Abstract
The different actin structures governing eukaryotic cell shape and movement are not only determined by the properties of the actin filaments and associated proteins, but also by geometrical constraints. We recently demonstrated that limiting nucleation to specific regions was sufficient to obtain actin networks with different organization. To further investigate how spatially constrained actin nucleation determines the emergent actin organization, we performed detailed simulations of the actin filament system using Cytosim. We first calibrated the steric interaction between filaments, by matching, in simulations and experiments, the bundled actin organization observed with a rectangular bar of nucleating factor. We then studied the overall organization of actin filaments generated by more complex pattern geometries used experimentally. We found that the fraction of parallel versus antiparallel bundles is determined by the mechanical properties of actin filament or bundles and the efficiency of nucleation. Thus nucleation geometry, actin filaments local interactions, bundle rigidity, and nucleation efficiency are the key parameters controlling the emergent actin architecture. We finally simulated more complex nucleation patterns and performed the corresponding experiments to confirm the predictive capabilities of the model.
Highlights
Actin assembles to form higher order structures [1] that are essential to cell morphogenesis, adhesion and motility [2]
Actin filaments can form aligned structures of anti-parallel filaments in stress fibers or transverse arcs, that are site of active contraction driven by myosin motors [24,25] and are responsible for the cellular mechanical response [26]
The binding partners guide the organization of actin filaments, and the binding of actin-associated proteins is sensitive to the architecture of the actin network [27,28]
Summary
Actin assembles to form higher order structures [1] that are essential to cell morphogenesis, adhesion and motility [2]. Actin filaments can form bundles of parallel filaments, creating finger-like protrusions in the membrane called filopodia [18] that explore the extracellular matrix [19]. Actin bundles can be used as tracks for protein or cargo transport [20,21]. These bundles can be formed by branched organization that merged into elongated parallel actin filaments [22,23]. Deciphering the principles governing the assembly of the different actin structural architectures is an important step towards a better understanding of the variety of cellular processes. Many excellent studies have focused on identifying the biochemical composition of the different actin organizations [6], but the physical and geometrical laws governing their architecture are still largely unknown
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