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Review
. 2011 Sep;40(9):1013-27.
doi: 10.1007/s00249-011-0741-0. Epub 2011 Aug 11.

Cell motility: the integrating role of the plasma membrane

Kinneret Keren  1
Affiliations
Review

Cell motility: the integrating role of the plasma membrane

Kinneret Keren. Eur Biophys J. 2011 Sep.

Abstract

The plasma membrane is of central importance in the motility process. It defines the boundary separating the intracellular and extracellular environments, and mediates the interactions between a motile cell and its environment. Furthermore, the membrane serves as a dynamic platform for localization of various components which actively participate in all aspects of the motility process, including force generation, adhesion, signaling, and regulation. Membrane transport between internal membranes and the plasma membrane, and in particular polarized membrane transport, facilitates continuous reorganization of the plasma membrane and is thought to be involved in maintaining polarity and recycling of essential components in some motile cell types. Beyond its biochemical composition, the mechanical characteristics of the plasma membrane and, in particular, membrane tension are of central importance in cell motility; membrane tension affects the rates of all the processes which involve membrane deformation including edge extension, endocytosis, and exocytosis. Most importantly, the mechanical characteristics of the membrane and its biochemical composition are tightly intertwined; membrane tension and local curvature are largely determined by the biochemical composition of the membrane and the biochemical reactions taking place; at the same time, curvature and tension affect the localization of components and reaction rates. This review focuses on this dynamic interplay and the feedbacks between the biochemical and biophysical characteristics of the membrane and their effects on cell movement. New insight on these will be crucial for understanding the motility process.

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Figures

Fig. 1
Fig. 1
Regulation of actin dynamics at the membrane. a An example of Arp2/3 mediated activation of actin polymerization by membrane localized factors. WASP is localized and activated at the membrane through multiple signals including binding to PIP2 lipids, Cdc42 protein, and a protein from the BAR-domain family containing an SH3 domain (e.g. Toca). WASP is further activated by dimerization/oligomerization (not shown) (Padrick and Rosen 2010). Activated WASP activates Arp2/3 which induces actin filament nucleation and network growth. Membrane curvature is induced by the BAR domain, and affected by the forces generated by actin polymerization. b Membrane composition regulates actin disassembly. PIP2 lipids in the membrane bind and inactivate cofilin (left panel). Reduced PIP2 levels induced by signaling events lead to release of membrane bound cofilin, which becomes active and severs actin filaments (right panel)
Fig. 2
Fig. 2
Membrane transport and recycling of adhesions. a Adhesion complexes assemble in a hierarchical fashion from integrins embedded in the membrane and cytosolic proteins. Nascent adhesions form at the leading edge and attach to the substrate. Actin network growth and flow away from the leading edge leads to a rearward flux of adhesions. In particular, rearward flux is observed for bound integrins. b Various possible mechanisms for recycling integrins back to the leading edge have been suggested. Passive transport by diffusion will tend to equilibrate the integrin density but may not be fast enough for efficient recycling. Active transport to the leading edge can occur with the help of motor proteins which drag the integrins within the membrane, by drift induced by bulk membrane flow, or by polarized membrane trafficking
Fig. 3
Fig. 3
Membrane tension in motile cells. a Membrane tension measurements using the tether-pulling assay. A membrane tether is generated by pulling a coated bead away from the cell surface by use of optical tweezers. The force the tether exerts on the bead can be measured from the displacement of the bead from the center of the trap. The apparent membrane tension, which is equal to the sum of the in-plane tension and the adhesion energy per unit area, can be calculated from the measured tether force. b The apparent membrane tension exerts forces perpendicular to the cell boundary (black arrows). In the absence of membrane flow, the apparent membrane tension has to be spatially homogenous. The membrane tension opposes actin network growth at the leading edge, while assisting retraction at the rear. c Endocytosis rates increase with decreasing tension whereas exocytosis rates decrease. It has been suggested that tension-dependent endocytosis and exocytosis are involved in surface area regulation and buffering of membrane tension: increased tension leads to excess exocytosis, leading to an increase in cell surface area and a decrease in tension, and vice versa. d Membrane invaginations, for example caveolae, provide means for rapidly increasing cell surface area and buffering membrane tension. Caveolae require ATP and actin for their synthesis. A rapid increase in tension (because of stretching or swelling of the cells) is buffered by rapid flattening of the caveolae, providing additional surface area
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