Optimality of intercellular signaling: direct transport versus diffusion

TL;DR

This paper compares the energy efficiency of diffusion and direct transport mechanisms in intercellular signaling, revealing conditions under which each method is optimal and explaining the prevalence of protrusion-based signaling in long-range communication.

Contribution

It introduces a model analyzing the optimal projection rate for direct transport and compares the efficiency of diffusion versus direct transport under various conditions.

Findings

Direct transport is more efficient for large molecule quantities.

A critical molecule number exists where both mechanisms are equally efficient.

Protrusion-based signaling is favored for long-range cellular communication.

Abstract

Intercellular signaling has an important role in organism development, but not all communication occurs using the same mechanism. Here, we analyze the energy efficiency of intercellular signaling by two canonical mechanisms: diffusion of signaling molecules and direct transport mediated by signaling cellular protrusions. We show that efficient contact formation for direct transport can be established by an optimal rate of projecting protrusions, which depends on the availability of information about the location of the target cell. The optimal projection rate also depends on how signaling molecules are transported along the protrusion, in particular the ratio of the energy cost for contact formation and molecule synthesis. Also, we compare the efficiency of the two signaling mechanisms, under various model parameters. We find that the direct transport is favored over the diffusion when transporting a large amount of signaling molecules. There is a critical number of signaling molecules at which the efficiency of the two mechanisms are the same. The critical number is small when the distance between cells is far, which helps explain why protrusion-based mechanisms are observed in long-range cellular communications.