment in later cellularization ensures the proper membrane and protein complement per compartment.
Fig. 3.
Fig. 3.. Membrane handling and exocytosis during cellularization.
Nuclei and microtubules/MTOCs shown in purple and gray, respectively. (A) F-actin shown in orange. In addition to exocytosis, an apical microvillar membrane reservoir also unfolds to fuel furrow growth (i.e. picture a wavy string straightening out to cover more distance). Pulling forces exerted at the furrow tips by plus-end directed microtubule motors may aid unfolding. Membrane and microvillar F-actin depletion are both linearly coupled to furrow ingression. By late cellularization the reservoir is gone, and the tops of cells are flat. (B) Three membrane trafficking routes, culminating in exocytosis, deliver components to the cell surface as indicated.
Fig. 4.
Fig. 4.. Actomyosin constriction during cellularization.
Nuclei and actomyosin shown in purple and green, respectively. Centrosomes shown in gray. (A) Actomyosin ring constriction occurs in three phases, as indicated, to close off the bottom of cells during cellularization. (B) Two conspicuous phenotypes are seen when either the actomyosin ring does not assemble properly (left) or ring constriction is mis-regulated (right). In loss of function mutants for discontinuous actin hexagon, and other mutants/perturbations that lead to an F-actin deficit in the ring, furrows are weakened and sometimes regress, generating multinucleate cells. In loss of function mutants for bottleneck, and other mutants/perturbation that lead to premature constriction of actomyosin rings, the nuclei are pinched by the ring and cellularization fails.
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