Maximum velocity of self-propulsion for an active segment

TL;DR

This paper investigates the optimal spatial organization of active elements in a cell's crawling layer to maximize velocity, revealing different configurations depending on whether contraction or protrusion dominates, consistent with experimental observations.

Contribution

It formulates a variational problem to determine optimal arrangements of adhesion complexes for different active mechanisms in cell motility, providing theoretical bounds and insights.

Findings

Optimal adhesion localization depends on the dominant active mechanism.

Contraction-driven motility favors trailing edge adhesion with 'pullers'.

Protrusion-driven motility favors leading edge adhesion with 'pushers'.

Abstract

The motor part of a crawling eukaryotic cell can be represented schematically as an active continuum layer. The main active processes in this layer are protrusion, originating from non-equilibrium polymerization of actin fibers, contraction, induced by myosin molecular motors and attachment due to active bonding of trans-membrane proteins to a substrate. All three active mechanisms are regulated by complex signaling pathways involving chemical and mechanical feedback loops whose microscopic functioning is still poorly understood. In this situation, it is instructive to take a reverse engineering approach and study a problem of finding the spatial organization of standard active elements inside a crawling layer ensuring an optimal cost-performance trade-off. In this paper we assume that (in the range of interest) the energetic cost of self-propulsion is velocity independent and adopt, as an optimality criterion, the maximization of the overall velocity. We then choose a prototypical setting, formulate the corresponding variational problem and obtain a set of bounds suggesting that radically different spatial distributions of adhesive complexes would be optimal depending on the domineering active mechanism of self-propulsion. Thus, for contraction-dominated motility, adhesion has to cooperate with 'pullers' which localize at the trailing edge of the cell, while for protrusion-dominated motility it must conspire with 'pushers' concentrating at the leading edge of the cell. Both types of crawling mechanisms were observed experimentally.