The mechanics of F-actin microenvironments depend on the chemistry of probing surfaces

To understand the microscopic mechanical properties of actin networks, we m onitor the motion of embedded particles with controlled surface properties. The highly resolved Brownian motions of these particles reveal the viscoel astic character of the microenvironments around them. In both non-cross-lin ked and highly cross-linked actin networks, particles that bind F-actin rep ort viscoelastic moduli comparable to those determined by macroscopic rheol ogy experiments. By contrast, particles modified to prevent actin binding h ave weak microenvironments that are surprisingly insensitive to the introdu ction of filament cross-links. Even when adjacent in the same cross-linked gel, actin-binding and nonbinding particles report viscoelastic moduli that differ by two orders of magnitude at low frequencies (0.5-1.5 rad/s) but c onverge at high frequencies (> 10(4) rad/s). For all particle chemistries, electron and light microscopies show no F-actin recruitment or depletion, s o F-actin microheterogeneities cannot explain the deep penetration (similar to 100 nm) of nonbinding particles. Instead, we hypothesize that a local d epletion of cross-linking around nonbinding particles explains the phenomen a. With implications for organelle mobility in cells, our results show that actin binding is required for microenvironments to reflect macroscopic pro perties, and conversely, releasing actin enhances particle mobility beyond the effects of mere biochemical untethering.