Abstract
Actin filaments created by the Arp2/3 complex form branched networks that grow and push against cellular membranes. We employ theory and simulation to describe how membrane surfaces accelerate filament assembly via clustering of proteins, including WAVE-family nucleation promoting factors, that bind actin monomers and/or profilin-actin complexes. Briefly, thermal fluctuations drive filament tips on constrained, two-dimensional random walks across the membrane, where they collide with actin-charged polymerases. At low soluble actin concentrations, filament elongation is limited by delivery of monomers to the membrane surface; at high actin concentrations, elongation depends on how quickly fluctuating filaments search the membrane. Using measured parameter values we conclude that surface-mediated polymerization can outpace solution-mediated elongation, even at high actin concentrations (>100 μM). The finite time required for profilin dissociation decreases the advantage conferred by surface-associated polymerases, but only in the absence of force. Load forces enhance the effect of surface polymerases, which can both accelerate elongation and increase the force required to stall filament assembly.