Volumetric Deformation of Live Cells Induced by Pressure-Activated Cross-Membrane Ion Transport

Hui, Tsz Hin; Zhou, Zhuo; Qian, Jin; Lin, Yuan; Ngan, A.H.W.; Gao, Huajian

doi:10.1103/physrevlett.113.118101

Cited by 51 publications

(57 citation statements)

References 32 publications

(34 reference statements)

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“…Here, we document that under compressive stress, multicell spheroids as well as cell monolayers will decrease their intracellular tonicity by effluxing sodium, and that although cytoskeletal filaments do not actively support compressive stress, actin polymerization is required for osmotic regulation. This finding is consistent with the work of Hui et al (12), who found that increased hydrostatic pressure induced active sodium efflux. Recent studies using C. elegans suggested that these organisms may have an absolute internal pressure set point (16).…”

Section: Discussionsupporting

confidence: 91%

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Osmotic Regulation Is Required for Cancer Cell Survival under Solid Stress

McGrail

McAndrews

Brandenburg

et al. 2015

Biophysical Journal

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For a solid tumor to grow, it must be able to support the compressive stress that is generated as it presses against the surrounding tissue. Although the literature suggests a role for the cytoskeleton in counteracting these stresses, there has been no systematic evaluation of which filaments are responsible or to what degree. Here, using a three-dimensional spheroid model, we show that cytoskeletal filaments do not actively support compressive loads in breast, ovarian, and prostate cancer. However, modulation of tonicity can induce alterations in spheroid size. We find that under compression, tumor cells actively efflux sodium to decrease their intracellular tonicity, and that this is reversible by blockade of sodium channel NHE1. Moreover, although polymerized actin does not actively support the compressive load, it is required for sodium efflux. Compression-induced cell death is increased by both sodium blockade and actin depolymerization, whereas increased actin polymerization offers protective effects and increases sodium efflux. Taken together, these results demonstrate that cancer cells modulate their tonicity to survive under compressive solid stress.

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Section: Discussionsupporting

confidence: 91%

“…2 B). This is consistent with previous studies that showed that hydrostatic pressure induces sodium efflux (12). Repeating this Biophysical Journal 109 (7) 1334-1337 experiment with modulation of actin filaments revealed that actin depolymerization blocked sodium efflux to a similar degree as NHE1 blockade.…”

Section: Sodium Efflux Under Compressive Solid Stresssupporting

confidence: 90%

Osmotic Regulation Is Required for Cancer Cell Survival under Solid Stress

McGrail

McAndrews

Brandenburg

et al. 2015

Biophysical Journal

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“…Interestingly, atomic force microscopy-based studies have demonstrated that the energy density of individual dormant cells (i.e., Bacillus spores) in response to cyclic humidity variations is at least one order of magnitude higher than any synthetic materials including DEs . Live cells were shown to volumetrically shrink or swell via cross-membrane ion transport upon applied mechanical pressure (Hui et al, 2014). These results highlight the distinct advantage of involving biologically based materials in DE actuation and energy harvesting, and open a new avenue to build DE-made soft machines with tunable mechanical, chemical as well as electrical properties to generate active force/ motion at the (sub)cellular scale for potential applications in biomaterials and biointerfaces Zhang et al, 2013).…”

Section: Concluding Remarks and Outlookmentioning

confidence: 91%

Mechanics of dielectric elastomers: materials, structures, and devices

Qian

2016

JZUS-A

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Dielectric elastomers (DEs) respond to applied electric voltage with a surprisingly large deformation, showing a promising capability to generate actuation in mimicking natural muscles. A theoretical foundation of the mechanics of DEs is of crucial importance in designing DE-based structures and devices. In this review, we survey some recent theoretical and numerical efforts in exploring several aspects of electroactive materials, with emphases on the governing equations of electromechanical coupling, constitutive laws, viscoelastic behaviors, electromechanical instability as well as actuation applications. An overview of analytical models is provided based on the representative approach of non-equilibrium thermodynamics, with computational analyses being required in more generalized situations such as irregular shape, complex configuration, and time-dependent deformation. Theoretical efforts have been devoted to enhancing the working limits of DE actuators by avoiding electromechanical instability as well as electric breakdown, and pre-strains are shown to effectively avoid the two failure modes. These studies lay a solid foundation to facilitate the use of DE materials, structures, and devices in a wide range of applications such as biomedical devices, adaptive systems, robotics, energy harvesting, etc.

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“…With the evolution of c Lþ at hand, the volumetric change of cells can then be determined by tracking the water efflux from (or influx into) the cell (9). Specifically, treating the cell as a droplet enclosed by an elastic membrane layer, permeable to water molecules only, its size change can be described by…”

Section: Theoretical Model Of Cell-size Manipulation By Electroosmotimentioning

confidence: 99%

“…Currently, the most convenient and popular way to alter the cellular volume is via osmotic shocks, that is, by the sudden addition/withdrawal of salt to/from the culture medium (6)(7)(8). Interestingly, a recent study has revealed that variations in the surrounding hydrostatic pressure can also lead to volumetric change of live cells (9). A common theme of these approaches is that, essentially, a step change to the microenvironment of cells (i.e., osmolarity or hydrostatic pressure) is introduced.…”

Section: Introductionmentioning

confidence: 98%

Regulating the Membrane Transport Activity and Death of Cells via Electroosmotic Manipulation

Hui

Kwan

Yip

et al. 2016

Biophysical Journal

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Although the volume of living cells has been known to heavily influence their behavior and fate, a method allowing us to control the cell size in a programmable manner is still lacking. Here, we develop a technique in which precise changes in the cellular volume can be conveniently introduced by varying the voltage applied across a Nafion membrane that separates the culture medium from a reservoir. It is found that, unlike sudden osmotic shocks, active ion transport across the membrane of leukemia K562 cells will not be triggered by a gradual change in the extracellular osmolarity. Furthermore, when subjected to the same applied voltage, different lung and nasopharyngeal epithelial cancer cells will undergo larger volumetric changes and have a 5-10% higher death rate compared to their normal counterparts. We show that such distinct response is largely caused by the overexpression of aquaporin-4 in tumor cells, with knockout of this water channel protein resulting in a markedly reduced change in the cellular volume. Finally, by taking into account the exchange of water/ion molecules across the Nafion film and the cell membrane, a theoretical model is also proposed to describe the voltage-induced size changes of cells, which explain our experimental observations very well.

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Volumetric Deformation of Live Cells Induced by Pressure-Activated Cross-Membrane Ion Transport

Cited by 51 publications

References 32 publications

Osmotic Regulation Is Required for Cancer Cell Survival under Solid Stress

Osmotic Regulation Is Required for Cancer Cell Survival under Solid Stress

Mechanics of dielectric elastomers: materials, structures, and devices

Regulating the Membrane Transport Activity and Death of Cells via Electroosmotic Manipulation

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