Intracellular softening and increased viscoelastic fluidity during division

Hurst, Sebastian; Vos, Bart E.; Brandt, Matthias; Betz, Timo

doi:10.1038/s41567-021-01368-z

Cited by 58 publications

(59 citation statements)

References 48 publications

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“…Effectively, the protocol harvests information from the colored noise, turns it into heat necessary for the transition between the two non-equilibrium states, and finally releases it to the surrounding environment. The ubiquity of non-equilibrium steady states in biological systems, including changes in the spectrum of the bath through time (for example during mitosis [18,19]) suggests exciting applications for the present findings.…”

mentioning

confidence: 78%

“…We further demonstrate that it is possible to drive the bead from one NESS to another through the sole change of the correlation time (i.e., the "color") of the active fluctuations. For instance, transitions between NESS are known to occur when biological matter undergoes a change in mechanical properties, such as during mitosis, and thereby a modification of the intracellular noise spectrum [18,19]. Modulating the color of the noise without changing its amplitude makes it possible to achieve heat production at constant energy input.…”

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confidence: 99%

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Harvesting information to control non-equilibrium states of active matter

Goerlich,

Pires,

Manfredi

et al. 2021

Preprint

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We propose to use a correlated noise bath to drive an optically trapped Brownian particle that mimics active biological matter. Thanks to the flexibility and precision of our setup, we are able to control the different parameters that drive the stochastic motion of the particle with unprecedented accuracy, thus reaching strongly correlated regimes that are not easily accessible with real active matter. In particular, by using the correlation time (i.e., the "color") of the noise as a control parameter, we can trigger transitions between two non-equilibrium steady states with no expended work, but only a calorific cost. Remarkably, the measured heat production is directly proportional to the spectral entropy of the correlated noise, in a fashion that is reminiscent of Landauer's principle. Our procedure can be viewed as a method for harvesting information from the active fluctuations.

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mentioning

confidence: 78%

mentioning

confidence: 99%

Harvesting information to control non-equilibrium states of active matter

Goerlich,

Pires,

Manfredi

et al. 2021

Preprint

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“…Mechanical phenotyping of tissues at multiple length scales have been of great interest in the field of mechanobiology. Optical based techniques such as optical stretchers [71], optical and magnetic tweezer-based modalities [33, 72, 73], real time deformation cytometry [74] have been employed to probe from nm scale to µm scale. However, many of these techniques for assessing material properties are unable to probe microscale mechanics for cells embedded in complex 3D tissues.…”

Section: Discussionmentioning

confidence: 99%

Multimodal microscale mechanical mapping of cancer cells in complex microenvironments

Nikolić

Scarcelli

Tanner

2022

Preprint

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The mechanical phenotype of the cell is critical for survival following deformations due to confinement and fluid flow. One idea is that cancer cells are plastic and adopt different mechanical phenotypes under different geometries that aid in their survival. Thus, an attractive goal, is to disrupt the cancer cells' ability to adopt multiple mechanical states. To begin to address this question, we aimed to quantify the diversity of these mechanical states using in vitro biomimetics to mimic in vivo 2D and 3D extracellular matrix environments. Here, we used two modalities Brillouin microscopy (~GHz) and broadband frequency (3-15kHz) optical tweezer microrheology to measure microscale cell mechanics. We measured the response of intracellular mechanics of cancer cells cultured in 2D and 3D environments where we modified substrate stiffness, dimensionality (2D versus 3D), and presence of fibrillar topography. We determined that there was good agreement between two modalities despite the difference in timescale of the two measurements. These findings on cell mechanical phenotype in different environments confirm a correlation between modalities that employ different mechanisms at different temporal scales (Hz-kHz vs. GHz). We also determined that observed heterogeneity in cell shape that is more closely linked to the cells' mechanical state. We also determined that individual cells in multicellular spheroids exhibit a lower degree of mechanical heterogeneity when compared to single cells cultured in monodisperse 3D cultures. Moreover, the observed decreased heterogeneity among cells in spheroids suggested that there is mechanical cooperativity between cells that make up a single spheroid.

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Section: Introductionmentioning

confidence: 99%

“…Cell division, where a single cell divides into two, is a crucial process in the cell cycle marked by substantial changes in cell morphology, biochemistry and mechanics [6,7]. Cell morphological change during division is driven by drastic remodeling of the cytoskeleton -a complex and dynamic network of proteins present in most animal cells [6,[8][9][10]. The cell cortex is composed of a thin actin protein network bound to the cell membrane with a dense crosslinked meshwork architecture [11] that determines cell deformation in response to intercellular and extracellular forces [12].…”

Section: Introductionmentioning

confidence: 99%

Enhanced mechanical heterogeneity of cell collectives due to temporal fluctuations in cell elasticity

Garrett¹,

Datta²,

Malmi-Kakkada³

2022

Preprint

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Cells are dynamic systems characterized by temporal variations in biophysical properties such as stiffness and contractility. Recent studies show that the recruitment and release of actin filaments into and out of the cell cortex -a network of proteins underneath the cell membrane -leads to cell stiffening prior to division and softening immediately afterward. In three-dimensional (3D) cell collectives, it is unclear whether the stiffness change during division at the single-cell scale controls the spatial structure and dynamics at the multicellular scale. This is an important question to understand as cell stiffness variations play an important role in tissue spatial organization and cancer progression. Using a minimal 3D model incorporating cell birth, death, and cell-to-cell elastic and adhesive interactions, we investigate the effect of mechanical heterogeneity -variations in individual cell stiffnesses that make up the tumor cell collective -on tumor spatial organization and cell dynamics. We discover that spatial mechanical heterogeneity characterized by a spheroid core composed of stiffer cells and softer cells in the periphery emerge within dense 3D cell collectives, which may be a general feature of multicellular tumor growth. We show that heightened spatial mechanical heterogeneity enhances single-cell dynamics and volumetric tumor growth driven by fluctuations in cell elasticity. Our results could have important implications for understanding how spatiotemporal variations in single-cell stiffness determine tumor growth and spread.

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Intracellular softening and increased viscoelastic fluidity during division

Cited by 58 publications

References 48 publications

Harvesting information to control non-equilibrium states of active matter

Harvesting information to control non-equilibrium states of active matter

Multimodal microscale mechanical mapping of cancer cells in complex microenvironments

Enhanced mechanical heterogeneity of cell collectives due to temporal fluctuations in cell elasticity

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