Possible Role of Contact Following in the Generation of Coherent Motion of Dictyostelium Cells

doi:10.1006/jtbi.2002.3124

Journal of Theoretical Biology

Volume 219, Issue 3, 7 December 2002, Pages 301-308

https://doi.org/10.1006/jtbi.2002.3124 Get rights and content

Abstract

After aggregation by chemotaxis, cells of the cellular slime mold Dictyostelium discoideum form a multicellular structure and show coherent motion such as vortices. Here, we present a mathematical model to explain both aggregation and coherent motion of cells in two-dimensional space. The model incorporates chemotactic response of cells and the cell's property, called “contact following”, to follow the other cells with which they are in contact. Analytical study and computer simulation using the model show that with contact following, cells form circular clusters within which cell rotation occurs. Unidirectional cell motion in a long belt of cells is another type of solution of the model. Besides, contact following has an effect to accelerate cell cluster merging. By considering the mechanism of cell movement, possible explanations of contact following are proposed.

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Cited by (23)

The intercellular expression of type-XVII collagen, laminin-332, and integrin-β1 promote contact following during the collective invasion of a cancer cell population
2019, Biochemical and Biophysical Research Communications
Citation Excerpt :
This study focuses on contact following, the phenomenon which provides intercellular adhesion for the movement of neighboring cells in the same direction, to investigate the mechanism in cancer cells which induces collectiveness. Contact following was proposed to account for the collective migration of Dictyostelium [10]. In addition, contact following also occurs in the collective migration of MDCK epithelial cells [11].
Cancer cells can invade as a population in various cancer tissues. This phenomenon is called collective invasion, which is associated with the metastatic potential and prognosis of cancer patients. The collectiveness of cancer cells is necessary for collective invasion. However, the mechanism underlying the generation of collectiveness by cancer cells is not well known. In this study, the phenomenon of contact following, where neighboring cells move in the same direction via intercellular adhesion, was investigated. An experimental system was created to observe the two-dimensional invasion using a collagen gel overlay to study contact following in collective invasion. The role of integrin-β1, one of the major extracellular matrix (ECM) receptors, in contact following was examined through the experimental system. Integrin-β1 was localized to the intercellular site in squamous carcinoma cells. Moreover, the intercellular adhesion and contact following were suppressed by treatment of an integrin-β1 inhibitory antibody. ECM proteins such as laminin-332 and type-XVII collagen were also localized to the intercellular site and critical for contact following. Collectively, it was demonstrated that the activity of integrin-β1 and expression of ECM proteins in the intercellular site promote contact following in the collective invasion of a cancer cell population.
How cellular movement determines the collective force generated by the Dictyostelium discoideum slug
2004, Journal of Theoretical Biology
Citation Excerpt :
On the other hand, some experiments suggest that the total motive force produced by the slug is proportional to its volume, and hence the total number of cells, which would rule out a `piggy-back' mechanism (Inouye and Takeuchi, 1980; Inouye, 1984). As will be discussed in more detail later, many have simply postulated that the active motive force is a volumetric force in their macroscopic description of slug movement (Inouye and Takeuchi, 1979; Umeda and Inouye, 1999, 2002; Vasiev et al., 1997). Others have also proposed descriptions in which interior cells can transfer momentum to the substrate (Umeda and Inouye, 1999; Bretschneider et al., 1997, 1999) without a detailed analysis of how this occurs.
How the collective motion of cells in a biological tissue originates in the behavior of a collection of individuals, each of which responds to the chemical and mechanical signals it receives from neighbors, is still poorly understood. Here we study this question for a particular system, the slug stage of the cellular slime mold Dictyostelium discoideum (Dd). We investigate how cells in the interior of a migrating slug can effectively transmit stress to the substrate and thereby contribute to the overall motive force. Theoretical analysis suggests necessary conditions on the behavior of individual cells, and computational results shed light on experimental results concerning the total force exerted by a migrating slug. The model predicts that only cells in contact with the substrate contribute to the translational motion of the slug. Since the model is not based specifically on the mechanical properties of Dd cells, the results suggest that this behavior will be found in many developing systems.
Dictyostelium morphogenesis
2004, Current Opinion in Genetics and Development
During starvation-induced Dictyostelium development, up to several hundred thousand amoeboid cells aggregate, differentiate and form a fruiting body. The chemotactic movement of the cells is guided by the rising phase of the outward propagating cAMP waves and results in directed periodic movement towards the aggregation centre. In the mound and slug stages of development, cAMP waves continue to play a major role in the coordination of cell movement, cell-type-specific gene expression and morphogenesis; however, in these stages where cells are tightly packed, cell–cell adhesion/contact-dependent signalling mechanisms also play important roles in these processes.
Cell sorting by differential cell motility: A model for pattern formation in Dictyostelium
2004, Journal of Theoretical Biology
In the slug stage of the cellular slime mold Dictyostelium discoideum, prespore cells and four types of prestalk cells show a well-defined spatial distribution in a migrating slug. We have developed a continuous mathematical model for the distribution pattern of these cell types based on the balance of force in individual cells. In the model, cell types are assumed to have different properties in cell motility, i.e. different motive force, the rate of resistance against cell movement, and diffusion coefficient. Analysis of the stationary solution of the model shows that combination of these parameters and slug speed determines the three-dimensional shape of a slug and cell distribution pattern within it. Based on experimental data of slug motive force and velocity measurements, appropriate sets of parameters were chosen so that the cell-type distribution at stationary state matches the distribution in real slugs. With these parameters, we performed numerical calculation of the model in two-dimensional space using a moving particle method. The results reproduced many of the basic features of slug morphogenesis, i.e. cell sorting, translocation of the prestalk region, elongation of the slug, and its steady migration.
A Biologically Inspired Model of Collective Bio-Nanomachine Rotation via Chemical and Physical Interactions
2023, IEEE Transactions on Nanobioscience
Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo
2023, Development (Cambridge)

