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Review
. 2014 Mar-Apr;4(2):39-46.
doi: 10.4161/bioa.29069. Epub 2014 May 20.

A membrane reservoir at the cell surface: unfolding the plasma membrane to fuel cell shape change

Lauren Figard  1 , Anna Marie Sokac  1
Affiliations
Review

A membrane reservoir at the cell surface: unfolding the plasma membrane to fuel cell shape change

Lauren Figard et al. Bioarchitecture. 2014 Mar-Apr.

Abstract

Cell surface expansion is a necessary part of cell shape change. One long-standing hypothesis proposes that membrane for this expansion comes from the flattening out of cell surface projections such as microvilli and membrane folds. Correlative EM data of cells undergoing phagocytosis, cytokinesis, and morphogenesis has hinted at the existence of such an unfolding mechanism for decades; but unfolding has only recently been confirmed using live-cell imaging and biophysical approaches. Considering the wide range of cells in which plasma membrane unfolding has now been reported, it likely represents a fundamental mechanism of cell shape change.

Keywords: actin; cell shape change; cell surface area regulation; cellularization; exocytosis; microvilli; morphogenesis; plasma membrane tension.

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Figures

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Figure 1. Microvilli are lost or gained coincident with cell surface expansion or shrinkage, respectively. Many cultured cells (A) alternate between a spherical shape in mitosis (left), and a flat spread shape in interphase (right). Spherical cells are decorated with dense microvilli, whereas their spread counterparts display a smoother surface, devoid of microvilli. In cellularization (B), the first tissue-building event in the Drosophila embryo, furrows form at the syncytial embryo’s surface (left) and ingress between ~6000 nuclei to generate a single layer of epithelial cells (right). This expands the apparent membrane surface area ~25-fold in one hour. At the beginning of cellularization, the embryo surface is covered in dense microvilli; by the end of cellularization, the microvilli are gone. (A-B: mitotic chromosomes or nuclei are shown in blue)
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Figure 2. Microvillar membrane unfolds and slides along the embryo surface during Drosophila cellularization. Schematic depicting how red fluorescent wheat germ agglutinin (WGA) was used to pulse-label apical microvilli in cellularizing Drosophila embryos. After the microvillar membrane label was applied, time-lapse imaging during furrow ingression allowed us to follow the membrane as it slid along the plane of the cell surface and into the furrows. (Nuclei are shown in blue; WGA is shown in red).
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Figure 3. Membrane stores are differentially utilized in different cell types. Macrophage phagocytosis (A) occurs with two phases of membrane expansion. The first phase (left) is fueled by unfolding of membrane projections on the cell surface. After unfolding is complete, plasma membrane tension spikes, signaling the transition to a second phase, which is fueled by exocytosis. Furrow ingression in Drosophila cellularization (B) also occurs in two phases of membrane expansion. Unlike the macrophage, membrane unfolding and exocytosis fuel both phases simultaneously. Any excess membrane that is not utilized by unfolding may be pruned away by endocytosis.
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