On Stretching, Bending, Shearing, and Twisting of Actin Filaments I: Variational Models

• Published in: Journal of chemical theory and computation Vol. 18; no. 8; pp. 4865 - 4878
• Main Authors: Floyd, Carlos, Ni, Haoran, Gunaratne, Ravinda S., Erban, Radek, Papoian, Garegin A.
• Format: Journal Article
• Language: English
• Published: Washington American Chemical Society 09.08.2022
• Subjects: Actomyosin; Degrees of freedom; Dynamic models; Filaments; Modelling; Modulus of elasticity; Molecular Mechanics; One dimensional models; Polynomials; Shearing; Spline functions; Stretching; Systematic errors; Twisting
• ISSN: 1549-9618; 1549-9626
• DOI: 10.1021/acs.jctc.2c00318

Mechanochemical simulations of actomyosin networks are traditionally based on one-dimensional models of actin filaments having zero width. Here, and in the follow up paper (arXiv, DOI 10.48550/arXiv.2203.01284), approaches are presented for more efficient modeling that incorporates stretching, shearing, and twisting of actin filaments. Our modeling of a semiflexible filament with a small but finite width is based on the Cosserat theory of elastic rods, which allows for six degrees of freedom at every point on the filament’s backbone. In the variational models presented in this paper, a small and discrete set of parameters is used to describe a smooth filament shape having all degrees of freedom allowed in the Cosserat theory. Two main approaches are introduced: one where polynomial spline functions describe the filament’s configuration, and one in which geodesic curves in the space of the configurational degrees of freedom are used. We find that in the latter representation the strain energy function can be calculated without resorting to a small-angle expansion, so it can describe arbitrarily large filament deformations without systematic error. These approaches are validated by a dynamical model of a Cosserat filament, which can be further extended by using multiresolution methods to allow more detailed monomer-based resolution in certain parts of the actin filament, as introduced in the follow up paper. The presented framework is illustrated by showing how torsional compliance in a finite-width filament can induce broken chiral symmetry in the structure of a cross-linked bundle.