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¹: Corresponding author. E-mail address: [email protected] (T. Umeda).

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Journal of Theoretical Biology

Abstract

References (26)

Chemomodulation of cellular movement, collective formation of vortices by swarming bacteria, and colonial development

Physica A

Dictyostelium discoideum aggregation fields as excitable media

J. theor. Biol.

The Acrasina

Adv. Morphog.

Intracellular movement and locomotion of cellular slime-mold amoebae

Spiral waves of cyclic AMP in a model of slime mold aggregation

Physica D

A mathematical model for cell sorting, migration and shape in the slug stage of Dictyostelium discoideum

Bull. Math. Biol.

Theoretical model for morphogenesis and cell sorting in Dictyostelium discoideum

Physica D

A hydrodynamic model for D. discoideum mound formation

J. theor. Biol.

Morphogenetic cell movement in Dictyostelium

Sem. Cell Dev. Biol.

A way of following individual cells in the migrating slugs of Dictyostelium discoideum

Proc. Natl Acad. Sci. U.S.A.

Life at the leading edge: the formation of cell protrusions

Annu. Rev. Cell Biol.

A discrete cell model with adaptive signalling for aggregation of Dictyostelium discoideum

Philos. Trans. R. Soc. London B

Cited by (23)

The intercellular expression of type-XVII collagen, laminin-332, and integrin-β1 promote contact following during the collective invasion of a cancer cell population

How cellular movement determines the collective force generated by the Dictyostelium discoideum slug

Dictyostelium morphogenesis

Cell sorting by differential cell motility: A model for pattern formation in Dictyostelium

A Biologically Inspired Model of Collective Bio-Nanomachine Rotation via Chemical and Physical Interactions

Quantitative videomicroscopy reveals latent control of cell-pair rotations in vivo

Regular ArticlePossible Role of Contact Following in the Generation of Coherent Motion of Dictyostelium Cells

Abstract

Physica A

J. theor. Biol.

Adv. Morphog.

Physica D

Bull. Math. Biol.

Physica D

J. theor. Biol.

Sem. Cell Dev. Biol.

A way of following individual cells in the migrating slugs of Dictyostelium discoideum

Proc. Natl Acad. Sci. U.S.A.

Life at the leading edge: the formation of cell protrusions

Annu. Rev. Cell Biol.

A discrete cell model with adaptive signalling for aggregation of Dictyostelium discoideum

Philos. Trans. R. Soc. London B

Regular Article
Possible Role of Contact Following in the Generation of Coherent Motion of Dictyostelium Cells