The importance of structured noise in the generation of self-organizing tissue patterns through contact-mediated cell–cell signalling

Michael Cohen,Mark Miodownik,Buzz Baum

doi:10.1098/rsif.2010.0488

Michael Cohen, Mark Miodownik + Show 1 more

Open Access

https://doi.org/10.1098/rsif.2010.0488

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Abstract

Lateral inhibition provides the basis for a self-organizing patterning system in which distinct cell states emerge from an otherwise uniform field of cells. The development of the microchaete bristle pattern on the notum of the fruitfly, Drosophila melanogaster, has long served as a popular model of this process. We recently showed that this bristle pattern depends upon a population of dynamic, basal actin-based filopodia, which span multiple cell diameters. These protrusions establish transient signalling contacts between non-neighbouring cells, generating a type of structured noise that helps to yield a well-ordered and spaced pattern of bristles. Here, we develop a general model of protrusion-based patterning to analyse the role of noise in this process. Using a simple asynchronous cellular automata rule-based model we show that this type of structured noise drives the gradual refinement of lateral inhibition-mediated patterning, as the system moves towards a stable configuration in which cells expressing the inhibitory signal are near-optimally packed. By analysing the effects of introducing thresholds required for signal detection in this model of lateral inhibition, our study shows how filopodia-mediated cell–cell communication can generate complex patterns of spots and stripes, which, in the presence of signalling noise, align themselves across a patterning field. Thus, intermittent protrusion-based signalling has the potential to yield robust self-organizing tissue-wide patterns without the need to invoke diffusion-mediated signalling.

Highlights

Tissue patterning and morphogenesis must be coordinated during development if groups of cells are to establish self-organizing patterns of gene expression as they divide, change shape and swap neighbours [1]
To gain an insight into the general features of this type of contact-mediated patterning, we present here a computational model of protrusion-based signalling in which we have systematically explored the roles of signalling noise and thresholds
Having previously described a specific role for these protrusions in bristle patterning the developing notum, here, we develop a logical framework in which to analyse the role of noise in pattern formation in general

Summary

Introduction

Tissue patterning and morphogenesis must be coordinated during development if groups of cells are to establish self-organizing patterns of gene expression as they divide, change shape and swap neighbours [1]. Few of the mechanisms enabling interacting groups of cells to pattern developing tissues are understood. Having previously described a specific role for these protrusions in bristle patterning the developing notum, here, we develop a logical framework in which to analyse the role of noise in pattern formation in general.

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