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Geometry-Driven Polarity in Motile Amoeboid Cells.

Nagel O, Guven C, Theves M, Driscoll M, Losert W, Beta C - PLoS ONE (2014)

Bottom Line: Their actin cytoskeleton exhibits a characteristic arrangement that is dominated by dense, stationary actin foci at the side walls, in conjunction with less dense dynamic regions at the leading edge.Our experimental findings can be explained based on an excitable network model that accounts for the confinement-induced symmetry breaking and correctly recovers the spatio-temporal pattern of protrusions at the leading edge.Since motile cells typically live in the narrow interstitial spacings of tissue or soil, we expect that the geometry-driven polarity we report here plays an important role for movement of cells in their natural environment.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physics und Astronomy, University of Potsdam, Potsdam, Germany.

ABSTRACT
Motile eukaryotic cells, such as leukocytes, cancer cells, and amoeba, typically move inside the narrow interstitial spacings of tissue or soil. While most of our knowledge of actin-driven eukaryotic motility was obtained from cells that move on planar open surfaces, recent work has demonstrated that confinement can lead to strongly altered motile behavior. Here, we report experimental evidence that motile amoeboid cells undergo a spontaneous symmetry breaking in confined interstitial spaces. Inside narrow channels, the cells switch to a highly persistent, unidirectional mode of motion, moving at a constant speed along the channel. They remain in contact with the two opposing channel side walls and alternate protrusions of their leading edge near each wall. Their actin cytoskeleton exhibits a characteristic arrangement that is dominated by dense, stationary actin foci at the side walls, in conjunction with less dense dynamic regions at the leading edge. Our experimental findings can be explained based on an excitable network model that accounts for the confinement-induced symmetry breaking and correctly recovers the spatio-temporal pattern of protrusions at the leading edge. Since motile cells typically live in the narrow interstitial spacings of tissue or soil, we expect that the geometry-driven polarity we report here plays an important role for movement of cells in their natural environment.

No MeSH data available.


Related in: MedlinePlus

Movement in narrow microchannels — random and persistent walkers.(A) Snapshots of cells moving outside the microchannels on a planar open surface. (B) Persistent walker moving inside a microchannel, scale bar 10 µm. (C) Position of the persistent walker as a function of time. (D) Position of a random walker inside a microchannel as a function of time. (E) Average velocities of persistent (filled) and random walkers (open circles) for different experiments. The numbers of persistent and random walkers were (1) 5 and 4, (2) 5 and 3, (3) 3 and 3, (4) 10 and 5.
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pone-0113382-g001: Movement in narrow microchannels — random and persistent walkers.(A) Snapshots of cells moving outside the microchannels on a planar open surface. (B) Persistent walker moving inside a microchannel, scale bar 10 µm. (C) Position of the persistent walker as a function of time. (D) Position of a random walker inside a microchannel as a function of time. (E) Average velocities of persistent (filled) and random walkers (open circles) for different experiments. The numbers of persistent and random walkers were (1) 5 and 4, (2) 5 and 3, (3) 3 and 3, (4) 10 and 5.

Mentions: Using bright field microscopy, we record the motion of adherent Dictyostelium cells in microfluidic devices, composed of narrow channels (10 µm wide and 20 µm high) that are connected by wider inlet regions (see the Figure S5 for the layout of the device). In the inlet regions, cells can be observed that do not touch any of the channel side walls and are freely moving on a planar open surface, see Figure 1A and the corresponding movie in the Supporting Information. These cells do not show a well-defined leading edge and perform an irregular random walk. Inside the microchannels, cells from the same population split into two subgroups with clearly distinct motile behavior. The majority of the cells move randomly inside the channel, displaying frequent changes in the direction of motion and a strongly varying cell shape. Movement of these cells is interrupted by frequent pauses and results in only a small net displacement, similar to the cells outside the channels. In contrast, a second subpopulation of about one quarter of the cells moves persistently at a constant high speed along the channel without changing their direction of motion, see Figure 1B for an example. In most cases, cells of this subpopulation maintain persistent motion at uniform speed throughout the entire duration of the recording, often for more than half an hour. We refer to the first subpopulation as the “random walkers” and designate the second subpopulation as “persistent walkers”. A systematic analysis based on several of our recordings revealed that about 28% of the total population (18 out of 64 cells) moved as persistent walkers through the microchannel.


Geometry-Driven Polarity in Motile Amoeboid Cells.

