Trends in Cell Biology
Volume 22, Issue 10, October 2012, Pages 527-535
Journal home page for Trends in Cell Biology

Review
Mechanical feedback between membrane tension and dynamics

https://doi.org/10.1016/j.tcb.2012.07.005Get rights and content

The plasma membrane represents a physical inelastic barrier with a given area that adheres to the underlying cytoskeleton. The tension in the membrane physically affects cell functions and recent studies have highlighted that this physical signal orchestrates complex aspects of trafficking and motility. Despite its undeniable importance, little is known about the mechanisms by which membrane tension regulates cell functions or stimulates signals. The maintenance of membrane tension is also a matter of debate, particularly the nature of the membrane reservoir and trafficking pathways that buffer tension. In this review we discuss the importance of membrane area and of tension as a master integrator of cell functions, particularly for membrane traffic.

Section snippets

Membrane tension and area

In the past, we have discussed the role that tension in the plasma membrane of animal cells plays in the mechanical functions of cell motility, endocytosis, and membrane resealing 1, 2, 3. It appears that tension acts as a break on the rate of those functions and coordinates them at the whole-cell level. Because of the large surface area to volume ratio of most mammalian cells, the tension seems to be primarily set by the adhesion between the membrane and the cytoskeleton. A recent review [4]

Plasma membrane area and plasma membrane reservoir

As cells change shape, the plasma membrane has to adapt to the new shape and the membrane area must be redistributed accordingly. This redistribution comes primarily from the readily available membrane reservoir, or buffer, present at the surface of the cell in the form of membrane superstructures 5, 13, 14.

Crosstalk between membrane trafficking and membrane tension

Increases in membrane tension have been described to activate exocytosis and inhibit endocytosis [31]. Conversely, a decrease in tension slows exocytosis and increases endocytosis [31]. These opposite effects will produce opposite changes in plasma membrane area and indicate that a major response to changes in membrane tension involves changes in membrane trafficking. However, the control of endomembrane trafficking by membrane tension is more difficult to tackle experimentally and is poorly

CLIC/GEEC pathways: fundamental regulators of membrane dynamics

The clathrin-independent endocytic pathways are major contributors to membrane dynamics (Figure 3). Quantitative ultrastructural measurements indicate that the CLIC pathway could account for up to 90% of the volume internalized by fibroblasts over short (15 s) timescales 41, 42. Unlike clathrin-mediated endocytic vesicles, which have a distinct spherical coated structure of about 100 nm in diameter, clathrin-independent endocytic pathways are diverse in shape. Caveolae, for instance, can combine

First experimental evidence

More than a decade ago, lamellipodium protrusion was shown to be inversely related to membrane tension [51]. At about the same time, separate findings suggested that membrane trafficking was directly linked to both membrane tension regulation and cell shape changes, particularly in mitosis [13]. However, with the exception of mitosis [17], these effects were primarily linked to externally or internally induced mechanical or chemical modifications.

Results from modeling

Several modeling studies supported the idea that

Concluding remarks

To play its role as a global regulator, the physical signal of tension needs to be transmitted to the well-established biochemical responses known to regulate functions such as trafficking and migration. During these processes, the physical aspect of the signal could also induce more biomechanical consequences, such as protein stretching and extension that could lead to biochemical signaling. Recent reviews and commentaries have already proposed some interesting hypotheses and future areas of

Acknowledgments

Funding was provided by a grant from the Singapore Government to the Mechanobiology Institute. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Glossary

Caveolae
protein-driven plasma membrane invaginations (of 60–80 nm diameter) enriched in cholesterol, sphingolipids, and caveolin protein oligomers.
Cortical tension
the tension borne by the actin cortex beneath the plasma membrane.
In-plane tension
the component of membrane tension due to osmotic pressure differences across the plasma membrane.
Membrane–cytoskeleton adhesion
the component of membrane tension due to the multitude of weak binding interactions between cytoskeletal components and membrane

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