Relation between the rate of cell movement under agarose and the positioning of cells in heterotypic aggregates

doi:10.1016/0014-4827(89)90233-4

Experimental Cell Research

Volume 180, Issue 1, January 1989, Pages 287-296

https://doi.org/10.1016/0014-4827(89)90233-4 Get rights and content

Abstract

Single-cell suspensions prepared from 9-day-old chick tissues (skeletal muscle, liver, and neural retina) were used to investigate a possible relationship between intrinsic mobilities of different cell types and their positioning behavior in mixed (heterotypic) cellular aggregates. The relative mobilities of the three cell types, determined by comparing their ability to migrate under an agarose layer, was muscle > liver > neural retina. The gyratory shaker method was employed to produce heterotypic aggregates from mixed suspensions of muscle, liver, and neural retina cells and the tissue-specific positioning of cells after 24 h in culture was determined from histological and autoradiograph sections. The hierarchy for “inside” positioning of segregated cells was muscle > liver > neural retina cells, correlating with the rate of movement of these cells in the migration assay. The implication of the results is that relative speed of movement may determine the positioning of cells in heterotypic aggregates.

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Cited by (11)

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2017, Biophysical Journal
Citation Excerpt :
However, there is disagreement on the rules regulating engulfment for a mixture of two cell types with different locomotion properties. Jones et al. (18) found that chick tissues sorted so that the fastest moving tissue ended up on the inside of a mixed cellular aggregate. In contrast, theoretical work showed that when full sorting occurred, faster cells surrounded slower ones and formed streams around them (16).
Cell sorting, whereby a heterogeneous cell mixture organizes into distinct tissues, is a fundamental patterning process in development. Hydra is a powerful model system for carrying out studies of cell sorting in three dimensions, because of its unique ability to regenerate after complete dissociation into individual cells. The physicists Alfred Gierer and Hans Meinhardt recognized Hydra’s self-organizing properties more than 40 years ago. However, what drives cell sorting during regeneration of Hydra from cell aggregates is still debated. Differential motility and differential adhesion have been proposed as driving mechanisms, but the available experimental data are insufficient to distinguish between these two. Here, we answer this longstanding question by using transgenic Hydra expressing fluorescent proteins and a multiscale experimental and numerical approach. By quantifying the kinematics of single cell and whole aggregate behaviors, we show that no differences in cell motility exist among cell types and that sorting dynamics follow a power law with an exponent of ∼0.5. Additionally, we measure the physical properties of separated tissues and quantify their viscosities and surface tensions. Based on our experimental results and numerical simulations, we conclude that tissue interfacial tensions are sufficient to explain cell sorting in aggregates of Hydra cells. Furthermore, we demonstrate that the aggregate’s geometry during sorting is key to understanding the sorting dynamics and explains the exponent of the power law behavior. Our results answer the long standing question of the physical mechanisms driving cell sorting in Hydra cell aggregates. In addition, they demonstrate how powerful this organism is for biophysical studies of self-organization and pattern formation.
Cell Sorting in Development
2011, Current Topics in Developmental Biology
Citation Excerpt :
The DITH differs from the DAH and the DSCH theories by combining cell contraction and adhesion and taking into account the possibility of additional properties of the cell (e.g., cytoplasm viscosity, density of the cell content) that are likely to influence interfacial tensions and, consequently, drive cell sorting. Various other mechanisms were proposed to explain cell sorting, such as differences in cell motility (Jones et al., 1989), specific adhesion (Curtis, 1960; Moscona, 1962; Townes and Holtfreter, 1955), chemotaxis, directed migration (Townes and Holtfreter, 1955), and the timing of sorting initiation (Armstrong, 1989; Curtis, 1961; Steinberg, 1996). Most of these mechanisms are likely to be insufficient to explain cell sorting, as the experimental patterns of cell sorting generally do not correspond to the patterns predicted by those mechanisms (Steinberg, 1996).
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Short noteRelation between the rate of cell movement under agarose and the positioning of cells in heterotypic aggregates

Abstract

Exp. Cell Res

Dev. Biol

J. Cell Biol

J. Cell. Sci

J. Exp. Zool

Cells into Organs

Short note
Relation between the rate of cell movement under agarose and the positioning of cells in heterotypic aggregates