Limits...
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

Localization of F-actin and myosin II in a persistant walker.(A) Fluorescence image showing the distribution of LimE-RFP, a marker for filamentous actin, inside a persistent walker. (B) Fluorescence image displaying the distribution of myosin II-GFP inside the same cell. Images in (A) and (B) were recorded by confocal microscopy, the cell is moving from left to right along the microchannel. Kymographs of (C) LimE-RFP distribution and (D) myosin II-GFP distribution along the cell border. Gray bars to the left of the kymographs indicate the average positions of the channel walls. — single cell example out of more than 10 cells.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4262208&req=5

pone-0113382-g003: Localization of F-actin and myosin II in a persistant walker.(A) Fluorescence image showing the distribution of LimE-RFP, a marker for filamentous actin, inside a persistent walker. (B) Fluorescence image displaying the distribution of myosin II-GFP inside the same cell. Images in (A) and (B) were recorded by confocal microscopy, the cell is moving from left to right along the microchannel. Kymographs of (C) LimE-RFP distribution and (D) myosin II-GFP distribution along the cell border. Gray bars to the left of the kymographs indicate the average positions of the channel walls. — single cell example out of more than 10 cells.

Mentions: In Figures 3A and B, snapshots of the actin and myosin II distributions in a persistent walker are displayed. We observe increased concentrations of F-actin at the sides of the cell that are in contact with the microchannel walls. In contrast, myosin II was mostly found at the back of the cell, where the cell body retracts. The time evolution of the cortical acto-myosin distribution is summarized in the kymographs displayed in Figures 3C and D (see Supporting Information for the corresponding movies). In Figure 3 C, the LimE-RFP fluorescence intensity is shown for each point on the cell boundary over time. The kymograph shows patches of increased actin concentration that persist at the wall-attached sides of the cell throughout the recording. To a lesser extent, F-actin also localizes at sites of protrusion formation at the cell front. A similar kymograph for the myosin II distribution is shown in Figure 3D. Here, we observe that myosin II is depleted from the actin rich areas at the wall-attached sides. At the cell front, moderate myosin II concentrations are found in places where protrusions retracted, while maximal accumulation of myosin II is observed at the back (around boundary positions 0 and 400). Additional experiments with myosin II knockout mutants demonstrate that myosin II is not essential for persistent unidirectional motion along the microchannels. Also among the myosin II deficient cells a subpopulation of persistent walkers is found similar to the wild-type (data shown in Figure S2).


Geometry-Driven Polarity in Motile Amoeboid Cells.

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

Localization of F-actin and myosin II in a persistant walker.(A) Fluorescence image showing the distribution of LimE-RFP, a marker for filamentous actin, inside a persistent walker. (B) Fluorescence image displaying the distribution of myosin II-GFP inside the same cell. Images in (A) and (B) were recorded by confocal microscopy, the cell is moving from left to right along the microchannel. Kymographs of (C) LimE-RFP distribution and (D) myosin II-GFP distribution along the cell border. Gray bars to the left of the kymographs indicate the average positions of the channel walls. — single cell example out of more than 10 cells.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0113382-g003: Localization of F-actin and myosin II in a persistant walker.(A) Fluorescence image showing the distribution of LimE-RFP, a marker for filamentous actin, inside a persistent walker. (B) Fluorescence image displaying the distribution of myosin II-GFP inside the same cell. Images in (A) and (B) were recorded by confocal microscopy, the cell is moving from left to right along the microchannel. Kymographs of (C) LimE-RFP distribution and (D) myosin II-GFP distribution along the cell border. Gray bars to the left of the kymographs indicate the average positions of the channel walls. — single cell example out of more than 10 cells.
Mentions: In Figures 3A and B, snapshots of the actin and myosin II distributions in a persistent walker are displayed. We observe increased concentrations of F-actin at the sides of the cell that are in contact with the microchannel walls. In contrast, myosin II was mostly found at the back of the cell, where the cell body retracts. The time evolution of the cortical acto-myosin distribution is summarized in the kymographs displayed in Figures 3C and D (see Supporting Information for the corresponding movies). In Figure 3 C, the LimE-RFP fluorescence intensity is shown for each point on the cell boundary over time. The kymograph shows patches of increased actin concentration that persist at the wall-attached sides of the cell throughout the recording. To a lesser extent, F-actin also localizes at sites of protrusion formation at the cell front. A similar kymograph for the myosin II distribution is shown in Figure 3D. Here, we observe that myosin II is depleted from the actin rich areas at the wall-attached sides. At the cell front, moderate myosin II concentrations are found in places where protrusions retracted, while maximal accumulation of myosin II is observed at the back (around boundary positions 0 and 400). Additional experiments with myosin II knockout mutants demonstrate that myosin II is not essential for persistent unidirectional motion along the microchannels. Also among the myosin II deficient cells a subpopulation of persistent walkers is found similar to the wild-type (data shown in Figure S2).

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