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Computational cell model based on autonomous cell movement regulated by cell-cell signalling successfully recapitulates the "inside and outside" pattern of cell sorting.

Maeda TT, Ajioka I, Nakajima K - BMC Syst Biol (2007)

Bottom Line: Development of multicellular organisms proceeds from a single fertilized egg as the combined effect of countless numbers of cellular interactions among highly dynamic cells.The model gives some insights about what cellular behaviors make an appropriate global pattern of the cell population.The simulation results suggested that direction of cell movement responding to its neighborhood and the cell's mobility are important for this specific rearrangement.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. ttmaeda@gsc.riken.jp

ABSTRACT

Background: Development of multicellular organisms proceeds from a single fertilized egg as the combined effect of countless numbers of cellular interactions among highly dynamic cells. Since at least a reminiscent pattern of morphogenesis can be recapitulated in a reproducible manner in reaggregation cultures of dissociated embryonic cells, which is known as cell sorting, the cells themselves must possess some autonomous cell behaviors that assure specific and reproducible self-organization. Understanding of this self-organized dynamics of heterogeneous cell population seems to require some novel approaches so that the approaches bridge a gap between molecular events and morphogenesis in developmental and cell biology. A conceptual cell model in a computer may answer that purpose. We constructed a dynamical cell model based on autonomous cell behaviors, including cell shape, growth, division, adhesion, transformation, and motility as well as cell-cell signaling. The model gives some insights about what cellular behaviors make an appropriate global pattern of the cell population.

Results: We applied the model to "inside and outside" pattern of cell-sorting, in which two different embryonic cell types within a randomly mixed aggregate are sorted so that one cell type tends to gather in the central region of the aggregate and the other cell type surrounds the first cell type. Our model can modify the above cell behaviors by varying parameters related to them. We explored various parameter sets with which the "inside and outside" pattern could be achieved. The simulation results suggested that direction of cell movement responding to its neighborhood and the cell's mobility are important for this specific rearrangement.

Conclusion: We constructed an in silico cell model that mimics autonomous cell behaviors and applied it to cell sorting, which is a simple and appropriate phenomenon exhibiting self-organization of cell population. The model could predict directional cell movement and its mobility are important in the "inside and outside" pattern of cell sorting. Those behaviors are altered by signal molecules and consequently affect the global pattern of the cell sorting. Our model is also applicable to other developmental processes beyond cell sorting.

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Final configurations of aggregates of randomly mixed cells with different GAP PREFERENCE. The common conditions to both cell types: ACTIVATION THRESHOLD = {0.3 or 0.4}; DRAGGING TIME = {6, 10, or 30}; SINGLE MOVING DISTANCE = 1. The areas of the inner cavities within the aggregates in (a) and (b) were 2.597 and 0.834, respectively (SSPs). The CELL DISTRIBUTION RATIOs of the light cell type in (c), (d) and (e) were 5.274 ± 2.402 (S.D.), 8.132 ± 3.406, and 5.326 ± 1.281, respectively. The PERIMETER RATIOs in (c), (d) and (e) were 0.077 ± 0.059, 0.061 ± 0.056 and 0.077 ± 0.058, respectively.
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Figure 8: Final configurations of aggregates of randomly mixed cells with different GAP PREFERENCE. The common conditions to both cell types: ACTIVATION THRESHOLD = {0.3 or 0.4}; DRAGGING TIME = {6, 10, or 30}; SINGLE MOVING DISTANCE = 1. The areas of the inner cavities within the aggregates in (a) and (b) were 2.597 and 0.834, respectively (SSPs). The CELL DISTRIBUTION RATIOs of the light cell type in (c), (d) and (e) were 5.274 ± 2.402 (S.D.), 8.132 ± 3.406, and 5.326 ± 1.281, respectively. The PERIMETER RATIOs in (c), (d) and (e) were 0.077 ± 0.059, 0.061 ± 0.056 and 0.077 ± 0.058, respectively.

Mentions: Although the Hm preference did not seem to contribute to the "inside and outside" configuration under the above-mentioned conditions, "inside and outside" cell sorting occurred when one cell type had an Hm preference and the other cell type had an Htr preference (Fig. 8c–e). The cell type with the Htr preference (shown as the light cells) was always located near the center of the aggregate and was surrounded by the cell type with the Hm preference (shown as the dark cells). When an ACTIVATION THRESHOLD = 0.3 and a DRAGGING TIME ≤ 10 were used, an SSP occurred (Fig. 8a,b).


