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A Membrane-Bound Biosensor Visualizes Shear Stress-Induced Inhomogeneous Alteration of Cell Membrane Tension.

ABSTRACT: Cell membrane is the first medium from where a cell senses and responds to external stress stimuli. Exploring the tension changes in cell membrane will help us to understand intracellular force transmission. Here, a biosensor (named MSS) based on fluorescence resonance energy transfer is developed to visualize cell membrane tension. Validity of the biosensor is first verified for the detection of cell membrane tension. Results show a shear stress-induced heterogeneous distribution of membrane tension with the biosensor, which is strengthened by the disruption of microfilaments or enhancement of membrane fluidity, but weakened by the reduction of membrane fluidity or disruption of microtubules. These findings suggest that the MSS biosensor is a beneficial tool to visualize the changes and distribution of cell membrane tension. Besides, cell membrane tension does not display obvious polar distribution, indicating that cellular polarity changes do not first occur on the cell membrane during mechanical transmission.

SUBMITTER: Li W

PROVIDER: S-EPMC6153118 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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A Membrane-Bound Biosensor Visualizes Shear Stress-Induced Inhomogeneous Alteration of Cell Membrane Tension.

Li Wang W Yu Xinlei X Xie Fei F Zhang Baohong B Shao Shuai S Geng Chunyang C Aziz Aziz Ur Rehman AUR Liao Xiaoling X Liu Bo B

iScience 20180908

Cell membrane is the first medium from where a cell senses and responds to external stress stimuli. Exploring the tension changes in cell membrane will help us to understand intracellular force transmission. Here, a biosensor (named MSS) based on fluorescence resonance energy transfer is developed to visualize cell membrane tension. Validity of the biosensor is first verified for the detection of cell membrane tension. Results show a shear stress-induced heterogeneous distribution of membrane te ...[more]

PMID: 30267679

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Project description:The plasma membrane hosts a wide range of biomolecules, mainly proteins and carbohydrates, that mediate cellular interactions with its environment. The crowding of such biomolecules regulates cellular morphologies and cellular trafficking. Recent discoveries have shown that the structure and density of cell surface polymers and hence the signaling machinery change with the state of the cell, especially in cancer progression. The alterations in membrane-attached glycocalyx and glycosylation of proteins and lipids are common features of cancer cells. The overexpression of glycocalyx polymers, such as mucin and hyaluronan, strongly correlates with cancer metastasis. Here, we present a mesoscale biophysics-based model that accounts for the shape regulation of membranes by crowding of membrane-attached biopolymer-glycocalyx and actin networks. Our computational model is based on the dynamically triangulated Monte Carlo model for membranes and coarse-grained representations of polymer chains. The model allows us to investigate the crowding-induced shape transformations in cell membranes in a tension- and graft polymer density-dependent manner. Our results show that the number of membrane protrusions and their shape depend on membrane tension, with higher membrane tension inducing more tubular protrusions than the vesicular shapes formed at low tension at high surface coverage of polymers. The shape transformations occur above the threshold density predicted by the polymer brush theory, but this threshold also depends on the membrane tension. Increasing the size of the polymer, either by changing the length or by adding side chains, is shown to increase the crowding-induced curvature. The effect of crowding is more prominent for flexible polymers than for semiflexible rigid polymers. We also present an extension of the model that incorporates properties of the actin-like filament networks and demonstrate how tubular structures can be generated by biopolymer crowding on the cytosolic side of cell membranes.

Dataset Information

A Membrane-Bound Biosensor Visualizes Shear Stress-Induced Inhomogeneous Alteration of Cell Membrane Tension.

Publications

A Membrane-Bound Biosensor Visualizes Shear Stress-Induced Inhomogeneous Alteration of Cell Membrane Tension.

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