Publication date: 25th July 2016
In most migrating cells actin filaments polymerizing against the plasma membrane generate the force to protrude a lamellipodial leading edge. The load experienced by each growing filament depends on the number of filaments pushing against a patch of membrane displaying a given lateral tension. It has been shown that lamellipodia can react to increasing external loads by increasing their pushing force before they eventually stall at excessive counter-forces. In line with such a concept of adaptive force generation, in vitro growing actin networks show loading history dependent changes in structure and polymerization speed. We performed quantitative morphometric analysis of zebrafish keratocytes as a prototypic model for lamellipodial locomotion. When fluctuations of projected cell area were measured over time they showed a faithful positive correlation with actin intensity at the leading edges, indicating that changes in membrane tension, which result from changes in cell spreading, might impact network density. Likewise, cells undergoing rapid shrinkage due to sudden rear-detachment showed an instantaneous but transient increase in protrusion speed, which was followed by a drop in leading edge actin density that sustained until surface area recovered. These correlative findings were confirmed by direct experimental manipulations of membrane tension by micropipette aspiration and osmotic treatments. Both approaches confirmed that lamellipodial actin responds to changes in membrane tension by adjusting filament density, as shown by dynamic quantitative imaging and by direct visualization of actin network geometry using electron tomography. This adaptation mechanism, which we also confirmed in other cell types, might effectively enable the cell to tune protrusive force to the mechanical load at the leading edge, thereby allowing it to buffer excessive fluctuations in protrusion speed and to react to external barriers.
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