Emergent complexity of the cytoskeleton: from single filaments to tissue

Abstract

Despite their overwhelming complexity, living cells display a high degree of internal mechanical and functional organization which can largely be attributed to the intracellular biopolymer scaffold, the cytoskeleton. Being a very complex system far from thermodynamic equilibrium, the cytoskeleton's ability to organize is at the same time challenging and fascinating. The extensive amounts of frequently interacting cellular building blocks and their inherent multifunctionality permits highly adaptive behavior and obstructs a purely reductionist approach. Nevertheless (and despite the field's relative novelty), the physics approach has already proved to be extremely successful in revealing very fundamental concepts of cytoskeleton organization and behavior. This review aims at introducing the physics of the cytoskeleton ranging from single biopolymer filaments to multicellular organisms. Throughout this wide range of phenomena, the focus is set on the intertwined nature of the different physical scales (levels of complexity) that give rise to numerous emergent properties by means of self-organization or self-assembly.

Mechanochemical pattern formation in simple models of active viscoelastic fluids and solids

“…The cytoplasm of the living cells is formed by filaments consisting of chains of actin protein organized in bundles by cross-linking proteins [1]. The continuous polymerization and depolymerization of filaments and the unbinding of cross-linkers may produce cytoplasmic flows at large scales of time, which permits the modeling of such flows in terms of active gel theories [2,3,4].…”

Keratin network modifications lead to the mechanical stiffening of the hair follicle fiber

“…An active field aims at understanding how the local structural and mechanical properties of bionetworks define its macroscopic mechanics from a molecular scale toward a cellular and tissue scale (4-6). One challenge is that the properties of these networks have to be considered over multiple length and force scales with macroscopic mechanical forces being transduced from the whole tissue scale down to the cellular and molecular level and vice versa.At the cellular level, the last decades witnessed for a considerable advancement toward a better understanding of how the cytoskeleton composed of actin, microtubules, and intermediate filaments (IFs) determines cellular mechanics (1,(6)(7)(8). In vitro studies on isolated cells (6) and reconstituted in vitro bionetworks with controllable architecture and composition (9-12) considerably advanced our knowledge of cytoskeletal mechanics.…”

“…At the cellular level, the last decades witnessed for a considerable advancement toward a better understanding of how the cytoskeleton composed of actin, microtubules, and intermediate filaments (IFs) determines cellular mechanics (1,(6)(7)(8). In vitro studies on isolated cells (6) and reconstituted in vitro bionetworks with controllable architecture and composition (9-12) considerably advanced our knowledge of cytoskeletal mechanics.…”

“…In vitro studies on isolated cells (6) and reconstituted in vitro bionetworks with controllable architecture and composition (9)(10)(11)(12) considerably advanced our knowledge of cytoskeletal mechanics. However, these models are only approximations of the complex tridimensional architecture of most tissues.…”

“…An active field aims at understanding how the local structural and mechanical properties of bionetworks define its macroscopic mechanics from a molecular scale toward a cellular and tissue scale (4)(5)(6). One challenge is that the properties of these networks have to be considered over multiple length and force scales with macroscopic mechanical forces being transduced from the whole tissue scale down to the cellular and molecular level and vice versa.…”