Computational cell model based on autonomous cell movement regulated by cell-cell signalling successfully recapitulates the "inside and outside" pattern of cell sorting.

Maeda TT, Ajioka I, Nakajima K - BMC Syst Biol (2007)

Final configurations of aggregates of randomly mixed cells with different GAP PREFERENCE. The common conditions to both cell types: ACTIVATION THRESHOLD = {0.3 or 0.4}; DRAGGING TIME = {6, 10, or 30}; SINGLE MOVING DISTANCE = 1. The areas of the inner cavities within the aggregates in (a) and (b) were 2.597 and 0.834, respectively (SSPs). The CELL DISTRIBUTION RATIOs of the light cell type in (c), (d) and (e) were 5.274 ± 2.402 (S.D.), 8.132 ± 3.406, and 5.326 ± 1.281, respectively. The PERIMETER RATIOs in (c), (d) and (e) were 0.077 ± 0.059, 0.061 ± 0.056 and 0.077 ± 0.058, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2100066&req=5

Figure 8: Final configurations of aggregates of randomly mixed cells with different GAP PREFERENCE. The common conditions to both cell types: ACTIVATION THRESHOLD = {0.3 or 0.4}; DRAGGING TIME = {6, 10, or 30}; SINGLE MOVING DISTANCE = 1. The areas of the inner cavities within the aggregates in (a) and (b) were 2.597 and 0.834, respectively (SSPs). The CELL DISTRIBUTION RATIOs of the light cell type in (c), (d) and (e) were 5.274 ± 2.402 (S.D.), 8.132 ± 3.406, and 5.326 ± 1.281, respectively. The PERIMETER RATIOs in (c), (d) and (e) were 0.077 ± 0.059, 0.061 ± 0.056 and 0.077 ± 0.058, respectively.
Mentions: Although the Hm preference did not seem to contribute to the "inside and outside" configuration under the above-mentioned conditions, "inside and outside" cell sorting occurred when one cell type had an Hm preference and the other cell type had an Htr preference (Fig. 8c–e). The cell type with the Htr preference (shown as the light cells) was always located near the center of the aggregate and was surrounded by the cell type with the Hm preference (shown as the dark cells). When an ACTIVATION THRESHOLD = 0.3 and a DRAGGING TIME ≤ 10 were used, an SSP occurred (Fig. 8a,b).

Bottom Line: Development of multicellular organisms proceeds from a single fertilized egg as the combined effect of countless numbers of cellular interactions among highly dynamic cells.The model gives some insights about what cellular behaviors make an appropriate global pattern of the cell population.The simulation results suggested that direction of cell movement responding to its neighborhood and the cell's mobility are important for this specific rearrangement.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. ttmaeda@gsc.riken.jp

ABSTRACT

Background: Development of multicellular organisms proceeds from a single fertilized egg as the combined effect of countless numbers of cellular interactions among highly dynamic cells. Since at least a reminiscent pattern of morphogenesis can be recapitulated in a reproducible manner in reaggregation cultures of dissociated embryonic cells, which is known as cell sorting, the cells themselves must possess some autonomous cell behaviors that assure specific and reproducible self-organization. Understanding of this self-organized dynamics of heterogeneous cell population seems to require some novel approaches so that the approaches bridge a gap between molecular events and morphogenesis in developmental and cell biology. A conceptual cell model in a computer may answer that purpose. We constructed a dynamical cell model based on autonomous cell behaviors, including cell shape, growth, division, adhesion, transformation, and motility as well as cell-cell signaling. The model gives some insights about what cellular behaviors make an appropriate global pattern of the cell population.

Results: We applied the model to "inside and outside" pattern of cell-sorting, in which two different embryonic cell types within a randomly mixed aggregate are sorted so that one cell type tends to gather in the central region of the aggregate and the other cell type surrounds the first cell type. Our model can modify the above cell behaviors by varying parameters related to them. We explored various parameter sets with which the "inside and outside" pattern could be achieved. The simulation results suggested that direction of cell movement responding to its neighborhood and the cell's mobility are important for this specific rearrangement.

Conclusion: We constructed an in silico cell model that mimics autonomous cell behaviors and applied it to cell sorting, which is a simple and appropriate phenomenon exhibiting self-organization of cell population. The model could predict directional cell movement and its mobility are important in the "inside and outside" pattern of cell sorting. Those behaviors are altered by signal molecules and consequently affect the global pattern of the cell sorting. Our model is also applicable to other developmental processes beyond cell sorting.

Show MeSH
Related in: MedlinePlus