Active biological materials

Abstract

Cells make use of dynamic internal structures to control shape and create movement. By consuming energy to assemble into highly organized systems of interacting parts, these structures can generate force and resist compression, as well as adaptively change in response to their environment. Recent progress in reconstituting cytoskeletal structures in vitro has provided an opportunity to characterize the mechanics and dynamics of filament networks formed from purified proteins. Results indicate that a complex interplay between length scales and timescales underlies the mechanical responses of these systems and that energy consumption, as manifested in molecular motor activity and cytoskeletal filament growth, can drive transitions between distinct material states. This review discusses the basic characteristics of these active biological materials that set them apart from conventional materials and that create a rich array of unique behaviors.

Figure 1

Crawling motility of a cell fragment containing no nucleus. Formed from a fish epidermal cell involved in wound healing, this fragment is able to crawl in a manner similar to the original cell. The active biological materials that drive this cell movement are capable of adaptive responses without nuclear control.

Figure 2

In vitro reconstitution of dendritic actin network growth. Cartoon and fluorescence image show labeled actin monomers in an actin network growing between a surface and the cantilever of an atomic force microscope. The growing network, similar to that at the leading edge of crawling cells, generates a force that displaces the cantilever, enabling the direct measurement of force and velocity. The dendritic actin network architecture is generated by molecules including actin monomers (red ), nucleation promoting factors ( green), and branching proteins ( yellow).

Figure 3

Two snapshots from a computer simulation of an elastic network comprising cross-linked semiflexible polymers. Line colors and thicknesses indicate each segment’s instantaneous longitudinal and transverse strain, respectively (with thick red lines representing the strongest deformations). Although these two configurations share some similarities in the way stress is distributed through the system, they also possess marked differences. These images demonstrate that in the course of natural thermal fluctuations, such a network accesses many distinct microscopic strain states on the length scale shown. Moving among these states requires collective redistributions of force. Fluctuations of this nature, neglected in both continuum and single-chain theories of actin networks, could contribute importantly to dynamical processes, such as elongation at the leading edge of a growing network or the initiation of a filopodium, that are sensitive to mechanical variations over a wide range of length scales.

Figure 4

Parallel actin filament protrusions against a bilayer membrane. A confocal fluorescence image shows narrow actin protrusions emerging from a reconstituted dendritic actin network growing against the outer surface of a giant unilamellar vesicle. Interactions between the dendritic network and the deformable bilayer membrane lead to the clustering and parallel growth of the membrane-bound filopodium-like protrusions.