Nagel O, Guven C, Theves M, Driscoll M, Losert W, Beta C - PLoS ONE (2014)

Movement in narrow microchannels — random and persistent walkers.(A) Snapshots of cells moving outside the microchannels on a planar open surface. (B) Persistent walker moving inside a microchannel, scale bar 10 µm. (C) Position of the persistent walker as a function of time. (D) Position of a random walker inside a microchannel as a function of time. (E) Average velocities of persistent (filled) and random walkers (open circles) for different experiments. The numbers of persistent and random walkers were (1) 5 and 4, (2) 5 and 3, (3) 3 and 3, (4) 10 and 5.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4262208&req=5

pone-0113382-g001: Movement in narrow microchannels — random and persistent walkers.(A) Snapshots of cells moving outside the microchannels on a planar open surface. (B) Persistent walker moving inside a microchannel, scale bar 10 µm. (C) Position of the persistent walker as a function of time. (D) Position of a random walker inside a microchannel as a function of time. (E) Average velocities of persistent (filled) and random walkers (open circles) for different experiments. The numbers of persistent and random walkers were (1) 5 and 4, (2) 5 and 3, (3) 3 and 3, (4) 10 and 5.
Mentions: Using bright field microscopy, we record the motion of adherent Dictyostelium cells in microfluidic devices, composed of narrow channels (10 µm wide and 20 µm high) that are connected by wider inlet regions (see the Figure S5 for the layout of the device). In the inlet regions, cells can be observed that do not touch any of the channel side walls and are freely moving on a planar open surface, see Figure 1A and the corresponding movie in the Supporting Information. These cells do not show a well-defined leading edge and perform an irregular random walk. Inside the microchannels, cells from the same population split into two subgroups with clearly distinct motile behavior. The majority of the cells move randomly inside the channel, displaying frequent changes in the direction of motion and a strongly varying cell shape. Movement of these cells is interrupted by frequent pauses and results in only a small net displacement, similar to the cells outside the channels. In contrast, a second subpopulation of about one quarter of the cells moves persistently at a constant high speed along the channel without changing their direction of motion, see Figure 1B for an example. In most cases, cells of this subpopulation maintain persistent motion at uniform speed throughout the entire duration of the recording, often for more than half an hour. We refer to the first subpopulation as the “random walkers” and designate the second subpopulation as “persistent walkers”. A systematic analysis based on several of our recordings revealed that about 28% of the total population (18 out of 64 cells) moved as persistent walkers through the microchannel.

Bottom Line: Their actin cytoskeleton exhibits a characteristic arrangement that is dominated by dense, stationary actin foci at the side walls, in conjunction with less dense dynamic regions at the leading edge.Our experimental findings can be explained based on an excitable network model that accounts for the confinement-induced symmetry breaking and correctly recovers the spatio-temporal pattern of protrusions at the leading edge.Since motile cells typically live in the narrow interstitial spacings of tissue or soil, we expect that the geometry-driven polarity we report here plays an important role for movement of cells in their natural environment.

View Article: PubMed Central - PubMed

Affiliation: Institute of Physics und Astronomy, University of Potsdam, Potsdam, Germany.

ABSTRACT
Motile eukaryotic cells, such as leukocytes, cancer cells, and amoeba, typically move inside the narrow interstitial spacings of tissue or soil. While most of our knowledge of actin-driven eukaryotic motility was obtained from cells that move on planar open surfaces, recent work has demonstrated that confinement can lead to strongly altered motile behavior. Here, we report experimental evidence that motile amoeboid cells undergo a spontaneous symmetry breaking in confined interstitial spaces. Inside narrow channels, the cells switch to a highly persistent, unidirectional mode of motion, moving at a constant speed along the channel. They remain in contact with the two opposing channel side walls and alternate protrusions of their leading edge near each wall. Their actin cytoskeleton exhibits a characteristic arrangement that is dominated by dense, stationary actin foci at the side walls, in conjunction with less dense dynamic regions at the leading edge. Our experimental findings can be explained based on an excitable network model that accounts for the confinement-induced symmetry breaking and correctly recovers the spatio-temporal pattern of protrusions at the leading edge. Since motile cells typically live in the narrow interstitial spacings of tissue or soil, we expect that the geometry-driven polarity we report here plays an important role for movement of cells in their natural environment.

No MeSH data available.


Related in: MedlinePlus