[Paper Review] Fiber plucking by molecular motors yields large emergent contractility in stiff biopolymer networks

Pierre Ronceray, Chase P. Broedersz+1 more|arXiv (Cornell University)|May 11, 2018

Cellular Mechanics and Interactions22 references11 citations

TL;DR

This paper proposes that transverse forces exerted by molecular motors on biopolymer filaments induce a geometrically amplified tension—termed 'fiber plucking'—that generates large-scale contractile stresses in stiff, densely connected networks. Unlike linear force transmission, plucking creates nonlinear amplification via transverse deflection, yielding contractility up to 17× greater than expected, especially in stiff networks where small angular deflections maximize tension amplification.

ABSTRACT

The mechanical properties of the cell depend crucially on the tension of its cytoskeleton, a biopolymer network that is put under stress by active motor proteins. While the fibrous nature of the network is known to strongly affect the transmission of these forces to the cellular scale, our understanding of this process remains incomplete. Here we investigate the transmission of forces through the network at the individual filament level, and show that active forces can be geometrically amplified as a transverse motor-generated force force "plucks" the fiber and induces a nonlinear tension. In stiff and densely connnected networks, this tension results in large network-wide tensile stresses that far exceed the expectation drawn from a linear elastic theory. This amplification mechanism competes with a recently characterized network-level amplification due to fiber buckling, suggesting that that fiber networks provide several distinct pathways for living systems to amplify their molecular forces.

Motivation & Objective

• To understand how active forces from molecular motors generate large-scale contractile stresses in biopolymer networks.
• To identify and characterize a new mechanism of force amplification at the single-filament level, distinct from filament buckling.
• To investigate how network stiffness and connectivity influence the emergence of large-scale contractility through plucking-induced tension.
• To clarify the conditions under which plucking dominates over buckling as a stress amplification pathway in cytoskeletal networks.

Proposed method

• A single-filament model is developed using two hinged, Hookean springs with bending penalty proportional to θ² for small deflections.
• The filament is anchored at both ends by stiff springs (stiffness k), modeling firm attachment to a rigid network.
• Active transverse forces F are applied perpendicularly at the hinge, inducing a plucking tension T_pluck ∼ F/θ that scales inversely with deflection angle θ.
• The model derives the force transmission pattern and quantifies the resulting far-field contractile stress, showing amplification beyond linear elasticity.
• The single-filament results are extended to multi-filament networks via numerical simulations, varying network connectivity and stiffness.
• The model compares plucking to buckling by analyzing force transmission patterns and stress amplification in both geometries.

Experimental results

Research questions

• RQ1 How does a transverse force applied by a motor on a filament lead to nonlinear amplification of contractile stress in a biopolymer network?
• RQ2 What role does network stiffness play in enabling geometric amplification through fiber plucking?
• RQ3 How does plucking-induced contractility compare quantitatively to buckling-induced stress amplification in stiff networks?
• RQ4 Under what conditions does plucking dominate over buckling as a mechanism for active stress generation?
• RQ5 Can plucking explain the emergence of large-scale contractility in reconstituted actomyosin networks?

Key findings

• Fiber plucking induces a transverse force amplification mechanism where tension T_pluck ∼ F/θ exceeds the applied motor force F, especially when deflection θ is small.
• In stiff, densely connected networks, plucking generates far-field contractile stresses up to 17 times larger than those from linear force transmission.
• The amplification is maximized at intermediate force levels and increases with network stiffness k, as smaller deflections θ lead to greater tension.
• Plucking is intrinsically contractile and independent of force orientation, reversing locally extensile forces into long-ranged contractile stresses.
• Plucking and buckling are distinct amplification mechanisms: plucking acts locally and geometrically, while buckling acts globally by increasing force transmission range.
• Plucking and buckling can cooperate: plucking-generated forces can exceed the buckling threshold, leading to further amplification through network-scale buckling.