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

Cohen M, Baum B, Miodownik M - J R Soc Interface (2010)

Bottom Line: Here, we develop a general model of protrusion-based patterning to analyse the role of noise in this process.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.

View Article: PubMed Central - PubMed

Affiliation: CoMPLEX, University College London, London, UK. m.cohen@ucl.ac.uk

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At different signal ranges and inhibitory thresholds, a broad scope of patterns can be achieved. (a–c) Each panel shows typical results after 1000 steps for simulations of inhibitory signalling carried out in a 20 × 20 hexagonally packed array of cells. Different signal ranges were implemented, as illustrated by the size of the hexagonal shells positioned on the left ((a) one cell, (b) two cells and (c) three cells). For each signal range, a selection of inhibitory thresholds is shown with and without temporal noise, Nt = 0.01. The active signalling cells and the neighbourhood of inactive cells are identified according to the key in (d). It is clear from this illustrative set of examples that different patterns are achievable ranging from spots through to stripes that may be in some cases realigned by the input of signal noise (e.g. (b), T = 10).
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RSIF20100488F5: At different signal ranges and inhibitory thresholds, a broad scope of patterns can be achieved. (a–c) Each panel shows typical results after 1000 steps for simulations of inhibitory signalling carried out in a 20 × 20 hexagonally packed array of cells. Different signal ranges were implemented, as illustrated by the size of the hexagonal shells positioned on the left ((a) one cell, (b) two cells and (c) three cells). For each signal range, a selection of inhibitory thresholds is shown with and without temporal noise, Nt = 0.01. The active signalling cells and the neighbourhood of inactive cells are identified according to the key in (d). It is clear from this illustrative set of examples that different patterns are achievable ranging from spots through to stripes that may be in some cases realigned by the input of signal noise (e.g. (b), T = 10).

Mentions: We recently demonstrated that cell–cell signalling can occur at multiple cell ranges as a result of dynamic filopodial protrusions [2]. Thus, we used our model to investigate the effect of signalling at these ranges of intercellular communication with different inhibition thresholds (T). We simulated the effect of communication via protrusions by incorporating larger neighbour shells (figure 5) into the model. In particular, we investigated the influence of communication between cells separated by one, two or three cells. Figure 5 shows some typical examples of the types of pattern that were seen with and without the influence of signalling noise. For the nearest-neighbour communication model (figure 5a), the emergent patterning is either isolated spots, which optimize their packing under signal noise, or alternatively rings of signalling cells. However, once the signal range extends to two or three cells, a diverse range of spots, clusters, stripes and rings is obtainable (figure 5b,c). As can be observed, the thickness of the emergent clusters or stripes is dependent on the signal threshold; however, as for the fine-grained patterns of spots, their average separation is fixed according to the signalling range. Notably, when noise is implemented, the stripes tend to align themselves with the cell boundaries.Figure 5.


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

Cohen M, Baum B, Miodownik M - J R Soc Interface (2010)

At different signal ranges and inhibitory thresholds, a broad scope of patterns can be achieved. (a–c) Each panel shows typical results after 1000 steps for simulations of inhibitory signalling carried out in a 20 × 20 hexagonally packed array of cells. Different signal ranges were implemented, as illustrated by the size of the hexagonal shells positioned on the left ((a) one cell, (b) two cells and (c) three cells). For each signal range, a selection of inhibitory thresholds is shown with and without temporal noise, Nt = 0.01. The active signalling cells and the neighbourhood of inactive cells are identified according to the key in (d). It is clear from this illustrative set of examples that different patterns are achievable ranging from spots through to stripes that may be in some cases realigned by the input of signal noise (e.g. (b), T = 10).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3104346&req=5

RSIF20100488F5: At different signal ranges and inhibitory thresholds, a broad scope of patterns can be achieved. (a–c) Each panel shows typical results after 1000 steps for simulations of inhibitory signalling carried out in a 20 × 20 hexagonally packed array of cells. Different signal ranges were implemented, as illustrated by the size of the hexagonal shells positioned on the left ((a) one cell, (b) two cells and (c) three cells). For each signal range, a selection of inhibitory thresholds is shown with and without temporal noise, Nt = 0.01. The active signalling cells and the neighbourhood of inactive cells are identified according to the key in (d). It is clear from this illustrative set of examples that different patterns are achievable ranging from spots through to stripes that may be in some cases realigned by the input of signal noise (e.g. (b), T = 10).
Mentions: We recently demonstrated that cell–cell signalling can occur at multiple cell ranges as a result of dynamic filopodial protrusions [2]. Thus, we used our model to investigate the effect of signalling at these ranges of intercellular communication with different inhibition thresholds (T). We simulated the effect of communication via protrusions by incorporating larger neighbour shells (figure 5) into the model. In particular, we investigated the influence of communication between cells separated by one, two or three cells. Figure 5 shows some typical examples of the types of pattern that were seen with and without the influence of signalling noise. For the nearest-neighbour communication model (figure 5a), the emergent patterning is either isolated spots, which optimize their packing under signal noise, or alternatively rings of signalling cells. However, once the signal range extends to two or three cells, a diverse range of spots, clusters, stripes and rings is obtainable (figure 5b,c). As can be observed, the thickness of the emergent clusters or stripes is dependent on the signal threshold; however, as for the fine-grained patterns of spots, their average separation is fixed according to the signalling range. Notably, when noise is implemented, the stripes tend to align themselves with the cell boundaries.Figure 5.

Bottom Line: Here, we develop a general model of protrusion-based patterning to analyse the role of noise in this process.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.

View Article: PubMed Central - PubMed

Affiliation: CoMPLEX, University College London, London, UK. m.cohen@ucl.ac.uk

Show MeSH
Related in: MedlinePlus